Prum reminds us that Darwin wrote two books that defined his concept of evolution. The first, On the Origin of Species by Means of Natural Selection, proposed the view that most describe as “survival of the fittest.” This firmly established the notion that species evolved via natural selection as individual characteristics best adaptive to the species given environment would propagate via sexual transmission and eventually become dominant in successive generations. This became, in most people’s minds, an all-encompassing concept that excluded other contributions to species evolution. Everything a member of a species did must be explained as an attempt to seek a better, more survivable version of itself. Prum refers to those who attempt to explain all data on evolution as driven by better adaption to an existing environment as “adaptionists” or neo-Darwinians.
Darwin was never convinced that natural selection, as defined in his first volume, could explain everything that he had observed. In particular, he was troubled by the evolved tail feathers of the male peacock. Prum provides a revealing quote from Darwin.
“It took Darwin a long time to grapple with this dilemma. He famously wrote, ‘The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!’ Because the extravagance of its design seemed of no survival value whatsoever, unlike other heritable features that are the result of natural selection, the peacock’s tail seemed to challenge everything that he had said in Origin. The insight he eventually arrived at, that there was another evolutionary force at work, was considered an unforgivable apostasy by Darwin’s orthodox, adaptionist followers. As a consequence, the Darwinian theory of mate choice has largely been suppressed, misinterpreted, redefined, and forgotten ever since.”
Darwin eventually published a second book on evolution: The Descent of Man and Selection in Relation to Sex. Natural selection certainly is operative, but before genes can be sexually propagated there is a mate selection process that takes place. The example of the peacock suggests that the outrageous and functionally useless tailfeathers are not a result of environmental adaptation, but of aesthetic choices by female peahens. They preferred to mate with males they found attractive. The consequences of this can be enormous because such choices need not lead to better adaption; rather, they can easily lead to maladaption.
If one considers how modern humans go about propagating their genes, the idea that mate selection might have little to do with adapting to climate change, for example, is not very revolutionary. However, in Darwin’s patriarchal era, the notion that female mate selection could alter the course of evolution was deemed absurd. Critics were much more comfortable with concepts of male-on-male competition as being determinant.
Prum devotes much of his book to demonstrating the peacock/peahen dynamic was not the exception, but the rule. His examples from the world of birds are fascinating—and compelling. Mate selection was always important, but each species seemed to deal with the issue differently. The critical issue seems to be the sexual conflict between males and females over who controls the mating process.
All species seems to deal with this conflict in different ways. And the two genders seem to have different goals. At one extreme there is the case where males dominate such as our relatives the chimps. In most of these cases, the alpha males are merely satisfied with having access to all females who are in estrous. Note that this is a random practice of mate selection and it is not likely to contribute to any change in species characteristics other than to propagate the male features that lead to dominance in the male hierarchy. Females seem to have another approach entirely to mate selection. They tend to find certain male characteristics attractive or pleasurable and will preferably select such males for mating. This is not a random process because the mating will result in males more likely to have the admired characteristics, and females more likely to appreciate those characteristics. There is a positive feedback mechanism that can grow and spread throughout the species, particularly if the majority of females settle in on the same set of characteristics.
Prum’s beloved birds consist of a huge multitude of species where female sexual autonomy is almost complete. Female birds have almost total control over mate selection leading males of each species to audition for females in an attempt to make themselves more attractive to any female who might wander by. Evolution under these circumstances has led to exotic ornamentation patterns for males and demanding courtship performances on their part. The result has been an explosion in species differentiation as localized clusters of birds of a given family have evolved in different ways from their relatives. Interestingly, most birds are descended from an ancestor that possessed a penis. Those birds no longer possess a penis. Prum suggests that since a penis is almost necessary if a male is to forcibly impregnate a female, the dominance of females in this sexual conflict might have rendered a male’s penis no longer of any value and it disappeared. Of course, there is no way to know if some other factor contributed to its loss and this allowed females to exert their sexual autonomy.
There are two cases of interest that are discussed by Prum in which male or female dominance are not fully resolved and both genders participate in mate selection. The first case is that of certain duck species in which males continue to wish to copulate with anyone they choose, and females continue to resist any forced impregnation. Prum describes in detail the manner in which male ducks have evolved ever longer, more complex, and more powerful penises in an attempt to defeat female defense mechanisms. The females, on their part, have evolved ever more complex vaginal channels to inhibit deep penetration by any male other than one for which the female will assume an accommodating posture. Scientists who study such matters have concluded that the females seem to be winning this battle, if they physically survive it, by preventing fertilization in all but a few percent of the forced copulations. This battle of the sexes is an excellent example of maladaptive evolution caused by mate selection. This mating process results in females being injured and killed; consequently, it results in a lower population for the species and an imbalance in gender ratio.
The second interesting case of contentious mate selection is that of the human species. Human males and females are both selective in who they choose to mate with, meaning each gender is capable of propagating its desired characteristics. It is not possible to tell the story of mate selection and its associated evolution among humans with any great accuracy, but Prum provides some interesting speculations that are certainly food for thought. Prum doesn’t draw such a distinct conclusion, but a reader of his might conclude that human physical evolution was greatly driven by the desire to enhance sexual pleasure.
In order to understand human evolution within the context of mate selection, one must enumerate the differences between us and the apes from which we evolved. Scientists tell us that homo sapiens descended from a line that broke off from the chimpanzee line about six million years ago. Chimps lead a male-dominated existence in which males compete for hierarchical dominance which produces benefits in terms of access to females. This type of system encourages characteristics that support male dominance. Males are considerably larger than females and are endowed with large canines that seem to be only useful in fighting other males or in intimidating females. Males don’t practice coercive sex because they don’t have to. When females go into estrus they mate with dominant males as well as many subdominant males over a period of several days. For their part, males will mate with any available female. This seemingly promiscuous female behavior is thought to be a minimal response to their lack of sexual autonomy.
Sexual conflict has caused a horrible maladaptive response from chimp males: infanticide. Females chimps bear almost total responsibility for raising their young. After estrus, a female will have months of gestation followed by three or so years of breast-feeding which inhibits ovulation. Females are then sexually unavailable for about four years. Often among chimps and other primates, a new male will become dominant and discover that there are few if any females available to impregnate. In a display of his dominance he will often kill infants of lactating females in order to render them sexually available again. This practice is quite common, and it can be the most significant cause of death for young chimps. The apparent promiscuity of chimp females is interpreted as an attempt to convince as many males as possible that they might be the parent of an infant in hopes that this possibility will inhibit a male from killing his own offspring. Fortunately, infanticide, as a male behavior, was eventually shed by our ancestors.
It is useful to note that there is another species of chimp that broke off from the main chimpanzee line even later than humans (a mere million years ago) and, being geographically isolated, evolved quite different characteristics. Both male and female bonobos form social structures that seem to share dominance in group affairs. Infanticide is thought to be nonexistent. Neither gender seems to be very selective in mate choice because the incidence of sexual interaction is quite prevalent, including same-sex contact. Bonobos have taken sexual pleasure and made it a foundation for their social order. Bonobos will express friendship and gratitude by offering sex. They will use sex as a means of lessening social conflicts. As someone once said, when unfamiliar groups of bonobos encounter each other it is more likely that an orgy will ensue rather than any form of violence.
Sexual motivations can drive a species in many directions.
Humans have clearly evolved considerably, both physically and socially, from the ape ancestors. If the bonobos can evolve quite different characteristics from the common chimpanzee in a mere million years, it seems rather dangerous to interpret human characteristics as being derived directly from our even more ancient ancestor.
Before considering how mate choice among humans might have coupled with natural selection to produce humans as they exist today, we should note a warning provided by Prum. Human evolution is a story of the sexual conflict between the sexes, and over the roughly six-million-year period since we set out on our own, female sexual autonomy grew dramatically. The males and females to which we evolved might have possessed quite different sexual and social habits than those that society has recently imposed on us in just the past few thousand years. The evolution of our bodies is more consistent with a bonobos-like interest in sexual pleasure than our recent history might suggest.
“….I think that the advances in female sexual autonomy that occurred over millions of years since our common ancestry with the chimpanzees….have been challenged by two relatively recent cultural innovations—agriculture and the market economy that developed along with agriculture….These twin inventions came into being a scant six hundred human generations ago and created the first opportunity for wealth and the differential distribution of wealth. When males gained cultural control over these material resources, new opportunities were created for the cultural consolidation of male social power. The independent and parallel invention of patriarchy in many of the world’s cultures has functioned to impose male control over nearly all aspects of female life, indeed human life. Thus the cultural evolution of patriarchy has prevented modern women from fully consolidating the previous evolutionary gains in sexual autonomy.”
In other words, women are now struggling to get back to where they were a thousand generations ago before men began convincing them they were the weaker sex and that sex itself was a male preoccupation—not one women should expect to enjoy.
“Viewing pleasure as the central, organizing force in mate choice, and mate choice as a major dynamic in evolutionary change, the aesthetic theory holds that women’s pursuit of pleasure is at the very heart of the evolution of human beauty and sexuality.”
Darwin lived in an era where the discussion of human sexuality was not conducted in open print, but he did suggest that the loss of human body hair could possibly be attributed to sexual selection—humans with little or no body hair were deemed more attractive, probably by both sexes. Prum suggests that this contention is possible, but unprovable. He is more interested in patches of hair that have remained because they are reminiscent of the ornamental displays birds have evolved to make themselves attractive. Also, the emergence of pubic hair and hair in the armpits at puberty suggests an explicitly sexual role for those adornments.
“Regardless of whether the reduction of body hair is an aesthetic trait or not, it is clear that another unique trait—the retention of specialized patches of hair in the armpits, pubic region, scalp and eyebrows—is ornamental. The fact that the retention of these patches of hair is the same in both sexes….strongly implies that it evolved through mutual mate choice, like the bright beaks and plumage of male and female puffins, parrots, and toucans. The hypothesis that underarm and pubic hair are evolved sexual signals is further supported by the observation that these patches of hair do not develop until puberty. These unusual patches of hair likely evolved for the purpose of pheromonal, sexual communication between mates, which is very common in mammals.”
Note that the loss of body hair for females would have been a big deal for females. Female chimps are in almost continual bodily contact with their infants. Chimps are born with a grasping reflex that allows them to clutch their mother’s hair and hold on as she went about collecting food (human infants are still born with that grasping instinct). The loss of that hair would mean that the mother would have to find another way of caring for her infant while she foraged. This would have required a dramatic change in group society whereby other mothers agreed to accept some responsibility for the care of the children of others, and/or male mates would have to also play a greater role in providing for their offspring. Such a male attribute would then become a mate selection factor for females as they preferred males who were more domesticable.
Prum suggests that requiring a greater contribution to child rearing would have the effect of making males more particular with regard to whom they would father a child with rather than having sex with any available female. From this would arise selected characteristics for females.
“….aesthetic male sexual preferences in human males evolved along with the increase in male parental investment….The result of this sexual choosiness has been the coevolution of distinctly female sexual ornaments—like permanent breasts and distinctive body shape—which are completely absent in other apes.”
Human females are the only mammals that have developed permanent breasts. Since all the other mammals reproduce and raise offspring successfully with breasts that come and go as needed, it is hard to view this feature as anything other than a desired sexual ornament.
“Among the more than five thousand species of mammals on earth, permanent breast tissue is unique to humans. The mammaries of all other animals increase in size only during ovulation and lactation, and they are not enlarged at other points in the life cycle. Human females, however, develop enlarged breasts with the onset of sexual maturity, and they retain enlarged breast tissue throughout their lives.”
Mate selection remodeled the female body internally as well externally. Human females, at some point became the only ape that no longer signaled when they ovulated as an invitation to males that they were ready to be impregnated. This would produce a profound effect on sexual interactions. Sex and reproduction were now only loosely coupled given a low probability of fertilization, allowing sex to be an activity focused mainly on pleasure. Humans who subsequently took a fancy to each other would then plan for many sexual experiences. This would elevate the roll of sexual pleasure in the interaction and emphasize the ability to produce sexual pleasure in a partner as a selection factor in evolution. One can only speculate about how the change to concealed ovulation came about. It could have been an adaptive attempt to perhaps limit the frequency of impregnations, or it could have come about because, like the bonobos, humans concluded that sexual pleasure had uses other than mere reproduction.
Male orgasm is easily understood. It is necessary that it occur in order to disperse sperm, and it is inevitable that evolution would deliver a pleasurable feeling in order to encourage the production of more offspring. However, female orgasm seems to have no function in reproduction, no matter how hard adaptionists have tried to invent one.
Human females may be unique in their ability to achieve a sexual orgasm. People who study such things are able to stimulate other female animals in laboratory situations until an orgasm-like response is attained, but because animal sex is usually of short duration it is not clear that the response is ever attained naturally. Prum provides this background.
“For example, copulation duration in gorillas and chimpanzees is measured in seconds. On average, human copulation lasts for several minutes and of course can continue for far longer than that.”
It is not difficult to anticipate women who face many sexual encounters with a prospective mate will select on attributions such as copulation duration in an attempt to maximize their own pleasure.
“Any evolutionary explanation for longer copulation times in humans is inherently about enhancing the pleasurable sensory experience of sex”
“….female sexual pleasure and orgasm are the evolutionary consequences of female desire and choice, and are ends unto themselves.”
Female mate selection would also have a role in remodeling the physical appearance of males. According to Prum, the human male’s penis and scrotum may be his most outstanding features. It seems again that males evolved in a manner designed to increase sexual pleasure.
“By any measure, the human penis requires a lot of explanation. It is substantially larger—both in absolute and relative size—than that of any of the other apes, even though humans are intermediate in body size between gorillas and chimpanzees. The erect gorilla penis is only an inch and a half long. The chimpanzee penis is three inches long when erect, very thin, smooth, and finely pointed at the tip. The human penis is both longer—averaging about six inches when erect—and wider than the penis of other apes. The human penis is also characterized by a distinctly bulbous glans and coronal ridge at its tip. Similar structures have evolved in other primates, but they are not present in African apes. We should also note that in contrast to their greater penis size and elaboration, humans have testes that are both relatively and absolutely smaller than those of our closest chimpanzee relatives.”
Since chimpanzee females are impregnated via copulation with multiple males, it would be natural for the males to develop large testicles in order to produce enough sperm to give them a chance to win that game of chance. Humans have no equivalent selection process operative. Chimpanzees then have a large scrotum to contain their large testes. Surprisingly, humans have an even larger scrotum to contain their smaller testes. How does one explain that?
There is another puzzling feature to the human penis. Humans are one of only two primates that have evolved away their penis bone, the baculum.
“The existence of a baculum in the other primates means that an erection is guaranteed by the presence of an ossified bone within the penis….we do know that aside from producing erections, the baculum functions in retracting the penis between erections. What its other functions might be is still not clear.”
So, we have human males evolving to state where they have a large floppy penis—permanently exposed—and coupled with a larger than necessary scrotum containing highly vulnerable testes. As the humans became bipedal and stood upright this ostentatious genital display would become even more pronounced. Male anthropologists like to view human males as aggressive warriors in frequent combat with other surly males. Given such a picture, how could these males have produced such a vulnerable genital package via natural selection. According to Prum, they didn’t. It evolved because females favored bigger penises and appreciated the visual display provided by a dangling penis and a large scrotum.
“The longer, thicker, broader human penis with the bulbous glans at the end is likely to have evolved through female preferences for mail copulatory organs that produce greater pleasure.”
It would seem likely that the males’ delight in observing large breasts would be matched by females’ delight at estimating the potential pleasure to be derived from a male’s genitals.
Human females’ sexual autonomy is not as complete as in the case of most birds. Both sexes are using choice to provide different influences in evolution. Males contribution to childrearing is significant, but it varies widely within humans. The desired male and female characteristics are also highly variable. Interestingly, females seem intent on diminishing what we see as dominant male features. It is as if there exists a species memory of a past when males exercised more coercive mating habits.
“….there is consistent evidence that females do not prefer the most ‘masculine’ facial features, which have been characterized as prominent square jaws, wide prominent brows, thick eyebrows, and thin cheeks and lips. Numerous studies have shown that women instead prefer intermediate or even what some researchers call ‘feminine’ facial features in men, and one study has shown that females prefer a light stubble over a more masculine full beard. According to a handful of disparate studies cited by Gangestad and Scheyd, these facial preferences seem consistent with the evidence on what women like to see in male bodies. They tend to like lean but somewhat muscular male bodies with broad shoulders and v-shaped torsos the most, and men with larger, more muscle-bound bodies the least.”
Richard Prum has produced a fascinating look at evolution, describing a process that is more arbitrary and more interesting than we had been led to believe. After reading his book it is difficult to think of evolution—and sex—in the same way as before.
