Macro-Evolution: The Vicissitudes of Life on Earth
Johan M.G. van der Dennen
Table: Geological Time Scale (not to scale and simplified)
Dates in millions of years ago (mya)
Note that the Paleozoic, Mesozoic and Cenozoic Eras together constitute the Phanerozoic Eon. The PrePhanerozoic consists of the Hadean (4,500-3,900 mya), Archean (3,900-2,500 mya), and Proterozoic (2,500-580 mya) Eons.
Maynard Smith & Szathmáry (1995) and Szathmáry & Maynard Smith (1995) propose a framework of eight 'major evolutionary transitions' defining the following nine 'stages':
1. The origin of simple autocatalytic systems with limited heredity;
2. The origin of polynucleotide-like molecules, providing unlimited heredity;
3. The origin of the genetic code in the context of the RNA world, before translation;
4. The origin of translation and encoded protein synthesis;
5. The replacement of RNA by DNA as the genetic code;
6. The emergence of hereditary regulative states in prokaryotes and simple eukaryotes;
7. The evolution of epigenetic inheritance with unlimited heredity: the emergence of animals, plants and fungi;8. The emergence of proto-language in Homo erectus - a cultural inheritance system with limited potential;
9. The emergence of human language with a universal grammar and unlimited semantic representation.
By tracing the different life-cycle setups attested throughout life's history, Naccache (1999) characterizes the successive modes of evolution with which they are associated as follows: basic; reptilian; archaic mammalian; progressive mammalian; sociocultural; extrasomatically enhanced sociocultural; tinkering; and finally parabiological. These represent, according to Naccache, eight hierachically nested modes of evolution that have governed the evolution of our lineage from the primeval cyanobacteria to present-day human societies. We shall come back to these different modes of evolution.
A strand of DNA (desoxyribonucleic acid) stores the blueprint, the hereditary information that ensures exact duplication of everything when the cell divides into two; enzymes direct the cell's biochemical reactions; small particles called ribosomes manufacture proteins (including enzymes); mitochondria break down compounds to release energy; in green plants chloroplasts make sugars with the aid of sunlight.
The DNA molecule defines the cell's nature, but more basic still, proteins are the key to the cell's existence. Proteins make up the structure of the cell, they regulate its processes and in the form of enzymes they catalyze its biochemical reactions. Proteins, in their turn, are made of amino acids, which are molecules of carbon, hydrogen, nitrogen and oxygen. Theoretically, a wide variety of amino acids could be formed from these basic ingredients, but in fact only 20 different kinds are used to build proteins. And it is always the same 20, whether in a single-cell bacterium, a leaf cell, or a human cell. So it could be said that amino acids, along with five nitrogenous molecules, plus glucose, some fats and sugars are the basic alphabet that spells out the story of life on Earth. As it happens, there are 29 characters (or compounds) in this basic alphabet of life, just three more than suffice for the English language (Reader, 1986).
According to Freeman Dyson (1985; as summarized by Newcombe, 1998: 82), the very earliest life consisted only of proteins, acting as catalysts (enzymes) on each other in complex reaction cycles and hypercycles. There were at first no self-reproducing genetic molecules like RNA (ribonucleic acid) and DNA. However, there were the energy-storage nucleotides ATP, GTP, etc., which are actually the monomers of RNA and DNA (i.e., units that can link up to form these larger self-reproducing macromolecules). Dyson hypothesized that these energy-storage nucleotides in some instances polymerized 'by accident' to the first RNA, which acted as a virus on the pre-existing all-protein life. Some of the infected cells sickened and died, but some learned to tolerate the parasite. The parasite became a symbiont. Eventually, over millions if years, the primal symbiosis of protein life with the self-reproducing RNA and DNA grew into a harmonious unity, the modern genetic apparatus. Because RNA could act not only as an enzyme like protein, but could also reproduce and store information like the later, more specialized DNA, it eventually became indispensable to early life. Ever since, proteins and nucleic acids (the common name for both RNA and DNA) have been so closely linked as to form an inextricably interconnected undecomposable system.
The idea that RNA-based replication and catalysis of metabolic processes may have preceded DNA-RNA-protein-based systems was first proposed in the late 1960s by Orgel and others. The discovery of ribozymes - catalytic RNA molecules - in the early 1980s provided support for this theory, and Walter Gilbert proposed the existence of an 'RNA-world'. Gilbert believes that, even at this state, RNA 'genes' contained primitive introns and exons. "Exon shuffling in an important evolutionary mechanism in DNA-based organisms and the evidence from genome sequences suggest that exons could have been a feature of early RNA life forms" (Gilbert quoted in Senior, 2000).
Gilbert predicts that the next few years may see a major shift in our view of early evolution. "It has always been thought that early prokaryotes lacked introns and that later organisms developed them. We now have strong evidence that bacteria have lost their introns during evolution". Gilbert speculates that bacteria may have evolved from larger, less efficient pre-eukaryotes, no examples of which survive. This theory is difficult to test, he says, but "in the next 5-10 years, genome-sequencing information from different organisms will resolve many issues. And further experiments on the nature of ribozymes should also provide important clues".
Not everyone, however, is convinced that an RNA world preceded our familiar DNA world. RNA is very unstable and some argue that it could not have survived the harsh conditions of the early Earth. Orgel speculates that a different nucleic acid was around before RNA and DNA but says that no acceptable candidate has been found (Senior, 2000: 814).
From bacteria to mammals, the DNA content of genomes has increased by three orders of magnitude in just 3 billions years of evolution. Early DNA association studies showed that the human genome is full of repeated segments, such as Alu elements, that are repeated hundreds of thousands of time. The vast majority of a mammalian genome does not code for proteins. Most researchers have assumed that these repetitive DNA elements do not have any function: they are simply useless, selfish (or parasitic) sequences that proliferate in our genome, making as many copies as possible: 'junk DNA'.
Lately, it has become apparent that transposable elements (or transposons) are not useless DNA. They interact with the surrounding genomic environment and increase the ability of the organism to evolve. They do this by serving as recombination hotspots, and providing a mechanism for genomic reshuffling and a source of 'ready-to-use' motifs for new transcriptional regulatory elements, polyadenylation signals, and protein-coding sequences (Makalowski, 2003).
With the emergence of this polynucleotide, the abiotic eons had ended, and the history of life on Earth begins. Over the following 3.8 billion years, life's realm extended from blue-green algae to human societies. Life's basic components being the physicochemical elements of the inorganic world, all of life's denizens obey the fundamental physicochemical laws that govern their components' behavior in nonliving matter. However, the physicochemical mechanisms only set limits to life, and do not govern its blooming. Clearly, within today's scientific worldview, the 'Darwinian' mechanism is the only candidate considered for that governing task (Naccache, 1999: 15).
Ever since a molecule for the first time started to replicate, i.e., to make copies of itself, life existed on earth and, with it, the process of natural selection. Those self-replicating entities which reproduced fastest or most efficiently, inevitably became the most numerous in the population of self-replicators. From a Darwinian perspective the defining property of life - besides self-maintenance or autopoiesis - is self-replication; any organism is a self-reproducing entity or 'machine'. It is important to understand that organic life as we know it - with its nucleotides, proteins, DNA, etc. - is not essential in this conception: the principles and the logic of selection would apply equally to self-reproducing robots. The matter of self-replicators is immaterial. The process of natural selection is an inevitable concomitant of reproduction and inheritance whatever chemical composition the reproducers are manufactured of. In any pool of self-replicators, some will replicate faster or more efficiently than others - and maybe even at the expense of others - and their replicas will eventually prevail (e.g., Dawkins, 1976 et seq.; Slurink, 1994; Tooby & Cosmides, 1992).
The population of replicators will tend to grow exponentially and soon there will be competition (Dawkins, 1996). Competition is often attributed to scarcity, but to understand fully the ubiquity of competition in a Darwinian world, it must be understood that competition occurs even in the absence of scarcity. Since natural selection is a matter of differential reproduction, competition appears even in the midst of abundance: there will simply be competition to acquire unequal proportions (G. Johnson, 1995).
Natural selection also explains the appearance of goal-directedness or teleonomy (not to be confused with teleology) in nature: the 'designoid' (as Dawkins calls it) quality of complex adaptations. The design of organisms will more and more reflect their 'purpose' to replicate themselves; their structure will increasingly behave as a program for optimal self-replication (Pittendrigh, 1958; Mayr, 1974; Slurink, 1989, 1994). In other words, "Natural selection guides the incorporation of design modifications over generations according to their consequences on their own reproduction. Over the long run, down chains of descent, this cycle of chance modification and reproductive feedback leads to the systematic accretion within architectures of design features that promote or formerly promoted their own propagation" (Tooby & Cosmides, 1992). So,we can be reasonably certain that selection will act on any feature or trait to the extent that it has a significant effect on reproduction.
What is abundantly clear is that all life - from bacterium to elephant - shares common characteristics at the level of molecules. There is a common thread that runs through the whole of biological existence. Individual genes on the ribosomal RNA are common to all life, and these are complex structures. We all share a common ancestor (Fortey, 1998).
All living things or life forms share four fundamental and inter-related characteristics: they are all cellular in structure; the protein in all cells is made up from basically the same 20 amino acid units; all cells use basically the same nucleotides in their genes; and all cells use ATP (adenosine triphosphate) as the molecule that energizes their life systems. These four characteristics are in effect a definition of life. Each is a very complex phenomenon and that they should be common to every living thing from microbe to man cannot be an accident. Such universality can only result from a common origin. It must mean that all living things have evolved from a single ancestral form. And that ancestral form was probably very similar to the smallest and simplest organisms alive on Earth today (See footnote 1) 1 .
The smallest and simplest living things are single-celled organisms with a simple DNA molecule (their genetic material) floating free within the cell. Since these cells do not keep their DNA in a separate enclosed nucleus, they are called prokaryotes, from the Greek pro, meaning 'before', and karyon, meaning 'kernel' or 'nucleus'. Prokaryotes are the most widely dispersed living things, inhabiting environments of all sorts - from the depths of the oceans to the vents of volcanoes; from the Polar ice-caps to the near boiling water of natural hot springs (Reader, 1986).
The crucial invention which defined the cell in the most literal sense was a container that confined its component parts (termed organelles) within, a thin barrier between the living and the inert worlds: this is the cell membrane. The first cells were bacteria (Foley, 1998).
Among the prokaryotes, the very simplest are a group called the methanogens, bacteria which are found in marshes, lake beds and the digestive tracts of animals. The methanogens are members of a small and exclusive group or organisms that are able to live off inorganic chemicals without the aid of any other source of energy. In the process they give off methane, marsh gas. The life process employed by the methanogens is called fermentation, well known as the means of leavening bread and making alcohol - prokaryotic bacteria are the active fermenting agents in both cases.
Two other kinds of bacteria that have the capacity to live off inorganic chemicals under extreme conditions (extremophiles) are the halobacteria that live in very salty environments, and the thermoacidophiles, which thrive in hot acidic environments (Reader, 1986). Other extremophile bacteria (archaebacteria or Archaea) are known by the most wondrous jargon such as 'chemolithoautotrophic hyperthermophiles' (Fortey, 1998).
These three kinds of bacteria would have been well equipped for life in the harsh environments that prevailed on the early Earth, when there was no oxygen in the atmosphere but plenty of heat and inorganic chemicals about. The inorganic chemical-consuming bacteria had the early Earth all to themselves for some considerable time - hundreds of millions of years (Reader, 1986).
... or Protozoa?
The very first modern organisms were, according to Ridley (1999: 20), not like bacteria; they did not live in hot springs or deep-sea volcanic vents. They were much more likely protozoa: with genomes fragmented into several linear chromosomes rather than one circular one, and 'polyploid' - that is, with several spare copies of every gene to help with the correction of spelling errors (during replication). Moreover, they would have liked cool climates. As Patrick Forterre has long argued, it now looks as if bacteria came later, highly specialized and simplified descendants of the Lucas (Last Universal Common Ancestors), long after the invention of the DNA-protein world. Their trick was to drop much of the equipment of the RNA world specifically to enable them to live in hot places. It is we that have retained the primitive molecular features of the Lucas in our cells; bacteria are much more 'highly evolved' than we are (Ridley, 1999: 20-21).
Eventually, somewhere among the teeming microscopic hordes, mutation produced an organism that was able to harness the radiant energy of the sun to its life processes. This was an innovation of immense significance that has marked the course of life ever since.
The essence of photosynthesis is the ability to convert the energy of light to another form, and this ability is related to the phenomenon of color. In the course of those countless mutations, some prokaryotes evolved with the capacity to produce and use porphyrins in their life processes. Porphyrins are light-absorbing compounds; their advent and incorporation in living matter was probably fortuitous, so too perhaps was the fact that they were colored. Until then life had been colorless, but now among the millions of organisms there were, for the first time, microscopic grains of color that today are called chlorophyll - the wonder ingredient that takes light from the sun and converts it into a tiny bank of energy into the core of the cell. Photosynthesis requires a source of hydrogen. The first photosynthesizers would have taken this very basic ingredient from the compound molecules they absorbed from the water around them, just as their antecedents had done. But time and evolution brought further refinement. Eventually, about three billion years ago, an organism arose that was able to absorb hydrogen direct by splitting the water molecule into its component parts: two parts hydrogen and one part oxygen. The hydrogen was used in photosynthesis; the gaseous oxygen was released as waste (Reader, 1986; Fortey, 1998).
It is thought likely that these first photosynthesizers lived mostly in dense, mat-like communities on the floor of shallow seas. Diversifying, limited only by the balance between water shallow enough to allow them sufficient light but deep enough to protect them from the destructive effects of the sun's ultraviolet radiation, the photosynthesizing prokaryotes spread around the Earth. By around 2.2 billion years ago they were the dominant life form, and the oxygen they released as waste began to have telling effects.
From among the diverse variety of single-celled organisms then existing, the methanogens and their kind retreated to the oxygen-free muds and other places similar to the habitats in which their descendants still flourish; any organisms that found no safe haven became extinct. Among the photosynthesizers natural selection favored forms that could tolerate increasing concentrations of oxygen. Meanwhile, the increasing amount of oxygen released by the photosynthesizers was also bringing about considerable changes to the environment. In the first instance it turned the oceans rusty. Eventually, the oxygen produced by the microscopic photosynthesizers swept the oceans clear of iron. Now for the first time free oxygen escaped from the oceans and began to accumulate in the atmosphere. This development brought further irreversible change to the environment of life on Earth (Reader, 1986).
Before the appearance of atmospheric oxygen, all forms of life must have been adapted to an oxygen-free (anaerobic) environment. Cyanobacteria (cyanophytes or blue-green algae) wreaked havoc with the planet. As oxygen concentrations rose two billion years ago, many early organisms probably fell victim to the 'oxygen holocaust'. Survivors only included cells that found refuge in some oxygen-free location, or had developed other protection against oxygen toxicity. One of the greatest turnabouts in evolution was the transformation of a once-fatal form of air pollution, highly destructive to all cells - oxygen - into a coveted resource (Margulis & Sagan, 1995; de Duve, 1996).
Oxygen was becoming a fact of life. Many more oxygen-tolerant forms has arisen, and some had even gone so far as to add a few molecules of oxygen to the fermentation process that alone had powered life until then. The result was very beneficial to the organisms concerned, releasing 18 times more energy than fermentation alone could release from the same amount of material. In effect the innovators held on to the waste product of fermentation and combined it with oxygen for another round of energy-producing reactions. This is called cellular respiration; basically it is why we breathe.
The respirators used the available resources more efficiently than any of their predecessors. They proliferated. At the same time there came the single-cell cyanobacteria (also known as the blue-green algae), still very small but more inclined to a communal life than anything that had come before. The cyanobacteria joined themselves together end-to-end to form strands of green living matter (Reader, 1986).
The first obvious biological structure was a humble, slightly tacky or slimy skin, comprising a community of microbes, something that covered the sediments in a tenuous bandage. These mats were our ultimate cradle. They are called stromatolites, and they have been present on Earth for well over 3,000 million years. It was within some sticky mat on some long-obliterated shore that the first more complex cells were born through symbiosis. The world is full of symbiosis - some of it obviously ancient. Lichens, for example, are a collaboration between fungi and algae (Fortey, 1998; Reader, 1986).
Photosynthesizers, respirators and cyanobacteria were now the dominant life-forms, churning out more and more oxygen, but still confined to those bands of water shallow enough to transmit sufficient sunlight for their life processes, and deep enough to filter out the sun's lethal ultraviolet radiation. Life was finally released from the tyranny of the ultraviolet rays by the indirect effects of life itself. Ozone (O3) has the capacity of absorbing ultraviolet radiation (Reader, 1986).
After the prokaryotes had been in existence for possibly two billion years, a major transition took place, hardly of less significance than the origin of life itself - a new type of cell appeared: the eukaryote (eu meaning 'true').
The four fundamentals of life - cellular structure, amino acids for proteins, DNA for genes, and ATP for energy transmission - link the eukaryotes and the prokaryotes as a flower to its stem (Reader, 1986).
All complex multicellular life forms, including humans, are composed of eukaryotic cells - cells with a membrane-bound nucleus. For the first two billion of life's 3.5 to 3.7 billion (3,700 million) years on earth, only prokaryotes (including archaebacteria and cyanobacteria or blue-green algae) existed. Prokaryotes turned out to be enormously successful (de Duve, 1996)
The first eukaryotes were single-celled organisms that appeared about 1.8 billion years ago, the simplest multicellular eukaryotes may have appeared some 1.4 billion years ago, and the first more complex, macroscopic animals about 700 to 800 million years ago (mya). All contemporary animals (as well as plants, fungi, and protists [or protoctists or protozoa]) are descendants of these original single-celled organisms. All animals, including humans, are, in fact, highly integrated supercolonies or supersocieties of symbiotic cells whose ancestors were once free-living organisms (G. Johnson, 1995; Margulis & Sagan, 1991, 1995).
Eukaryotic cells may have originated as an obligate federation, a symbiotic union between ancient prokaryote hosts and what have now become cytoplasmic organelles, especially the mitochondria (Corning, 1995; Margulis & Sagan, 1991, 1995; de Duve, 1996).
The 'symbiosis' hypothesis suggests that the eukaryote organelles were once independent cells that evolved the behavioral capacity to enter and live inside another prokaryote, and subsequently became part of a give-and-take relationship that bestowed benefits on both parties (Reader, 1986).
One suggested scenario, as told by G. Johnson (1995), is that the original host cell was invaded by a smaller predatory bacterium (the mitochondrial ancestor) that normally killed its prey. In some cases, however, the host apparently survived, rendering its predatory invader a nonlethal infection. The originally uneasy partners then coevolved, with the mitochondrion gaining food from what had been waste products of the host and the host gaining energy from the mitochondrion's oxidative metabolism.
Maynard Smith & Szathmáry (1995) and de Duve (1996) favor an enslavement scenario, in which a phagocytic host progressively enslaved its captured endosymbiont prisoners. The host cells may have kept proto-mitochondria as humans keep pigs: for controlled exploitation.
The descendants of this alliance probably later acquired other endosymbionts, perhaps initially by ingesting but not killing them. Whatever the particular events, the combinations were apparently mutually beneficial, and they eventually evolved into highly integrated new organisms (Margulis & Sagan, 1991, 1995).
Prokaryote reproduction is conducted by the relatively simple procedure of binary fission. In eukaryotes reproduction is essentially a process of division too, but it is rendered much more complex by the number of different elements and larger quantities involved. Each organelle has to be duplicated and apportioned, and as the nucleus divides each part must receive the right number of chromosomes. Sometimes the component parts of the genetic material may be slightly reshuffled, so that duplication is not necessarily exact. The complexity of their reproductive process broadens the potential effects of mutation in eukaryote cells.
Margulis believes it may have taken one billion year to perfect the eukaryote cell. And the perfect eukaryote cell is the foundation upon which the living world is built (Reader, 1986).
For about 100 years, the scientific community has repeatedly changed its collective mind over what viruses are. First seen as poisons, then as life-forms, then biological chemicals, viruses today are thought of as being in a gray area between lving and nonliving: they cannot replicate on their own but can do so in truly living cells and can also affect the behavior of their hosts profoundly. The categorization of viruses as nonliving during much of the modern era of biolgical science has had an unintended consequence: it has led most researchers to ignore viruses in the study of evolution. Finally, however, scientist are beginning to appreciate viruses as fundamental players in the history of life (Villarreal, 2004: 77).
A virus consists of nucleic acids (DNA or RNA) enclosed in a protein coat that may also shelter viral proteins involved in infection. By that description, a virus seems more like a chemistry set than an organism. But when a virus enters a cell (called a host after infection), it is far from inactive. It sheds it coat, bares its genes and induces the cell's own replication machinery to reproduce the intruder's DNA or RNA and manufacture more vital protein based on the instructions in the viral nucleic acid. The newly created viral bits assemble and, voilà, more virus arises, which also may infect other cells. Viruses may, somewhat poetically, be said to lead "a kind of borrowed life".
Viruses have their own, ancient evolutionary history, dating to the very origin of cellular life. For example, some viral-repair enzymes - which excise and resynthesize damaged DNA, mend oxygen radical damage, and so on - are unique to certain viruses and have existed almost unchanged probably for millions of years. Viruses directly exchange genetic information with living organisms - that is, within the web of life itself. Most known viruses are persistent and innocuous, not pathogenic. They take up residence in cells, where they remain dormant for long periods or take advantage of the cells' replication apparatus to reproduce at a slow and steady rate. These viruses have developed many clever ways to avoid detection by the host immune system - essentially every step in the immune process can be altered or controlled by various genes found in one virus or another. Furthermore, a virus genome (the entire complement of DNA or RNA) can permanently colonize its host, adding viral genes to host lineages and ultimately becoming a critical part of the host species' genome. The huge population of viruses, combined with their rapid rates of replication and mutation, makes them the world's leading source of genetic innovation: they constantly "invent" new genes. And unique genes of viral origin may travel, finding their way into other organisms and contributing to evolutionary change (Villarreal, 2004: 81).
Villarreal and others contend that the cell nucleus itself is of viral origin. The advent of the nucleus - which differentiates the eukaryotes, including humans, from prokaryotes, such as bacteria - cannot be satisfactorily explained solely by the gradual adaptation of prokaryotic cells until they became eukaryotic. Rather the nucleus may have evolved from a persisting large DNA virus that made a permanent home within prokaryotes.
From single-celled organisms to human populations, viruses affect all life on earth, often determining what will survive. But viruses themselves also evolve. New viruses, such as the AIDS-causing HIV-1, may be the only biological entities that researchers can actually witness come into being, providing a real-time example of evolution in action (Villarreal, 2004: 81).
At the same time the concentration of oxygen in the atmosphere was slowly but steadily increasing. The scene was ripe with potential: after some 2.5 billion years life was at last poised to move beyond the microscopic stage of its existence. The key to this step was the advent of the multicellular organism, when some cells developed the characteristic of living together as a colony of cells that itself was a distinct organism, bestowing advantages of nutrition, security and mobility on each of its component parts.
The oldest known multicellular fossil comes from deposits that are about 750 million years old, but their evolution probably began before then. With time and mutation and the pressure of natural selection, some component cells evolved special functions or features that were specific to themselves but beneficial to the whole. New organisms arose, creating and exploiting new opportunities in environments that were becoming increasingly interactive with life itself (Reader, 1986).
Multicellular organisms - plants, animals, and fungi - are genetically preprogrammed to accomplish the process of cell death. Morphogenetic processes associated with individual development, and the autumn leaf fall are only a few of the numerous examples of programmed cell death (PCD). PCD helps an organism 'keep up order' and secures the normal functioning of a biological system by eliminating cells which (1) are useless or damaged; (2) have completed their life cycle; or (3) represent potentially dangerous results of mutations (Samuilov, Oleskin & Lagunova (2000).
Two different kinds of cell death have been disinguished: apoptosis and necrosis. Necrosis can be easily distinguished from apoptosis, since only the former results in an inflammation process. Inflammatory responses are characteristic of destructive processes. On the other hand, PCD in animals represents a cell's death for the sake of life on the organismic level. PCD serves as a mechanism maintaining homeostasis in a normal organism. Hence PCD, like cell division and differentiation, contributes to the normal development and functioning of an organism.
Apoptosis is a multi-stage process. In the first stage, a cell receives a signal (a herald of death) that is generated outisde or inside the cell. The signal impinges on a receptor; the message is analyzed. This signal is consecutively transferred via receptors to a sequence of intermediary molecules (messengers) and ultimately to the nucleus, where the cell suicide program is activated. The program implicates the activation of lethal and/or the repression of anti-lethal genes. Some cells (e.g., in the embryonic nervous system) activate the apoptosis mechanisms if they do not receive sufficient amounts of apoptosis-suppressing signals (also termed survival factors) from other cells. The physiological reason behind this process is that excessive nervous cells are eliminated, which otherwise would compete for the limited pool of vital resources. Epithelial cells are doomed to PCD once separated from the extracellular matrix producing survival factors (Samuilov, Oleskin & Lagunova (2000).
The invention of sex - the crucial development in the history of life as Maynard Smith called it - was evidently an ancient, Precambrian innovation because so many plants and animals - even fungi - show evidence of sexual reproduction. The sexual imperative runs into deep time (Fortey, 1998).
It is thought likely that the eukaryotes began to reproduce sexually around one billion years ago. This was an especially significant innovation for, by sharing (and recombining) the genetic material of two parents among the offspring, both the chance of mutation and the potential degree of mutation between generations was increased. In effect, sexual reproduction enhanced the mechanism by which evolution operates and thereby accelerated the process. Increased diversity and proliferation of life-forms was inevitable.
Meanwhile, lifestyles were changing too. For a long time all the single-cell inhabitants of the Earth's seas fed off the same, basically chemical, resources of the planet. Eventually, however, some began to eat others and predation began. Here was a particularly dynamic force that could well have accelerated the evolutionary process still further (Reader, 1986).
The eukaryotes generally exchange genetic material: sex appears on the stage. Sex does not exist for organisms. Sex was created by and for genes. Sex probably began in bacteria-like creatures that were genetically mutilated by solar radiation. When these bacteria found ways to replace their damaged DNA with imported DNA, with DNA from outside their bodies, that was the first sex. The two principal features of sex, recombination and outcrossing, both originated for the purpose of repairing gene damage (Margulis & Sagan, 1991, 1995; Michod, 1995). Michod emphasizes that sex did not originate for the purpose of reproduction. The association of sex with reproduction came much later in the history of life, when anisogamy (different-sized gametes) was invented, and with it the different reproductive strategies pursued by males and females, and the concomitant 'battle of the sexes'.
Strange to contemplate, death evolved also, and in the wake of sex. 'Programmed' death as the final stop of a lifelong metabolism was absent at the origin of life, and for a very long time afterward. Like genes, bacteria are 'immortal'. Fatefully for the future history of life forms such as ourselves, in protists sexuality, in the form of meiosis, became inextricably linked to death: "The cells in our animal bodies are in a diploid, or double chromosome, state except for the protist-like ova and sperm, which are in a haploid, single chromosome, state. Each animal body is a sort of diploid husk, morbidly discarded by those haploid sex cells that manage to produce each generation a fresh new body and thus continue beyond the death of the 'individual'. The diploid body pays the ultimate price - death - for transmission of haploid sex cells" (Margulis & Sagan, 1995).
Needless to say, bodies, too, are created by and for genes. Within bodies, not all is peace and harmony. The cells of animals form competitive reproductive lineages. There is competition and conflict within the multicellular organism. The nervous and endocrine systems may have evolved, G. Johnson (1995) suggests, for the same reason as governments among social organisms - to inhibit conflict and induce cooperation.
Cell membranes, eukaryotic and multicellular organisms - increasingly complex 'survival machines' for the replicators - may have evolved as a direct consequence of competition between similar replicators. Competition is a universal aspect of life because organisms are basically 'selfish' (i.e., they are 'programmed' to propagate their own genes), and they have incompatible and conflicting goals, needs and demands in a world of limited resources; they are indeed, as Spencer and Darwin acknowledged, engaged in a continual struggle for existence. The more (phylogenetically) related and (specifically) similar organisms are, the more they tend to compete for the same resources - which is one of the reasons why intraspecific aggression (a behavioral strategy in the service of contest competition [Barash, 1982]) is ubiquitous at least in the 'higher' organisms (the phyla arthropoda and chordata [e.g. Scott, 1969]).
The process of natural selection is entirely opportunistic and utterly amoral. At the risk of being repetitious, let me once more emphasize that organisms have been selected over evolutionary time to do whatever it takes to advance their own genetic interests, "even when these interests look unpleasant or contrary to the well-being of the species as a whole" (Wrangham & Peterson, 1996).
In this view, organisms are temporary biodegradable vehicles with only one 'purpose': to transmit their genes to future generations. The organism is ephemeral and mortal. The genes are, in principle, immortal and have the 'selfish' interest (due to their biochemical properties) to spread as many copies of themselves as possible. Natural selection in fact selects for reproductive success.
Bacterial sex, in outline, is almost as simple as cell fission. When two compatible bacteria find themselves next to one another, they may form a thin living conduit between them. One of the bacteria, called the donor, then transfers some of its DNA through the conduit to the recipient. This process is called conjugation, and afterwards the recipient can be thought of as the offspring of the union. The donor may give all its DNA to the recipient, or it may pass only a short stretch. After conjugation the recipient may use its DNA repair and recombination enzymes to splice the received DNA and its own DNA into one long strand. The donor cell, if it gives away too much of its DNA, ceases to exist. Recombination, permitted by the existence of repair enzymes, thus allowed bacteria to create more variety, to bring together genes from different individuals into one body (Gribbin & Cherfas, 2001).
The Evolution of Anisogamy
Some of these organisms 'invented' sex as a reproductive strategy. The meaning and origin of sexual reproduction, is considered to be "the deepest mystery in all biology" (Trivers, 1985; see also Ghiselin, 1974; Maynard Smith, 1989).
Many organisms reproduce asexually, by means of budding, fission or parthenogenesis, and they have been doing so successfully for millions of years. Then what is so special about sexual reproduction (needing two different morphs who each contribute only one half of their genes to the offspring), the way all animals best known to us, the mammals, and we ourselves do it? (See footnote 2) 2 This question becomes especially enigmatic when we realize the costs involved in sexual reproduction. Sexual reproduction is wasteful, error-prone and inefficient: it uses energy, materials and time. With anisogamy and separate sexes there is the cost of males. A female that could produce female progeny asexually with the same efficiency as by fertilization would have a twofold advantage. In anisogamous species - all 'higher' plants and animals - the female provides cytoplasm to support the male genome. This results in the twofold cost of males, or cost of genome dilution (e.g., Crow, 1987; Stearns, 1988). Biologically speaking, a female is by definition that sex that specializes in the production of a few, large, nutritious, and relatively immobile gametes (ova), while the male is by definition that sex that specializes in the production of a huge quantity of small, non-nutritious, motile gametes (sperm). Sperm producers (males) survive by parasitizing the investment of ovum producers (females) (Parker, 1984). As Gribbin & Cherfas (2001) pithily expressed it: "Men are at best parasites on women, and at worst totally redundant in the immediate evolutionary scheme".
For many male organisms, the highest cost of all is the damage and even death incurred in the cut-throat competition for mates. It was these costs which first convinced G.C. Williams (1975) and Ghiselin (1974) that the prevalence of sexual reproduction poses a serious problem for evolutionary theory. The advantages of sex to the individual have to be very large if sex is to be maintained by natural selection in any population in which parthenogenesis can arise. What could the possible benefits be that transcend the substantial costs involved?
The usual textbook answer to this vexing question is: "For the preservation of the species, of course". And, like so many textbook answers, it is wrong.
Sexual reproduction serves the perpetuation of sexual reproduction genes. It may well be a purposeless hangover, a legacy, from an earlier era of evolution (Gribbin & Gribbin, 1993; Margulis & Sagan, 1991, 1995).
Once gametes are produced which must fuse to produce a new organism, there will be a strong selection pressure toward stable anisogamy, because it is difficult for gamete cells to be both rich in nutrients and highly mobile. This simple constraint underlies the basic differences between eggs and sperms: "Eggs are specialized in the nurture function and sperms are specialized in mobility and the mate finding function. Together two specialized gametes (anisogamy) are better able to produce a healthy zygote than are two identical gametes (isogamy)" (Michod, 1995).
It has been hypothesized that gender was invented as a means of resolving the conflict between the cytoplasmic genes of the parents: "Rather than let such conflicts destroy the offspring, a sensible agreement was reached. All the cytoplasmic genes would come from the mother, none from the father" (Ridley, 1993).
The main arguments for the evolutionary advantages and maintenance of sexual reproduction and recombination include adjusting to a changing environment by the production of genetically diverse offspring (gene reshuffling) and getting rid of deleterious mutations. Sexual reproduction and recombination are also thought to be advantages in a coevolutionary race against parasites and disease organisms. Disease organisms and parasites have a fundamental advantage in an evolutionary arms race. They can adapt themselves quickly to a specific host genotype. This brings the host population under strong frequency-dependent selection, for it pays to have a rare genotype during an epidemic. This is known as the 'Red Queen' hypothesis (so called after Lewis Carroll's Alice in Wonderland, in which the Red Queen has to run very fast in order to stay in the same place; see especially Ridley, 1993). (See footnote 3) 3
Every season, a female cod may release many millions of eggs in the ocean for external fertilization. At the other extreme, human, chimpanzee and elephant females gestate, lactate, and intensively care for a relatively small number of young during their life times. These extremes represent two basic evolutionary strategies concerning reproduction: low parental investment in quantity (called r-selected) versus high parental investment in quality of offspring. In the latter case, the species is described as K-selected.
K-selection is generally associated with a number of other characteristics such as greater birth interval, more parental investment in progeny, slower development and longer juvenile phase, slower sexual maturation and later menarche, etc. (e.g., E.O. Wilson, 1975; Daly & Wilson, 1978; Hrdy, 1981; Foley, 1987; Mealey, 2000; Low, 2000).
A slight increase in the chance of reproduction when young is worth more than a sexual triumph long delayed. This means that evolution favors youthful vigor at the expense of later decline. Why should it worry if the price of sex is to become a burned-out wreck? Any gene able to help its carriers to copy their DNA will spread, however evil its effects - if they are long enough deferred. Selection favors only those who can pass on the genes and cares not at all for those who cannot. Age is a tax on sex, levied by natural selection. It is as much a product of the struggle for existence as are the black wings of the peppered moth (Jones, 2000: 99).
J.B.S. Haldane, Peter Medawar and George Williams separately put together the most satisfying account of the ageing process. Each species, it seems, comes equipped with a program of planned obsolescence chosen to suit its expected life-span and the age at which it is likely to have finished breeding. Natural selection carefully weeds out all genes that might allow damage to the body before or during reproduction. It does so by killing or lowering the reproductive success of all individuals that express such genes in youth. All the rest reproduce. But natural selection cannot weed out genes that damage the body in post-reproductive old age, because there is no reproduction of the successful in old age (Ridley, 1999: 201).
Sexual selection depends on the success of certain individuals over others of the same sex, in relation to propagation of the species; whilst natural selection depends on the success of both sexes at all ages, in relation to the general conditions of life. The sexual struggle is of two kinds; in the one it is between individuals of the same sex, generally the males, in order to drive away or kill their rivals. whilst in the other, the struggle is likewise between individuals of the same sex, in order to excite or charm those of the opposite sex, generally the females, which no longer remain passive, but select the more agreeable partners (Darwin, 1871).
This is how Darwin introduced the concept of sexual selection. The first kind of the sexual struggle is now better known as male-male and female-female competition. The second kind of the sexual struggle envisaged by Darwin is now known as epigamic selection or, simply, the principle of female choice. Darwin explained the sexually dimorphic characteristics of many species, including humans, as the result of sexual selection. The gorgeous and exuberant plumage of male birds-of-paradise and the gaudy peacock's tail, for example, are the results of such a kind of runaway sexual selection, based on the attractiveness to the females of the most exuberant-looking males. When sexual selection operates among males, adult males tend to become larger, heavier, showier, more competitive and better armed, and their behavior patterns and ecological requirements tend to diverge from those of the females. This is one of the reasons why E.O. Wilson (1975) calls sex "an antisocial force in evolution"; it generates and exacerbates conflicts of interests.
A whole array of traits is associated with the greater sexual competitiveness of males in a wide range of species. These include not only greater size and gaudiness, but also the price males have to pay for this: greater vulnerability and frailty in development (due, among other factors, to the deleterious properties of testosterone for the immune system), and shorter lifespans due to senescence, high risk-taking and mortality from fighting.
G. Miller (2000) explains many exuberant and biologically 'superfluous' human behaviors and characteristeristics as products of sexual selection.
The ultimate basis of sexual selection is greater variance in mating success within one sex (first formulated by Bateman, 1948). In humans, for example, some powerful men may have many wives and children, while many poor, low-status men have neither kith nor kin. This differential in reproductive success underlies the formulation of Parental Investment Theory, developed mainly by Trivers (1972, 1985).
Parental Investment Theory
The concepts of 'differential parental investment', and 'male confidence of paternity' provide the basis for an understanding of the ubiquitous phenomena relating to the conflict-ridden and uneasy coexistence of the sexes, known as the perpetual 'battle' or even 'war' of the sexes.
Basically, the evolutionary rationale behind the 'battle of the sexes' is simple and straightforward: males and females invest differently in their reproductive success. For mammalian species female reproductive success is limited only by the amount of resources (time, energy, nutrients, etc.) she has to invest in offspring. But for the male, the female herself is the limiting resource: one male can inseminate many females and male reproductive success is only limited by the number of matings a male can achieve. Even in species where males typically invest in their offspring, such as humans, the temptation of enhancing reproductive success by means of securing extra-pair copulations, and inseminating other females without further investment, tends to select for a mixed male strategy of pair-bonding and philandering, and (at least in relatively monogamous species) a female counter-strategy of carefully assessing the male's potential and willingness to invest in her offspring. Thus there is a basic asymmetry in female and male parental investment strategies.
Trivers (1972) defined parental investment as "any investment by the parent in an individual offspring that increases the offspring's chance of surviving (and hence reproductive success) at the cost of the parent's ability to invest in other offspring".
This definition highlights the costs and trade-offs: parents who invest in one offspring sacrifice the opportunity to invest in other offspring. Since greater parental investment in one offspring implies lesser parental investment for other offspring, the sex that invests more heavily in its offspring (usually the female) becomes a limiting resource for the other sex. To the degree that they are freed from parental investment in their offspring, members of the sex with the lesser investment can increase their reproductive success by leaving offspring with more members of the opposite sex.
More generally, an animal's parental investment is part of its total reproductive effort, which also includes the effort expended in finding and winning mates [mating effort]. With a finite amount of time, energy, and resources, that can be devoted to reproduction, each animal should strive to distribute its reproductive effort so as to maximize inclusive fitness... The common denominator of all such investments is 'the expenditure of the animal's remaining reproductive potential'...
The concept of differential parental investment provides an explanation for the fact that males are almost universally the more competitive and aggressive sex. In general, females invest considerably in the nurture of each of a relatively small number of offspring, while male fitness depends on maximizing mating efforts and frequency. The resultant competition is not something that malescan afford to take lightly. The prize is substantial, and the greater the prize (e.g., a harem of females), the greater will be the risk that the hopeful male should venture in order to secure it: "For a big enough prize it will even be worth his while to risk death" (Daly & Wilson, 1978).
In most mammalian species, males provide little if any direct investment in offspring (Clutton-Brock, 1989). As a result, the reproductive effort of males tends to be largely focused on mating effort and the associated male-male competition and the reproductive effort of females tends to be largely focused on parental effort and the associated female choice (e.g., to get the best genes for their offspring). The dynamics of sexual selection are much more complicated for species - which includes humans - where males show some level of direct parental investment. When both the mother and the father invest in offspring and there are individual differences in the quality of care or genes that parents provide to these offspring, then female-female competition and male choice become important features of sexual selection, in addition to male-male competition and female choice (Parker & Simmons, 1996; Geary, 1998).
Male-male reproductive competition can take several forms (Borgia, 1979; Parker, 1987): gametic competition for copulations and inseminations (sperm competition); harem competition for control of females; resource competition for territories or commodities that attract females; and labor competition to provide services that females need for their eggs or their offspring. In other words, males compete through a variety of behaviors including territoriality, dominance, female guarding, nuptial feeding, and sperm production.
Although less attention has been paid to female-female competition, several forms have been identified: direct competition for resources necessary for producing and nurturing gametes, fetuses and offspring; competition for parental investment of high ranking males; competition for males of high genetic quality; nest and offspring destruction of other females, and even induced abortion (Hrdy, 1981; Kevles, 1986; Parker, 1987).
Male sexual competitiveness and promiscuity, aggression and rivalry, and other secondary sex differences are not inherent, intrinsic aspects of maleness, rather these are the resultants of sex differences in reproductive strategies. In those (few) cases in which males provide significant parental investment, there is intense female-female competition for males, and females are the larger and more aggressive sex (G.C. Williams, 1966, 1975; Ghiselin, 1974; Symons, 1979; E.O. Wilson, 1975; Hrdy, 1981; Trivers, 1985; van der Dennen, 1992; a.o.). These behavioral sex differences do, therefore, not depend on the possession of a particular pendulous sexual organ, as Freud and other psychoanalysts were inclined to believe.
To a male the costs of parental investment in another male's offspring are very substantial, therefore males are expected to provide parental investment pari passu with their certainty of paternity.
Buried some 550 million years ago in the Burgess Shale is a slim silvery creature, like a narrow leaf, about eight centimeters long. The front end has a small coronet of tentacles around an opening through which it sucks in water. There is nothing that could be called a head, only a small, light-sensitive spot that might evolve to be an eye; there are no fins or limbs. but there is something familiar about it. Like no other creature in those early seas, it undulates, sending a series of rhythmic waves down the length of its body; the waves push the water backwards and move the animal forwards. To do this it must have a series of muscles attached to a firm internal structure. This animal, called Pikaia, has a rudimentary backbone called a notochord. Across vast expanses of time and space, Pikaia, or else the more recently discovered Cathaymyrus diadexus (from China), stands at the very beginning of the vertebrate progression that ultimately produced mankind (Reader, 1986).
Once, the vertebrates - the group to which mammals, birds and fish belong - seemed to have had a timorous childhood. Today's versions of their predecessors - the lancelet and the hagfish - feed on soft tissues. The lancelet and the young hagfish filter particles from the water, while the hagfish adult is more interested in the flesh of dead or crippled fish. They are not, perhaps, a noble set of ancestors for the lords of creation.
Now, the image of our past has changed and the lost world from which we descend has at last been revealed. An abundant but enigmatic fossil was the key. Many chunks of limestone contain thousands of tiny pointed objects. Conodonts, as they are called, were discovered in Russia in the nineteenth century and have since turned up all over the world. Because they are so widespread, and because their shape changes over geological time, they are much used to identify from which layer a particular rock might come. The animal who made them was quite unknown.
In 1982, in some rocks from the shore near Edinburgh, were found the preserved remains of the animal itself. It had a soft eel-like body a few inches long, with large paired eyes, a stiff rod down the back, and tail fins. The conodonts themselves were not separate beings, but its teeth.
Before these dozen or so specimens - the first examples of the animals that made the tens of millions of conodonts seen by geologists over a century and more - the vertebrate skeleton was thought to have started as a set of defensive plates on the body of a primitive fish. The first vertebrates were, it seemed, victims, prey rather than predators. The complete conodonts changed all that. The first sign of the skeleton was, it seems, in the mouth. Sets of conodont teeth, when pieced together, look as if they were used to shear flesh. The conodonts flourished and diverged before they were driven out. More - and larger - conodont animals have now been found, from Wisconsin to South Africa. One, the size of a small fish, even preserves a pair of eyes (themselves at first classified as the remains of a plant). The conodonts prove that our predecessors were not grazers, sifters or suckers, but carnivores (Jones, 2000: 284-85).
The strong flexible backbone makes the ostracoderm (meaning 'bony shield'), the first known true vertebrates, but they were very primitive fish indeed; they could not yet swim in true, fish-like fashion, but nuzzled along the bottom. They did not have jaws.
One hundred million years stretch between the rudimentary backbone of Pikaia in the Burgess Shale and the firm backbone of the ostracoderms in the Devonian, and absolutely nothing is known what happened in between.
The ostracoderms flourished. For 60 million years, from 410 to 350 million years ago, these primitive fish exploited their aquatic niche. They multiplied, and diversified into a variety of different species; then, almost as suddenly as they had entered the story of life, they disappeared from it, leaving only their fossil remains in the rocks as evidence of their existence, and today's parasitic lamprey and the scavenging hagfish as their sole descendants and inheritors of their once revolutionary lifestyle.
The most probable reason for the sudden disappearance of the jawless primitive fish was the development from among their kind of a creature with jaws that acquired the habit of eating them. Just as the jawless fishes had multiplied and diversified dramatically, so the advent of the jaw set off an explosion in the number and variety of jawed fishes - largely at the expense of their jawless antecedents, who became a prime source of food (Reader, 1986).
The placoderms (or 'plate-skinned' fish), the world's earliest true fish, represent the arrival of the vertebrate killer in the story of life on Earth. There were many different species and they came in all sizes: some were gigantic - up to nearly ten meters long. Like their jawless antecedents, most were armored in some way, with heavy scales attached to bony plates in the skin, and they all had well-developed lateral fins, usually in two pairs: pectoral fins just behind the head and pelvic fins at the rear, as in modern fish. Although some species hugged the sea floor, the placoderms were accomplished swimmers. Guided by sight, propelled by muscles pulling on a strong internal skeleton, steered by paired fins, armed with jaws and a formidable array of teeth, the entire ocean was their niche, and any creature their prey (Reader, 1986).
For 3 billion years the story of life on earth was the story of (animal) life in the oceans. Fossils reveal that animals evolved earlier than plants or fungi. Animals - exclusively marine animals - began leaving a rich fossil record in the early Paleozoic. But there is no trace of plants or fungi until more than three hundred million years after shelly animals appeared (Margulis & Sagan, 1995).
The Evolution of the Plants
While the placoderms were ruling the oceans, the water's edge still marked the limit for life on earth. So far nothing had ventured into the terrestrial environments. The move was inevitable, however, and the plants were the first to break the barrier, beginning with algal patches at the water's edge (Reader, 1986).
Some of the plants in the tidal waters of the shallow seas of the Silurian period gradually adapted to drier conditions, with their descendants eventually spreading onto the land (about 400 mya) (Hunt, 1997).
The reed-like plants evolved and spread further from the water. Bushes and trees evolved from the reeds and by the end of the Devonian period, 345 mya, forests covered a great deal of the land surface - very strange looking forests, with trees standing high on exposed branching roots, their stems as scaly as a reptile's skin. Insects evolved from among the aquatic invertebrates and followed the vegetation ashore, but for a long time the vertebrates remained on the other side of the water's edge (Reader, 1986).
The land offered many advantages. Both the light and the carbon dioxide needed for photosynthesis were more readily available, and the land was unoccupied by competing forms of life. But even under relatively favorable circumstances the move from an aquatic to a terrestrial environment called for some fairly major evolutionary adaptations. The technical problems that need to be overcome to make a viable, upright plant are problems of plumbing and engineering, chemistry and aerodynamics (Fortey, 1998). There was the matter of support, for instance; in the water even the most flaccid plants were held aloft by internal air, but on land they would simply collapse. The embracing water also brought nutrients directly to the plant, and carried away the reproductive spores; there was no service like that on the land, only the sun and air which would eventually suck all the moisture from any aquatic plant.
Initially, therefore, the first land plants would have occupied an in-between zone, perhaps on land regularly exposed by the departing tide. Here they gradually evolved the adaptations needed to survive in the air, while regular inundation allowed them access to the services of the sea. A waxy covering, a cuticle to prevent drying-out, might have been the first adaptation, possibly in a small, flat, photosynthesizing seaweed fixed to the shore at the edge of the tidal zone. The cells that held it in place developed into roots capable of seeking out nutrients (Reader, 1986).
With the development of the cuticle to ward off dessication, small openings were needed to permit and regulate the exchange of gases between the plant and the air around it - thus the stomata evolved. Now that water and minerals could only be absorbed throught the proto-roots, instead of through the plant's entire surface, some kind of conduit was needed to carry these, and the products of photosynthesis, to the growing parts of the plant. As this conduit system evolved - in the form of the xylem to carry water and minerals (from the roots to the shoots), and the phloem for photosynthesized sugars (from the leaves to the rest of the plant) - the plant's structure took on a form that was more efficiently adapted to its function: the stem evolved, holding aloft branches with the reproductive organs at their ends (Reader, 1986). The tough, organic building material lignin subsequently further reinforced the structure (Fortey, 1998).
These were the first vascular plants. The earliest known is called Cooksonia, it stood about six centrimeters tall and was well established along the shores of equatorial Britain about 410 mya.
Not too long after Cooksonia, certainly by the beginning of the Devonian period 395 mya, the vascular plants had evolved into a dozen or so species. Some of these were destined for extinction, but others were the beginning of the two major evolutionary lines from which has come all the world's vegetation. One was Zosterophyllum, a creeping rhizome-rooted plant with thin branched stems, about 20 centimeters tall, from which the clubmosses have evolved; the other was Rhynia, slender as a reed, about 17 centimeters tall, from which have come the ferns, the horsetails and the seed plants.
The primitive plants grew in dense clusters around the water margins of the early continents. Deltas, coastal flats, river and stream banks were all soon colonized. Competition for light and space favored greater height and a larger photosynthesizing surface. Simple, spiny leaves appeared on Asteroxylon, a relative of Zosterophyllum, while the descendants of Rhynia became taller and more branched (Reader, 1986).
As the roots of the living plants pried into and broke apart their growing medium in search of nutrients, bacteria moved in and hastened the decay of dead matter and the first true fertile soils began to form. The plants were now firmly established on land; they were poised to colonize every available square meter, but their expansion was restricted by one very important factor - the need of water to assist their reproductive process. The terrestrial plants were still not entirely free of their aquatic ancestry (Reader, 1986).
Gymnosperms and angiosperms
In time, however, a family of plants evolved with an innovative device that freed them to colonize drier parts of the terrestrial environment. The device was the seed, and the plants were the gymnosperms, which means simply 'naked seed'. This group includes the modern conifers, cycads and maidenhair trees. The first seeds arose about 350 mya (Reader, 1986).
As the trees climbed so did the insects (an enormously successful and diverse group of animals, probably comprising millions of species). And as the insects became ever more adept at exploiting the vegetative food source - extracting sap, devouring leaves, spores, pollen and seeds - the vegetation evolved defensive responses, such as poisons and hard crusty shields. Some plants went a stage further and made a virtue of a vice: they used the pollen-eaters as pollinators.
Relying on the wind to carry pollen to the ovule was a very wasteful procedure, calling for clouds of pollen when only one grain was needed for the job. If an insect could be enticed to take the pollen direct it was welcome to all the pollen it could eat. Thus the flowering plants evolved - the angiosperms, meaning 'seed borne in a vessel'. Attracted by the color, nectar and scent of a profusion of flowers, the exploiting insects were in turn exploited. By the end of the Cretaceous 65 mya most modern groups were present. Today the flowering plants constitute over 80% of all green plants (Reader, 1986).
Plants moving into regions where seasonal temperatures varied between hot and cold needed an adaptation that would see them through the coldest times of year. They found it in the practice of shedding leaves at the beginning of the cold season and suspending growth until temperatures rose again, when the protected buds would burst forth with fresh leaves and flowers. This was the advent of the deciduous plants.
The earliest flowering plants were predominantly of a woody structure; they were trees and small shrubs, capable of reproducing themselves year after year. But although they were long-lived, the spread of the ancestral woody plants was limited by the length of time they needed to reach maturity. Clearly there was a niche in the early forests for plants with more opportunistic lifestyles. This niche was filled soon enough with the evolution of the herbaceous plants which today provide the bulk of mankind's food and without which it is doubtful if the mammalian line could ever have achieved much significance (Reader, 1986).
The herbaceous flowering plants maintain no lasting parts above ground. They all sprout, flower, set seed, wither and die in a matter of months. A short reproductive cycle, that is the strategy that sees them through the vagaries of climate and which has taken them into every available niche on Earth. Some are annuals which mature and die in a season, ensuring species survival through the extremes of climate and season with a crop of seed. Others are perennials, which also produce seed annually but remain alive themselves as well, storing nutrients in enlarged roots underground after the parts above ground have died. The roots will sprout again en reproduce whenever conditions become favorable. Tubers, bulbs and seeds; leaves, flowers and fruit - the bounty of the angiosperms.
And it really was a bounty, a veritable basket of evolutionary adaptations expressly intended to attract (rather than repel) and feed animals. And with the disappearance of the dinosaurs, the symbiotic, simultaneous rise of the mammals and the flowering plants, especially the herbaceous flowering plants, laid the ground plan for the way the Earth looks today (Reader, 1986).
The appearance of grasses in the Tertiary was of crucial importance to the modern mammal fauna, for many of the animals that figure prominently in human history feed, predominantly, upon grass. It has remarkable property: its leaves grow from concealed bases - not from the tips of shoots, as is the case with most plants. So grass can be cropped - its leaves endlessly nibbled - without compromising its generative heart. Grass makes meadows, which virtually nothing else does. 'All flesh is grass', so the Book of Isaiah tells us, and indeed much of it is (Fortey, 1998).
The Primitive Brain
From the time of these humble beginnings, multicellular organisms had two viable options, two different strategies of life regarding their energy supplies. Plants we call those organisms which are autotrophic (bind solar energy by means of photosynthesis for their growth and reproduction), and are relatively immobile. Animals we call those organisms which are heterotrophic, i.e., which parasitize on plants (herbivores) or on each other (carnivores) for their 'fuel'. The parasitic lifestyle is incompatible with the immobility of the plants. Slurink (1994) explains this with great clarity:
"To collect enough fuel to grow and reproduce, it may be necessary to move and look around. But moving and looking around pose new energy problems, for which the most natural solution may be to steal the energy which another parasite has collected. But other parasites may have found that solution as well. So, there is an extra reason to be mobile: to prevent other parasites from using your valuable life as fuel. Animal mobility, therefore, can be interpreted as an optimal strategy that allows individual survival machines to collect fuel without being collected as fuel themselves".
Mind, also, is fully an evolutionary phenomenon. "Hundreds of millions of years before organic beings verbalized life, they recognized it. Discerning what could kill them, what they could eat, and what they could mate, roughly in that order, were crucial to animal survival" (Margulis & Sagan, 1995). Kill, avoid being killed, and copulate: this has been the key to reproductive success down evolutionary time.
Besides these problems of survival, there is one other problem: a mobile organism needs information about the outside world, about its position and orientation in relation to its immediate surroundings. Sensors and receptors sensitive to certain patterns of variability of physical properties of the environment (e.g., light contrasts, sound waves, etc.) thus evolved as part of the emergency or alarm systems of the mobile survival machines. The more sensors and receptors an organism has at its disposal, the greater the need to coordinate and synchronize, make sense of, and adequately react to, the various information flows. Therefore central nervous systems and brains evolved as coordinating sensory information and motor control centers.
The evolution of knots or ganglia of nerves, and brains, was possible only after the evolution of cephalization and bilateral symmetry. For things that travel it is obviously advantageous to have a forward end and the mechanical advantage of a symmetric body. With a head end evolved it would normally be advantageous to have the mouth within it, and especially so to have set within the head the eyes or other sense organs that help direct motion. Such a gathering of sensitive and motor organs needs a corresponding concentration of nerve tissue: primitive brains (Kroeber, 1948).
Organisms have, from the very beginning, fed and preyed upon one another and engaged in life-and-death competition. Competition and predatory behavior probably represent the major motivated states for several hundred million years. "This implies that primitive brains, from gnathostomes to reptiles, must have been adjusted to continuous hunting and predation, and aggression. About 60 million years after Agnatha (460 mya), the Acanthodian fishes appeared, armed with formidable jaws, efficient teeth, and large eyes, all of which contributed to active hunting of prey. The morphological and neurological templates for predation and aggression were clearly drawn in fishes, and some of them, like the Chondrichthyes (such as the shark) have been among the world's most active and insatiable predators. Many eons of evolutionary time would pass before neural circuits for protection of young, dominance, territoriality, and the like were wired into the brains of more phylogenetically advanced organisms: the reptiles" (Bailey, 1987).
It is important to understand that brains did not evolve to think, or solve academic puzzles, but to act, or at least to make optimal decisions for the animal to act upon in the light of its survival interests. The picture of the outside world the senses and the brain reconstruct from the signals they receive has only to be 'adequate for survival', not to provide deep insights into the objective world an sich.
"So, everything the animal encounters must be valued from the viewpoint of its survival interests. This may also explain the evolution of emotions and of consciousness. Pugh (1978) claims that emotions can be compared to the values that govern decisions in the so-called 'value-driven decision system'. Pugh proposes that a key problem for an imaginary 'evolutionary designer' is that one cannot predict the situations that an animal will encounter. The program of a survival machine with only a fixed set of responses will result in a high number of wrong decisions. Thus, the evolution of a more flexible decision system in which alternatives can be weighed in relation to their contribution to evolutionary goals and subgoals becomes understandable" (Slurink, 1994).
The human being likes to think of itself as the tabula rasa organism par excellence. There are sound theoretical reasons, however, why such a blank slate organism (i.e., an organism without some kind of built-in value-driven decision system) could not possibly evolve. Consider the evolutionary fate of an organism that would not immediately and appropriately react to any contingencies in its environment - the appearance of a predator, say - but instead would sine ira et studio contemplate the potential impact of this event. In order to contribute to survival, the emotions - the values of the value-driven decision system - must have a compulsory character: they must be able to force the organism to behave in an appropriate and adaptive fashion. Organisms, thus, are moved by emotions, both figuratively and literally. 'Motive', 'motion' and 'emotion' are very close in derivation and in meaning. Similarly, consciousness may be expected to be linked with emotions more than with pure informational or cognitive content. Human beings exhibit unprecedented emotional complexity, especially regarding kinship, courtship and sex: "[W]e have evolved a nervous system that acts in the interests of our gonads, and one attuned to the demands of reproductive competition" (Ghiselin, 1974).
The Cambrian Explosion
The evolution of the eukaryotes from prokaryotes was, together with the so-called Cambrian explosion (in which all the major radiations of multicellular architecture occurred in a relatively short period) about 530 mya, one of the most significant - and puzzling - events in the earth's history (e.g., Leakey, 1979; Gould, 1994). These events should, however, not be construed as evidence of inevitable progress and complexification inherent in the evolutionary process; on the contrary, the great success story of life's pathway were and are the bacteria.
During a period stretching over roughly three and a half billion years, life forms evolved from the primitive 'mother' molecule, whose phenotype consisted of only one catalytic enzyme, to the exuberant life forms participating in the trophic chain of the Cambrian era. Sexual reproduction emerged during that period, as well as multicellular organisms endowed with central nervous systems that could sustain more than simple reflex activities (Mackie, 1990: 917). It is to the earliest organisms displaying exceedingly simple sense organs that we can trace the roots of our intellectual abilities. The senses that developed in order to mediate the pre-Cambrian organisms' interactions with their environments had an inherent tendency to "organize the sensory field into groups and patterns of sense-data, to perceive forms rather than a flux of light-impression. This unconscious appreciation of forms is the primitive root of all abstraction, which in turn is the keynote of rationality" (Langer, 1941: 89). Towards the end of that period, organisms might already have acquired forms of associative learning (Arbas et al., 1991; Carew & Sahley, 1986) (Naccache, 1999: 16). These organisms followed an individualistic survival strategy that did not take into account their offspring. The life-cycle setup defines what Naccache (1999: 16) calls the 'Basic Mode of Evolution' (BoE).
It seems that even one geological second after the appearance of Cambrian skeletons there also arose something recognizably like a modern marine ecology, with hunters and hunted, grazers and filterers. Cellularity had become a food chain, gobbling began, and voracity has never gone away. If there were a point in history at which Tennyson's famous phrase 'Nature, red in tooth and claw' could be said first to apply, this was it, not the age of the dinosaurs - still less that of mammals (Fortey, 1998).
The animals that evolved in the Cambrian would have crawled over one another to be first to mate, evading the attention of predators on the way. Competition was introduced into ecology; these animals led exciting lives; vying with one another, sculpted for fitness. By contrast, the mat-formers which populated the endless stretches of Precambrian times, and even the Ediacara fauna, may have led lives almost devoid of incidents. Indeed, competitiveness still governs all biological life: 'Getting and spending, we lay waste our powers'. And all getting is some other creature's expense (Fortey, 1998).
Almost as an unexpected corollary of the growth of different feeding habits there arose strategies for survival, whether the organism concerned happened to be a filter feeder or a grazer, hunter or hunted. When other grow rich there is a living to be made as a parasite.
As we saw previously, there were predators in the Cambrian, too, but in the Ordovician it looks as if they swarmed in every habitat provoking an 'arms race' of protective devices. Many shellfish became larger, and acquired thicker shells (Fortey, 1998).
There is evidence around the world of a massive deterioration of climate as the Ordovician period drew to a close. It became colder and colder. As a result of the climatic change, many kinds of animals became extinct; in fact, well over half of all the species previously living. Those animals and plants that survived went on to make the modern world; had the list of survivors been one jot different, then so would the world today (Fortey, 1998).
To a paleontologist, death is a fact of life, and extinction is a fact of evolution. Some thirty billion species are estimated to have lived since multicellular creatures first evolved, in the Cambrian explosion. According to some estimates, thirty million species populate today's Earth. This means that 99.9 percent of all species that have ever lived are extinct.
Earth history evidently is not one of gradualistic progression, as Lyell and Darwin fervently desired, but one of sporadic and spasmodic convulsions. Some of these were of moderate extent, in which 15 to 40 percent of marine animal species disappeared, but a few others were much larger. This last group - known as the Big Five - comprises biotic crises in which at least 65 percent of such species became extinct in a brief geological instant. In one of them, which brought the Permian period and the Paleozoic era to a close, it is calculated that more than 95 percent of marine animal species vanished.
The Big Five, from oldest to most recent, are: the end-Ordovician (440 million years ago), the Late Devonian (365 million years ago), the end-Permian (225 million years ago), the end-Triassic (210 million years ago), and the end-Cretaceous (65 million years ago).
The most famous of such shifts, of course, was the end-Cretaceous event, sixty-five million years ago, which saw an end to 140 million years of terrestial domination by dinosaurs. In the subsequent Cenozoic era, mammals came to dominate vertebrate life on land. Similarly, the great Permian extinction dealt a near fatal blow to the mammal-like reptiles, which had ruled terrestrial life for eighty million years. They never recovered, and their role was soon taken by the dinosaurs (Leakey & Lewin, 1995; see also Wuketits, 1999).
Tetrapods and Homeobox Genes
Flies and people are just variations on a theme of how to build a body that was laid down in some worm-like creature in the the Cambrian period. They still retain the same genes doing the same job.
This means that arthropods and vertebrates are upside-down versions of each other. Some time in the ancient past they had a common ancestor. St.Hilaire guessed this fact in 1822, from observing the way embryos develop in different animals and from the fact that the central nervous system of an insect lies along its belly while that of a human being lies along its back (Ridley, 1999).
Vertebrates, with their dorsal nerve cords and ventral hearts, are upside-down descendants of annelid-like ancestors. "In all animals studied so far, from cnidarians to higher metazoans, a homologous genetic regulatory system for relative positional information seems to be present. This is best illustrated by the Hox gene cluster. The essential point is that, in many animal phyla, there is a stage in development when a series of homologous genes are expressed along the anteroposterior axis, specifying the morphological structures that will later develop. Although different structures in fact develop in different phyla, the signals that elicit them are similar. In all probability, this system for relative position is very ancient, and was present in the common ancestor of all animals (Maynard Smith & Szathmáry, 1995: 252). This has led Slack et al. (1993) to propose that this character is the defining synapomorphy (shared ancestral trait) of the kingdom Animalia, and should be called the zootype".
The time of the Cambrian explosion, between 540 and 520 mya, was a time of free experimentation in body design, a bit like the mid-1980s in computer software. It was probably the moment when the first homeotic genes were invented by one lucky species of animal from which we are all descended. This creature was almost certainly a mud-burrowing thing known - with delicate contradiction - as the Roundish Flat Worm or RFW. It was probably just one of many rival body plans, but its descendants inherited the earth or large chunks thereof (Ridley, 1999).
Moving from head to rear, the genes are switched on one after another and each new gene turns that part of the embryo into a more posterior body part (Ridley, 1999).
The switches in control of development are called the homeobox genes. They are arranged in groups of ten or so. Invertebrates have a single copy of each group, stretching over a hundred thousand or so DNA bases. Mammals have four, with many tasks in the embryo (and others in the adult; with mutations in homeoboxes leading to baldness and even to leukaemia). Ray-finned fish have seven or eight copies of the crucial segments. They lay claim to twenty-five thousand species, from sturgeon to salmon - as many as all other vertebrates combined. Such fish put mammals to shame, with seahorses, flatfish, anglerfish, eels and thousands more. Perhaps their extra homeoboxes, the masters of development, allow them to experiment with new and eccentric sets of body form.
The switches are arranged in series, each in charge of a separate part of the body's battalions. Their sequence, from front to back, is the same as that of the organs for which they are responsible. Homeoboxes lead from the front. Those nearer the head can control structures behind them, while those further back have less influence on parts of the body further forward. Changes in such genes persuade different segments to develop into head, heart or tail.
All land vetebrates are termed tetrapods - literally 'four feet' - and it is obvious that most amphibians, reptiles and mammals do indeed have four limbs. In creatures where they are lost, as in snakes, this loss is an evolutionary change from ancestors that initially also had four limbs. Where a pair of limbs is transformed, as wings are in birds, it is equally apparent that the wing is the equivalent of a limb, but changed for a different function - wings were not sprouted anew. A biologist would say that the wing and the limb are homologous structures - that is, they share a deep evolutionary identity. Limbs may be lost, but they cannot be re-invented, because the blueprint is fixed. Further, cats and humans alike have five toes. So do nearly all the tetrapods: where the number has changed - as it has, for example, in the horse, which has but a single toe - this is because of a proven reduction and loss of toes; the primitive number was still five. But why five?.
Nowadays, the basic kit of fingers is five, although some animals, such as chickens and horses, lost digits as they evolved. Early tetrapods were better endowed: a Russian specimen called Tulerpeton had six digits on each limb, Ichthyostega (claimed to be little more than 'walking fish') had seven on its hind limbs, and Acanthostega (half fish and half tetrapod, and dating from 360 mya) had eight digits on both arms and legs.
In this lumbering Devonian world seven was as good as five. At some stage one of these fish-like land-dwellers with five toes pulled ahead of the rest, and this was the founding father (or mother) of five-ness in all subsequent terrestrial vertebrates (Fortey, 1998).
The first fingers may have evolved by a lucky accident of misplaced genes, when a control gene responsible for coordinating brain development was duplicated elsewhere in the genome. But what benefit would fingers have been to our fishy ancestors? Ahlberg points out that the water margins were probably weed-choked, and that digits would have been very handy to manipulate the thick vegetation, allowing early tetrapods to move around more easily (McLeod, 2000: 31).
Gradually, from other such fossils, it became clear that the hand we all possess developed in a curious way from the fish's fin: by the development of a forward-curving arch of bones in the wrist from which digits were flung off towards the rear (little-finger) side (Ridley, 1999: 183-84).
The tetrapods from the Devonian were largely aquatic. All were big predators, measuring over a meter long, with tail fins, more than five digits and the crocodilian body form. The fossil record suggests that tetrapods were fashioned according to this template until the beginning of the Carboniferous, about 354 mya. For the next 20 million years the record is silent. This period, known as the Tournaisian, must have seen a huge diversification of the tetrapods, because after this gap in the record we see a variety of body forms that are much more like today's land animals. Fossils from East Kirkton in Scotland date from just after the Tournaisian gap. They reveal that by about 338 mya, tetrapods had conquered land and lived fully terrestrial lives (McLeod, 2000: 32).
The Animal Colonization of the Land
As the Devonian drew to a close the Earth's climate became more extreme. Around the world lakes and rivers dried out completely, trapping millions of fish as their aquatic environments turned terrestrial.
Numerous species of fish must have migrated from salt to fresh waters as the Age of Fishes progressed, but those doing so as drought became commonplace in the late Devonian must often have found themselves in water appreciably warmer that the sea they left behind. The shallow waters of lagoons, estuaries, rivers and lakes warm up rapidly. As water becomes warmer its oxygen content is reduced, making it difficult for fish to breathe. Many suffocated, but among the early colonizers of the shallow warm waters some fish developed the trick of gulping air from the surface and holding it in the gullet, where fine blood vessels absorbed the oxygen direct. With the passage of time and countless generations, this system of air-breathing evolved to find its most lasting expression in the lungfish, which could survive in oxygen-depleted waters while gill-breathing fish died in their thousands.
It was thought no so long ago that the strategy of mobility on dry land evolved in a group known as the lobe-finned fish. Reader (1986), for example states: The basic equipment they employed was common to all the placoderms' descendants: two pairs of fins, one pair just behind the head and another near the tail. But the lobefins were powered with a greater mass of muscle than their cousins, and their fins were longer, stronger, and constructed in a way that was quite new. The limbs that have carried the vertebrates through the story of life evolved from the fins of the lobe-finned fishes. The basic structure of shoulder, elbow and wrist, and hip, knee and ankle, was already present in the fish that lived 350 mya, although its initial significance lay only in enabling the lobefins to support their own weight and to waddle from pond to pond down the riverbed and between lakes as the drought advanced. This also of course gave them access to the food that the terrestrial environment had on offer - a vast unexploited niche. The lobefins, such as Eusthenopteron, could already breath air out of water; once they had evolved fins capable of lifting their bellies off the ground they were poised to lead the vertebrates' invasion of the land (Reader, 1986).
During the Devonian a new world emerged as complex plant ecosystems formed on land for the first time. Just after the first full-size trees evolved, a group of lobe-finned fishes called the panderichthyids emerged. Even at this early stage, the panderichthyids had the body form of a four-legged land animal. In fact, with their flattend heads and long tails they were almost crocodilian in shape, apart from having fins instead of limbs (McLeod, 2000: 28-9).
The puzzle is still far from complete, but it is becoming clear that most of the major changes needed for life on dry land happened in the water. The epic journey from water to land began about 400 mya.
Lungs pre-date the move to land by around fifty million years, and they may have evolved to allow fish to survive in oxygen-depleted waters. In any case, panderichthyids, with their lungs and gills, would have been able to breathe out of water as well as in it. They filled their lungs by forcing air in from the mouth - a technique known as buccal pumping, which is still used by amphibians today. Panderichthyids also had their eyes on the top of their heads, rather like a mudskipper's, suggesting that they would have functioned above the waterline (McLeod, 2000: 29-30)
So, it appears that one of the earlies changes in the evolution of tetrapods was a move from front-wheel to rear-wheel drive. Fish tend to have their motor at the front in the form of powerful pectorial fins, but in Acanthostega (which looked similar to the panderichthyids except that it had limbs with digits instead of lobe-fins) and most other tetrapods, the power comes from the hind limbs (McLeod, 2000: 30).
Lobe-finned fishes or lungfishes?
The tetrapods had been regarded as descending from a curious group of lobe-finned fishes, a view often repeated in popular books (Fortey, 1998).
But there were other kinds of fish living in the streams and lakes of the Devonian. Among them were the earliest lungfishes. There are several species of lungfish still living today, of which the most primitive is Neoceratodus, a slow-moving animal clothed in large scales which now lives only in Australia and copes with low oxygen conditions in water by breathing air, an adaptation that may have seen it through many hard times since the Permian period when its fossil relatives lived. Neoceratodus lacks limb-like fins altogether. The cladists go to work, analysing all the characteristics of lungfish, including subtle features of the bones of the head as well as obvious ones like lungs. They compared these features with what they shared with lobe-finned fish on the one hand, and tetrapods on the other. A heterodox answer was returned: it was the lungfishes, not the classical lobe-fins, that were more closely related to the tetrapods. Our coelacanth was shuffled sideways off the main line of descent.
The cladists were probably right. Now that the molecular sequences of molecules can be elucidated (providing yet another list of characteristics) there is additional evidence supporting their view. A return to the fossils showed that early fish like Eusthenopteron had fins which might, after all, be candidates for conversion into limbs. Later descendants of the Devonian lungfish, like Neoceratodus, had lost them over the passage of millions of years. In sum, it was a revolution about the understanding of those seminal days on Devonian shores (Fortey, 1998) (See footnote 4) 4 .
Elginerpeton was unearthed in the 19th century near Elgin in Scotland. It is a monstrous predator - at least 1.5 meters long - with teeth that are much more fishlike than those of most other tetrapods. Comparative anatomy and computer analysis reveal that Elginerpeton is at the base of the tetrapod family tree, but its evolutionary history is not straightforward. The hind limb was 'very good as a paddle but pretty lousy as a walking limb', says Ahlberg. Yet some of the skeleton is adapted for bearing weight, which suggests that at some point it came onto dry land. It seems that Elginerpeton evolved to become more aquatic again after some initial adaptation to life on land (McLeod, 2000: 31).
The landward transformations were probably already underway in the Silurian, but were completed in the Devonian period - that is, between 410 and 360 mya. The only satisfactory explanation as to why plants and animals pushed further and further into hostile territory is that their daring was rewarded by overwhelming success in reproduction in this virgin habitat (Fortey, 1998).
Animal life followed plant life onto the land. Ancestors of creatures such as millipedes made the transition easily and early. Amphibian forms moved on to the land to eat the plants and insects at the end of the Devonian period (about 360 mya), "not in some natural ascent up the glorious ladder of evolution, but because they found life too tough in the seas" (Gribbin & Gribbin, 1993).
The fish-amphibian transition was not a transition from water to land, but a transition from fins to feet that took place in the water. The very first amphibians seem to have developed legs and flipper-like feet from fins to scud around on the bottom in the water. They had both lungs (an ancient fish trait that was later transformed into swim bladder) and internal gills. One line (Hynerpeton) bore weight on all four feet, developed strong limb girdles and muscles, and quickly became more terrestrial (Hunt, 1997).
While the plants changed the face of the land, the vertebrates remained tied to the water for some time. By the mid-Devonian, about 370 mya, the lobe-finned fishes or lungfishes already possessed the equipment necessary for the move ashore. They possessed the necessary equipment, but never made the behavioral adaptation. This was left to the amphibians, who were the direct descendants of these ancestral fishes. The earliest fossil amphibians were dubbed labyrinthodonts by Richard Owen (1804-92), an early pioneer in the scientific study of fossils. He described the ancient creatures as probably resembling gigantic salamanders, measuring anything from one or two to eight meters long (Reader, 1986).
Accounts of vertebrate evolution often tell how the move from water to land was restrained only by the early amphibians' reproductive procedures, which still demanded an aquatic environment. The story evokes the image of a pioneer glimpsing a new world, anxious to enjoy the unexploited resources it has found but held back by a tedious need to produce young in the water.
The reality is less dramatic: the large labyrinthodonts were tied to the water by their food requirements (they were exclusively carnivorous), and were probably quite content there. They were preceded ashore by much smaller amphibians, who consumed invertebrates in the water and made equally sustaining meals of the invertebrates they found in the course of exploratory forays on to the land. This probably occurred during the warm, humid Carboniferous period, when plant life and invertebrates were abundant on land and the waters swarmed with an impressive variety of large predacious carnivores.
The little amphibians probably first ventured ashore seeking refuge from the aquatic predators, who followed only some millions of years later when the climate changed and seasonal droughts favored the organisms that could waddle down to the next pool as the rivers and swamps dried out. It was this that brought the labyrinthodonts and their descendants ashore; they do not colonize the land directly, but were stranded there by the retreating waters, and managed to survive. Eventually, by the end of the Carboniferous, the terrestrial way of life prevailed. Amphibians of various sizes fed upon one another down to the smallest, which in turn fed upon the insects, worms and spiders that must have been plentiful in the forests. None of the vertebrates fed directly upon the abundant vegetation. They left the invertebrates to process it for them and, indeed, could never have survived on land if the invertebrates had not been there first (Reader, 1986).
It may have been in the thick of some Carboniferous forest that the first amniote egg evolved, one protected from desiccation by a tough surrounding membrane; and thus the first reptile was born (Fortey, 1998).
Some time before the climatic crisis began to affect the amphibious lifestyle, the vertebrates went through a crucial stage in their evolution. Some among their numbers evolved the practice of producing their young neatly packaged inside a hard enclosing capsule: the egg. This wonderful miniature ancestral pond, in which the young could grow until they were old enough to fend for themselves, did not need to be anywhere near the water. The practice of laying eggs on dry land probably evolved while the coal forest swamps were still well watered, as a means of keeping the young away from predators, although it had other important benefits too. As the swamps dried out most of the amphibians died out, but the egg-layers among them were able to survive away from water, wherever there was some vegetation and some invertebrates to process it for them. These were the first vertebrate animals to live entirely on land - the first reptiles.
Once established ashore, the early terrestrial reptiles evolved rapidly. At first there was still a sizeable aquatic element in their diet and preying upon each other was common among the largest of them. Inevitably, however, some evolved the dental and digestive equipment needed to take advantage of the plant food that was at first so abundantly available. This development cut the last thread that tied the vertebrates to the water.
What followed next was a spectacular instance of what paleontologists have termed 'adaptive radiation'. Through the Permian period, between 270 and 225 mya, the early reptiles diverged at a rate that has hardly been matched before or since (Reader, 1986).
All animals that succesfully adjusted to terrestrial life had to solve a number of problems: respiration (obtaining oxygen), dehydration, and reproduction.
Between 225 and 200 mya, the reptiles, rose to dominance. They were the first completely terrestrial vertebrates. With the evolution of internal fertilization, reptiles were no longer required to return to water in order to reproduce. After fertilization, the embryo is contained in an amniotic egg, maintaining the moist environment, and surrounded by a thick leathery shell preventing dehydration. The egg (a major evolutionary development) also contains a food supply, as well as a number of other evolutionary novelties (Poirier, 1993). Eventually, land-dwelling organisms would evolve ways of taking the sea with them by first packaging water in cells and later by inventing circulatory systems that bathed each cell in a seawater-like fluid (Michod, 1995).
From the reptiles we inherit our 'reptilian brain' (MacLean, 1990), which together with the paleomammalian (limbic system) and the neomammalian brain (in humans including the enormous neocortex) constitutes the 'triune brain' (three brains in one package; an uneasy and conflictuous coexistence). This is its contribution to our psychology:
"However disconcerting to us today, sexual jealousy, same-gender violence, rape, and hierarchical obedience were keys to the survival of the prolific and diverse reptiles that, in the millions of years of the late Paleozoic era, preceded any mammals. Male bloodthirstiness, cunning, and a quickness to make and carry out threats worked to repulse other males. Other behaviors bonded reptiles into dangerous alliances capable of extinguishing rival groups. It would seem that at the level of the reptilian body-mind sex and violence are in a strange concord" (Margulis & Sagan, 1991).
According to Naccache (1999), we note a qualitative development in the life-cycle setup when the parent phenotype started contributing, in an organic way, to the organic growth of the next generation genome. This happened with the emergence of the amniote egg, a protected environment provided by the parent phenotype for the expression of the offspring's genome (Naccache, 1999: 17).
The evolutionary development of the sensory fields' ability to organize data into patterns (Langer) or 'self-categorization' (Edelman), and, from there, progressively into scenes, led to the emergence of of 'primary consciousness' which "provides a means of relating an individual's present input to its acts and past rewards" (Edelman, 1992: 118-23; see also Edelman, 1989; Gazzaniga, 1995). This enhanced behavioral plasticity and adaptability not only increased the individual organism's fitness, but it enabled the oviparous reptiles that possessed it to choose a favorable environment in which to lay their eggs. This greatly improved the chances of survival of their offspring who were ready to carry on in the appropriate environment as soon as they hatched. Note that these developments took place without any noticeable enlargement of the brain between amphibians and early reptiles.
The amniote egg, in conjunction with primary consciousness (and a scaly skin protection), opened to vertebrates all the terrestrial environments already colonized by plants and insects. Currently estimated to have emerged some 300 mya, these developments of the life-cycle setup affected the survival of the next generation phenotype massively enough to justify considering that, with them, a new Mode of Evolution (MoE) had emerged, which Naccache (1999: 18) calls the 'Reptilian MoE'.
Reptilian Ritual Behavior
Reptiles, as exemplified by extant lizards, show the following ritual displays (MacLean, 1990: 100):
- Ritualistic display in defense of territory
- Formalized intraspecific fighting in defense of territory
- Triumphal display in successful defense
- Submissive (surrender) displays
- Establishment of social hierarchy by ritualistic display
- Courtship displays
Carpenter (1961, 1967) appears to have been the first to attempt a detailed analysis of lacertian displays. He referred to them as display action patterns (DAPs). Greenberg (1977) distinguishes (1) signature ('assertive'); (2) challenge ('territorial'); (3) courtship; and (4) submissive ('appeasement', 'assentive') displays. MacLean (1990: 109-139) gives the following details:
In social situations the signature display (a single pushup with the upper extremities followed by two head bobs or nods) is typically performed under three conditions. When it occurs upon the meeting of two or more lizards, it appears to serve as a form of greeting not too unlike the gestures used by human beings. It is usually the initial expression of a territorial male when encountering an intruder. And it is commonly the first overture of a male in the act of courtship.
If an adult blue spiny male trespasses on the territory of another, the tenant may at first respond with a simple 'take-notice' signature display. It the intruder does not retire, the tenant will give him an emphatic warning by performing a challange display - a term introduced by Carpenter. It consists of a pushup followed by as many as 12 head bobs, extension ofthe gular (throat) fold, and an expansion of the body profile, exposing the blue coloration on its chest and belly. If the intruder still fails to retreat, the territorial male will head for him in a loping gait, and as he draws near will turn the body sidewards somewhat in the manner of a football player attempting to block. Because of the sagittal expansion the sidewards approach serves to give full accent to an apparent increase in size. If the intruder stands its ground, there is a side-to-side 'face-off' (circling parallel display), followed by nudging, pushing, and tail lashing. As the struggle continues with rapid circling, each contender attempts to in down the other by a jawclamp on the neck or tail. If the fight is particularly vigorous, one animal may lose its tail. The struggle will go on until one member retreats or assumes a submissive bow characterized by a head down position.
In describing marine lizards, Eibl-Eibesfeldt (1961) commented: "From my observations I noticed that strict order reigned among them. In every case a male inhabited a certain piece of rock which he shared with some rather smaller females, and he jealously watched over this [rock] as his own territory". If two neighbors found themselves too close, both would show a threatening attitude, raising themselves on stiff legs and strutting up and down with their dorsal combs elevated. But if the intruder failed to back off, fighting would occur. Eibl-Eibesfeldt's choice of words in describing the first encounter he witnessed is reminiscent of the 'face-off' displays of the rainbow and Komodo lizards: "With stiff, stilted gait, the rivals stalked round each other, each one making himself appear as big as he could and endeavoring to show off by keeping himself broadside against the other". Then with lowered heads, each kept butting the other until the intruder was pushed over sideways. The defender nodded his head up and down in triumph. The intruder made another comeback, but once more was defeated. This time he collapsed in an abject posture before the victor, his dorsal comb flattened and his legs stretched out.
As applies to a wide range of animals, the courtship display of a blue spiny male lizard has some similarities to the challenge display. One sees it performed by a sexually active male when a reproductive female comes within range and signals her interest in him by a swish of her arched tail. In response to her solicitation display (swinging tail in a wide arc), the blue spiny male may perform a signature display and then launch into a full courtship display. The latter is characterized by a pushup and a series of head bobs performed while he lopes toward the female. The loping gait recalls the same kind of approach preceding a close-in challenge display. The courtship situation may also give the impression of a pugnacious encounter, because following the display, the male will aggressively give the female a number of side nudges and attempts to get a grabbing bite on her neck.
Because of their protective and survival value, submissive displays are recognized as an indispensable part of an animal's behavioral repertoire. Their value is that in signaling compliance, they serve to forestall, reduce, or terminate the punishing, and potentially deadly, actions of a dominating animal. In blue spiny lizards, Greenberg describes a 'bodydown-alert' posture, which he equates with 'submission' or 'subordination'.
The strutting gait
Thus, in animals generally the following components of agonistic displays seem to be universal: (1) expansion of the body profile (apparent increase in size); (2) lateral (parallel) display; and (3) a strutting gait. These displays are easily understandable as intimidations and deterrents.
MacLean (1990: 232-33) notes that certain features of the aggressive displays of mammals have a striking similarity to the 'close-in' challenge display of territorial lizards. The lacertians rise up on all fours and present themselves sideways while stepping in a stilted, staccato manner that makes them appear off balance. Some rodents perform a similar broadside display, but it happens so rapidly that observers may fail to notice it. Barnett (1963: 87) has described the broadside display of rats as follows: "The back is maximally arched, all four limbs are extended and the flank is turned toward the opponent. While in this attitude the rat may move round his victim with short, mincing steps, still presenting his flank. Stonorov (1972: 92; quoted in MacLean, 1990) has described the stereotyped, stiff-legged display of the brown or so-called 'grizzly' bear (Ursus arctos): With canines showing and ears flat, the bear walks "with its head down and muscles tensed, and it front knees appear to be locked".
MacLean had been unaware that the 'challenge' display of two adult, rival gorillas incorporated lacertian features until Dian Fossey presented a seminar at his laboratory and acted out what she refers to as the 'parallel display' of two silverbacks. When she mimicked their sideways presentation and their walking with stilted, awkward steps, MacLean was immediately reminded of the close-in display of certain lizards (MacLean, 1990: 232). The so-called parallel display of gorillas had been earlier referred to by Schaller (1963: 235-36) as the 'strutting walk'. Phrased in his words, the gorilla displays the side of the body; the arms are bent outward at the elbow, giving them a curious curved appearance and making the hair on the forearm look impressive; the body is held very stiff and erect, the steps are short and abrupt, and except for brief glances, the head it turned slightly away from the opponent. Reminiscent of voiceless lizards, the silverbacks that strut within 10 feet of each other utter no vocalizations during the display. A similar strutting walk is seen in courtship.
In the case of chimpanzees, Goodall (1968: 276) has described a bipedal swagger that appears to correspond to the strutting display of the gorilla. The chimpanzee "stands upright and sways rhythmically from foot to foot with his shoulders slightly hunched and his arms held out and away from the body, usually to the side". Her description calls to mind the posture and movements of a Japanese wrestler.
As in the case of lizards, the stilted, staccato steps of the displays of the great apes seems to carry the message of a series of exclamation marks. The Schrägstellung gait of the Komodo dragon calls to mind the goose step of a military parade.
The question naturally arises as to whether the striking similarity between the challenge displays of animals as diverse as lizards and gorillas represent 'convergent' or 'parallel' evolution. Among different species the sideways presentation and the stilted, staccato steps have such an uncanny resemblance that it would almost seem that the challenge display had been genetically packaged and handed up the phylogenetic tree of mammals.
Gajdusek (1970: 58-59), in an article on Stone Age Man, has called attention to the parallel between the display behavior of squirrel monkeys and certain rituals of Melanesian tribes. Referring to our observations on squirrel monkeys he says: "I have noted a quite similar presentation and display in both spontaneous and socially ritualized behavior in some New Guinea groups. It is similarly used to express both aggression and dominance... When frightened, excited, elated, or surprised, groups of Asmat men and boys spontaneously meet the precipitating event by a penile display dance, which involves much the same sequence as the presentation display of the squirrel monkey".
Neural mechanisms involved in oral, genital, and agonistic behaviors converge in the hypothalamic, amygdala and septopreoptic region. It would appear that the close functional relationship between the amygdala and the septal division and their descending pathways is owing to the olfactory sense [bulbus olfactorius], which, dating far back in evolution, plays a role in both feeding and mating, as well as in the fighting that frequently precedes (MacLean, 1990: 375).
As has been emphasized, reptiles are slaves to routine, precedent, and ritual. Obeisance to precedent often has survival value. If, for example, a particular crevice served as an escape from a predator on one occasion, it may do so again. As Lorenz (1966: 72) has observed, "If one does not know which details of the whole performance are essential for its success as well as for its safety, it is best to cling to them all with slavish exactitude".
Xenophobia (fear of, and hostility toward, strangers) is another reptilian residue. Strangeness and familiarity night be regarded as opposite sides of the same coin. The recognition of what is strange or novel depends on a contrast with what is familiar. Lizards, living communally in cages or in territorial groups, have been shown over and over again, to be capable of immediate recognition of a stranger (Greenberg & Noble, 1944; MacLean, 1990: 140). The unanswered question regarding neural mechanisms underlying an animals' response to what is alien or different has much human interest in regard to human intolerance of aliens.
MacLean describes 'ganging up' behavior of communal groups of lizards against a newcomer. In each case, the subdominant males, which were lorded over by a 'tyrant', joined him in driving away an adult male intruder. Evans (1938; 98) has also observed that several spayed female lizards (Anolis carolinensis) living in the same cage and dominated by one or two others "all showed pugnacity toward an intruding female". His observations suggest that an animal's disposition toward strangers is at least partially under hormonal influence.
Juvenile lizards run the risk of being treated as 'strangers' by adults of their own species, since they may be cannibalized by them.
Among birds and mammals, immature animals with various kinds of blemishes (strangeness) may be killed or driven off from the home territory by continual harassment (MacLean, 1990: Ch. 29).
Xenophobia is a widespread trait throughout the animal kingdom, according to Southwick et al. (1974), but it is by no means universal. It has been shown experimentally in various species of social insects, especially bees and ants (e.g., E.O. Wilson, 1971; 1975), but it evidently does not occur among other aggregational insects. Among vertebrates, xenophobic aggression has been demonstrated experimentally in a great number of species, especially those with prominent territorial and/or relatively closed social groups, which are organized on a hierarchical basis (Holloway, 1974; Southwick et al., 1974; E.O. Wilson, 1971, 1975; See van der Dennen, 1987 for a review). The introduction of unfamiliar conspecifics to such groups (e.g., rodents such as mice, rats, molerats, etc., and many primate species, such as monkeys and apes) may release massive attacks and even killing from the resident animals. Primate social units appear, in general, to be intolerant to close proximity of extra-group conspecifics. Moreover, Goodall (e.g., 1986) documented discrimination of, and even attack on, a group member deformed and paralyzed by poliomyelitis (who was probably perceived as a fear-inspiring stranger due to his 'odd' behavior).
On the other hand, xenophobic behavior has not been observed, nor would it be expected to occur, in most typical encounters of vertebrates with relatively open societies.
It is important to point out, according to Southwick et al. (1974), that xenophobic aggression is not the same as territorial aggression or aggression related to dominance hierarchies. In both territorial and hierarchical behavior, aggression is often directed toward socially familiar animals. The territorial animal may interact aggressively most often with his nearest neighbor, and the socially-ranked animal may interact most often with his nearest-ranked peer. The essence of xenophobia is an aggressive response toward a complete social stranger. This may occur, of course, in either territorial or socially ranked animals, so there is considerable overlap in these behaviors, but there are also significant differences. Territorialism and hierarchical behavior are very often maintained by display, whereas xenophobic aggression frequently involves lethal violence.
When it occurs in natural settings, xenophobia is a functional and adaptive trait in that it maintains the integrity of the social group. It ensures that group members will be socially familiar. It limits the flow of individuals between groups, and can therefore affect patterns of both social and genetic evolution. Xenophobia has apparently evolved in those species and populations where discrete, bounded social groups are adaptively favored (Southwick et al., 1974).
Hebb & Thompson (1968) cite the evidence in favor of the mammal's xenophobia; the fear of and hostility towards strangers, even when no injury has ever been received from a stranger. The enmity aroused by conspecifics which are different (in anatomy, in coloration, in behavior, in language use) or by strangers, may easily lead toward discrimination, ostracism and cruelty in animals as well as man. Children too will attack another child who is perceived as being an outsider. In observing young children in her own nursery school during the 1920s and 30s Susan Isaacs (1933) found extreme hostility toward newcomers. Adults, as well as children, often 'test out' newcomers or strangers by violent behavior. Aggressive behavior may also serve the newcomer as a means of winning his way into the group. Markl (1976) deduced the following general rule from observations such as these: Species with highly cooperative social behavior within the group are particularly apt to be very aggressive towards conspecifics that are not members of their group.
One group of reptiles, the synapsids took a radical different path than the other reptiles, evolving homeothermy, a larger brain, better hearing (eardrum) and more efficient teeth. One group of synapsids, called the therapsids (or mammal-like reptiles), took these changes particularly far, and apparently produced the mammals.
In all probability mammals descended in a line from the ancient mammal-like reptiles of the pre-dinosaur Permian-Triassic periods called therapsids (the subclass synapsida that branched off from the diapsida line that eventually produced the great dinosaurs many years later), who represent a branching of the ancient reptile line (cotylosaurs). Therapsids appeared approximately 230 mya (Cory, 1998).
It is a curious fact that much of the early evolution of land animals was about biting more effectively. Early land vertebrates like Ichthyostega could do little more than snap their jaws shut. Clamping the jaws together, or chewing, requires altogether more subtle and flexible musculature. Rearrangements of the muscles entailed rearrangements of the bones. Today, only tortoises and turtles are reptiles with no major skull openings, apart from those in the eye sockets. These animals, one might say, adopted the bony alternative, sealing themselves thoroughly in. As a survival mechanism it seems to have worked rather well, a moral already appreciated by Aesop in his fable on the tortoise and the hare. At the other extreme are those with two pairs of openings (diapsids) in the skull besides the eye sockets - a group including many lizard-like animals, and crocodiles, together with all the dinosaurs, and birds. Synapsids had only a single opening on either side of the skull, positioned rather low down. One set of reptiles had this structure, a group of extinct animals which is accepted by most palaeontologists as including the closest relatives of the mammals. This is reflected in their vernacular name: the 'mammal-like reptiles'. Although they started small, mammal-like reptiles had evolved by the Permian, and in the Triassic some comparatively massive species appeared which could be three meters or more in length. Their teeth show that they had also evolved several different life habits. Much more compact and muscular mammal-like reptiles were known as therapsids, and included some fearsome predators, like Anteosaurus. These were able to cull herds of their herbivorous relatives, which included dicynodonts (looking nothing so much as a reptilian hippopotamus).
At the same time as these dietary changes, the waddling posture which had been typical of the early reptiles was being replaced by a more upright gait that allowed the legs to be tucked more under the body. This led both to greater speed and to greater load-bearing capacity (Fortey, 1998).
The first reaction of any lay person encountering a threrapsid would probably be to hasten to some safe and distant place. Large, rotund, stocky creatures, with short legs, powerful stubby tails and large heads, often with protruding fangs, the mammal-like reptiles were distinctly unattractive - imagine a cross between a hippopotamus and a crocodile - but they were undoubtedly the ancestors of all the mammals, including man (Reader, 1986).
As a generalization, paleontologists point out that successive therapsids become progressively more mammal-like with respect to their locomotor skeleton, skull, teeth, jaw joint, and middle ear.
Romer regards the Phthinosuchia as the parent stock of the family tree of the therapsids leading to two great groups of therapsids characterized as being predominantly carnivorous (Theriodontia) and herbivorous (Anomodontia). The successive carnivorous therapsids are the therocephalians, gorgonopsians, cynodonts, bauriamorphs, ictidosaurs, and tritylodonts. The mammals are believed to have been derived from the cynodonts (MacLean, 1990: 86).
The therapsid assumption of a more upright posture (limbs more underneath the body) was accompanied by a change in the phalangeal formula. The therocephalians appear to be the first to have acquired the 2-3-3-3-3 mammalian phalangeal formula familiarly illustrated by our fingers and toes (MacLean, 1990: 87).
The advanced mammal-like reptiles may have become endothermic. It is one of the intriguing aspects of neurobehavioral evolution that a number of postures and autonomic changes seen in thermoregulation acquire symbolic significance in animal communication. For example, the piloerection and ruffling of feathers that serve, respectively, in mammals and birds to insulate against the cold may also serve to enhance the animal's size in aggressive or defensive encounters. Greenberg (1978) has cited references to four species of lizards that "use a similar kind of posture in thermoregulation as in a show of aggression" (MacLean, 1990: 90-91).
By the early Triassic, a little after 250 mya, the carnivorous Cynognathus was around. The therapsid that most closely resembled a mammal came slightly later, and its remains are found in rocks from the Early Jurassic, just after 200 mya. This was Probainognathus, a member of the sub-order of therapsids known as the cynodonts. It had a skull, jaw and teeth very like those of mammals. They were probably furry, warm-blooded creatures; they may even have suckled their young (Gribbin & Gribbin, 1993; Boyd & Silk, 1997).
The mammal-like reptiles may, for the first time in evolution, have shown parental care. The skull of a tiny, immature cynodont (Thrinaxodon liorhinus) was found next to an adult female (MacLean, 1990: 92).
The therapsids were nearly overwhelmed by another wave of reptilian adaptive radiation - dinosaurs, the 'fearfully great lizards', arrived on the Permian scene.
Beginning in the early Triassic period, about 225 mya, first the therapsid carnivores and then the herbivores were replaced by the ancestral dinosaurs. By 190 mya the mammal-like reptiles were just a thin line on the evolutionary map, all but overwhelmed by the great bulge of the dinosaurs' adaptive radiation. They would be around for 140 million years.
The dinosaurs were very specialized in their ways of life and, for reasons as yet not fully understood, they went extinct some 70 mya. But the dinosaurs did not leave the Earth unpopulated; as their numbers declined, others increased (Reader, 1986).
Sinocodon (208 mya), Kuehneotherium, and a group of early proto-mammals called morganucodonts (205 mya), are thought to be ancestral to all three groups of modern mammals - monotremes, marsupials, and placentals. Placentals appear to have arisen in East Asia and spread to the Americas by the end of the Cretaceous (Hunt, 1997).
In the early Jurassic, cynodonts had all but disappeared from the scene. The survivors, the lineage from Probainognathus to ourselves, got by "by evolving into small, mouse-like creatures, too insignificant for dinosaurs to take much notice of, probably leading a nocturnal life style and living off insects and, perhaps, plants" (Gribbin & Gribbin, 1993).
The end of the Permian saw the reconstruction of the natural world. It was, truly, a mass extinction, a carnage of a magnitude that had never troubled the Earth before. As a corollary, the Permian extinctions subsequently prompted the appearance of the majority of animals that dominate the living world today. The transformation was evidently greatest in the sea, where it has been claimed that up to 96 per cent of all species died out (Fortey, 1998).
The differences between reptile and mammal that had to be bridged in the evolution of one from the other are considerable. Reptiles are cold-blooded (poikilothermic) and rely solely on external heat sources to raise their body temperature to the level required for activity. Mammals, on the other hand, generate heat internally (they are warm-blooded, a condition called endothermy or homoiothermy or homeothermy) and retain it with insulating fats and furs; a consistent body temperature means that mammals can sustain a higher and more continuous level of activity, which in turn calls for greater and more regular supplies of food than reptiles require. More activity calls for a more efficient system of inhaling and transporting oxygen, along with nutrients, to the muscles where metabolism takes place, hence the larger lungs, the diaphragm and rib-cage, four-chambered heart and circulatory system of the mammals. More efficient metabolism requires a more efficient means of removing metabolic waste material from the cells, hence the kidneys and the separation of the urinary and fecal excretory tracts (which are combined in the reptiles).
The mammals also have a system of reproduction which leaves the young to develop more fully inside the mother after conception and grants them a period of parental care after birth, when the mothers' mammary glands provide a reliable and nourishing diet of ready-processed food long after the reptiles have been left to hatch and fend for themselves. All this gives the mammals a higher infant survival rate than the reptiles can ever achieve and, equally important, allows time for the development of a more complex organism and the cerebral software that transcends the purely instinctive capabilities of the reptilian ancestors.
The features distinguishing the mammals from the reptiles did not evolve all at once, nor is it possible to put each of them in sequence in terms of evolution. They constitute a mosaic of features, each independently evolved and enhancing the whole, and all dependent upon and contributing to the most crucial distinction of all: mammals are simply more efficient at catching and processing their food than reptiles. The teeth of mammals are adapted to cut up and crush food, and their digestive system is fast and efficient, which of course is linked to the high level of activity that mammals can sustain (Reader, 1986).
The mammal-like reptiles were already a good way up the evolutionary tree from which all the mammals stemmed. The cynodonts (dog-toothed mammals), for instance, already had the bony platform separating nasal and food passages in the head, which enabled them to eat and breathe at the same time. Then there is the separation of the reptiles' simple dentition into an arrangement of food-gathering incisors and canines at the front with a row of complex food-processing teeth behind - the molars.
The jaw shortened, and sling of muscle grew along and around it; thus, for the first time in any animal, the vertebrate jaw was able to effect a degree of sideways chewing motion as well as the basic up-and-down action to which the reptiles were restricted. As the jaw evolved towards its single-bone structure, the now superfluous angular, articular and quadrate bones of the reptile jaw took on an entirely new function, becoming the tympanic, malleus and incus of the mammals' inner ear (Reader, 1986). The bone that developed into the stapes was originally part of the gill system in fish (McLeod, 2000: 31).
Also during this period vital changes were taking place in the reproductive strategies. None of this is preserved in the fossil record, such things do not fossilize, but from the evidence of animals living today we know that at a critical point the mammalian line ceased laying eggs like reptiles and began bearing live young. At first the young were born at a very early stage in their development and immediately transferred to a pouch on the mother's belly where they found modified sweat glands secreting milk; these were the mammary glands that give the mammals their name. The young suckled in the pouch until they had grown to the point of being able to fend for themselves. These were the first marsupials (Reader, 1986).
The mammal-like reptiles had smaller pelvises, thus a narrower egg-laying channel. The eggs had to get smaller, which meant less room for yolk sac and shorter growth within the egg. The young hatched earlier and less developed, requiring more and more parental care. The development of mammary glands was to take the place of yolk.
Mammary glands probably derived from sweat glands. They were used to keep eggs humid while incubating. Hatchlings would lick them to get water. Gradually, minerals, trace elements, nourishing organic compounds were added to the fluid. Nursing increases and intensity of interactions between parent and offspring.
The earliest mammals evolved to avoid competition with reptiles. Early mammals were nocturnal, which led to increased potential for intelligence. At night, you can't rely exclusively on visual clues, but must also use hearing. The early mammals evolved a larger skull to hold more neural tissue, increasing the amount of tissue available for things like hearing, etc. (http:// corona.eps.pitt.edu/www_GPS/courses/GEO0871/Primates/primates.html)
Mammals are animals whose females suckle their young upon modified sweat glands. They thus embody milk and maternity: they are nurture encapsulated. Most mammals are hairy, and even those that are not had hairy ancestors (Fortey, 1998).
Placental mammals, those having a womb in which to nourish their babies to some degree of maturity before birth, are considered to be comparatively advanced. The most primitive living mammals are the monotremes, which retain the characteristic of laying eggs from a reptilian ancestor. Marsupials, on the other hand, give birth to tiny little babies that crawl their way through moistened fur to a special pouch (the marsupium), in which they can suckle and grow. [See Fortey (1998) for a fascinating account of the many strange, weird, and/or gigantic extinct marsupials and placentals.]
The mammalian modifications, differentiations, and elaborations, to the early vertebrate and ancestral amniote brains had the effect of introducing endothermy, maternal nursing, enhanced mechanisms of skin contact and comfort, as well as enhanced visual, vocal, and other cues to bond parents to offspring and serve as the underpinning for the extended and complex family life of humankind. The mammalian modifications, therefore, added greatly enhanced affectional, other-interested behavior to the primarily (although not exclusively) self-preservational, self-interested behaviors of ancestral amniotes and early vertebrates (not necessarily their modern representatives) (Cory, 1998).
There are about 4,500 species of mammals on Earth and they come in all shapes and sizes - from the tiny shrew to the elephant, from the mole to the whale, tigers, dogs, squirrels, giraffes, bears and, of course, people. The mammals are a diverse group, certainly the most conspicuously successful animals on Earth. They have crawled, climbed, run, burrowed and swum their way into all the major habitats that the Earth has to offer (See footnote 5) 5 .
The mammals are very active, consciously aware of their surroundings, often inquisitive, and always protective of their young. All mammals suckle the new-born. They all share, to a greater or lesser extent, the inheritance of a brain that is capable of performing more than just the instinctive responses that their ancestors required. In primitive vertebrates the brain was little more than a bundle of nerve endings at the head of the spinal cord, which acted as a sort of central switchboard for turning on and off the power needed to activate certain muscles and bodily functions in response to particular stimuli. The behavior of the animal was wholly instinctive, as indeed it had to be if the flick of the tail was to remove a fish from the danger its eye had perceived, or if the heart was to maintain a rate appropriate to the activity of the moment.
But in the mammals evolution took the function of the brain a stage further. The outer surfaces grew larger and denser, wrapping around the instinctive 'hardware' of the brainstem a layer of 'software' in which, to press the computing analogy just a little further, stimuli were processed, analysed and evaluated before instructions for action were passed on the muscles and organs of the body. This part of the brain is called the cerebral cortex (Reader, 1986).
On the northern supercontinent, probably in response to environmental circumstances, the mammals had taken the marsupial reproductive strategy a stage further. Instead of transferring their delicate and tiny young to an external pouch they retained them in the body, in the uterus, where they received nutrients and oxygen from the maternal bloodstream via a remarkable innovation called the placenta.
The important thing about parental care is not only that the infant is protected from danger but also that it is spared the business of having to find its own food, as the ancestral had to do from birth. Finding food is the basic instinctive drive, and not having to exercise it directly left the infant free to acquire and use other kinds of knowledge and experience. This brought the mammals the ability to learn, which in turn required more cerebral capacity, and still more time for the brain to grow and more parental care, with more time for learning. and so on, in a cycle of cause and effect which was to have profound effects upon the subsequent history of the mammals. One of the first results of this evolutionary development was the prompt extinction of most of the South American marsupials by placental carnivores, once the Central American landbridge afforded them access from the northern continent. None of this happened overnight; over many millions of years is a more realistic timescale (Reader, 1986).
From the fossil record it appears that for close on 140 million years the mammals were never much larger than a mouse. While the dinosaurs diversified in such spectacular style, the little mammals hardly changed at all.
The mammals were confined to the only parts of the big wide world that the dinosaurs could not reach: the nocturnal world, which lay in the dimension of time when the cold-blooded (?) dinosaurs were inactive, and the interstices of the dinosaurs' daylight world - rocky crags, forest undergrowth and holes in the ground. Here they acquired talents that not only outwitted the dinosaurs, but served to outlast them as well.
The world of the small nocturnal mammal is immensely more complex than the world of large diurnal creatures. In the first instance there is the matter of scale. The small animal's world is relatively so much larger. Climbing in and out of a dinosaur's footprint, for example, would have required the small mammals to scale heights far in excess of their own body size - something dinosaurs were rarely if ever required to do. The mammals must have been at it all the time - shinning over branches, under roots, between rocks. Such activity called for agility and a high degree of physical coordination, calling in turn for substantial and regular supplies of food, which again was affected by the matter of size. Because their metabolic rate is relatively higher, small mammals require proportionately more food than big ones do. A shrew must eat at least its own body weight each day, for example.
There was also the problem of being so agile and active in the dark, which called for a high degree of sensory perception. Eyes became relatively large, hearing more acute, vocal cords more distinctively tuned, the nose more sensitive, and whiskers brought a fine sense of touch and spatial presence. All these factors combined to give the small early mammals an awareness of their environment which demanded constant fine-tuning of the integration between cerebral and physical equipment. This is turn provided the opportunity for adaptations of a unique kind: reproductive strategies, maternal behavior, parental care, communication between individuals, learning (Reader, 1986).
An important mammalian feature, as we have seen, is the ability to generate heat and maintain a constant body temperature (endo- or homeothermy). Warm-blooded mammals could exploit and inhabit a wider range of habitats than those available to reptiles. Homeothermic mammals with their higher metabolic rate - including the ability to run fast - "swept their somnolent predecessors from the evolutionary stage" (Gribbin & Gribbin, 1993).
Mammals also have evolved different kinds of teeth specialized for different functions (heterodontism); canines and incisors for jabbing, cutting and slicing, premolars and molars for grinding. The mammalian mode of reproduction (internal fertilization, placentation and early stages of development in the mother's womb) is significant in understanding mammalian evolutionary success. The reproductive mode of one group, the placentals, allows an extensive period of prenatal development. Mammals also have fewer births per parturition, and the mammalian mother protects, nurses and nourishes the neonates by providing milk secreted by mammary glands. The developmental period among the young is extended by nursing, and the infant's longer period of attachment to its mother increases the potential period of learning behaviors necessary (or at least helpful) for survival. Also play behavior is an important means of environmental exploration, and of practicing social behaviors and communication skills, as well as physical coordination. Not surprisingly, mammals are generally more intelligent than their reptilian predecessors (Poirier, 1993).
The evolution of affiliative bonding
Eibl-Eibesfeldt (e.g., 1998: 23-25) realized that there is a basic difference in the social behavior of reptiles on the one hand and birds and mammals on the other. Reptilian social behavior is based upon dominance and submission (even their courtship behavior consists of dominance displays by the males. Females ready for copulation accept these overtures by assuming a submissive posture, lying flat on their bellies - as do defeated males). Furthermore, reptiles do not form groups bonded by individual acquaintance. They aggregate but do not discriminate between individuals on the basis of 'us' and 'others'. In contrast mammals and bird often live in pairs or even in larger groups of bonded individuals that clearly distinguish group members from others. Furthermore, in addition to patterns of dominance and submission, a rich repertory of affiliative nurturant behaviors can be observed. Comparative studies revealed that the capacity for such affiliative bonding evolved with the development of nurturant individualized care of the young, involving feeding, cleaning, warming, and defending, as well as the motivation for infant care. Conversely, the young evolved the motivation to seek protection and care, as well as signals triggering caretaking behaviors from the parents. In addition, in mother and offspring the capacity of mutual individual recognition and for individualized bonding evolved. Once present, the adaptations were available for bonding between adults. We may thus say that the evolution of nurturant individualized broodcare constitutes a turning point in the evolution of vertebrate social behavior, since it paved the way for long-lasting, truly affiliative friendly interaction and love between individuals. In humans, the capacity for individualized bonding is also familial in origin. With the distinction of 'us' versus 'others', a new quality of social behavior came into the world as well as a potential for further evolution. Members of the same species became distinguished according to their relatedness as friend or foe. Agonistic behavior is certainly old. In reptiles, rivals fight each other, the latter being mainly members of the same sex. But reptiles know only 'others', such as potential mates or rivals. The capacity to distinguish 'us' from 'others' developed in the societies of birds and mammals. This new ability found a variety of expressions in the pair-bond, the family, in human individualized groups, and even in anonymous mass societies such as nations (Eibl-Eibesfeldt, 1998: 32).
The next development of the reproductive life-cycle setup that qualitatively modified the processes of survival of the second-generation phenotype was the emergence of a parental behavioral contribution to the organic growth of the next generation genome. The morphological correlate of this development is the emergence of mammalian viviparity (Wourms & Callard, 1992), its behavioral correlate is parental protection and care of the offspring. To succeed as a reproductive strategy, viviparity must necessarily be paired with parentalcare, and, for extended parental care to be possible, the brain must have the ability to use concepts. Naccache (1999) therefore proposes that 'conceptual categorization' emerged some 200 mya, in conjunction with the emergence of viviparity [in synapsids or mammal-like reptiles: Dilkes & Reisz, 1996)] and the allometric increase in encephalization detectable in archaic mammals. Among mammals it is usually a parent, and more specifically the mother, that teaches its offspring. Without providing a distinct neuroanatomical correlate, Edelman speculates that, on the road to higher-order consciousness, 'conceptual categorization' was followed by the mergence of "new forms of symbolic memory and new systems serving social communication and transmission" (Edelman, 1992: 125). A parent needs these abilities in order to teach its offspring. Inferring back from the distribution of teaching behavior among present-day species, and from the fossil record (Northcutt & Kaas, 1995), Naccacche submits that it is the appearance of neocorticalization in the mammalian brain, with its attendant flexures and fissures, that provides the morphological underpinnings of parental teaching behavior. These 'apparently revolutionary changes' (of the Progressive Mammalian MoE) occurred during the Upper Eocene epoch some thirty million years ago in conjunction with an upward displacement of the brain to body ratio shared among many mammalian species (Jerison, 1973: 319).
Incomplete as it is, and over-interpreted as it may be, the record of the past is forceful evidence of the reality of human evolution. We descend, with all other mammals, from a rat-sized creature of a hundred and sixty million years ago whose descendants lived modest lives around the feet of the dinosaurs until those giants were wiped out. The first fossil primates are found soon after that event in the warm and wet Africa of sixty million years ago. Some six thousand kinds have lived since then (and two hundred or so remain today, from the quarter-pound mouse lemur to the gorilla, a thousand times heavier). Once, the world had many more species of apes than of monkeys, but now just five great apes are left (one of which is us) while monkeys flourish; proof that there was no inevitable progress toward mankind (Jones, 2000: 425-26).
Angiosperm forests spread across the earth during the late Cretaceous (94 to 64 mya). About 58 to 55 mya, some small, insectivorous, tree shrew-like mammal (possibly Purgatorius, looking nothing like a primate to modern eyes) climbed into the trees in search for insects. Its descendants came to rely substantially on edible plant parts from the canopy; a change that set the stage for the emergence of the primate order (Milton, 1993; see also Martin, 1992).
Natural selection strongly favors traits that enhance foraging efficiency. Hence as arboreal plant foods assumed increasing importance over evolutionary time, selection gradually gave rise to the suite of traits (mostly facilitating arboreal foraging) characteristic of the primates: physical agility, stereoscopic (3D) and color vision, enhanced depth perception and visual acuity; agile and prehensile hands and feet, adept at grasping and clutching, with opposable thumb; small number of, or single, offspring; prolongation of gestation and infancy; complexity of social behavior; behavioral flexibility, and the capacity to learn and remember the identity and locations of edible plant parts, correlated with larger brains than other same-sized mammals. Primates with relatively large brains have larger home ranges, perhaps because species with large home ranges need to remember complex information (cognitive maps) about food distribution (Harris, 1975; Harvey & Read, 1992; Milton, 1993).
Other diagnostic features of the primates include: mobile shoulder joint with rotatable arm, flat nails instead of claws, sensitive tactile pads on all digits, reduced olfactory apparatus, relatively large brain, dental formula of 126.96.36.199 (Old World monkeys and apes), among others. (Anthropologists disagree about why natural selection favored the basic features of primate morphology). Primates radiated extensively between 58-34 mya (Eocene). The Eocene epoch was even wetter and warmer than the preceding Paleocene, with great tropical forests covering much of the globe. Primate fossiles from this period have been found in both North America and Europe. It is in these Eocene primates that we see the defining features of modern primates for the first time (http://corona.eps.pitt.edu/www_GPS/courses/GEO0871/Primates/primates.html) .
The primates "kept the full variety of teeth found in the ancestral mammal forms (incisors, canines, premolars and molars) in a fairly neat all-purpose package. Finding the variety of food, making use of the good eyesight and coordinating the agile limbs in speeding through the trees all took a reasonably sophisticated nervous system, and so primates also evolved relatively large brains for their body size. Another characteristic feature, which probably evolved from the need to hold small babies safely in the treetops, is that female primates have a pair of milk glands on the chest. The whole package is, hardly surprisingly, recognizably human" (Gribbin & Gribbin, 1993).
The primates are generally regarded as an arboreal order. Yet, about a quarter of all primate species has become terrestrial again, especially species belonging to the most recently evolved group of the catarrhines (the Old World monkeys) and apes (Foley, 1987).
While other branches of the mammalian line had found their niches on the ground, some tiny insectivorous furry creatures took to the trees and adopted an arboreal way of life. The trees of the tropical forests offered a rich and varied diet - leaves, buds, fruit, insects, birds' eggs and nestlings - but they placed unusual demands upon their earliest mammalian occupants. The animals had to be agile and strong, but more important than the physical demands were the mental requirements. Life in the trees called for a shift in the emphasis of environmental awareness, and an unprecedented degree of sensory and physical coordination. Although the nose had probably been the most useful sensory organ of the early ground-dwelling mammals, sniffing out food and giving advance warning of approaching enemies, in the trees the eyes were much more important. Because a tree is a restricted and potentially dangerous environment, an arboreal animal must know if the enemy is in the same tree, or the fruit at the end of a safe branch. It must be able to see very clearly and judge distances very accurately as it moves about through the branches. Inadequate vision could be fatal, so among the arboreal mammals of the Paleocene natural selection must have quite quickly sorted out the species in which the eyes had tended to look forwards rather than sideways, integrating the two fields of vision to give a stereoscopic image of the surroundings, with perhaps even the first tints of color.
Life in the branches also demanded a special kind of agility. The ability to flex the paws and grasp things evolved. The front limbs became the principal means of holding while the rear limbs became more the means of propulsion and static support. Thus the animals became able to sit with the back erect, the head turning with a perceptive eye, the ears twitching. Sounds, differentiated between species and among individuals, became increasingly important.
All these things - vision, agility, communication - called for yet more cerebral development. A larger brain relative to body size evolved; a larger brain needed more room and some restructuring of the skull began. This in turn was affected by the kinds of food the animals were eating: fruit, leaves, insects and meat. An omnivorous diet requires neither the specialized canines and slicers of the carnivores, nor the grinding molars of the herbivores. A neat set of general all-purpose teeth would do. The jaws broadened and shortened, the face became longer, the eyes moved to the front and the expanding brain took up more and more of the room at the back of the skull: an interactive and interdependent suite of features evolving through millions of years and eventually producing the order of mammals known as primates.
Basically, the primates are distinguished from all other placental mammals by the fact that they have retained the four kinds of teeth found in the ancestral mammals (incisors, canines, premolars and molars); they can hold things between their fingers and thumbs; and they have two mammary glands on the chest, frontally directed eyes and a relatively large brain. They evolved from the ancestral mammals about 70 mya and are represented on Earth today by 193 living species, of which all except one are covered with hair (Reader, 1986).
From its beginnings in the dense forests of tropical Africa, which then still lay at the core of the supercontinent, Gondwanaland, the primate line split about 45 mya into two groups - the prosimians (lower primates) and the anthropoids (higher primates). Time and natural migration spread these groups throughout the continental forests and some, such as the lemurs of Madagascar, were isolated as the continents drifted apart.
When South America broke away from Gondwanaland the new continent carried with it into isolation a branch of the lower primates known in terms of their location as the New World monkeys and, more formally, in terms of their physiognomy as the platyrrhines - flat-nosed - in acknowledgement of their flat, wide faces.
The higher primates as a group are called the catarrhines - thin-nosed - acknowledging their thin, long faces, and soon after the isolation of the lower primates they split into two main groups, probably along the lines of diverging dietary requirements. One group adopted an herbivorous diet while the other retained more omnivorous habits. The first gave rise to the evolutionary line known as the Old World monkeys, whose living representatives includes the baboons and the rhesus monkeys; the other group produced the hominoids, which are easily (if superficially) distinguished from all other primates by their lack of a tail and are represented today by the gibbons, the orang-utan, the gorilla, the chimpanzee - and man (Reader, 1986).
For many years systematists classified the plesiadapiforms within the primate order. But most paleontologists now believe that the plesiadapiforms were a separate, but related, groups of organisms (Boyd & Silk, 1997); Dunbar & Barrett (2001) regard the plesiadapids as ancestral to the primates.
Plesiadapis was a little larger than a squirrel and had the strong dependence on vision and the flexible wrists and ankles typical of modern primates. However, Plesiadapis also had some unusual features which make it unlikely to have been a direct ancestor of the modern primates, including, of course, ourselves.
The Eocene primates are classified into two families, Omomyidae and Adapidae, both of which resembled modern prosimians. The omomyids were similar to modern tarsiers. They had huge orbits, sharp shearing teeth, and long, grasping hands - features that suggest they were arboreal insectivores who hunted at night. The absence of sexual dimorphism suggests they were solitary or lived in monogamous pairs. The adapids (55-40 mya) were more like contemporary lemurs. They had smaller orbits and more generalized dentition, suggesting they were diurnal herbivores. At least one species showed substantial sexual dimorphism, a feature that points to life in nonmonogamous social groups. Paleontologists are uncertain whether the modern anthropoids evolved from the omomyids or the adapids (Boyd & Silk, 1997); Dunbar & Barrett (2001) regard the adapids as ancestral to the primates.
Ross, Williams & Kay (1998), and Ross (2000) recently found support for the tarsier-anthropoid clade nested within omomyids, which unites Tarsius, Anthropoidea and Omomyiformes within a clade, Haplorhini. Anthropoidea is a clade of primates including Platyrrhini and Catarrhini. The early anthropoids were insectivore-frugivores with unfused mandibular symphyses, small brains, and either dichromatic or trichromatic vision. The evolution of larger brains, symphyseal fusion, and definitive trichromacy occurred (much) later in anthropoid evolution. Definitive fossil anthropoids include the early Oligocene Propliopithecidae and the late Eocene-early Oligocene Parapithecidae and Oligopithecidae. Middle Eocene Eosimiidae are probably fossil anthropoids from Asia (Ross, 2000).
Recent fossil discoveries, phylogenetic analyses, revised reconstructions of continental drift, and accumulating molecular evidence have all yielded new information relating to anthropoid origins within the broader context of primate evolution. There is an emerging consensus among molecular studies that four superorders of eutherian mammals can be recognized: Afrotheria, Euarchontoglires (to which primates belong), Laurasiatheria, and Xenarthra. Overall, molecular phylogenies for mammals agree with some statistical analyses of the primate fossil record in indicating an early origin for primates around 85 Mya ago, and the divergence of haplorhines and strepsirrhines at ca. 77 Mya. Such an ancient date for the origin of haplorhines is some 17 Mya prior to the first known possible primate, and some 22 Mya before the earliest fossil evidence of undoubted euprimates. Because anthropoid fossils date back at least to the late Eocene and perhaps to the middle Eocene, and given indications of an early origin for primates, it is unlikely that ancestral anthropoids arose within any other currently known clade of fossil primates (adapiforms, omomyiforms, strepsirrhines, or tarsiiforms). Current evidence best supports a relatively ancient Gondwanan origin for primates, as well as a Gondwanan (African or Indo-Madagascan) origin for anthropoids at least as old as that of any other currently documented major primate clade. Available fossil evidence at present seems to be most compatible with the African hypothesis, but it is noteworthy that primates are included not in Afrotheria but in Euarchontoglires (Miller, Gunnell & Martin, 2005).
Primates similar to modern monkeys first appear in the fossil record at the Eocene-Oligocene boundary (36 to 33 mya). The dental pattern of the early Fayum deposit site (in Egypt) monkeys was the same as that of modern Old World monkeys and apes (188.8.131.52), and different from that of contemporary New World monkeys (184.108.40.206). This suggests that the lineage leading to the New World monkeys had already diverged from the lineage leading to Old World monkeys and apes.
Primates appear in South America for the first time during the Oligocene (beginning 34 mya), but the origin of these primates is a mystery (South America separated from Africa more than 100 mya) (Boyd & Silk, 1997).
The Old World monkeys split from the apes in the early Oligocene, about the time of Aegypthopithecus (about 23 mya).
The later Fayum fossils are divided into two groups, propliopithecoids and parapithecoids. The largest of the propliopithecoids is named Aegyptopithecus zeuxis, a medium-sized monkey, perhaps as big as a female howler monkey (6 kg, or 13.2 lb). It was a diurnal, arboreal quadruped with a relatively small brain. The shape and size of the teeth suggest that it ate mainly fruit. Males were much larger than females, which indicates that they probably lived in nonmonogamous social groups. It is possible that modern monkeys and apes are derived from members of this family (Boyd & Silk, 1997).
The true origins of the Anthropoidea remain obscure. Among the earliest fossil anthropoid primates known are Catopithecus browni, Serapia eocaena, Arsinoea kallimos, and Proteopithecus sylviae, from the late Eocene quarry L-41, Fayum Depression, Egypt. Two of these taxa, C. browni and S. eocaena, may be the oldest known members of the Propliopithecidae and Parapithecidae.
The Asian primates Pondaungia, Amphipithecus, and Siamopithecus are not likely ancestors for African anthropoids (Gunnell & Miller, 2001).
The Miocene epoch began approximately 25 mya and ended 5 mya. It began as warm and moist but ended much cooler and more arid.
The first hominoid apes did not evolve until the Miocene epoch. These early apes, known collectively as dryopiths, were all forest dwellers who spent most of their time in the trees and ate mostly fruit. The Miocene climate was warmer than that of the present day and tropical forests were much more widespread, so the dryopiths were able to spread over a wide area of Africa and Eurasia (Haywood, 1995: 15).
The oldest hominoids are members of the genus Proconsul. This genus includes five species (the best-known being Proconsul africanus [early Miocene], a sexually dimorphic, fruit-eating, arboreal quadruped which was probably ancestral to all the later apes and humans) ranging from the size of a macaque (10 kg, or 22 lb) to at least the size of a bonobo (38 kg, or 84 lb). The earliest fossils were found at the Fayum Depression in Egypt (in honor of this it is known as Aegyptopithecus), and at Losidok in northern Kenya, date to about 27 or 28 mya, during the late Oligocene. A number of other species of hominoids lived in Africa during the late Oligocene and early Miocene. Peter Andrews of the British Natural History Museum classifies all these creatures as proconsulids. The middle Miocene epoch (15-10 mya) saw a new radiation of hominoids and the expansion of hominoids throughout much of Eurasia (well-known examples include Kenyapithecus, Oreopithecus, Dryopithecus, Afropithecus, Nyanzapithecus, Equatorius africanus, and Sivapithecus).
The evolutionary history of the apes of the Miocene is poorly understood. There were many different species, and the phylogenetic relationships among them remain largely a mystery. We have no clear candidates for the ancestors of any modern apes, except for the orangutan, which shares a number of derived skull features with Sivapithecus of the middle Miocene.
We know that at least one ape species survived the environmental changes that occurred during the late Miocene because molecular genetics tells us that humans, gorillas, bonobos, and chimpanzees are all descended from a common ancestor that lived sometime between 5 and 7 mya (Boyd & Silk, 1997).
The non-gibbon apes divided into two lines: Sivapithecus, which moved to Asia and gave rise to the orangutan, and Kenyapithecus (about 16 mya), which stayed in Africa and subsequently gave rise to the African great apes and humans (Haywood, 1995).
Under the microscope, the most striking and obvious difference between ourselves and all the other great apes is that we have one pair of chromosomes less. The reason, it immediately becomes apparent, is not that a pair of ape chromosomes has gone missing in us, but that two ape chromosomes have fused together in us. Chromosome 2, the second biggest of the human chromosomes, is in fact formed from the fusion of two medium-sized ape chromosomes, as can be seen from the pattern of black bands on the respective chromosomes (Ridley, 1999: 24).
Whatever the mechanism, we can guess that our ancestors were a small, isolated band, while those of the chimpanzees were the main race. We can guess this because we know from the genes that human beings went through a much tighter genetic bottleneck (i.e., a small population size) than chimpanzees ever did: there is much less random variability in the human genome than the chimp genome.
So let us picture this isolated group of animals on an island, real or virtual. Becoming inbred, flirting with extinction, exposed to the force of the genetic founder effect (by which small populations can have large genetic changes thanks to chance) (See footnote 6) 6 , this little band of apes shares a large mutation: two of their chromosomes have become fused. Henceforth they can breed only with their own kind, even when the 'island' rejoins the 'mainland'. Hybrids between them and their mainland cousins are infertile (Ridley, 1999: 31).
The primates, cetaceans, and proboscids underwent a further upward deviation on top of the basic mammalian shift, that is, that at every growth stage they display a regularly higher ratio of brain to body size than do other mammals (Deacon, 1997). This increase was part of a larger trend toward slower maturation and greater longevity, linked to a larger body size, enhanced learning and sociality, and increased parental investment (Smith & Tompkins, 1995). Social communication among members of a species had existed for eons. However, slower maturation and greater longevity enabled and propelled an increase in intergenerational interaction. This development, which, on the basis of the evidence at hand, took place only among some families of elephants (Mackenzie, 1999), whales (Reiss, 1998; Whitehead, 1998) and hominoids, led to a radical extension of the 'pre-human language' communication system. It can carry emotional, behavioral, and/or cognitive information over a much longer time span than an individual life, and across great social distances, giving rise to what is conservatorily referred to as culture (e.g., Boesch & Tomasello, 1998; Whiten et al., 1999). Its intrinsic development is 'Lamarckian' (or rather 'Spencerian' [Ruse, 1986: 125]) (Naccache, 1999: 19-22). Great apes of six million years ago had the neural prerequisite to use their shared prelinguistic 'grammar' of action to intentionally communicate information through voluntary oro-facial or gestural signals (Rizzolatti & Arbib, 1998; Worden, 1998; see also Aboitiz & García, 1997). Prior to the emergence of this extension in communication, behavioral phenotypes had remained bound to one organism. With it, temporally and geographically distant members of a social group could affect, through phenotypical traits they had acquired, the life-cycle setup between any parent and offspring in the group (Boesch & Tomasello, 1998). We refer to this extension as 'social memory', a more descriptive term than 'culture'. and propose to call the MoE to which it gave rise the 'sociocultural MoE'. A comparison of the proboscids' and hominoids' phylogenetic trees places the onset of the sociocultural MoE sometimes before six million years ago, the time of the last pongid and hominid common ancestor. Its neuroanatomic correlate would be, among the hominoids, the increase in brain size displayed by the great apes over that of the baboons (Jerison, 1973: 394) (Naccache, 1999: 22-23).
The word 'hominid' (Hominidae) refers to members of the family of humans; hominids are included in the superfamily of all apes, the Hominoidea (J.Foley, 1997, 2004). Some scientists prefer to use the term 'hominin' (from 'homininae' a kind of subfamily) for the group which will be discussed below.
R.Foley (1995; 1996) proposes a "phylogenetic and chronological context for human social evolution" that identifies the eight "key 'events' and time periods":
1. 35 million years (35 Myr): the anthropoids and the origins of society;
2. 25 Myr: finite social space and kinship as the basis for social organization;
3. 15 Myr: catarrhine social phylogeny and the evolution of male kin-bonding;
4. 5 Myr: savanna socioecology;
5. 2 Myr: expensive offspring and the socioecological basis of encephalization;
6. 300,000 (300 Kyr): the 1000 gram brain and evolution of human life history strategy;
7. 100 Kyr: dispersal, group size, and territoriality;
8. 30 Kyr: demography and the agricultural revolution.
There are two current hypotheses about human origins and the early stages of hominid evolution, According to the linear (or scalar) or 'tidy' model, the distinctive hominid anatomy evolved only once, and was followed by a ladder-like ancestor-descendant series. In this model there is no branching (cladogenesis) until well after 3 million years ago. The bushy, or 'untidy' model sees hominid evolution as a series of successive adaptive radiations - evolutionary diversification in response to new or changed circumstances - in which anatomical features are 'mixed and matched' in ways that we are only beginning to comprehend. This model predicts that because of the independent acquisition of similar shared characters (homoplasy), key hominid adaptations such as bipedalism, manual dexterity and a large brain are likely to have evolved more than once (Collard & Wood, 2000; Wood, 2002).
The evolution of man, as distinct from all other kinds of vertebrate animals, began with the establishment of the hominoid lineage between 20 and 30 mya. A shadowy beginning in the ancient African rain forests, but thereafter illuminated from time to time by evidence from the fossil record.
From the sands of Fayum, just south east of Cairo, where 30 million years earlier dense tropical rain forests lined the banks of broad meandering rivers, fossil hunters over the years since 1961 have recovered the fossil remains of a creature known to science as Aegyptopithecus zeuxis, but more colloquially dubbed the 'dawn ape': a small arboreal primate, about the size of a domestic cat, with a supple, sinuous back and long limbs, all four feet capable of both grasping branches and conveying food to the mouth. In all probability they were also sexually dimorphic: male canines were appreciably larger than females ones, and more suited to threatening and aggressive behavior than to the mere consumption of food.
The next link in the hominoid chain was found three and a half thousand kilometers to the south, in early Miocene deposits on Rusinga Island, near the Kenyan shores of Lake Victoria: Proconsul africanus. It was a tree-dwelling, fruit-eating primate about the size of a baboon, unspecialized, with the backbone of a gibbon, the shoulder and elbow joints of a chimpanzee and the wrists of a monkey; quite unlike any of the living apes in its overall configuration, but a likely ancestor of them all, and of man too.
When the African continental plate butted against Europe during the Miocene, about 17 mya, the event not only raised high mountains around the buckling edges of the plate, it also created a new landbridge between Africa and Eurasia. The climate was distinctly seasonal now; grasslands were spreading but woodland and forest were still a substantial part of the landscape.
The landbridge granted the African mammals access to Asia and Europe, and here the fossil record affords some more tantalizing glimpses of hominoid evolution. In Greece, fossil hunters of a fossil ape in deposits that were otherwise filled with the fossil impressions of ancient oak leaves and called it Dryopithecus - the oak ape. In the Siwalik Hills of northern India other expeditions found fossils of another slightly (and supposedly) more ape-like creature that they named Ramapithecus, and then another that they named Sivapithecus.
The consensus view now is that the ramapithecine and sivapithecine fossils probably represent ancestors of the orang-utan on its evolutionary and migratory journey that has led to the animals still living on isolated islands in South-east Asia, while the dryopithecines were probably close cousins headed only for extinction.
Then there is a gap of more than 16 million years. A long, long blank in which crucial developments and adaptations occurrred, leaving few clues as to their precise timing.
The only near certainty is that these critical stages of human evolution occurred in Africa. Sometime after Proconsul the hominoid line split into the pongids, which subsequently became the gorilla and chimpanzee, and the hominids, which led to man (Reader, 1986).
According to Verhaegen, McPhail & Munro (1999), in the period of 12 to 8 mya, the great apes that had pongid and/or hominid features, such as Dryopithecus, Graecopithecus, Ankarapithecus and Sivapithecus, lived in Europe, Anatolia and India (e.g., Andrews, 1995, Algaput et al., 1996). This suggests Asian pongids and African hominids may have split somewhere near the Middle East (Stewart & Disotell 1998).
A cladogram based upon several different molecules shows that humans are more closely related to chimpanzees than they are to gorillas, and all three may be more closely related one to another than to Pongo, the orang-utan. But maybe all the apes - and man - should be placed together in the same zoological family, since they descended from a common ancestor (Fortey, 1998). Diamond (1991) suggested in his book The Third Chimpanzee to call humans a third chimpanzee species.
Molecular biology, biochemistry and cytogenetics suggest that humans and pongids (the great apes) are close relatives. Wrangham (1987) used the method of phylogenetic comparison to identify possible conservative features in social organization of humans and the African apes in an attempt to characterize the hominid-pongid common ancestor. According to this approach, shared features of social organization among humans, chimpanzees, bonobos, and gorillas are likely to have been present in the common ancestor, and can be viewed as part of an 'ancestral suite' of behaviors likely to have characterized hominids (and pongids) at any point in their evolutionary history. From the correspondences in the behavioral repertoires of these species, Wrangham (1987; Wrangham & Peterson, 1996) concluded that the last hominid-pongid common ancestor probably had closed social networks (i.e., some degree of ethnocentrism and xenophobia), hostile and male-dominated intergroup relationships with stalk-and-attack interactions (i.e., male coalitional psychology and lethal male raiding), female exogamy and a lack of alliance bonds between females, and males having sexual relationships with more than one female (i.e., polygyny). Wrangham considered territoriality to be too labile a trait (depending on ecological conditions) to reliably attribute it to the common ancestor.
If this reconstruction of the hominid-pongid common ancestor is correct, it would mean that lethal male raiding, warfare, is at least five million years old. The 'battle' type of warfare, as exemplified by chance encounters of monkey groups, may even be much older.
There were major climatic fluctuations during these times, ranging from hot and dry to wet and very cold. The tropical forests retreated to their equatorial origin, woodlands became dominant and grasslands advanced. And with the vegetation changes animal populations changed too. Many species died out, particularly browsers, and grazers became more numerous. From some small and perhaps insignificant niche among the trees the human ancestor emerged. The fossil record takes up the story again between 3 and 4 million years ago with a creature named Australopithecus - the southern ape - originally described by Raymond Dart in 1925.
Already Kortlandt (1972) hypothesized that "nothing seems more plausible than the assumption that the Australopithecines evolved from a member of the Dryopithecine stock [Proconsul] located east of the Nile-Zambezi barriers [after the tectonic formation of the East-African Rift Valley system], during the time epoch of the fossil black-out from 14 to 5 million years ago. This would explain both the absence of apes and the presence of hominins during the last 5 million years in that subcontinent, which otherwise is so rich both in fossils of the past and wildlife of the present. It also explains why the African apes and man, according to biochemical and behavioral evidence, apparently belong to the same family, the Hominidae".
The shared derived characteristics (synapomorphisms) that distinguish modern humans from other living hominoids are bipedal locomotion, a larger brain, and several features of dental morphology (e.g., reduced canines, parabolic dental arcade [(the dental arcades of apes are shaped more like three sides of a rectangle), and thicker enamel]). Australopithecus afarensis was one of the the earliest hominids, and sexually dimorphic in body size (Boyd & Silk, 1997).
A. ramidus, found by Tim White's team in Ethiopia in 1992, and named in 1994 (White et al., 1994; Wood, 1994) and originally dated to 4.4 mya, but since then discovered to go as far back as 5.8 mya, may be the common ancestor of humans and chimpanzees. It is interesting that Ardipithecus ramidus appears to have lived in a more forested environment than Australopithecus afarensis or A. anamensis (Boyd & Silk, 1997; White et al., 1994, 1995).
A. ramidus was considered until recently to be the oldest known hominid species. Most remains are skull fragments. Indirect evidence suggests that is was possibly bipedal, and that some individuals were about 122 cm (4'0") tall. Other fossils found with A. ramidus indicate that it may have been a forest dweller. This may cause modification of current theories about why hominids became bipedal, which often link bipedalism with a move to a savannah environment (J.Foley, 1997). Recently, Haile-Selassie (2001) assigned a number of fragmentary fossils, dating from 5.2 to 5.8 million years old, to a new subspecies, Ardipithecus ramidus kadabba (J.Foley, 2001) and then later to a new species Ardipithecus kadabba (Haile-Selassie et al., 2004; J. Foley, 2004)).
A French-Kenyan team has found a fossil claimed to be both considerably older than any other hominid (at 6 million years) and more advanced than the australopithecines. The limb bones are about 1.5 times larger than those of Lucy, and suggest that it was about the size of a female chimpanzee. Its finders have claimed that Orrorin was a human ancestor adapted to both bipedality and tree climbing. The fossil, originally nicknamed 'Millennium Man', has been named Orrorin tugenensis, and is claimed to be a direct ancestor of humans, relegating the australopithecines to a side branch (Senut et al., 2001). These claims are being treated with caution so far (Aiello & Collard, 2001) (J.Foley, 2001, 2004).
An even older hominid may have been discovered by Michel Brunet and his team in Chad (Toros-Menalla). The fossils - the cranium, a jaw fragment and several teeth - allegedly belong to a primitive hominid - affectionaly known as Toumaï - that is an astonishing 6-7 million years old (Brunet et al., 2002; Wood, 2002). Brunet et al. (2002) compared their new evidence with what has been published about two other claimants for the title of 'earliest hominid', Ardipithecus ramidus from the Middle Awash and Orrorin tugenensis from Lukeino. They satisfied themselves that the teeth of the new fossils are taxonomically distinctive, and accordingly assigned the fossils to a new species and genus, Sahelanthropus tchadensis.
What is remarkable about the chimp-sized cranium TM 266-01-060-1 (of approximately 350 cc) discovered by Brunet et al. is its mosaic nature. Put simply, from the back it looks like a chimpanzee, whereas from the front it could pass for a 1.75-million-year-old advanced australopith. The hominid features involve the structure of the face, and the small, apically worn, canine crowns. Other hominid features are found in the base of the cranium and in the separate jaw fragment. If we accept these as sufficient evidence to classify S. tchadensis as a hominid at the base, or stem, of the modern human clade, then it plays havoc with the 'tidy' model of human origins. Quite simply, a hominid of this age should only just be beginning to show signs of being a hominid (Wood, 2002).
Not everybody, however, is convinced that the specimen is indeed a hominid. Wolpoff and Brigitte Senut, among others, are convinced that the cranium belonged to a young female gorilla.
A. anamensis (named after the Turkana name for 'lake', and dated to between 3.9 and 4.2 mya, about half a million years older than A. afarensis) was bipedal but had a more apelike skull than later australopithecines. Fossils of other animals found at Kanapoi and Allia Bay suggest that A. anamensis lived in a mixture of habitats including dry woodlands, gallery forests lining rivers, and more open grasslands (Boyd & Silk, 1997; Leakey et al., 1995).
A. anamensis has a mixture of primitive features in the skull, and advanced features in the body. A partial tibia (the larger of the two lower leg bones) is strong evidence of bipedality (J.Foley, 1997).
In March 2001, a team of paleoanthropologists, among whom Meave Leakey (Leakey et al., 2001), discovered a 3 to 3.6 million-year-old hominid in Kenya which was baptized Kenyanthropus platyops ('platyops' refers to its orthognatism or flat face) (J.Foley, 2001). The partial skull has an unusual mixture of features.
Australopithecus garhi has been named from fossils found near Bouri in Ehiopia. This small-brained, large-toothed hominid was found near antelope bones which had been butchered by stone tools (Asfaw et al., 1999; J.Foley, 2001).
In 1999 (Suplee, Washington Post on Internet April 23), beside the Awash River in Ethiopia, the partial remains of a previously unknown 2.5 million-year-old creature were uncovered that might well have been the immediate predecessor of contemporary human beings. Also found was what appears to be the earliest known evidence of ancient hominids using stone tools to butcher animal carcasses and prepare meat. The presumptive new species, which the discoverers named Australopithecus garhi (from the local word of 'surprise'), has a projecting face like Lucy's (A. afarensis), a small brain case about one-third the size of modern humans, and large front teeth. It also has massive back teeth that are different in form from those of the later robust forms of Australopithecus, which had huge, powerful molars for chewing tough vegetation. That combination fits neither A. afarensis nor A. africanus.
Moreover, arm and leg bones found nearby - which may or may not be from the same species - suggest that the area's hominids had a transitional body plan. The upper leg bones of the 4½-foot-tall individual are relatively long, as in modern humans; but the forearms are proportionately much longer than ours, resembling those of today's apes or early Australopithecus species that were adept at swinging from tree branches.
The Afar hominids (Australopithecus afarensis), among whom was a half-skeleton of a young female affectionately known as Lucy, date from between three and four million years ago. None was more than 125 centimeters tall and each individual must have weighed between 25 and 50 kilograms; slight figures indeed in the ancient landscape, although adult males, it appears, may have between 50 and 100 per cent larger than adult females (a condition known as sexual dimorphism). The fossils suggest that the brain was about the size of an ape's brain, the hands were capable of a powerful grasp and the hip, knee and ankle joints of Lucy and her companions leave no doubt that they walked with the habitual striding bipedal gait of modern man. Their pelvis and leg bones far more closely resemble those of modern man.
No recognizably fashioned tools have been found at Laetoli or Afar, but this does not mean that the hominids of the day had not already crossed the first threshold of reason and were unable to identify problems and the means of solving them. They were probably using sticks and stones and other items quite habitually as the casually acquired implements of everyday life, and such things are not likely to have been preserved as recognizable tools.
The environment of Australopithicus afarensis at Hadar consisted of a fluctuating mosaic of riverine gallery forests and more open savanna habitats, and it presumably moved through both (the arid grassland environment in which the Laetoli hominids left their tracks was almost certainly not typical of where they found the bulk of their sustenance). What's more, though robust, A. afarensis was small-bodied and, being bipedal, it wasn't very fast. Presumably, then, this hominid was pretty vulnerable to open-country predators, and as a reasonably accomplished climber it would hardly have refrained from using trees for shelter, particularly at night (Tattersall, 1995: 155-6).
A. afarensis had an apelike face with a low forehead, a bony ridge over the eyes, a flat nose, and no chin. They had protruding jaws with large back teeth. Cranial capacity varied from about 375 to 500 cc. The skull is similar to that of a chimpanzee, except for the more humanlike teeth. The shape of the jaw is between the rectangular shape of apes and the parabolic shape of humans (J.Foley, 1997).
The 'robust' australopithecines
A. afarensis became extinct about 3 mya and was replaced by two types of australopithecine: a 'gracile' form, Australopithecus africanus, and a number of 'robust' forms (Australopithecus aethiopicus, A. robustus and A. boisei) (the oldest A. boisi fossils are dated 2.1 mya). The terms 'gracile' and 'robust' refer not to body size but to their teeth and jaws which are thought to be signs of dietary specialization. The robust australopithecines had massive jaws and large molars, suitable for grinding tough plant foods (Haywood, 1995: 24).
Many people are now using the genus name Parantropus, originally given to robustus, to refer to the robust australopithecines (robustus, boisei, and aethiopicus). This change makes sense if all these species form a clade (all of the species descended from a common ancestor) but it is not yet known if this is the case (J.Foley, 2001).
The robust australopithecines seem to have existed alongside their more gracile cousins successfully enough for a million years or more, but then they disappear from the fossil record without trace. Extinction is presumed to have been their fate, though why they should have become extinct remains a matter of debate. Their disappearance roughly coincides with the proliferation of Homo habilis and stone tool manufacture (Reader, 1986).
A. africanus existed between 3 and 2 mya. It is similar to afarensis, and was also bipedal, but body size was slightly greater. Brain size may also have been slightly larger, ranging between 420 and 500 cc. Although the teeth and jaws of africanus are much larger than those of humans, they are far more similar to human teeth than those of apes. The shape of the jaw is now fully parabolic, like that of humans, and the size of the canine teeth is further reduced compared to afarensis (J.Foley, 1997).
Australopithecines have also been found in an apparently wooded area in Chad (Brunet et al., 1995), later to be called Australopithecus bahrelghazali.
It has been suggested that the Australopithecus-Homo transition - the AH-Erlebnis as Slurink (2002) humoristically calls it - was essentially a herbivore-carnivore transition (e.g., Stanley, 1996).
Fossils of early Homo, a hominid with a larger brain and more humanlike teeth, have been discovered at many sites in East Africa. In 1960, while working at Olduvai Gorge with his parents, Louis and Mary Leakey, Jonathan Leakey found pieces of a hominid jaw, cranium, and hand. The Leakeys assigned this specimen, labeled Olduvai Hominid 7 (OH 7), to the genus Homo. Louis Leakey named the species Homo habilis, or 'handy man', because he believed he had found the hominid responsible for the simple, flaked stone tools discovered nearby [collectively referred to as the Oldowan tool industry] (Boyd & Silk, 1997).
H. habilis existed between 2.4 and 1.5 mya. It is very similar to australopithecines in many ways. The face is still primitive, but is projects less than in A. africanus (trend from prognathism to orthognathism). The average brain size, at 650 cc, is considerably larger than in australopithecines. Brain size varies between 500 and 800 cc, overlapping the australopithecines at the low end and H. erectus at the high end. The brain shape is also more humanlike. The bulge of Broca's area, essential for speech, is visible in one habilis brain cast, and indicates it was probably capable of rudimentary speech. H. habilis is thought to have been about 127 cm (5'0") tall, and about 45 kg (100 lb) in weight, although females may have been smaller (J.Foley, 1997).
The advent of H. habilis and stone tool manufacture coincides with the first evidence that the early hominids might have established occasional home bases in their cycle of nomadic wanderings.
The infants of large-brained adults must be born before their heads are too big to pass through the birth canal, even though they are hardly ready for it by that time, and early birth demands an extended period of parental care after birth. In theory, a secure home base and the division of labor between male and female along modern lines might thus have made some sense already at the habilis stage of human evolution (Reader, 1986).
There has been a great deal of controversy over the way of life of this earliest human. Some have seen H. habilis as a quite sophisticated hunter-gatherer bringing food back to semi-permanent home bases or 'living floors' and perhaps even building shelters or wind breaks. The predominant view, however, sees H. habilis as being much less human in its behavior, scavenging meat and bones from predator kills, sleeping in trees like modern baboons, and relying more on muscle power than tool use (H. habilis was at least as strong as an adult chimpanzee which is capable of tearing off a human's arm).
Those who support the 'scavenging hypothesis' argue that H. habilis would not have needed to have been an active hunter to include meat in its diet. The East African savannah supports vast herds of herbivores, some of which die of natural causes and many more of which are killed by predators like lions. After the predators have eaten their fill there is usually plenty left over for scavengers like hyenas and wild dogs but, despite their powerful jaws, they would have had difficulty getting at the brains and the nutritious marrow in the long leg bones. By using its simple tools to break open skulls and leg bones, H. habilis could exploit a food source for which there was effectively no competition. If H. habilis was lucky enough to reach a carcass before the hyenas, it could use its tools to cut throught the toughest hide and slice meat off the bones quickly and carry it away to be eaten in the safety of a tree. Simple though they were, modern experiments have shown that Oldowan tools are quite adequate even to butcher an elephant (Haywood, 1995: 26-27).
Fossils traditionally assigned to H. habilis are quite variable. As a result, some anthropologists believe there were two species of early Homo. Some believe that the pronounced difference in size among specimens assigned to H. habilis could represent sexual dimorphism within a single species. Others believe that there were two species of relatively large-brained hominid present in East Africa 2 mya. They believe that the small-brained, less-robust individuals should be classified as H. habilis while the large-brained, more robust ones with more modern postcrania are a second species of early Homo that should be named Homo rudolfensis [after Lake Rudolf, the former name of Lake Turkana] (Boyd & Silk, 1997).
Homo habilis is a controversial species, with much diagreement over which specimens belong in habilis, and which do not. A number of scientists now use the name H. rudolfensis to refer to ER 1470 and some similar fossils. The smaller habilis-like specimens such as ER 1813 and ER 1805 are variously assigned to H. habilis, H. ergaster, or to another as yet unnamed species. The name H. microcranous has been proposed for ER 1813, but does not seem to be widely used. Wood & Collard (1999) have argued on theoretical grounds that H. habilis and H. rudolfensis should be moved into the genus Australopithecus (J.Foley, 2001).
H. erectus existed between 1.8 million and 300,000 years ago. Like habilis, the face has protruding jaws with large molars, no chin, thick brow ridges, and a long low skull, with a brain size varying between 750 and 1225 cc. Early erectus specimens average about 900 cc, while late ones have an average of about 1100 cc. Some Asian erectus skulls have a sagittal crest. The skeleton is more robust than those of modern humans, implying greater strength. Body proportions vary; the 'Turkana Boy' is tall and slender, like modern humans from the same area, while the few limb bones found of 'Peking Man' indicate a shorter, sturdier build. There is evidence that erectus probably used fire, and their stone tools are more sophisticated than those of habilis (J.Foley, 1997).
The pelvis of female H. erectus indicates that the ratio of the size of the mother's birth canal to the size of the newborn head was the same in H.erectus as it is for modern humans. If true, then young H. erectus would have matured slowly and been dependent on their mothers for an extended period of time, much as modern children are.
Prolonged dependence of infants and the reduction of sexual dimorphism may be linked. Females may have had difficulty providing food for themselves and their dependent young. If H. erectus hunted regularly, males might have been able to provide high-quality food for their mates and offspring. Monogamy would have increased the males' confidence in paternity and favored paternal investment. Females might have shared plant foods with their mates as a means of reciprocation.
H. erectus was much less sexually dimorphic than previous hominids were. H. erectus males were only 20% to 30% larger than females. This in turn suggests there was less competition among males for access to females, perhaps as a result of a shift toward a monogamous mating system with substantial paternal investment in offspring (Boyd & Silk, 1997).
"It seems certain that loss of oestrus, by liberating the female from the frenzy of the rut, allowed her to persist in the careful maternity which her slow-maturing, large-brained offspring needed to grow to adulthood" (Keegan, 1993: 116).
Some scientists have also proposed splitting Homo erectus. The Turkana (or Nariokotome) Boy and ER 3733 fossils would then become Homo ergaster (Tattersall, 1993). H. erectus would have a larger average brain size than ergaster, and the brow ridges may have a different shape, flaring out to the side more (Burenhult, 1993).
It has also been proposed that the names Homo heidelbergensis and Homo neanderthalensis should be restored as species names for archaic Homo sapiens and the Neandertals. Recent claims of genetic and anatomical differences between modern humans and Neandertals have added support to a species status for Homo neanderthalensis (Krings et al., 1997; Hublin et al., 1996; Tattersall & Schwartz, 1996) (J.Foley, 2001).
A new startling find of an unknown hominin was described by Brown et al. (2004), Morwood et al. (2004), and Lahr & Foley (2004). It is of a pygmy-sized, small-brained hominin, which lived as recently as 18,000 years ago, and which was found on the island of Flores (Indonesia) together with stone tools, dwarf elephants and Komodo dragons. The Flores fossils add a new and surprising twig to the hominin family tree. Its most remarkable features are its diminutive body (about a meter in height) and brain size (at 380 cm3, the smallest of any known hominin. Homo floresiensis is believed to be a long-term, isolated descendant of Javanese H. erectus, but it could be a recent divergence. Island dwarfism (or insular dwarfism) is well known among mammals. Released from predation pressure or constrained by restricted resources, and limited by population size, the phenomenon can be dramatic. H. floresiensis is clear evidence that, in spite of their 'cultural niche', hominins were subject to the same evolutionary rules as other widespread mammals, with local isolation and small population sizes producing differentiation in size and form (Lahr & Foley, 2004).
Homo antecessor was named in 1977 from fossils found at the Spanish cave site of Atapuerca, dated to at least 780,000 years ago, making them the oldest confirmed European hominids. The mid-facial area of antecessor seems very modern, but other parts of the skull such as the teeth, forehead and browridges are much more primitive. Many scientists are doubtful about the validity of antecessor, partly because its definition is based on a juvenile specimen, and feel it may belong to another species (Bermudez de Castro et al. 1997; Kunzig 1997, Carbonell et al. 1995) (J.Foley, 2004).
Homo sapiens (archaic) (also Homo heidelbergensis)
Archaic forms of Homo sapiens first appear about 500,000 years ago. The term covers a diverse group of skulls which have features of both Homo erectus and modern humans. The brain size is larger than erectus and smaller than most modern humans, averaging about 1200 cc, and the skull is more rounded than in erectus. The skeleton and teeth are usually less robust than erectus, but more robust than modern humans. Many still have large brow ridges and receding foreheads and chins. There is no clear dividing line between late erectus and archaic sapiens, and many fossils between 500,000 and 200,000 years ago are difficult to classify as one or the other. (J.Foley, 1997).
Modern forms of Homo sapiens first appear about 120,000 years ago (a subspecies Homo sapiens idàltu recently uncovered by Tim White's team may even be some 160,000 years old). Modern humans have an average brain size of about 1350 cc. The forehead rises sharply, eyebrow ridges are very small or more usually absent, the chin is prominent, and the skeleton is very gracile. About 40,000 years ago, with the appearance of the Cro-Magnon culture, tool kits started becoming markedly more sophisticated, using a wider variety of raw materials such as bone and antler, and containing new implements for making clothing, engraving and sculpting. Fine artwork, in the form of decorated tools, beads, ivory carvings of human and animals, clay figurines, musical instruments, and spectacular cave paintings appeared over the next 20,000 years (J.Foley, 1997, 2004).
Homo neanderthalensis (formerly Homo sapiens neanderthalensis)
Neandertal (or Neanderthal) man existed between 230,000 and 30,000 years ago. The average brain size is slightly larger than that of modern humans, about 1450 cc, but this is probably correlated with their greater bulk. The brain case however is longer and lower than that of modern humans, with a marked bulge at the back of the skull. Like erectus, they had a protruding jaw and receding forehead. The chin was usually weak. The midfacial area also protrudes, a feature that is not found in erectus or sapiens and may be an adaptation to cold. There are other minor anatomical differences from modern humans, the most unusual being some peculiarities of the shoulder blade, and of the pubic bone in the pelvis. Neandertals mostly lived in cold climates, and their body proportions are similar to those of modern cold-adapted peoples: short and solid, with short limbs. Men averaged about 168 cm (5'6") in height. Their bones are thick and heavy, and show signs of powerful muscle attachments. Neandertals would have been extraordinarily strong by modern standards, and their skeletons show that they endured brutally hard lives. A large number of tools and weapons have been found, more advanced than those of Homo erectus. Neandertals were formidable hunters, and are the first people known to have buried their dead, with the oldest known burial site being about 100,000 years old. They are found throughout Europe and the Middle East. Western European Neandertals usually have a more robust form, and are sometimes called "classic Neandertals". Neandertals found elsewhere tend to be less excessively robust (Trinkaus and Shipman 1992; Trinkaus and Howells 1979; Gore 1996) (J.Foley, 2004). See also my account of the continuing story of Neanderthal Man.
Homo sapiens (sapiens)
Taxonomically, humans belong to the kingdom Animalia, the phylum Chordata, the subphylum Vertebrata, the class Mammalia, the subclass Eutheria or Placentalia, the order Primates, the suborder Anthropoidea, the superfamily Hominoidea, the family Hominidae, the genus Homo, the species sapiens, and the subspecies sapiens. Each of these categories has uniquely contributed some morphological and/or behavioral features to what we are here and now. I fully agree with Margulis & Sagan's (1991) statement that "virtually each of humanity's ancestors has left its mark, has helped mold human flesh and human nature in its ambiguity and complexity", from bacteria, to reptiles, to mammals, to primates, to apes, to hominids.
Man likes to think of himself as the ultimate outcome of a long line of evolutionary progress and inevitable complexification: the crown of creation. In reality, however, progress and complexity are not even a primary thrust of the evolutionary process, and Man is but a tiny, late-arising, and very contingent twig on life's enormously arborescent bush: "Humans arose rather as a fortuitous and contingent outcome of thousands of linked events, anyone of which could have occurred differently and sent history on an alternative pathway that would not have led to consciousness" (Gould, 1994; but see Wright  for a more 'directional' long-term perspective, due to 'nonzerosumness' or 'synergism' as Corning  already called the same 'progressionist' process).
The human being: A success story? Yes, for now. "Yet the remarkable truth is that we come from a long line of failures. We are apes, a group that almost went extinct fifteen million years ago in competition with the better-designed monkeys. We are primates, a group of mammals that almost went extinct forty-five million years ago in competition with the better-designed rodents. We are synapsid tetrapods, a group of reptiles that almost went extinct 200 million years ago in competition with the better-designed dinosaurs. We are descended from limbed fishes, which almost went extinct 360 million years ago in competition with the better-designed ray-finned fishes. We are chordates, a phylum that survived the Cambrian era 500 million years ago by the skin of its teeth in competition with the brilliantly successful arthropods. Our ecological success came against humbling odds" (Ridley, 1999: 25-26).
The origin of H. sapiens was from among a series of populations spanning a time interval between 700,000 and 125,000 years ago. Some of these really do show a mixture, or mosaic, of features between H. erectus and H. sapiens. One of the most famous of such fossil specimens is the Petralona skull, discovered in 1959 in a cave close to the village that gives it its name, which is not far from Thessaloniki, in Greece. Its brain capacity is large, but its brow ridges are like those of a typical H. erectus. It is something like 220,000 years old. These early populations gave rise to what was formerly referred to as 'archaic Homo sapiens', whose fossil remains are known from a dozen or so sites, mostly through Africa, but also in Europe and at least as far as the Middle East. Archaic humans, too, had spread beyond the mother continent. The tendency at the moment is to distinguish the same specimens as a different and distinct species (some would even recognize more than one species). This nomenclature quibbling is the product of the theory which has all modern humans - H. sapiens by anybody's measure - originating only 40,000 years ago. If this 'Out of Africa' theory is correct, modern man by definition cannot be the same either as the older 'archaics' or the Neanders. On this reasoning, therefore, they were separate species. Thus it was that our direct ancestors pushed aside the Neanderthal men, and displaced the archaics. This may or may not have been accomplished by violence - but it would be a mistake to assume that warfare was necessarily part of the diaspora, for shifting climatic conditions alone may have sufficed to make some of the specializations of Neanderthals redundant (Fortey, 1998).
Half a million years ago, Homo erectus was distributed throughout the tropical and temperate regions of the Old World. This has led to a debate between those who think that existing human races evolved in situ from the local populations of H. erectus (the 'multiregional' or 'regional-continuity' or 'candelabra' model - advocated by Wolpoff a.o.), and those who think that H. sapiens originated once only, probably in Africa (although that is not certain), and subsequently spread round the world, replacing the local populations of H. erectus. The latter view, of a single origin (the 'Out-of-Africa' or 'Mitochondrial Eve' [or 'African Eve' or 'Black Eve'] model - first proposed by Stringer & Andrews, 1988), has been greatly strengthened by molecular (mitochondrial DNA) data (Cann et al., 1987). We are left with the conclusion that we are descended from a rather small human population, probably living in Africa some 200,000 years ago. This conclusion from the molecular data is consistent with the fossil and archaeological evidence (Maynard Smith & Szathmáry, 1995: 278)
Recent studies have raised questions about the 'purity' of mitochondrial DNA. Two teams of scientists led respectively by Hagelberg and Maynard Smith have uncovered significant data suggesting that recombination also takes place outside the nucleus and that than an offspring's mitochondrial DNA includes contributions from both parents (Proc. Royal Soc. Ser, B., 266, March, 1999). A new study conducted by a team of scientists led by Underhill has turned to the male line of descent and examined the mutations that are displayed on the non-combining region of the Y chromosome, the sex chromosome that fathers transmit to their sons. The analysis of ca. 160 sites identified on the DNA material of more than 1000 globally representative individuals has produced results suggesting that "a minority of contemporary East Africans and Khoisan represent the descendants of the most ancestral patrilineages of anatomically modern humans that left Africa between 35,000 and 89,000 years ago (Underhill et al., 2000: 358). These findings provide another confirmation of the African origin of modern humans, but the proposed chronology of the Out-of-Africa expansion raises questions (Bichakjian, 2000: 9-10).
By analyzing Y-chromosome DNA from people in all regions of the world, geneticist Spencer Wells has recently concluded that all humans alive today are descended from a single man who lived in Africa around 60,000 years ago (Wells, 2003; Mayell, 2002).
If the replacement model is correct, all humans on earth right now are descended from a lineage that radiated around (maximum) 200,000 to (minimum) 60,000 years ago. This means that genetic differences between contemporary groups originated relatively recently, and we should expect them to be relatively minor (Boyd & Silk, 1997).
Recently, two excavations have seriously questioned the Out-of-Africa theory: Mungo man from Australia and 'Java Gal' (SM3) from Java. The mtDNA analysis by Adcock et al. (2001) indicates that Mungo man belongs to a lineage both older and distincly different from the African ancestor. The authors have claimed this is strong evidence for the multiregional model of human evolution, but other experts have challenged this (J.Foley, 2001; see also Cooper et al., 2001). Java Gal died at least 100,000 years ago somewhere in Central Java, appearing to combine features of both H. erectus and H. sapiens (Soares, 2001).
Gribbin & Cherfas (2001), in their The First Chimpanzee: In Search of Human Origins, basing their reconstruction of the hominid evolution on the molecular clock research by Vincent Sarich and Alan Wilson already published in 1967, summarize is as follows:
Our starting point is the fact - not hypothesis, or even theory, but a measured piece of evidence - that man, chimp and gorilla are not only very closely related, but are all almost equally close to one another. There is no way you can group any two of them together to the exclusion of the third on evolutionary grounds, although there is just a hint that the gorilla line split off from the one leading to the other two apes just before the human-chimp split (but only just before) (277).
Thanks to a large part to Sarich's ground-breaking work, and the later developments of the technique by people like Simon Easteal, we now know that human genetic material is 98.4 per cent the same as the genetic material of chimpanzees - not 98.3 per cent, and not 98.5 per cent, but 98.4 per cent - and similarly close to the genetic material of the gorilla. And the reason that the three of us are so similar is because until very recently our genes did not exist within the cells of separate species but dwelt together in a shared common ancestor. The three lineages only became distinct, to follow their separate evolutionary paths, less than 4 million years ago. This fact is possibly the single most significant discovery pertaining to the mystery of human origins and evolution since Darwin's own day.
There is no longer any room to doubt that man evolved from an ancestor that he shared with the gorilla and the chimpanzee. The evolutionary explanation is established. But there is plenty of room for doubt and debate over the traditional, and still establishment, view of what exactly the human species evolved from, and when, and where - and, indeed, why (278).
The combined results of the fossil evidence and the timings of the molecular clock present this new timetable:
The placental mammals originated and began to diverge from the marsupials no more than 100 million years ago, which sets an upper limit on all the rest of the important events on the human family tree. The origin of the primates cannot have occurred more than 75 million years ago; the primates of the New and Old Worlds diverged no more than 35 million years ago (comfortably agreeing, by the way, with geophysical evidence for the break- up of the former supercontinent); Old World monkeys split from the hominoids no more than 20 million years ago, and the modern ape family began to radiate approximately 15 million years ago; gibbon and orang-utan diverged 11 and 8 million years ago and finally (ignoring the more recent divergences into pygmy and modern chimp, mountain and lowland gorilla) there was the three-way split between man, chimp and gorilla no more than 4 million years ago (283).
By 4 million years ago our ancestors were already very manlike and well on the road to human intelligence and a cooperative, sharing society. They were also able to walk upright, but retained the ability to climb trees effectively (284).
But what sort of animal was it that was able not only to cope with, but also take advantage of the changing environment? It was almost certainly very like a modern ape in many respects, able to progress efficiently on the ground by knucklewalking, the result of its past as a brachiator. And it came from Asia. We know that the modern apes are brachiators, modified by evolution and natural selection to enable them to swing through the trees, hanging below the branches. We also know that man, in his anatomy, bears the unmistakable stamp of brachiation.
The molecular evidence solves the mystery. It tells us that the five hominoid lines - gibbon, chimp, orang-utan, man and gorilla - share a common ancestor no more than 12 million years ago. That common ancestor was a fully developed tree-dweller whose brachiating lifestyle and anatomy we have inherited and make so much of in our sports and games. We are brachiators because for many millions of years our ancestors depended on brachiation to make a living, and because their adaptations served us well in our new life on the ground. The mystery brachiator ho is the ancestor of all modern apes and ourselves was probably the only surviving line of a multitude of dryopithecines, one of which also gave rise to the dead end that is Ramapithecus (285-86).
The ancestor of the apes must have been a tree-dweller, a way station between the arboreal monkeys and the terrestrial great apes. And because the gibbons and the orang-utan, the modern tree-dwelling apes, are found in the jungles of Asia, it is safe to assume that the common ancestor of the African threesome arose in those same jungles. The Asian jungles suffered less during the climatic changes leading up to the Ice Epoch than the African jungles; nevertheless, and despite the more gentle nature of the changes, retreating forests and spreading savannah played their part in luring some of the Asian apes down on the ground. There was no forest connection between Asia and Africa at the end of the Miocene, some 6 to 8 million years ago, but that provides no block; the ancestor of the African apes could very easily have made the journey overland, knuckle-walking as the modern great apes (and, occasionally, man) still do.
The ancestors that arrived in Africa must have been fairly well adapted to life on the ground. Whether they already walked upright is impossible to say, but seems likely. In the common parlance, by 4 million years ago, at the latest, they were more 'man-ape' than 'ape-man'. In any case, when they arrived in Africa they were faced with new ecological opportunities. The forests still existed, though in much smaller areas since the climate had changed, and savannah was the dominant theme (286).
As far as we know, there were no tree-dwelling apes in Africa at the time (Ramapithecus may have been around, but what little evidence we have suggests that it got its food on the ground) so that this niche was temptingly empty. Those members of the Asian immigrants that sought a return to a life in the trees would have encountered little resistance, and once they settled into the new lifestyle evolution by natural selection would have encouraged the redevelopment of their tree-climbing skills, while their ability for upright walking atrophied. Perhaps the entire population of immigrant Asian apes, in all likelihood restricted to a few pioneers, took to the trees for a few hundred thousand years, going back to that life and increasing in numbers. But the forests continued to shrink, and the very success of the species in its new niche contributed to the squeeze on the population. As in Asia before, some individuals moved out of the trees and on to the plains at the edges of the forest. Several niches were open, and the ancestral man-ape split to exploit alternative lifestyles. Some became chimps, other gorillas, others hominids (287).
Gribbin & Cherfas suggest, then, that the split between man and the other African apes did indeed occur within the past 4 million years, but that it did not occur in the direction that conventional wisdom implies. The last ancestor shared by man and the apes was already almost human and well adapted to life on the plains, honing their skills and eventually becoming fully human, some tribes took advantage of a period or periods of climatic amelioration to choose the soft option of life among the trees and free lunch all round (208).
On the one hand, we have two related species (Australopithecus robustus and the more slender Australopithecus africanus), large and small variations on a theme, that split from a common ancestor with the human line around 4 million years ago. They were fruit-eaters, and can be traced in the fossil record to one million years ago. On the other hand, we have two hairy apes living in African today, one large (the gorilla) and one small (the chimpanzee), both close relatives of the human line, from which they diverged about 4 million years ago. Both of them eat fruit, but paleontologists will tell you that no recent ancestors of either chimp or gorilla have been found in the fossil beds (Gribbin & Cherfas, 2001: 212).
Brain and Bipedalism
In 1975-76 the remains of up to 13 more specimens of Australopithecus afarensis were found at a single site in the same area. It is thought that they may have been victims of a flash flood. This group included males, females, and infants and was quickly dubbed the 'First Family' (Johanson & O'Farrell, 1990). This discovery revealed that Australopithecus afarensis showed marked sexual dimorphism (i.e., difference in size between the sexes): as with the gorilla and many other primates the male was much larger than the female. In 1976 further evidence that early hominoids were bipedal was discovered at Laetoli in Tanzania when the footprints of two adult and one infant hominid were found in a bed of volcanic ash 3.6 million years old.
Lucy was no more intelligent than a chimpanzee, so bipedalism is unlikely to have been an adaptation to free the hands for more effective toolmaking. In any case, there is no evidence that Australopithecus afarensis made tools. Why then did the early hominids adapt to bipedalism? The answer probably has something to do with climate change. The chimpanzee-hominid lineage divided about 5 mya, at the end of the Miocene epoch. In the following epoch, the Pliocene (5-1.5 mya), the global cooling which had begun in the Miocene continued and with it the continued drying out of the African continent and the shrinking of its forests. In East Africa, which fossil evidence points to as the birthplace of the hominids, the drying effect was probably exacerbated by the geological upheavals that led to the uplift of the East African plateau and the great East African Rift Valley. The hominoid apes of the region would have been split up into isolated groups as their habitat shrank to form 'islands' of forests. Such conditions are ideal for the evolution of new species as genetic changes can spread very quickly through a small breeding population where they might be swallowed up in a large one (Haywood, 1995: 22-23).
Savanna origin of bipedalism
Ideas on the origin of human bipedalism, the first change that differentiated apes and humans, require the reconstruction of many unknowns. Darwin (1871) argued that bipedalism arose when our ancestors "lived somewhat less in trees and more on the ground", which was due "to a change in subsistence patterns or to a change in environmental conditions".
Shipman (1984) suggested that human bipedalism was an adaptation to the pattern of scavenging meat. Although bipedal running is neither fast not efficient when compared to the quadrupedal gaits, bipedal walking is more energetically efficient than quadrupedal walking. Bipedalism increased the energetic efficiency of human travel, and this increased efficiency was an important factor in the origin of bipedalism (Rodman & McHenry, 1980). Bipedalism is an efficient means of covering large areas slowly, and Shipman argued that it is an appropriate adaptation for a scavenger who must cover large areas. Bipedalism elevates the head, thereby improving the ability to locate items at a distance. Combining bipedalism with agile climbing ability (of which there may be evidence in such early hominids as Australopithecus afarensis) further improves the opportunities to exploit the environment. Bipedalism frees the hands and makes them available for carrying items (babies, tools, weapons, water, etc.). "Such a steadily desiccating habitat behind an isolating barrier would necessitate any semi-bipedal ape to develop regular upright gait, i.e., to become a (pseudo)-hominid or 'humanoid', in order to carry his defense weapons, food and drinking water (juicy fruit) with him in his hands" (Kortlandt, 1972).
Sinclair et al. (1986) suggested that bipedalism developed along with long-distance migration, and they agree with Shipman that scavenging was important to the evolution of bipedalism. They argued that early hominids scavenged migrating ungulate (hooved mammal) populations, the only population that existed in large enough numbers to provide sufficient food for scavengers. Because many migratory animals die from starvation, carcasses would be available to scavengers, who would not necessarily have to contend with predators for a kill. A migratory scavenger has access to an abundant and constant food supply.
The migration hypothesis suggests that habitual tool use developed from a need to speed up the butchering of carcasses and avoid competition with other, stronger mammal predators. The opportunity for hominid migration was enormous because savanna Africa was dominated by migration ecosystems.
Wheeler (1984) drew a connection between upright body posture and heat stress. He argued that an upright hominid presented to the sun only about 40 percent of the body area that it would present if it were a quadruped. Thus, the bipedal hominid would reduce its heat load and bipedalism would have been a factor allowing early hominids to occupy a noonday scavenging niche that was out of harm's way and avoided competition from other scavengers who rested during the heat of the day (this hypothesis is connected with the 'radiator theory' of brain enlargement developed by Fialkowski and Falk).
Lovejoy's (1981, 1984) provisioning hypothesis concentrated on the acquisition of bipedalism by males as a means of supplying food for a female who is encumbered by a slowly maturing infant, but Tanner (1981) sugggested a hypothesis that centers on the acquisition of bipedalism by females. Tanner noted that bipedalism accomodated the increased infant dependency on its mother, which meant that the mother had to carry the child ('helpless baby theory').
McHenry (1982) questioned Lovejoy's scenario. For example, evidence indicates that early humans were polygynous and not monogamous as Lovejoy suggested. A distinct possibility is that early humans were already serial monogamists, as suggested by Fisher (1993) (Poirier, 1993).
Rodman & McHenry (1980) conjectured that the ancestors of terrestrial monkeys were arboreal quadrupeds who fed on the tops of branches, while the ancestors of the hominids were suspensory feeders (hanging below branches to feed, as modern orangutans do; which is not quite the same as 'brachiation' - what gibbons do). Selection might have favored quadrupedalism among animals descended from above-the-branch feeders and favored bipedalism among animals descended from suspensory feeders - in each case because that form of ground locomotion required fewer anatomical changes (Boyd & Silk, 1997).
Any or all of these hypotheses may be correct. Bipedalism might have been favored by selection because it was more efficient than knuckle walking (Rodman & McHenry, 1980), because it allowed early hominids to keep cool (Wheeler, 1984), because it enabled them to carry food or tools from place to place (Darwin, 1871), and/or because it enabled them to feed more efficiently (Kevin Hunt, 1997; chimps rarely walk bipedally, but they spend much more time standing bipedally as they harvest food from small trees) (Boyd & Silk,1997).
Arboreal origin of bipedalism
The following is an account of Potts (1996), as summarized by Davies (ASCAP, 1998).
The almost universally accepted account of humankind's ancestral environment is the savanna hypothesis. The fundamental difficulty is that this presumed static world provides no obvious reason for the increase in brain size. The expensive overhead cost of the brain would have been a heavy burden and a serious handicap in competition with other species.
One credible attempt, which comes in various guises, to explain the evolution of intelligence is an 'arms race'. Greater intellect was selected for because of the Machiavellian, social competition between humans in the same or competing groups. Unfortunately, this arms race hypothesis in undermined by the relatively small brains of all other primates. In no other case (and in no other animal) did an arms race in reasoning ability occur. For example, chimpanzees, living in relatively large social units, did not experience any equivalent growth in brain size as a result of internal or external social competition.
Another, seemingly tenable explanation of intellligence is based upon a hypothesized absolute increase in the number of human social contacts during the EEA (Environment of Evolutionary Adaptedness). Social species (dogs) are not more intelligent per se than solitary ones (cats), either for reasons of social competition or number of companions.
Potts' paradigm-breaking contribution to the debate is to show that human evolution did not occur in a static environment. Acordingly, the savanna hypothesis per se is refuted.
The explanation, according to Potts, starts with the world's climate. The amount of the sun's radiation that falls upon the earth is not constant but fluctuates in three independent rhythms of 100,000 years, 41,000 years, and 23,000 years respectively. The regular oscillations sometimes reinforce and, at other times, offset each other.
The longest cycle is due to the gravitational effects of the larger outer planets. Over a period of 100,000 years, the earth's orbit gradually shifts from a more circular to a more elliptical orbit and back again.
The 41,000 year fluctuation derives from the earth's tilted axis of rotation with regard to the sun.
The shortest cycle is due to the earth's wobble around its axis of rotation, a phenomenon known as precession.
The Serbian mathematician, Milankovitch, demonstrated that these three cycles supplied the initial push to the earth's climatic variability.
In general, the earth has become drier and cooler over the last fifty million years. Habitats fractured into distinct zones. Savannas spread. Fluctuations in the amount of the sun's radiation striking the earth led to ever more marked periodicity in the world's climate. Tectonic plate movements changed the geography of the world's continents, which had pervasive climatic consequences. Weather patterns were rendered more extreme and chaotic. Volcanic action intensified, itself disturbing habitats and climate in significant, often random ways. Crucially, feedback mechanisms began to amplify the climatic swings.
The critical stage of Potts' argument is to show that hominid evolution, and that of many other species, coincided with, and reflected, these climatic fluctuations. Potts demonstrates, for instance, that the evidence for increasing climatic fluctuation during the past six million or so years of hominid evolution is overwhelming. Moreover, key evolutionary events (the appearance and extinction of hominid and other species) are linked with ever more severe climatic oscillations. On the other hand, eras in which hominid evolution, and the evolution of other species, decreased, were marked by less climatic variability.
For the preceding reasons, Potts argues that the savanna hypothesis is mistaken. Thus, bipedalism was not an adjustment to a savanna lifestyle, but, rather, the adaptation of arboreal primates to climatic variability. The first biped (the progenitor of the australopithecines) is now dated to more than four million years ago, and was, in effect, an upright chimpanzee. Its upper body remained that of an ape. Bipedalism was an adaptation to arboreal uncertainty, not the savanna.
Australopithecines and earlier bipeds, Potts explains, could cope with arboreal habitats that had become segregated and variable. The most recent research supports Potts: "Yet our evidence suggests that the earliest bipedal hominid known to date lived at least part of the time in wooded areas" (Leakey & Walker, 1997).
The amplitude of climatic oscillations jumped sharply between three million and two million years ago. At that time some bipedal apes abandoned an arboreal existence in favor of a terrestrial subsistence.
Stone tools are associated with some of these hominids. Potts makes the point that the stone tools of Homo erectus were a more flexible adjustment to rougher diets than the specialized teeth of the Australopithecus robustus. The first stone tools can be regarded, he claims, as external, more adaptable teeth.
The design of the first stone tools remained unchanged for a million years. First stones were picked up, made into tools and possibly only used at that location.Then, later, tools were carried up to six miles. Finally, after 600,000 years or so, stores of tools, constructed from more easily worked materials, were left at strategic locations throughout the home range. The hominids' concept of the future had become more sophisticated (Potts, 1996; Davies, 1998).
Why is the climate so unstable? In part it turns on the Earth's orbit, an ellipse whose shape changes with a rhythm of about a hundred thousand years. At its most extreme it causes winters to be colder and summers hotter as the planet moves further from and closer to its source of heat. A series of cold winters is enough to tip the globe into frost. The sequence is modulated by a shorter cycle in the Earth's tilt and wobble. As forests bloom - and later rot - in warm periods, carbon dioxide and methane escape into the air. These allow energy from the sun to pour in, but trap the ground's own long-wave radiation to give a 'greenhouse effect' that pushes the temperature up still further. Because ice can pass through a glacier at five miles a year, it does not take much of a drop in temperature for it to race across the landscape, or much of an increase for an ice cap to shrink (Jones, 2000: 326).
Yet, it remains unclear why bipedalism would have evolved in the context of woods, because the ancestors of the Australopithecines did quite well without bipedalism in their Miocene forests (Slurink, 2002).
Aquatic origin of bipedalism
The savanna and arboreal models do not exhaust the possibilities of the origin of bipedalism. A serious third candidate is the 'Aquatic Ape Theory' (Morgan, 1982, 1990, 1997; Richards, 1987; Roede et al., 1991; Van der Dennen, 1995; Verhaegen, 1987 et seq.), or in a 'weaker' version: the 'Lacustrine-Riverine Habitat' hypothesis. Bipedalism could have evolved from wading. In water, the body is almost automatically erected and 'forced' into a bipedal stance.
It is important to note, however, as Verhaegen, McPhail & Munro (1999) point out, that such a bipedal wading gait is very different from the hopping bipedalism that some primates use when moving on the ground. This latter gait incorporates bent knees and hips rather than the linear stature preferred for wading. The advantage of the erect wading posture is that it allows primates to hold their body, arms and head as far as possible above the water surface, allowing them to cross deeper stretches of water.
There is increasing evidence that the initial habitat of the first hominids was mosaic, savanna as well as woods and lakes, rivers and swamps. The climate was most probably warm and wet. Bipedalism is therefore not easily explained as a savanna adaptation. Furthermore, the profuse perspiration and water need of hominids cannot possibly be construed as savanna adaptation. "Especially Verhaegen's argument that the human cooling system is extremely water and sodium-wasting and therefore unfit for a dry environment seems very convincing (Verhaegen, 1987)" (Slurink, 2002).
A riverine-lacustrine habitat provides fish, shellfish in abundance, in addition to bird and turtle eggs, insects, small birds, amphibians and reptiles, aquatic plants, etc., so there is little need for hunting or scavenging in this initial phase. Moreover, during the dry season many savanna animals tend to congregate around the remaining water resources and the early hominids could have used this opportunity for 'harvesting' meat. Finally, water provides almost perfect protection against big feline predators.
Proboscis monkeys cross shallow stretches of water between mangrove trees on two legs, and lowland gorillas go wading for reed sedges and aquatic herbs in forest swamps. Bonobos also have been observed wading bipedally and catching fish (De Waal, 1988; Verhaegen, McPhail & Munro, 1999; Verhaegen & Munro, 2001; Slurink, 2002). Perhaps in a similar way, only more frequently, our apelike ancestors waded in shallow waters of forest clearings, gallery forests or mangrove areas, in search of fallen fruits, herbs, sedges or molluscs (Verhaegen & Munro, 2001).
Early dryopithecine fossils have been found in marine near-shore sands along the Tethys Sea (Heliopithecus ca.17 Mya at the Persian Gulf, and Austriacopithecus ca.14 Mya in what are now the Alps) (Verhaegen & Munro, 2001).
Most sites where early hominids were recovered are in the close vicinity of lakes or rivers (e.g., Tabarin, Hadar, Omo, Koobi Fora, Olduvai) (R.Foley, 1987; Andrews, 1992; Slurink, 2002). Furthermore, Homo fossils, as opposed to australopithecines, are typically found near shellfish (e.g. Chiwondo, Chemeron, Nariokotome, Zhoukoudian, Boxgrove, Terra Amata, Rabat, Hopefield, Gibraltar) (Verhaegen & Munro, 2001).
At the first stage the early hominids may have foraged at the border of the savanna and at the edges of marshes and lakes during the day and they may have climbed into the trees during the nights for refuge and sleep. In later stages, when the climate became cooler and drier during the Pliocene, they may have been forced to rely more and more on the ability to migrate across the savanna, as sugggested by Verhaegen, McPhail & Munro (1999) and Slurink (2002).
Verhaegen & Munro argue the early apes led a climbing-wading lifestyle in forest swamps, where they became bigger (for thermo-regulatory and gravitational reasons), lost their tail (which was of no use for wading, and thermo-regulatorily disadvantageous in water), and became arm-hangers and more bipedal (for wading and grasping branches and perhaps fruit above the water). A population of wading-climbing great-apes in the coastal forests between Africa and Eurasia may have given rise to the Eurasian dryopithecines and later the African australopithecines.
During the Ice Ages, the climate cooled and dried, sea levels dropped, coastal forests shrank, and vast tidal flats and estuaries emerged on the continental shelves along the Indian Ocean. Our tool-using and bipedally wading ancestors were ideally preadapted to colonize these new shellfish-rich niches. They lost their climbing adaptations, and presumably collected shellfish and other seafoods by wading and later by diving too. Humans, much more than nonhuman primates, have efficient diving and breath-hold capabilities, which could have been preadaptive for the development of voluntary sound production and speech. It was at the seashore, these authors believe, that these wading-diving beach-combers acquired their huge brain, voluntary speech, stone tool technologies and extreme dexterity, as well as their external nose, naked skin, thicker subcutaneous fat, linear swimming-build and long wading-legs.
Recently, several authors have argued independently that the common ancestors of humans, chimpanzees and gorillas were already partly bipedal (Verhaegen, Puech & Munro, 2001). This has been confirmed by discoveries of early hominids (or hominoids) with probably both bipedal and climbing adaptations: Oreopithecus bambolii (Sardinia, ca. 9-7 mya: Rook et al., 1999); Orrorin tugenensis (Kenya ca. 6 mya: Senut et al., 2001), and Ardipithecus ramidus (Ethiopia ca. 5 mya: Wolde et al., 2001).
Our australopithecine ancestors adopted an upright posture at least 4 mya, long before there was any substantial increase in brain size. Australopithecines had ape-sized brains, about one-third the size of modern human's. By the Homo erectus stage, the brain had doubled in size. Even so, the tools of Homo erectus were technically uninventive. Their most elaborate tool was the handaxe, fashioned from a single block of stone and worked on both surfaces. It was more innovative than any tool used by chimpanzees. Chimpanzees use hammerstones and anvils in the wild in some habitats: in captivity, they can be taught to make and use flint flakes.
It is a striking fact that handaxes (if indeed they were handaxes - Calvin (1986) doubts this: the first thing the user would have cut is his own hand), which first appeared about 1.5 mya, continued to be made for more than a million years. Only after the evolution of the earliest Homo sapiens, around 250,000 years ago, are there signs of slightly more skilled toolmaking and a more varied toolkit. However, tools and tool materials generally remained conservative, even after the appearance of fully modern, large-brained people around 100,000 years ago. The burst of technological innovation came relatively recently, only about 40,000 years ago.
It is hard to suppose, therefore, that the increase in brain size, by a factor of almost three, could have been a response to selection for improved technical skill. What selective force did lead to our larger brains? It is conceivable that the relevant factor was the evolution of language. It seems more likely, however, that language as we now know it evolved rather recently, and that is was responsible for the dramatic changes that have occurred in the past 100,000 years, not for the increase in brain size that took place earlier. Dunbar (1992) has pointed out that, if one compares the forebrains of existing primates, the best predictor of brain development is the size of the social group in which an individual lives. He therefore suggests that the main selective force favoring increased intelligence in primates arises from social interactions. An individual who can act appropriately in a variety of social contexts will be fitter than one who cannot. Extending this argument to our own ancestors, the increase in brain size was an adaptation to living in society (Maynard Smith & Szathmáry, 1995: 276-278).
Taphonomic evidence suggests that early hominids may have acquired meat both by scavenging and by hunting (Boyd & Silk, 1997). Big brains, meat eating, slow development, the 'neotenized' (or pedomorphic) retention into adulthood of childhood characters (bare skin, small jaws and a domed cranium) - all these went together. Without the meat, the protein-hungry brain was an expensive luxury. Without the neotenized skull, there was no cranial space for the brain. Without the slow development, there was no time for learning to maximize the advantages of big brains. Driving the whole process, perhaps, was sexual selection (Ridley, 1999: 33; Miller, 2000).
The control of fire has probably been among the most momentous and far-reaching of human discoveries. Controlled and purposeful use of fire involved conquering the fear that exists toward fire among mammals generally. With purposeful use of fire, humans began to shape the world according to their design. For example, by bringing fire into its living space, H. erectus carved zones of light and warmth out of darkness that provided relative protection from predators. Fire, by changing living habits, may have indirectly altered the brain's structure and enhanced the ability to learn and communicate.
The earliest evidence of fire with possible human connection comes from sites at Lakes Baringo and Turkana in Kenya. Burnt clay at these sites dates between 1.5 and 1.4 mya. Although some researchers (Gowlett et al., 1981) suggest an association between this evidence and human occupation, most are unconvinced of such a purposeful association. It is not difficult to find traces of fires early in Africa. The problem is distinguishing between controlled fire used by humans and naturally occurring fires (Poirier, 1993).
If fire at lakes Baringo and Turkana is not associated with humans, then the earliest possible evidence of fire associated with humans may be the discoveries from the South African cave site of Swartkrans. The evidence, dated to 1 mya, has been reported by Brain & Sillen (1988). The Swartkrans site contains skeletal remains of both A. robustus and H. erectus, and it is not certain which group was using the fire. Evidence of fire use from other parts of the world is only found in association with H. erectus.
Fire was probably originally obtained from such ready-made sources as volcanic eruptions, brush fires, or gas and oil seepages. Hunters may have camped near fire, whuch was a natural resource as were game, water, and shelter. From the beginning fire may have been used to keep predators away. Perhaps humans became regular cave dwellers only after they learned to use fire to drive predators away from the cave, as suggested by Sillen & Brain (1990).
Fire may have been used in hunting to stampede prey. Fire may also have been used to produce more effective spears. Fire hardens the core and makes the outer part crumbly and easier to sharpen. The earliest possible fire-hardened spear, however, dates to only approximately 80,000 years ago and was found in Germany. Psychological changes may have accompanied the use of fire; for example, cooking may have produced behavioral restraint, that is, control of a tendency to do things on the spur of the moment (Poirier, 1993).
H. erectus probably controlled fire. It is hard to believe that H. erectus could have survived the winter in environments such as China unless they knew how to control fire (Boyd & Silk, 1997).
Archaeologist Randy Bellomo of the University of South Florida has recently conducted a series of experiments strongly indicating that the baked earth at Koobi Fora is the remains of an ancient campfire. Thus, it seems likely that hominids have been controlling fire for more than a million and a half years.
Recent excavations at Swartkrans Cave in South Africa uncovered more evidence of fire use by H. erectus (Boyd & Silk, 1997).
One of the characteristics of the Paleolithic (40,000-10,000 before present [BP]) revolution is a move toward miniaturization in toolmaking. The arrival of modern humans in Europe is marked by the appearance in the archeological record of a new style of toolmaking based on the production of long thin blades of a standardized size and shape. Though this new technique was demanding, it could produce three to 12 times the length of cutting edge from the same weight of stone as the Neanderthals' Mousterian flake-producing technique (Haywood, 1995).
The earliest style of tools associated with modern humans in Europe, known as the Aurignacian, dates from between 30,000 and 40,000 years ago and is found over a wide area from the Balkans to Spain. However, during the remainder of the Upper Paleolithic many regional and even local styles developed. What this pattern seems to indicate is that the first modern humans to move into Europe came from a single homogeneous group. Descendants of this group spread rapidly across Europe taking their distinctive tool kit with them but as they settled down into relatively isolated populations, differences began to develop (cultural evolution paralleling physical evolution in this respect).
These differences are stylistic rather than functional, so they probably served as badges of ethnic or tribal identity, expressing each group's awareness of itself as a distinct social unit. Some tools, such as the laurel-leaf blades of the French Solutrean culture (22,000-16,000 BP), were so finely worked that they were probably intended to be display objects or gifts to be exchanged at festivals to cement alliances between groups of individuals (Haywood, 1995: 66-68).
The first art [in Europe] appears around 32,000 years ago, a few thousand years earlier than any surviving art found elsewhere in the world. At first artists made only simple paintings and engravings of animals and human sexual organs, but by 25,000 BP they were blowing or brushing pigment around their hands to make imprints on cave walls. Around this time too the remarkable so-called 'Stone-Age Venus' figurines were fashioned. These are sculpted figurines and bas-reliefs of females with greatly exaggerated breasts and buttocks and usually without hands, feet, and faces. Some appear to be pregnant. Whatever their actual significance (they are usually explained as fertility symbols), the Venus figurines were associated with a widespread set of beliefs as they are found across Europe from the Ukraine to France.
The greatest period of Upper Paleolithic art, the Magdalenian (named after the important site at La Madeleine), began about 18,000 years ago at the height of the last glaciation. This is the period of the stunning cave murals from Lascaux in France, Altamira in Spain, and other sites, but wealth of portable art, from ivory carvings to decorated spear throwers, was also created. Cave art is almost entirely devoted to depictions of animals (Haywood, 1995: 73-74).
The view that the earliest modern Africans were behaviorally primitive stems from a profound Euro-centric bias and a failure to appreciate the depth and breadth of the African archaeological record. In fact, many of the components of the 'human revolution' claimed to appear at 40-50 ka are found in the African Middle Stone Age tens of thousands or years earlier. These features include blade and microlithic technology, bone tools, increased geographic range, specialized hunting, the use of aquatic resources, long distance trade, systematic processing and use of pigment, and art and decoration. These items do not occur suddenly together as predicted by the 'human revolution' model, but at sites that are widely separated in space and time. This suggests a gradual assembling of the package of modern human behaviors in Africa, and its later export to other regions of the Old World. The African Middle and early Late Pleistocene hominid fossil record is fairly continuous and in it can be recognized a number of probably distinct species that provide plausible ancestors for H. sapiens. The appearance of Middle Stone Age technology and the first signs of modern behavior coincide with the appearance of fossils that have been attributed to H. helmei, suggesting the behavior of H. helmei is distinct from that of earlier hominid species and quite similar to that of modern people. If on anatomical and behavioral grounds H. helmei is sunk into H. sapiens, the origin of our species is linked with the appearance of middle Stone Age technology at 250-300 ka (McBrearty & Brooks, 2000).
Also Geoffrey Miller (2000: 22) pointed to this Eurocentric bias:
"[A]n overreliance on archeological data may lead scientists to underestimate the antiquity of some of our most distinctive abilities. Many have assumed that if there is no archeological evidence for music, art, or language in a certain period, then there cannot have been any. Historically, European archeologists tended to focus on European sites, but we now know that our human ancestors colonized Europe tens of thousands of years after they first evolved in Africa a hundred thousand years ago. This Eurocentric bias led to the view that music, art, and language must be only about 35,000 years old. Some archeologists such as John Pfeiffer claimed there was an 'Upper Paleolithic symbolic revolution' at this date, when humans supposedly learned how to think abstractly and symbolically, leading to a rapid emergence of art, music, language, ritual, religion and technological innovation. If these human abilities emerged so recently in Europe, we would not expect to find them among African or Australian peoples [the Aborigines colonized Australia at least 50,000 years ago] - yet there is plenty of anthropological evidence that all humans everywhere in the world share the same basic capacities for visual, musical, linguistic, religious, and intellectual display".
Among other behaviors enhanced by the sociocultural MoE is tool use, that is, using natural objects lying around in order to help perform an action. The progressive freeing of the hands [due to bipedal stance] evolved independently of the sociocultural MoE, but in conjunction with it, was decisive in shaping the further evolution of the lineage. Culturally propelled tool use and manufacture among the hominoids evolved from prepared twigs to the two-and-a-half-million year-old Oldowan choppers recovered in Gona, Ethiopia. This development must have been gradual. Chimpanzees not only use tools, but display rudimentary tool preparation, the first stage of industry, and the earliest lithic industry, achieved some two million years ago after the freeing of the hominoids' hands, was still within the competence of an 'ape adaptive grade' (Wynn & McGrew, 1991; Susman, 1994; Benefit & McCrossin, 1995; Bradshaw, 1997; Tobias, 1998; Wood & Collard, 1999; Gibson & Ingold, 1993) With lithic culture, the hominoid phenotype has acquired a power-enhancing and durable extrasomatic extension that could be shared across generations (Naccache, 1999: 24). After five million years and more of the workings of the sociocultural MoE, during the last half of which the extrasomatic extension played its enhancing role, some artifacts were intentionally made to carry a specific reference to a social memory shared by a group, that is, to carry a symbolic message. [This might be as early as the consummately crafted 400,000-year-old wooden spears found recently near Hanover; or it might be as recent as the 50,000-year-old 'depictive image' from the Golan Heights (Marshack, 1996)]. Humble beginnings [symbolic systems] had, but levered on top of the 'Lamarckian' sociocultural MoE, the growth rate was explosive. So explosive that it is perceived as a succession of nested, ever-accelerating revolutions: 1. The Upper Paleolithic cognitive revolution some 30,000 years ago; 2. The symbols' revolution of the Levantine Epipaleolithic that ushered in the first pemanent settlements and then agriculture some 14,000 years ago; 3. The urban revolution 5,000 years ago; 4. The scientific revolution 500 years ago; 5. [And at present the progressive elimination of the causes of 'natural selection' in human populations (through hygiene, medicine, and population movements and other still-emerging modes of evolution which Naccache calls the 'tinkering MoE' and the 'parabiological MoE'] (Naccache, 1999: 27-29)
Before turning his attention to Arago, Henry de Lumley undertook a salvage excavation of a site known as Terra Amata, in the southern French town of Nice. This site, more securely dated than Arago to about 400 kyr ago, is interesting from several points of view. Among other things it contains, in the forms of hearths, what may be the earliest evidence in Europe of the domestication of fire (although it's possible that the Spanish sites of Torralba and Ambrona, which may be as old or even a little older, should take the laurels here). More important, though, Terra Amata apparently represented a seasonal hunting camp whose inhabitants built shelters of saplings placed into the ground in ovals and brought together at the top. If this interpretation is correct, Terra Amata provides the earliest evidence from anywhere of such activity.
Several sites excavated during this time offer evidence for human activity in the western areas of Europe in the period following about 1 million years ago. Significant among these are the localities of Soleilhac and Le Vallonet in France, and Isernia La Pineta, in Italy, all of which contain simple flake tools and appear to be over 700 kyr old. A very recent find of a hominid mandible at Dmanisi, in ex-Soviet Georgia, however, places the entry of humans into Eurasia much further back than anything documented from the west; the specimen may be as much as 1.6 myr old, and is no younger than 900 kyr.
Further south, excavations during the early 1960s at the site of 'Ubeidiya, in Israel, produced Acheulean artifacts that are pretty firmly dated to about 1 myr ago or even earlier. This is good proof that by this time handaxe makers had managed to leave Africa, where these bifacially fashioned tools were first produced some 1.5 myr ago. It's thus maybe a little surprising that the earliest European archaeological sites are bereft of handaxes; but it seems to be a general phenomenon that these tools get rarer the further away from Africa you go. Indead, as far back as the 1940s Hallam Movius noticed that Paleolithic tool assemblages from India east to the Pacific rim tended to lack handaxes entirely, consisting instead purely of chopper and flake tools. The significance of the 'Movius line' between the handaxe-making cultures to the west and the nonhandaxe-makers to the east has long been argued over (Tattersall, 1995: 176-7).
Several aspects of the human revolution have led some anthropologists to hypothesize that ethnic groups first appeared during the Upper Paleolithic (sometime between 35,000 and 45,000 years ago). First, the rapid change in tool industries and the fact that distinctive industries existed at the same time in different places suggest that, for the first time, different traditions were maintained among genetically similar people. Second, Upper Paleolithic sites show stylistic differences in utilitarian objects like stone tools. Finally, the increased degree of ecological specialization during the Upper Paleolithic is also consistent with more cultural subdivision among people living in close geographical proximity (Boyd & Silk, 1997).
It is important to grasp the variability that is inherent in human nature, as variation is often mistakenly seized upon as evidence for the cultural or historical rather than natural. Many adaptive responses are by design variable, depending on the conditions. Among the many behavioral examples are ethnocentrism and falling in love: the evidence is strong that it is a species-typical adaptation, but when, where, with whom, and so on are quite variable. Adaptations of this sort are described as 'facultative' (as opposed to 'obligate') (D.E. Brown, 2000).
The Agricultural Revolution
One type of complex hunter-gatherer society, known as the Natufian, developed in the uplands of the Levant around 12,000 BP. As the climate warmed up toward the end of the Ice Age, the region was colonized by plants like wild emmer wheat and wild barley, almond, oak, and pistachio trees. These abundant supplies of easily stored cereal and nut foods allowed the Natufian hunter-gatherers to settle permanently in villages of substantial stone and wood huts. The Natufians developed all sorts of specialized tools for processing these tooth-cracking plant foods, including querns, grindstones, mortars and pestles, stone storage bowls, and bone-handled reaping knives for harvesting cereals. Though heavily dependent on plant foods, the Natufians also hunted gazelle in large numbers (Haywood, 1995: 102-3).
Until recently, historians and archeologists regarded the discovery of agriculture as an unmixed blessing, one of the great breakthroughs of human progress. Surviving skeletal evidence shows that the hunter-gatherers of the Upper Paleolithic were well nourished and lived healthy lives. In contrast, the skeletons of early farmers from all over the world show signs of malnutrition and stunted growth, arthritis, and other signs of wear and tear caused by hard manual work, excessive tooth wear, disease, and reduced life expectancy. There were two causes of these problems. The first was the tendency of farmers to rely on a limited range of high-yielding crops. The second factor was the increased birth rate of farming societies. Frequent periods of malnutrition were the inevitable result. The farmers' health also suffered because infectious diseases were transmitted more easily in the often insanitary conditions of the permanent settlements. Starch-rich diets led to increased tooth decay among farmers and their teeth wore down quickly as a result of eating flour containing grit from grindstones. Women's health may have suffered even more than men's. Women spent hours a day bent over grindstones and querns, processing grain, making them vulnerable to osteoarthritis of the lower back: increasing childbearing also took its toll. Early farmers also had to spend an average of 50-100 percent more time working than hunter-gatherers and the work was usually physically more demanding too. With all these disadvantages, why did people abandon hunting and gathering for farming. The short answer is that they had no choice in the matter. The slowly rising populations exerted a constant incentive to find still more intensive methods of exploiting food resources. Over-hunting reduced game stocks and the hunter-gatherers were forced to increase their reliance on plant foods (Haywood, 1995: 106-7).
Cavalli-Sforza and coworkers uncovered five different contour maps of gene frequencies within Europe. One was a steady gradient from south-east to north-west, which may reflect the original spread of neolithic farmers into Europe from the Middle East: it echoes almost exactly the archaeological data on the spread of agriculture into Europe beginning about 9,500 years ago. This accounts for twenty-eight per cent of the genetic variation in his sample. The second contour map was a steep hill to the north-east, reflecting he genes of the Uralic speakers, and accounting for twenty-two per cent of genetic variation. The third, half as strong, was a concentration of genetic frequencies radiating out from the Ukrainian steppes, reflecting the expansion of pastoral nomads from the steppes of the Volga-Don region in about 3,000 BC. The fourth, weaker still, peaks in Greece, southern Italy and western Turkey, and probably shows the expansion of Greek peoples in the first and second millennium BC. Most intriguing of all, the fifth is a steep little peak of unusual genes coinciding almost exactly with the greater (original) Basque country in northern Spain and southern France. The suggestion that Basques are survivors of the pre-neolithic peoples of Europe begins to seem plausible.
Genes, in other words, support the evidence from linguistics that expansions and migrations of people with novel technological skills have played a great part in human evolution (Ridley, 1999: 188-89).
Because the power of the chief is insecure, chiefdoms are highly competitive societies. A chief must always try to increase the resources at his disposal to reward his followers, whether peacefully, through agricultural improvements, or by violent plunder and conquest. The increased importance of warfare led to the emergence of elite warrior classes in many chiefdoms, such as among the Maya and Olmec of Mesoamerica or the Celts of Bronze and Iron Age Europe. Defensive refuges, often built on commanding hilltops or other defensible positions, are also common features of chiefdoms in all parts of the world (Haywood, 1995: 128).
Population pressure is seen as a major factor in some theories of the emergence of civilization. As populations expanded, they suggest, the kinship links which formed the basis of tribes and chieftaincies became too attenuated to hold large communities together, forcing the development of more complex social structures. In areas of dense population where expansion was not possible, groups would be forced to compete for resources. Under these circumstances communities will tend to get larger, the better to defend themselves against attack or to increase their chances of success in attacking others. Tribes would amalgamate into chiefdoms and chiefdoms would amalgamate into states. Successful war leaders may have been able to acquire a wider authority in the community, establishing themselves as a ruling class, while the populations of conquered areas might be absorbed by the victors as a lower class. In this way the hierarchical class structure of a state society would emerge. Even if a military class originally emerged as a response to outside aggression, once established it had the means to maintain its positions within its own community by force if necessary (Haywood, 1995: 132).
Sumerian civilization entered a new and troubled phase in the Early Dynastic period (3000-2300 BC). Massive defensive walls were built around the cities, bronze weapons were produced in increasing quantities and war begins to feature prominently as the subject of official art with rulers often being shown trampling on their enemies. The gap between rich and poor widenened and slavery appears in the records for the first time.
Lacking the spiritual authority of the priesthood, the new secular rulers established their authority through law. The earliest surviving law code is that of Urukagina, ruler of Lagash c. 2350 BC. Urukagina's law code was humane and showed great concern to protect the poor from arbitrary bureaucratic decisions and from exploitation by the wealthy. Use of the death penalty was rare, even for violent crimes. The best-known of these law codes is Babylonian ruler Hammurabi's (approximately 1770 BC).
Around 2350 BC, Sumeria began to decline in power and importance as vigorous new urban civilizations developed in northern Mesopotamia - ironically, largely due to Sumerian influence. In 2334 BC Sargon, the ruler of the northern city of Agade, conquered a vast swathe of territory from Syria's Mediterranean coast to Sumeria and the Persian Gulf. In doing so, Sargon created a new type of state, the empire, uniting peoples of many different ethnic and cultural identities under his sole rule (Haywood, 1995: 140-41).
Aboitiz, F. & V.R. Garcia (1997) The evolutionary origin of the language areas in the human brain: A neuroanatomical perspective. Brain Res. Rev., 25, p. 393.
Adcock, G.J. et al. (2001) Mitochondrial DNA sequences in ancient Australians: Implications for modern human origins. Proc. Nat. Acad. Sci. USA, 98, pp. 537-42.
Aiello, L. & M. Collard (2001) Our newest oldest ancestor? Nature, 410, pp. 526-7.
Algaput, B. et al. (1996) A new specimen of Ankarapithecus meteai from the Sinap Formation of central Anatolia. Nature, 382, pp. 349-51.
Andrews, P. (1988) Hominoidea. In: Tattersall et al. (Eds.).
Andrews, P. (1995) Ecological apes and ancestors. Nature, 376, pp. 555-6.
Arbas, E.A. et al. (1991) Evolution in nervous systems. Ann. Rev. Neurosci., 14, pp. 9-38.
Asfaw, B. et al. (1999) Australopithecus garhi: A new species of early hominid from Ethiopia. Science, 284: 629-35.
Bailey, K.G. (1987) Human Paleopsychology: Applications to Aggression and Pathological Processes. London: Erlbaum.
Barash, D.P. (1982) Sociobiology and Behavior. New York: Elsevier.
Barkow, J.H; L. Cosmides & J. Tooby (Eds.) (1992) The Adapted Mind: Evolutionary Psychology and the Generation of Culture. New York: Oxford Univ. Press.
Barnett, S.A. (1963) The Rat: A Study in Behaviour London: Methuen.
Bateman, A.J. (1948) Intra-sexual selection in Drosophila. Heredity, 2, 3, pp. 349-68.
Bellomo, R.V. (1994) Methods of determining early hominid behavioral activities associated with the controlled use of fire at FxJj 20 main, Koobi Fora, Kenya. J. Human Evol., 27, pp. 173-96.
Benefit, B.R. & M.L. McCrossin (1995) Miocene hominoids and hominid origins. Ann. Rev. Anthropol., 24, pp. 237-56.
Bermudez de Castro J.M., Arsuaga J., Carbonell E., Rosas A., Martinez I., and Mosquera M. (1997) A hominid from the lower Pleistocene of Atapuerca, Spain: possible ancestor to Neandertals and modern humans. Science, 276, pp. 1392-5.
Bichakjian, B.H. (2001) An Australian challenge to the Out-of-Africa theory. LOS Forum, 32, pp. 5-6.
Boesch, C. & M. Tomasello (1998) Chimpanzee and human cultures. Current Anthropol., 39, 5, pp. 591-614.
Borgia, G. (1979) Sexual selection and the evolution of mating systems. In: M.S. Blum & N.A. Blum (Eds.) Sexual Selection and Reproductive Competition in Insects. New York: Academic Press, pp. 19-80.
Boyd, R. & J.B. Silk (1997) How Humans Evolved. New York: Norton.
Bradshaw, J.L.(1997) Human Evolution: A Neuropsychological Perspective. Hove.
Brain, C.K. & A. Sillen (1988) Evidence from the Swartkrans cave for the earliest use of fire. Nature, 336, pp. 464-66.
Brown, D.E. (1991) Human Universals. New York: McGraw-Hill.
Brown, D.E. (1999) Human nature and history. History & Theory, 38, 4, pp. 138-57.
Brown, P. et al. (2004) A new small-bodied hominin from the Late Pleistocene of Flores, Indonesia. Nature, 431, pp. 1055-61.
Brunet, M. et al. (2002) A new hominid from the Upper Miocene of Chad, Central Africa. Nature, 418, pp. 145-51.
Burenhult, G. (1993) Towards Homo sapiens, 2,5 million years ago - 35,000 years ago: Habilines, Erectines, and Neanderthals. In: Burenhult, G. (Ed.) The First Humans: Human Origins and History to 10,000 B.C. San Francisco: HarperCollins.
Calvin, W.H. (1986) The River that Flows Uphill: A Journey from the Big Bang to the Big Brain. New York: Macmillan.
Cann, R.L. (1988) DNA and human origins. Ann. Rev. Anthropol., 17, pp. 127-43.
Cann, R.L., M. Stoneking & A.C. Wilson (1987) Mitochondrial DNA and human evolution. Nature, 325, pp. 31-36.
Carbonell, E. et al. (1995) Lower Pleistocene hominids and artifacts from Atapuerca-TD 6 (Spain). Science, 269, pp. 826-30.
Carew, T.J. & C.L. Sahley (1986) Invertebrate learning and memory: From behavior to molecules. Ann. Rev. Neurosci., 9, pp. 435-87.
Carpenter, C.C. (1967) Aggression and social structure in iguanid lizards. In: W.W. Milstead (Ed.) Lizard Ecology. Columbia: Univ. Missouri Press.
Carpenter, C.C. (1977) A survey of stereotyped reptilian behaviour patterns. In: S. Gans & D. Tinkle (Eds.) Biology of the Reptilia, Vol. 7. London: Academic Press.
Cavalli-Sforza, L.L. et al. (1998) Genes, Peoples and Languages. New York: North Point Press.
Clutton-Brock, T.H. (Ed.)(1988) Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. Chicago: Chicago Univ. Press.
Cooper, A. et al. (2001) Human origins and ancient human DNA. Science, 292, pp. 1655-6.
Corning, P.A. (1983) The Synergism Hypothesis: A Theory of Progressive Evolution. New York: McGraw-Hill.
Corning, P.A. (1995) Co-operative genes: Synergy and the bioeconomics of evolution. Paper ESS Conf., Cambridge. Aug. 3-6, 1995. Also in: Van der Dennen, Smillie & Wilson (Eds.), 1999, pp. 26-45.
Cory, G.A. (1998) MacLean's triune brain concept: in praise and appraisal. ASCAP, 11, 7, pp. 6-19.
Crow, J.F. (1987) The importance of recombination. In: Michod & Levin (Eds.), pp. 56-73.
Daly, M. & M. Wilson (1978) Sex, Evolution and Behavior. North Scituate MA: Duxbury Press.
Dart, R.A. (1925) Australopithecus africanus: The man-ape of South Africa. Nature, 115, pp. 195-99.
Darwin, C.R. (1871) The Descent of Man, and Selection in Relation To Sex. (2 Vols.) London: Murray.
Davies, M.(1998) Understanding the EEA - A book review of Rock Potts' Humanity's Descent: The Consequences of Ecological Instability. ASCAP, 11, 3, 1998, pp. 7-11.
Dawkins, R. (1976 / 1989) The Selfish Gene. Oxford: Oxford Univ. Press.
Dawkins, R. (1986) The Blind Watchmaker: Why the Evidence of Evolution Reveals a Universe without Design. London: Longmans.
Dawkins, R. (1995) River out of Eden: A Darwinian View of Life. New York: Basic Books.
Dawkins, R. (1996) Climbing Mount Improbable. New York: Viking.
De Duve, C. (1996) The birth of complex cells. Sci. Amer., 274, 4, pp. 28-45.
De Waal, F.B.M. (1988) The communicative repertoire of captive bonobos (Pan paniscus) compared to that of chimpanzees. Behav., 106, 3-4, pp. 183-251.
Deacon, T.W. (1997) The Symbolic Species: Co-Evolution of Language and the Brain. New York: Norton.
Diamond, J. (1991) The Rise and Fall of the Third Chimpanzee: Evolution and Human Life. London: Hutchinson.
Dilkes D.W. & R.R. Reisz (1996) First record of a basal synapsid ('mammal-like reptile') in Gondwana. Proc. Roy. Soc. London, B263, pp. 1165-70.
Dunbar, R.I.M. (1992) Mating and parental care. In: Jones, Martin & Pilbeam (Eds.), pp. 150-54.
Dunbar, R.I.M. (1992) Neocortex size as a constraint on group size in primates. J. Human Evol., 22, pp. 469-94.
Dunbar, R.I.M. & L. Barrett (2001) Apen. Onze verwanten. Baarn: Bosch & Keuning.
Dyson, F. (1985) The Origins of Life. Cambridge: Cambridge Univ. Press.
Easteal, S. & G. Herbert (1997) Molecular evidence from the nuclear genome for the time frame of human evolution. J. Molecular Evol., 44, pp. S121-32.
Edelman, G.M. (1989) The Remembered Present: A Biological Theory of Consciousness. New York: Basic Books.
Edelman, G.M. (1992) Bright Air, Brilliant Fire: On the Matter of the Mind. New York: Basic Books.
Eibl-Eibesfeldt, I. (1998) Us and the Others: the familial roots of ethnonationalism. In: I. Eibl-Eibesfeldt & F.K. Salter (Eds.) Indoctrinability, Ideology and Warfare: Evolutionary Perspectives. New York: Berghahn, pp. 21-54.
Evans, L.T. (1938) Cuban field studies on territoriality of the lizard, Anolis sagrei. J. Comp. Psychol., 25, pp. 97-125.
Fisher, H.E. (1993) The Anatomy of Love: The Natural History of Monogamy, Adultery and Divorce. New York: Simon& Schuster.
Foley, J. (1996) Prominent hominid fossils. http://www.talkorigins.org/faqs/homs/specimen.html
Foley, J. (1997/2001/2004) Hominid species and recent developments in paleoanthropology. http://www.talkorigins.org/faqs/homs/recent.html.
Foley, R.A. (1987) Another Unique Species: Patterns in Human Evolutionary Ecology. Harlow: Longman.
Foley, R.A. (1995) Humans Before Humanity. Oxford: Blackwell.
Foley, R.A. (1996) An evolutionary and chronological framework for human social behavior. In: Runciman, Maynard Smith & Dunbar (Eds.), pp. 95-117.
Foley, R.A. (1998) Genes, evolution, and diversity: Yet another look at the problem of modern human origins. Evol. Anthropol., 6, 6, pp. 191-93.
Foley, R.A. (2001) In the shadow of the modern synthesis? Alternative perspectives on the last fifty years of paleoantropology. Evol. Anthropol., 10, 1, pp. 5-14.
Fortey, R. (1998) Life: An Unauthorized Biography. New York: HarperCollins.
Furlow, B. (2000) The enemy within. NewScientist, 2252, Aug. 19, pp. 38-41.
Gajdusek, D.C. (1970) Physiological and psychological characteristics of Stone Age man. In: Engineering and Science. Pasadena: Calif. Inst. Techology.
Gazzaniga, M. (Ed.) (1995) The Cognitive Neurosciences. Cambridge MA: MIT Press.
Geary, D.C. (1998) Male, Female: The Evolution of Human Sex Differences. Washington DC: Amer. Psychol. Assoc.
Ghiselin, M.T. (1974) The Economy of Nature and the Evolution of Sex. Berkeley: Univ. of California Press.
Gibson, K.R. & T. Ingold (Eds.)(1993) Tools, Language and Cognition in Human Evolution. New York: Cambridge Univ. Press.
Goodall, J. (1968) The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Anim. Behav. Monogr., 1, 3, pp. 161-311.
Goodall, J. (1986) The Chimpanzees of Gombe: Patterns of Behavior. Cambridge MA: Harvard Univ. Press.
Gore R. (1996) Neandertals. National Geographic, 189, Jan., pp. 2-35.
Gould, S.J. (1994) The evolution of life on the earth. Sci. Amer., Oct., pp. 63-69.
Gowlett, J.A.J. et al. (1981) Early archaeological sites, hominid remains, and traces of fire from Chesowanja, Kenya. Nature, 294, pp. 125-29.
Greenberg, B. & G.K. Noble (1944) Social behavior in the American chameleon (Anolis carolensis Voigt).Physiol. Zool., 17, pp. 392-439.
Greenberg, N. & P.D. MacLean (1978) The Behavior and Neurology of Lizards. Washington DC: USGPO.
Gribbin, J. & J. Cherfas (2001) The Mating Game: In Search of the Meaning of Sex. London: Penguin.
Gribbin, J. & J. Cherfas (2001) The First Chimpanzee: In Search of Human Origins. London: Penguin.
Gribbin, M. & J. Gribbin (1993) Being Human: Putting People in an Evolutionary Perspective. London: Dent.
Gunnell, G.F. & E.R. Miller (2001) Origin of Anthropoidea: Dental evidence and recognition of early anthropoids in the fossil record, with comments on the Asian anthropoid radiation. Amer. J. Phys. Anthropol., 114, 3, pp. 177-91.
Haile-Selassie Y. (2001) Late Miocene hominids from the Middle Awash, Ethiopia. Nature, 412, pp. 178-81.
Haile-Selassie Y., Suwa G., and White T.D. (2004) Late Miocene teeth from Middle Awash, Ethiopia, and early hominid dental evolution. Science, 303, pp. 1503-5.
Harris, D.R. (1992) Human diet and subsistence. In: Jones, Martin & Pilbeam (Eds.), pp. 69-74.
Harris, M. (1975) Culture, Man, and Nature. 2nd ed. New York: Thomas Lowell.
Harrison, G.A. et al. (1988) Human Biology. 3rd ed. Oxford Univ. Press.
Harvey, P.A. & A.F. Read (1992) Home range and territory. In: Jones, Martin & Pilbeam (Eds.), pp. 155-56.
Haywood, J. (1995) The Illustrated History of Early Man. London: Bison Books.
Hebb, D.O. & W.R. Thompson (1968) The social significance of animal studies. In G. Lindzey & E. Aronson (Eds.) The Handbook of Social Psychology. Reading MA: Addison-Wesley, pp. 729-774
Holloway, R.L. (Ed.) (1974) Primate Aggression, Territoriality and Xenophobia: A Comparative Perspective. New York: Academic Press.
Hrdy, S.B. (1981/1991) The Woman that Never Evolved. Cambridge MA: Harvard Univ. Press.
Hublin, J.J. et al. (1996) A late Neanderthal associated with Upper Palaeolithic artefacts. Nature, 381, pp. 224-26.
Hunt, K.D. (1997) Transitional vertebrate fossils FAQ. Talk Origins Archive.
Isaacs, S. (1933) Social Development in Young Children. London: Routledge.
Jerison, H.J. (1973) The Evolution of the Brain and Intelligence. New York: Academic Press.
Johanson, D.C. & K. O'Farrell (1990) Journey from the Dawn: Life with the World's First Family. New York: Villard Books.
Johnson, G.R. (1995) The evolutionary origins of government and politics. In; & A.O. Somit & J.A. Losco (Eds.) Research in Biopolitics: Vol. 3: Human Nature and Politics. Greenwich CT: JAI Press, pp. 243-305.
Jones, O.D. (1997) Evolutionary analysis in law: An introduction and application to child abuse. North Carolina Law Rev., 75, pp. 1117-1242.
Jones, S. (2000) Almost like a Whale: The 'Origin of Species' Updated. New York: Anchor Books.
Jones, S.; R. Martin & D. Pilbeam (Eds.) (1992) The Cambridge Encyclopedia of Human Evolution. Cambridge: Cambridge Univ. Press.
Keegan, J. (1993) A History of Warfare. New York: Vintage Books.
Kevles, B. (1986) Females of the Species: Sex and Survival in the Animal Kingdom. Cambridge MA: Harvard Univ. Press.
Kinzey, W.G. (Ed.) The Evolution of Human Behavior: Primate Models. Albany: SUNY Press.
Kortlandt, A. (1972) New Perspectives on Ape and Human Evolution. Amsterdam: Stichting voor Psychobiologie.
Krings M. et al. (1997) Neandertal DNA sequences and the origin of modern humans. Cell, 90, pp. 19-30.
Kroeber, A.L. (1948) Anthropology: Race, Language, Culture, Psychology, Prehistory. rev. ed., London: Harrap.
Kunzig R. (1997) The face of an ancestral child. Discover, 18, pp. 88-101.
Lahr, M.M. & R. Foley (2004) Human evolution writ small. Nature, 431, pp. 1043-44.
Langer, S. (1941) Philosophy in a New Key: A Study in the Symbolism of Reason, Rite, and Art. Cambridge MA: MIT Press.
Leakey, M. & A. Walker (1997) Early hominid fossils from Africa. Sci. Amer., 276, 6, pp. 74-79.
Leakey, M. et al. (1995) New four-million-year old hominid species from Kanapoi and Allia Bay, Kenya. Nature, 376, pp. 365-71.
Leakey M. et al. (2001) New hominin genus from eastern Africa shows diverse middle Pliocene lineages. Nature, 410, pp. 433-40.
Leakey, R.E. & R. Lewin (1979) People of the Lake: Man; His Origins, Nature, and Future. London: Collins.
Leakey, R.E. & R. Lewin (1995) The Sixth Extinction: Patterns of Life and the Future of Humankind. New York: Doubleday.
Lorenz, K. (1966) On Aggression. London: Methuen.
Lovejoy, C.O. (1981) The origin of man. Science, 211, 4480, pp. 341-50.
Lovejoy (1988) Evolution of human walking. Sci. Amer., 259, 5, pp. 118-25.
Low, B.S. (2000) Why Sex Matters: A Darwinian Look at Human Behavior. Princeton: Princeton Univ. Press.
Mackenzie, P. (1999) Elephant information repository. http://www.elehost.com.
Mackie, G.O. (1990) The elementary nervous system revisited. Amer. Zool., 30, p. 917.
MacLean, P.D. (1990) The Triune Brain in Evolution: Role in Paleocerebral Functions. New York: Plenum Press.
Makalowski, W. (2003) Not junk after all. Science, 300, pp. 1246-47.
Margulis, L. & D. Sagan (1991) Mystery Dance: On the Evolution of Human Sexuality. New York: Summit Books.
Margulis, L. & D. Sagan (1995) What is Life? New York: Simon & Schuster.
Margulis, L. & D. Sagan (1997) What is Sex?. Old Tappan NJ: Simon & Schuster.
Marshack, A. (1996) A Middle Paleolithic symbolic composition from the Golan Heights: The earliest known depictive image. Current Anthropol., 37, pp. 357-64.
Martin, R.D. (1992) Primate Origins and Evolution: A Phylogenetic Reconstruction. Princeton: Princeton Univ. Press.
Mayell, H. (2002) 'Journey' redraws humans' family tree. http://news.nationalgeographic.com.news/2002/12/1212_021213_journeyofman.html
Maynard Smith, J. (1989) Games, Sex, and Evolution. Harvester & Wheatsheaf.
Maynard Smith, J. & E. Szathmáry (1995) The Major Transitions in Evolution. Oxford: Freeman.
Mayr, E. (1974) Behavioral programs and evolutionary strategies. Amer. Narturalist, 62, pp. 650-59.
McBrearty, S. & A.S. Brooks, (2000) The revolution that wasn't: A new interpretation of the origin of modern human behavior. J. Human Evol., 39, 5, pp. 453-63.
McHenry, H.M. (1982) The pattern of human evolution: Studies of bipedalism, mastication, and encephalization. Ann. Rev. Anthropol., 11, pp. 151-73.
McLeod, M. (2000) One small step for fish, one giant leap for us. NewScientist, 2252, Aug. 19, pp. 28-32.
Mealey, L. (2000) Sex Differences: Developmental and Evolutionary Strategies. San Diego: Academic Press.
Michod, R.E. (1995) Eros and Evolution: A Natural Philosophy of Sex. Reading MA: Addison-Wesley.
Michod, R.E. & B.R. Levin (Eds.) (1987) The Evolution of Sex: An Examination of Current Ideas. Sunderland: Sinauer.
Miller, G.F. (2000) The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature. London: Heinemann.
Miller, E.R., G.F. Gunnell, G.F. & R.D. Martin (2005) Deep time and the search for anthropoid origins. Yearbook of Physical Anthropology, 48, pp. 60-95.
Milton, K.(1993) Diet and primate evolution. Sci. Amer., August, pp. 70-77.
Moran, L. (1993) Random genetic drift. http://www.talkorigins.org/faqs/ genetic-drift.html
Morgan, E. (1982) The Aquatic Ape. London: Souvenir Press.
Morgan, E. (1990) The Scars of Evolution: What Our Bodies Tell Us about Human Origins. Harmondsworth: Penguin.
Morgan, E. (1997) The Aquatic Ape Hypothesis - The Most Credible Theory of Human Evolution. London: Souvenir.
Morwood, M.J. et al. (2004) Archaeology and age of a new hominin from Flores in eastern Indonesia. Nature, 431, pp. 1087-91.
Naccache, A.F.H. (1999) A brief history of evolution. History & Theory, 38, 4, pp. 10-32.
Newcombe, H. (1998) Transformations of aggression. Peace Res. Rev., 14, 5, pp. 81-88.
Northcutt, R.G. & J.H. Kaas (1995) The emergence and evolution of mammalian neocortex. Trends in Neurosciences, 18, pp. 373-79.
Orgel, L.E. & F.H.C. Crick (1980) Selfish DNA: The ultimate parasite. Nature, 284, pp. 604-7.
Parker, G.A. (1984) Evolutionarily stable strategies. In: J.R. Krebs & N.B. Davies (Eds.) Behavioural Ecology: An Evolutionary Approach. Oxford: Blackwell, pp. 30-61.
Parker, G.A. (1978) The evolution of competitive mate searching. Ann. Rev. Entomol., 23, pp. 173-96.
Parker, G.A. (1984) Sperm competition and the evolution of animal mating strategies. In: R.L. Smith (Ed.), pp. 1-60.
Parker, G.A. & L.W. Simmons (1996) Parental investment and the control of selection: Predicting the direction of sexual competition. Proc. Roy. Soc. London, B263, pp. 315-21.
Parker, S.T. (1987) A sexual selection model for hominid evolution. Human Evol., 2, 3, pp. 235-53.
Pittendrigh, C.S. (1958) Adaptation, natural selection, and behavior. In A. Roe & G.G. Simpson (Eds.), Behavior and Evolution. New Haven: Yale Univ. Press, pp. 390-416.
Poirier, F.E. (1993) Understanding Human Evolution. Englewood Cliffs: Prentice-Hall.
Potts, R.B. (1996) Humanity's Descent: The Consequences of Ecological Instability. New York: William Morrow.
Pugh, G.E. (1978) The Biological Origins of Human Values. London: Routledge & Kegan Paul.
Reader, J. (1986) The Rise of Life: The First 3.5 Billion Years. London: Collins.
Reiss, D. (1998) Cognition and communication in dolphins: A question of consciousness. In: S.R. Hameroff et al. (Eds.) Toward a Science of Consciousness. Cambridge MA: MIT Press, pp. 551-60.
Reynolds, V.; V.S.E. Falger & I. Vine (Eds.) (1987) The Sociobiology of Ethnocentrism: Evolutionary Dimensions of Xenophobia, Discrimination, Racism and Nationalism. London: Croom Helm.
Richards, G. (1987) Human Evolution: An Introduction for the Behavioural Sciences. London: Routledge & Kegan Paul.
Ridley, M. (1993) Evolution. Boston: Blackwell.
Ridley, M. (1994) The Red Queen: Sex and the Evolution of Human Nature. New York: Macmillan.
Ridley, M. (1999/2000) Genome: The Autobiography of a Species in 23 Chapters. London: Fourth Estate.
Rizzolatti, G. & M.A. Arbib (1998) Language within our grasp. Trends in Neurosciences, 21, pp. 188-94.
Rodman, P.S. & H.M. McHenry (1980) Bioenergetics and the origin of hominid bipedalism. Amer. J. Phys. Anthropol., 52, pp. 103-6.
Roede, M.J. et al. (1991) The Aquatic Ape: Fact or Fiction? London: Souvenir Press.
Rook, L. et al. (1999) Oreopithecus was a bipedal ape after all, Proc. Natl. Acad. Sci. USA, 96, pp. 8795-9
Ross, C.F. (2000) Into the light: The origin of the Anthropoidea. Ann. Rev. Anthropol., 29, pp. 147-94.
Ross, C.F.; B. Williams & R.F. Kay (1998) Phylogenetic analysis of anthropoid relationships. J. Human Evol., 35, 3, pp. 221-306.
Runciman, W.G.; J. Maynard Smith & R.I.M. Dunbar (Eds.) (1996) Evolution of Social Behaviour Patterns in Primates and Man. Oxford: Oxford Univ. Press.
Ruse, M. (1986) Taking Darwin Seriously: A Naturalistic Approach to Philosophy. Oxford: Blackwell.
Samuilov, V.D.; A.V. Oleskin & E.M. Lagunova (2000) Programmed cell death. Biochemistry (Moscow), 65, 8, pp. 873-87.
Sarich, V.M. & A.C. Wilson (1967) Immunological time scale for hominid evolution. Science, 158, pp. 1200-1203.
Sarich, V.M. & A.C. Wilson (1969) A molecular time scale for human evolution. Proc. Nat. Acad. Sciences, 63, pp. 1088-1093.
Schaller, G.B. (1963) The Mountain Gorilla: Ecology and Behavior. Chicago: Univ. Chicago Press.
Scott, J.P. (1969) The biological basis of human warfare: An interdisciplinary problem. In: M. Sheriff & C.W. Sheriff (Eds.) Interdisciplinary Relationships in the Social Sciences. Chicago: Aldine, pp. 121-36.
Senior, K. (2000) So just how did life start on Earth? The Lancet, 355, March 4, p. 814.
Senut, B. et al. (2001) First hominid from the Miocene (Lukeino Formation, Kenya). Comptes Rendus de l'Acad. Sciences Paris, 332, pp. 137-44.
Shipman. P. (1984) Scavenger hunt. Natural History, 93, pp. 20-27.
Sillen, A. & C.K. Brain (1990) Old flame. Natural History, April, pp. 6-11.
Sinclair, A.R.E.; M.D. Leakey & M. Norton (1986) Migration and hominid bipedalism. Nature, 324, pp. 307-8.
Slack, J.M.W.; P.W.H. Holland & C.F. Graham (1993) The zootype and the phylotypic stage. Nature, 361: 490-2.
Slurink, P. (1989) Natuurlijke selectie en de tragiek van de menselijke idealen. Delft: Eburon.
Slurink, P. (1994) Causes of our complete dependence on culture. In: R.A. Gardner et al. (Eds.) The Ethological Roots of Culture. Dordrecht: Kluwer, pp. 461-74.
Slurink, P. (1999) Culture and the evolution of the human mating system. In: Van der Dennen, Smillie & Wilson (Eds.), pp. 135-61.
Slurink, P. (2002) Why Some Apes Became Humans: Competition, Consciousness and Culture. Nijmegen: P.S. Press.
Smith, R.L. (Ed.) (1984) Sperm Competition and the Evolution of Animal Mating Systems. New York: Academic Press.
Smith, B.H. & R.L. Tompkins (1995) Toward a life history of the Hominidae. Ann. Rev. Anthropol., 24, pp. 257-79.
Soares, C. (2001) Talking heads. New Scientist, April 14, pp. 26-29.
Southwick, Ch.H. et al. (1974) Xenophobia among free-ranging rhesus groups in India. In: Holloway (Ed.), pp. 185-210.
Stanley, S.M. (1996) Children of the Ice Age: How a Global Catastrophe Allowed Humans to Evolve. Washington DC: Science News Books.
Stearns, S.C. (Ed.)(1988) The Evolution of Sex and its Consequences. Basel: Birkhauser Verlag.
Stewart C.-B. & T.R. Disotell (1998) Primate evolution: In and out of Africa. Current Biol., 8, pp. R582-588.
Stringer, C.B. & P. Andrews (1998) Genetic and fossil evidence for the origin of modern humans. Science, 239, pp. 1263-68.
Susman, R.L. (1994) Fossil evidence for early hominid tool use. Science, 265, pp. 1570-73.
Suzuki, D.T. et al. (1989) An Introduction to Genetic Analysis. 4th ed. Freeman, NY.
Symons, D. (1979) The Evolution of Human Sexuality. Oxford: Oxford Univ. Press.
Szathmáry, E. & J. Maynard Smith (1995) The major evolutionary transitions. Nature, 374, pp. 227-32.
Tanner, N.M. (1981) On Becoming Human: A Model of the Transition from Ape to Man and the Reconstruction of Early Human Social Life. Cambridge: Cambridge Univ. Press.
Tattersall, I. (1993) The Human Odyssey: Four Million Years of Human Evolution. New York: Simon & Schuster.
Tattersall, I. (1995) The Fossil Trail: How We Know What We Think We Know About Human Evolution. New York: Oxford Univ. Press.
Tattersall, I. & Schwartz (1999) Hominids and hybrids: The place of Neanderthals in human evolution. Proc. Nat. Acad. Sciences USA, 96, pp. 7117-19.
Tattersall, I.; E. Delson & J. van Couvering (Eds.) (1988) Encyclopedia of Human Evolution and Prehistory. New York: Garland.
Tobias, P.V. (1998) Water and human evolution. Out There, 35, pp. 38-44.
Tooby, J. & L. Cosmides (1992) The psychological foundations of culture. In: Barkow et al. (Eds.), pp. 19-136.
Trinkaus E. & Howells W.W. (1979) The neanderthals. Sci. Amer., 41, 6, pp. 118-33.Trinkaus E. & Shipman P. (1992) The Neandertals: Changing the Image of Mankind. New York: Alfred E. Knopf.
Trivers, R.L. (1972) Parental investment and sexual selection. In: B. Campbell (Ed.) Sexual Selection and the Descent of Man, 1871-1971. Chicago: Aldine, pp. 136-79.
Trivers, R.L. (1985) Social Evolution. Menlo Park: Benjamin/Cummings.
Underhill, P.A. et al., (2000) Y chromosome sequence variation and the history of human populations. Nature Genetics, 26, pp. 358-61.
Van der Dennen, J.M.G. (1987) Ethnocentrism and in-group/out-group differentiation. In: Reynolds, Falger & Vine (Eds.), pp. 1-47.
Van der Dennen, J.M.G. (Ed.) (1992) The Nature of the Sexes: The Sociobiology of Sex Differences and the 'Battle of the Sexes'. Groningen: Origin Press.
Van der Dennen, J.M.G. (1995) The Origin of War: The Evolution of a Male-Coalitional Reproductive Strategy. Groningen: Origin Press.
Van der Dennen, J.M.G.; D. Smillie & D.R. Wilson (Eds.) (1999) The Darwinian Heritage and Sociobiology. Westport CT: Greenwood Press.
Verhaegen, M.J.B. (1987) Origin of hominid bipedalism. Nature, 325, pp. 305-6.
Verhaegen, M.J.B. (1993) Aquatic versus savanna: Comparative and paelo-environmental evidence. Nutrition & Health, 9, pp. 165-91.
Verhaegen, M.J.B. (1985) The Aquatic Ape Theory: Evidence and a possible scenario. Medical Hypotheses, 16, 16-17.
Verhaegen, M,J.B. & S. Munro (2001) New ideas on ape and human evolution. http://www.onelist.com/community/AAT.
Verhaegen, M.J.B., N. McPhail & S. Munro (1999) Bipedalism in chimpanzee and gorilla forebears. ESS Newsletter, 50, pp. 4-12.
Villarreal, L.P. (2004) Are viruses alive? Sci. Amer., 291, 6, Dec., pp. 77-81
Wells, S. (2003) The Journey of Man: A Genetic Odyssey. Princeton: Princeton Univ. Press
Wheeler, P.E. (1984) The evolution of bipedality and loss of functional body hair in hominids. J.Human Evol., 13, pp. 91-98.
White, T.D.; G. Suwa & S. Asfaw (1994) Australopithecus ramidus: A new species of early hominid from Aramis, Ethiopia. Nature, 371, pp. 306-12.
White, T.D.; G. Suwa & S. Asfaw (1995) Corrigendum. Nature, 375, p.88.
Whitehead, H. (1998) Cultural selection and genetic diversity in matrilineal whales. Science, 282, pp. 1708-11.
Whiten, A. et al. (1999) Cultures in chimpanzees. Nature, 399, pp. 682-85.
Williams, G.C. (1966) Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton: Princeton Univ. Press
Williams, G.C. (1975) Sex and Evolution. Princeton: Princeton Univ. Press.
Wilson, E.O. (1971) The Insect Societies. Cambridge MA: Belknap Press.
Wilson, E.O. (1975) Sociobiology: The New Synthesis. Cambridge MA: Harvard Univ. Press.
Wilson, E.O. (1978) On Human Nature. Cambridge MA: Harvard Univ. Press.
Wolde, G. et al. (2001) Geology and paleontology of the Late Miocene Middle Awash Valley, Afar Rift, Ethiopia. Nature, 412, pp. 175-78.
Wood, B.A. (1992) Origin and evolution of the genus Homo. Nature, 355, pp. 783-90.
Wood, B.A. (1994) The oldest hominid yet. Nature, 371, pp. 280-81.
Wood, B.A. (2002) Hominid revelations from Chad. Nature, 418, pp. 133-35.
Wood, B.A. & M. Collard (1999) The changing face of genus Homo. Evol. Anthropol., 8, 6, pp. 195-207.
Worden, R.P. (1998) The evolution of language from social intelligence. In: J.R. Hurford et al. (Eds.) Approaches to the Evolution of Language: Social and Cognitive Bases. Cambridge: Cambridge Univ. Press.
Wourms, J.P & I.P. Callard (1992) A retrospect to the symposium on evolution of viviparity in vertebrates. Amer. Zool., 32, pp. 251-55.
Wrangham, R.W. (1987) The significance of African apes for reconstructing human social evolution. In: W.G. Kinzey (Ed.), pp. 57-71.
Wrangham, R.W. & D. Peterson (1996) Demonic Males: Apes and the Origins of Human Violence. Boston: Houghton Mifflin.
Wright, R. (2001) Nonzero: History, Evolution & Human Cooperation. London: Abacus.
Wuketits, F. (1982) Grundriss der Evolutionstheorie. Darmstadt: Wissenschaftliche Buchgesellschaft.
Wuketits, F.M. (1999) Die Selbstzerstörung der Natur. Evolution und die Abgründe des Lebens. Düsseldorf: Patmos.
Wynn, T. & W.C. McGrew (1991) An ape's view of the Oldowan. Man, N.S., 24, pp. 383-98.
1. About a thousand genes are shared by every organism, however simple or complicated. Although their common ancestor must have lived more than a billion years ago, their shared structure can still be glimpsed. It shows how the grand plan of life has been modified through the course of evolution.
Such genes show that animals with backbones are close to starfish; and that worms and snails live on a different branch from insects and roundworms (both of whom shed their coats as they grow). Their shared root lies within an ancestor who lived hundreds of millions of years before any life appeared in the rocks.
Biology's greater divisions are at first sight self-evident. Men and chimps are close kin, each is less related to worms, and bananas and bacteria are quite separate. However, new taxonomy has transformed the tree of life into an exotic plant. Men and chimps are indeed more related than men and bananas, but humans, insects and plants are - DNA shows - all mere twigs on the same branch. Its trunk has suffered some radical changes of shape.
Living beings were once divided into five kingdoms of more or less equal size (animals, plants, fungi, protozoa - such as the familiar amoeba - and bacteria). Bacteria were out on somewhat of a limb, as their genes are not contained in a cell nucleus. They seemed otherwise not much more distinct from other beings than plants were from animals. Now a radical new logic has emerged. The DNA reveals that plants and animals lie close together. Mushrooms deserve a branch on their own, closer to animals than to plants (Jones, 2000: 376-77).
The genes do for life what the Plan du Métro does for Paris: they reveal the real and unexpected contours of the great city of existence.
On the true chart of the genes, the bacteria occupy a great Wimbledon of life: a large neighborhood of their own, with the archaea in the suburb next door. Three groups known as the diplomonads, trichomonads and microsporidians are diffused through a nearby district. They sound obscure, but among them are the gut parasite that causes severe cases of travellers' diarrhoea and a single-celled creature responsible for inflammation of the vagina. Although they have a cell nucleus, such creatures lack mitochondria.
The rest of town is filled with creatures blessed with both those useful structures. Kinetoplastids - single-celled animals with a tail that lashes them through the water include agents of disease such as the trypanosome that might, perhaps, have infected Darwin in South America and led to his many years of invalidism. Next door is a thriving group of amoeba-like creatures; and two separate groups of slime moulds (much used in the study of development). Alveolates include the ciliates (single-celled animals covered with fine mobile hairs), the agent of malaria, and the dinoflagellates, creatures enclosed within the solid shells that make up much of the chalk that covers southern England.
Some areas traditionally seen as one are, like the East End of London, in fact several, of different character. The algae - seaweeds, waterweeds and the green film found on tree trunks - comprise three separate groups, each with an identity as distinct as is that of the animals from the plants. Red algae, on a branch of their own, include the seaweeds much eaten in Japan, together with others that make reefs. The brown algae contain familiar seaweeds such as kelp, but they belong with diatoms, tiny shelled creatures that abound in the ocean, in a group called the stramenopiles. Green algae, found in freshwater ponds, are different again, and live close to the familiar plants. Plants, animals and fungi are near neighbors in a well-explored but minor part of the metropolis of life (Jones, 2000: 383-84).
2. Margulis & Sagan (1997), in their magnificent book What is Sex?, note that in humans the sexual urge has fused with love and pair bonding:
"The poets speak of the special light in which the beloved is bathed. Novelists write of infatuation. Many romances depict the dangers lovers bring upon themselves by following their urges to sexually couple. Powerful biochemical changes - from the production of the natural amphetamine-like drug phenylethylamine during the initial 'rush' of physical attraction to elevated levels of the hormone oxytocin during and after orgasm - correlate with lust, love and pair bonding. These inevitable body-produced, mind-altering drugs are part of the biochemical arsenal by which our natures entice us to seek mates and produce offspring. We, like many other animals, sometimes risk our own survival for the chance to inject our genes into the next generation".
3. Endogenous retroviruses
Researchers agree that the key to the puzzle of autoimmunity must lie in the major histocompatibility complex (MHC) - our immune system genes. The MHC is an usually diverse region of the genome, which probably reflects our intense and ongoing co-evolutionary arms race with countless disease organisms. Each MHC gene in a population can have dozens of versions - or alleles - although only a couple of these will be present in any given individual. Over 200 MHC genes are packed tightly together in our genome and their job is to produce proteins that detect and destroy invaders.
But some MHC alleles or haplotypes - combinations of alleles - have a major drawback: people who carry them are more likely to get an autoimmune disease. The widely accepted view is that a risky allele must be switched on before it turns traitor. The trigger is thought to be bits of foreign proteins, from food or infectious invaders, that resemble the body's own proteins. But Graham Boyd does not attribute autoimmune diseases to molecular mimics at all. Instead, Boyd and a growing number of like-minded theorists point to what at first glance may seem an unlikely culprit: ancient viruses stuck in the human genome, known as endogenous retroviruses or ERVs.
Outlandish as it sounds, we are the genetic descendants of viruses as well as primates. The viral ancestors of ERVs invaded the cells of out forebears durings infections millions of years ago and liked it so much they decided to stay. Happily integrated into their new home, ERVs have become part of our own genome, passed down through the generations.
ERVs are relatively simple creatures, genetically speaking. Like wild retroviruses - which include HIV - they have a few genes coding for enzymes and structural proteins. These are sandwiched between long terminal repeat sequences (LTRs), which act like on-off switches regulating the production of viral genes. They are called retroviruses because their genes are encoded in RNA rather than DNA and they infiltrate the host genome by creating DNA copies of themselves. Infected cells may then be tricked into duplicating the viral genes as though they were merely instructions for one of the body's own cellular proteins. ERVs also have the nasty habit of hopping around the genome, duplicating as they go (Furlow, 2000: 38).
Boyd sees viruses and the hosts they live in as opposing teams in a dynamic co-evolutionary arms race. Boyd likens it to long-running tribal warfare. "As the years went by," he says, "there would be a sort of truce whereby the survivors from both sides would generally agree that all aggression should be curbed.". But Boyd believes the truce is an uneasy one. "There would always be renegade rogues on both sides," he says. [O]nce ERVs start producing molecules that look like antigens from wild viruses, MHC genes may kick in to fight off the perceived invasion. The result is an immune attack against your own cells. The question then is why natural selection hasn't eliminated those MHC alleles prone to mistake ERV products for infections. Boyd argues that hosts are in an evolutionary bind, a Darwinian catch-22. So long as wild relatives of ERVs exist in nature and pose a threat, there will be a survival advantage in possessing MHC alleles that can fight them off - even though individuals carrying such alleles are susceptible to autoimmune disease (Furlow, 2000: 40-41).
4. Before cladistics, four-legged vertebrates as a whole - lizards, kangaroos and mammals - were thought to descend from the ancient lobe-finned fish, most of which disappeared four hundred million years ago. Their fins do have a structure at their axis that might have turned into legs. The discovery of a member of this group, the coelacanth, off the coast of Africa in the 1930s was hailed as a 'missing link' between fish and ourselves. Cladistics showed this to be untrue. The coelacanth is not on the same branch as vertebrates with four legs. The honor belongs instead to another great group, the lungfish, who flourished at the same time. Although most modern forms of these fish lack fins altogether (and even those of their fossils are not at all leg-like), an objective look at skeletons puts them closer to ourselves. Now, the molecules have made the case: the coelacanth is indeed further from today's four-legged animals than is any lungfish (Jones, 2000: 374).
5. Bones and molecules, objectively arranged, reveal the truth, according to modern cladistics. The insectivores as an entity disappear altogether and their members shuffle off to other places. The hedgehog is on a first and separate branch in the mammalian family, and the elephant shrew, the golden mole and the aardvark (all once included as insectivores) join manatees, elephants and hyraxes in a conjunction of mammals that evolved in Africa. Other mammals, too, change their alliances. Not only do whales group with hippopotami, but dogs and cats join on as more distant members of their coalition. Men and apes are, it transpires, quite close to rabbits and bats (Jones, 2000: 374).
6. Random genetic drift is a stochastic process (by definition). One aspect of genetic drift is the random nature of transmitting alleles from one generation to the next given that only a fraction of all possible zygotes become mature adults. In a large population this will not have much effect in each generation because the random nature of the process will tend to average out. But in a small population the effect could be rapid and significant. The final result of this random change in allele frequency is that the population eventually drifts to p=1 or p=0. After this point, no further change is possible; the population has become homozygous. A different population, isolated from the first, also undergoes this random genetic drift, but it may become homozygous for allele 'A', whereas the first population has become homozygous for allele 'a'. As time goes on, isolated populations diverge from each other, each losing heterozygosity. The variation originally present within populations now appears as variation between populations (Suzuki et al;, 1989: 704).
Of course, random genetic drift is not limited to species that have few offspring, such as humans. Drift is also not confined to diploid genetics; it can explain why we all have mitochondria that are descended from those of a single woman who lived hundreds of thousands of years ago (This does not mean that there was a single female from whom we are all descended, but rather that out of a population numbering perhaps several thousand, by chance, only one set of mitochondrial genes was passed on).
But random genetic drift is even more than this. It also refers to accidental random events that influence allele frequency, such as 'bottlenecks' caused by natural disasters. Genetic drift caused by bottlenecking may have been important in the early evolution of human populations when calamities decimated tribes. Several examples of bottlenecks have been inferred from genetic data. For example, there is little genetic variation in the cheetah population. This is consistent with a reduction in the size of the population to only a few individuals - an event that probably occurred several thousand years ago. An observed example is the northern elephant seal which was hunted almost to extinction by 1890.
Another example of genetic drift is the founder effect. In this case a small group breaks off from a larger population and forms a new population. This effect is well known in human populations. The founder effect is probably responsible for the virtually complete lack of blood group B in American Indians, whose ancestors arrived in very small numbers across the Bering Strait during the end of the last Ice Age, about 10,000 years ago. More recent examples are seen in religious isolates like the Dunkers and Old Order Amish of North America. These sects were founded by small numbers of migrants from their much larger congregations in central Europe. There are many well studied examples of the founder effect. All of the cattle on Iceland, for example, are descended from a small group that were brought to the island more than one thousand years ago.
Thus, it is wrong to consider natural selection as the only mechanism of evolution (Moran, 1993; Suzuki et al., 1989; Harrison et al., 1988).