Neoteny and Two-Way Sexual Selection in Human Evolution:

A Paleo-Anthropological Speculation on the Origins of Secondary-Sexual Traits, Male Nurturing and the Child as a Sexual Image

an article by David Brin, Ph.D.

Copyright David Brin. All rights reserved. No duplication or resale without permission.

Much progress has been made in tracing the story of human origins, yet mysteries still shroud how we acquired such unique traits as bipedalism, concealed ovulation, and our prodigious brains. Paleo-anthropology suffers from both a dearth of hard data and a surfeit of enthusiastic opinions -- for example, drawing detailed conclusions about evolution from peculiar patterns of fat deposits in male and female anatomies. Or consider the question of why humans have lost nearly all their hair. It has been suggested that this adaptation enabled our ancestors to fill a niche unavailable to other predators -- keeping cool while chasing game under the noonday sun. Alas, this fails to explain why males (the presumed hunters) retain more ancestral hairiness than females, while children have the least of all.¹

As Herbert Spencer once commented about biological speculation -- there is nothing so tragic as a beautiful theory, foiled by an inconvenient fact. Especially in the area of human sociobiology, where evidence is scant and emotions can run high, hypotheses should be offered with good-natured humility.

In that spirit I will focus on the trait of neoteny -- or the retention of childlike characteristics in mature members of a species. This process appears so amplified in humanity that we have been called the neotenous clan of apes. Humans much more closely resemble chimp or gorilla infants than adults of either species, e.g., in the smooth, vertical dome of the forehead and the relative ease of bipedality displayed by very young apes.

Furthermore, even aged humans often retain a plasticity of behavior that is typically found among animals only in the young. Human emphasis on learned, rather than inherited, behavior, has been widely accepted as a chief driver of this trend, requiring our minds to remain supple and receptive for ever-longer spans.

This range of physical and mental traits may have a variety of unrelated causes and/or mechanisms, nevertheless they fall under the same overall theme of retention of childlike characteristics. More formally, William Calvin (1991) identifies paedomorphosis ("becoming child-shaped") as juvenilization of the appearance of the end-product, without implications about the mechanism by which it came about. Neoteny has been taken by many authors to mean the slowing of some or all aspects of somatic development.

Rather than discussing the general neotenization of our species over the last few million years, I wish to concentrate on how neoteny may have become enmeshed as part of a powerful selective cycle, going far beyond its original causes. A complex cycle of sexual selection that may have proved crucial in making human beings unique among animal species.

Our starting point is a perceived dichotomy between adult men and women -- and thus potentially hazardous ground. Although evolutionary biology has lately been defended from a feminist perspective by Patricia Adair Gowaty (1992) and others, caution remains essential when stepping into this arena, hence I will at times seem to belabor the obvious. Let me also emphasize that Homo sapiens appears less riven by sexual dimorphism than most species, and exceptions exist to nearly every generalization. Nevertheless, it seems clear that past and present human dimorphisms are legitimate topics for careful discussion.

While certain neotenous traits seem to be shared equally among the sexes (e.g., curiosity and plasticity of behavior), human females certainly do appear more paedomorphic in outward physical appearance than males. Although they mature at an earlier age, women do not go on to acquire the toughened skin, coarse body hair, thyroid cartilage, bony eye ridges, or deepened voices which are the common inheritance of most adult hominoids and other primates. Jones and Hill (1993) have shown that this generalization remains valid across racial, ethnic and cultural boundaries. Difference in degree of paedomorphism is one of the few truly decisive human sexual-dichotomies, used by most of us in visually distinguishing women from men.

How did this dichotomy come about? In exploring one possible explanation, we may come to see the heritage of human beings as stranger and more poignant than previously thought.

We'll return to the subject of neoteny, but only after first covering some preliminary ground. Often, the hardest step in speculative paleo-anthropology lies in overcoming assumptions. So let us back up and begin by asking a very basic question: Why is it that a human female generally has to compete with other women to get a mate?

May we stipulate that women do often vie over men? In one contemporary society, the United States, nearly all of the most popular magazines for women trumpet articles advising their readers how to stay competitive in what is portrayed as a desperate struggle to find and keep a mate. American women spend many times more each year on cosmetics than the nation appropriates for space research. (If we add fashion, diet food, plastic surgery, and related activities, costs compare to the defense budget.)² Granted, contemporary America is an extreme case, and even women in secure marriages work on their appearance for a complex of other cultural reasons. Still, no one can reasonably dispute that female humans often do engage in zero-sum contention over an apparently limited supply of suitable males.

Now of course men compete over women, too. But among animals this is only normal. Except for some spermatophore-donating insects, and a few fish and birds, competition between males for sexual opportunity seems almost universal.

Also nearly universal is the far calmer mate-selection process engaged in by females of most species, either accepting the victor in male-male struggles or actively choosing among candidates. This is not to say that females don't compete in nature! The struggle to raise successful offspring is deadly serious. Ethologist Sarah Blaffer Hrdy (1981) has shown that, among our primate cousins, inter-female competition for status and access to resources may seem quieter than the flashy violence of males, but it is also generally more relentless and complex. Darwin's image of females as demure, passive watchers-and-choosers greatly oversimplified a vast domain of intricate and assertive behaviors, with rivalry as much a feature of the female sex as its vaunted propensity for cooperation.³

Still, we are discussing a particular type of competition... rivalry to win a mate. And in this narrow area Darwin retains his original authority. Nature's story is nearly always about two sexes with markedly different agendas. For a male, each time he prevents one of his rivals from copulating with a female, that is one more womb which might be induced to carry forward his genetic heritage.⁴ The same is not normally true for a female, looking at males. Once engaged in gestation, her reproductive success is unaffected by copulations taking place nearby. When there is an abundance of food, one female gets little or no direct benefit by denying any other female a chance to reproduce, or to be inseminated by the same male.⁵

So we return to our central question -- why do human females engage in rivalry over access to suitable mates?

A leading hypothesis holds that humans became paragons of adaptability by emphasizing general, species-wide behavioral and mental neoteny. Further, our offspring are born nearly unformed, or altricial, replacing reflex instinct with lessons drawn from experience and the accumulated wisdom of the tribe, channeled by only the most general of innate predispositions. This process takes a long time, during which our children are helpless as no others in the history of life on Earth.

The presumption goes that human mothers need long-term, dependable partnership to help them carry big-brained, dependent children across the hazardous, exhausting stretch from embryo to maturity. And while some human societies have used brother-sister alliances to fill this need, or communal role-sharing, the majority have left mothers primarily dependent on continued loyalty and aid from the fathers of their children.

To put this in perspective with nature at large, consider the extreme case of the elephant seal.

During each annual mating season, females congregate onshore. If food is plentiful and the beach roomy enough, there is small cause for struggle between females, so most behaviorists used to be drawn to the noisy, extravagant displays of competing males. Known as a "beach master," each bull elephant seal outweighs any female many times over. By threat, bluster, and frequent bloody fights, he drives off all male interlopers to secure a local monopoly over insemination. Females acquiesce to this situation. Indeed, should the bull be away at the far end of his territory, and a rogue male attempt mating on the sly, females will often squall for the beach master to come drive the invader out.

Why do female elephant seals prefer to share one male rather than get individual attention? Turn the question around and consider -- what does the female really need from a male? The answer is sperm, and little else. Female elephant seals, like those of most species, are generally capable of rearing their pups alone. So choice of a mate is determined solely by factors which might reflect the quality of his genes -- his heritable fitness. Is he a healthy specimen, likely to father quality offspring? Will the males he sires likely become beach masters themselves? (Of course these questions are never posed, per se. But natural selection serves up appropriate answers, just as if they had been asked.) It matters little if the bull she has chosen also impregnates scores of other females. That he is able to drive off all comers and defend a beach is testimony to potency he might pass on in his genes. Having secured impregnation, the cows depart with no apparent sentimentality. They got what they came for.

In her book, The Woman That Never Evolved, Sarah Hrdy (1981) shows that harem systems differ dramatically. Some, such as the gray langur monkey, can be much more stressful than that of elephant seals. Langur mothers don't cycle through well-timed mating seasons, but re-enter estrus when their latest child either weans or dies. Also, while a mother langur doesn't need provisioning by a mated male, she does require the security of her troop. For these reasons, the bull langur has no single rutting season. To maximize reproduction, he must "police" his harem year-round. And, since his prime period averages only a few years, it is in his Darwinian interest to see that all local females serve his reproductive needs. One bloody consequence is that a new bull, on taking over a langur troop, often kills unweaned infants so that their mothers will resume ovulating sooner.

So while female elephant seals, gorillas and reindeer can be relatively complacent with their males, females in yet other polygynous species must look on their mates warily.⁶ Nevertheless, in all of these species the purely sexual aspects of selection are classically Darwinian... featuring inter-male struggle and various degrees of female choice. Inter-female competition, while pervasive, seldom extends to jealousy over copulation itself.

Let us assign reindeer, langurs and elephant seals to one end of a spectrum labeled harem size -- the number of "wives" a prime male in a species impregnates during his lifetime. Along the vertical axis we then chart ratio of size between adult males and adult females for each mammalian species. By plotting this chart, R.D. Alexander and others (1979) discovered a significant correlation. Species like elephant seals, where solitary bulls struggle to hold herds of breeding females, show exaggerated size differentials between the sexes. Clearly this is not in order for male to dominate female, or else females would presumably have also grown, to compensate. Rather, it is simply because a big male is better at driving off competing would-be inseminators. Successful bulls pass on the trait of largeness to their male offspring.

At the other end of the spectrum are species whose male/female size ratio is near unity, and where harem size is reduced effectively to one. Roughly four percent of mammalian species form "monogamous" pair bonds, with the rate a bit higher among primates, such as gibbons. (It is virtually the rule for birds. Chicks must grow fast to achieve flight before the seasons change. This, plus a high metabolism, means few avian young survive on the labor of one parent alone.)

Now by definition, monogamous species have approximately equal numbers of successful male and female breeders, so one might expect both to behave similarly, competing the same amount with others of the same sex. Each should be as choosy in selecting a mate, and exhibit the same degree of jealousy about copulation. But this is not the case, because most "monogamous" males are not purely monogamous in every sense of the word. Generally, these males do not give their mates so much absolute fidelity as devotion... meaning they will do anything and everything to serve and protect the nest and their offspring. But, given an opportunity to engage in outside sex without risk or harm, they will often take advantage. Such opportunistic philandering by so-called "monogamous" males was until recently hardly discussed. Now, however, we know that it plays a distinct role in the behavior patterns of most such species.

For example, the females of many bird species force prospective mates to engage in lengthy, exhausting courtship "dances" and other displays, before becoming sexually receptive. For years this was thought to involve species identification -- preventing hybrid insemination by a related species. But plumage, scent, and a thousand other simpler markers are available to accomplish the same end. Now it is thought that mating dances serve more directly pragmatic role, by culling out philanderers. Few already-mated males can afford the time and energy -- exhausting themselves in an effort at wooing -- if they already have a mate and nest elsewhere. To male birds, monogamy may not mean absolute fidelity, but it does mean having priorities.⁷

Thus, even monogamous species retain dimorphisms of sexual motivation and behavior. Monogamous females must remain careful and choosy, and even "monogamous" males must still prove themselves in order to win fatherhood.

So where do human beings fit in this spectrum? Few comparative ethnologists call humanity a truly monogamous species, even by bird standards. Indeed, many men, in both behavior and avowed fantasies, lean toward the attitude of male gorillas, if not elephant seals! Our position on the male-female size ratio chart would appear to suggest that humans have a modest "natural harem size" -- between one point one and one point four -- yet some men spend their lives aiming to achieve the milestone of their bedded "hundred," or even "thousand."

Nevertheless, we also share traits with pair-bonding species. Many men and women are capable of forming tight, long-lasting and devoted associations. Moreover, our offspring are altricial, helpless, nearly impossible for a mother to rear successfully in the wild without at least some outside aid. For a very long time any woman who chose a loyal, dependable mate almost certainly had advantages over one who failed to do so.

In summary, then:

1. It is reasonable to suggest a selected tendency in human females to prefer mating with males who offer effective, committed support, along with their sperm.

2. Given the nurturing demands to be placed on the male she chooses, one can expect female humans to prefer not to share their mates with many other women.

So far we may seem to be belaboring the obvious, but we are discussing matters all-too often associated with strong opinion and emotion, so it's best to move in careful steps.

Now ideally, given desiderata 1) and 2) above, men ought to behave like male birds, and indeed, the "best" of them do seem to follow that pattern. While such men may stray on rare occasions, they seldom do so if it seems home or family might be jeopardized. But human males show an incredible range of motivation and behavior.⁸ One does not have to reach speculatively back into the Pleistocene to illustrate the difference between mating with "bird-like" or "elk-like" men. Contemporary American society shows the calamitous consequences when women bear children fathered by the latter type, who promise anything, then depart when it's convenient. Hence we have driver number three:

3. A large fraction of human males are not (from a solemn female point of view) suitable for pair-bonding or fatherhood. High male variability probably meant that choice remained an important, even crucial, activity for our female ancestors.

Are quality males a scarce commodity? That's no problem in polygynous species, where females simply share the alphas. But such a scarcity presents severe, even desperate difficulties where females prefer pairing! Adding factor three poses the problem starkly. Human females began competing for mates because they needed the kind of competent, collaborative devotion received by female birds -- but which only a fraction of human males seem inclined or capable of delivering. Hence it is a combination of limited supply and high demand which has created the unusual situation of competition among women for successful mating.

Put in this way, it seems a prosaic, not particularly surprising conclusion to reach after so many paragraphs. And yet, the quandary of human females, and their contention for quality mates, goes far beyond the clichéd plaint of the woman nightclub comic, who bemoans (to fervent feminine applause) the scarcity of "decent men." I contend, in fact, that this dilemma has already radically shaped the flow of human development.

Next... why do fools fall in love?

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¹ Joseph Carroll suggests that the discovery of fire may have been a driver for both hairlessness and the acquisition of clothing. "Removable fur has obvious advantages if you are experimenting with fire." (Personal correspondence.) This might also explain why the smell of burning hair is so repugnant to most people. (back to where you left off)

² Ironies abound. Are nine-hundred dollar toilet seats worse than facial creams whose ingredients cost five cents, but which are sold at the equivalent of five thousand dollars a gallon? One cosmetics company executive explained, "We don't sell products. We sell hope." (back to where you left off)

³ Dr. James Moore, of UCSD, tells of female grey langur monkeys inciting males into battle over them. The female role certainly needn't be passive. It remains, however, nearly universally selective. (back to where you left off)

⁴ Even where males don't battle directly over matings, competition exists. Male chimpanzees often take turns mating with females in estrus. But they also have huge testicles, producing vast amounts of sperm. Reproductive advantage apparently goes to the male who produces enough to overwhelm his rivals' contributions. Male gorillas, who practice close harem-tending, have testes that are minuscule, by comparison. (back to where you left off)

⁵ Exceptions include red phalaropes and jacanas, species of birds in which the nurturing parent is the male, who is left alone with the egg while the female goes off in search of yet another male. Among phalaropes it is the female who is larger and brightly feathered, and who performs elaborate mating rituals to prove her worth to the selective male. The "choosy" sex is generally that with the most to lose from a bad call. (back to where you left off)

⁶ Hrdy has shown that philandering by females can be adaptive in stress-filled situations such as the langur monkey troop. Females often evade the chief bull to mate with promising young male outsiders who stand a chance of ousting him. This apparently helps confuse those outsider males over paternity, causing them to refrain from infanticide when and if they do take over. Such an adaptive path might have been followed by human females, explaining both concealed estrus and the ability to engage in subtle sexual deception. In any event, this mode of female philandering is distinct from the issue we are discussing -- how women were trapped into having to compete for the ability to reproduce at all. (back to where you left off)

⁷ A stereotype appears to have some basis, then. The spectrum of males ranges from langurs and reindeer (animal Don Juans?) all the way to swans and storks (Jimmy Carters?)... from committed polygamists all the way to those who are almost completely reliable -- who are tempted, but then ponder home and say, "I guess not." (back to where you left off)

⁸ For "variability" we might replace "volatility" or even "instability." To illustrate this, from 1960 to 1986, the proportion of women attending University of California Medical Schools rose from under five percent to forty percent. Over the same period, the female population of California prisons also started around five percent... and stayed there. Clearly women are learning assertiveness, but being selective about applying it. Males' former near monopoly on violent crime has not shifted, despite all recent changes in the stressful lives of American women. This is not to say that men are automatically bad guys. Rather they appear to show a degree of variability that is exaggerated even among primates. Consider why this high variability makes sense. First, humanity's recent rate of evolution appears to have been rapid, and Darwin showed that selection acts on variability. Among males, especially, a successful sport can pass on new, adaptive traits generously, while omitted male "failures" have little consequence. If this argument smacks of "group selection," careful re-phrasing can put the same idea in context of "selfish genes." Finally, the twin forces of sexual selection and change of reproductive strategy, have very probably contributed to making human males unstable, variable, and perhaps a little "crazy." (back to where you left off)