Evolution and Human Sexual Behavior

Peter B. Gray, Justin R. Garcia

• Publisher: Harvard University Press
• Year: 2013
• ISBN:
  9780674074392
• Topic: Scienze biologiche
• Subtopic: Evoluzione

Few things come more naturally to us than sex—or so it would seem. Yet to a chimpanzee, the sexual practices and customs we take for granted would appear odd indeed. He or she might wonder why we bother with inconveniences like clothes, why we prefer to make love on a bed, and why we fuss so needlessly over privacy. Evolution and Human Sexual Behavior invites us into the thought-experiment of imagining human sex from the vantage point of our primate cousins, in order to underscore the role of evolution in shaping all that happens, biologically and behaviorally, when romantic passions are aroused.Peter Gray and Justin Garcia provide an interdisciplinary synthesis that draws on the latest discoveries in evolutionary theory, genetics, neuroscience, comparative primate research, and cross-cultural sexuality studies. They are our guides through an exploration of the patterns and variations that exist in human sexuality, in chapters covering topics ranging from the evolution of sex differences and reproductive physiology to the origins of sexual play, monogamous unions, and the facts and fictions surrounding orgasm.Intended for generally curious readers of all stripes, this up-to-date, one-volume survey of the evolutionary science of human sexual behavior explains why sexuality has remained a core fascination of human beings throughout time and across cultures.

CHAPTER ONE

The Evolution of Sex, Sex Differences, and Human Sexuality

The human being, like the immortals, naturally places sexual intercourse far and away above all other joys—yet he has left it out of his heaven! The very thought of it excites him; opportunity sets him wild; in this state he will risk life, reputation, everything—even his queer heaven itself—to make good that opportunity and ride it to the overwhelming climax.

—Mark Twain, Letters from Earth

WITH DUE RESPECT to Mark Twain, humans are hardly the only creatures whose passions are stoked by the prospect of sexual intercourse. Indeed, not far from Las Vegas, where one of us lives, some unusual vertebrates scamper around the deserts of the U.S. Southwest and northern Mexico. Among the many species of whiptail lizard are some that have abandoned sexual reproduction. These species reproduce clones of themselves—that is, they are parthenogenic (Nelson 2011).

Among these parthenogenic whiptails, females live without males, and females produce more females. However, there are some interesting twists in how they do this. Females must go through the mating motions with other females in order to reproduce. They engage in mating postures with other females, who play the role of males—one female mounts the other and they pseudocopulate in order to facilitate the cloning process and egg development.

Why have some species of whiptail lizard evolved without sex? Genetic research suggests such parthenogenic species represent the amalgamation of sexually reproducing species. These parthenogenic species have double the number of chromosomes. This suggests a mechanism by which sexual reproduction is hindered, but it does not tell us whether parthenogenesis has been favored by selection. Yet consideration of the lizards’ desert ecology could suggest some adaptive reasons for just such a selection process: imagine how difficult it is to find a potential whiptail mate, let alone to survive. The search costs of mate seeking, especially in novel terrain, could act against sexual reproduction. Indeed, among some other vertebrates that fluctuate between sexual and asexual reproduction, such as the island-dwelling Komodo dragon, the very real challenges of finding a mate might favor an ability to reproduce asexually.

THE EVOLUTION OF SEXUAL REPRODUCTION

The asexual reproduction we see in parthenogenic lizards is rare among vertebrates (Roughgarden 2004). Instead, sexual reproduction is the norm and has evolved repeatedly on Earth, in many and various lineages of plants and animals. For this reason it must be the case that sex offers selective advantages that outweigh its costs. Notwithstanding recent biomedical success with cloning (actually only partial success, since cloned mammals live shorter lives than their noncloned counterparts), which makes sexual reproduction unnecessary, human sexual reproduction is part of a legacy extending back at least a billion years.

So just what are the adaptive benefits of sexual reproduction? For that matter, what are the costs?

The costs spill out whenever you see excess male mortality (deaths related to mating competition, as among adolescent males when they do things that reduce their survival odds) or, less dramatically, the routine costs of contemporary human courtship—money spent on things like flowers, chocolates, jewelry, and romantic nights out, or the other expenses of seeking sexual partners. Were it not for the need to reproduce sexually, organisms, including people, would have no need to devote time and effort to seeking, courting, and maintaining mates. Were it not for the need to reproduce sexually, organisms, including people, would be less likely to engage in same-sex competition for mates, competition that can range from hurtful jealous bickering to physical aggression. All of this comes under the cost of one of life’s most primitive, complex, and essential pleasures—sex.

Another major cost of sexual reproduction is the loss of half your genetic legacy. Sexual reproduction requires that your gametes mix with those of another organism to produce an offspring who carries both your genetic heritage and your mate’s. Thus, sexual reproduction effectively serves as a 50 percent estate tax on one’s genetic legacy, a significant cost to you as an organism. For such costs, organisms surely must receive significant benefits, but what are they?

In fact, sexual reproduction offers several major potential benefits (Geary 2010). One is that harmful mutations (changes in the genetic code) can be weeded out. In other words, sexual reproduction can take deleterious mutations, shuffle them, and yield offspring that may or may not have them. Without this shuffling, an asexually reproducing organism would be stuck with passing the harmful mutation to its offspring, perhaps to the demise of its own lineage. Another benefit is the generation of novelty (Rice 2002). Sexual reproduction enables a shuffling of the genetic deck, creating novel combinations that may prove beneficial in the face of shifting selective pressures. To be sure, the shuffling also breaks up winning genetic hands, but that cost can be offset by the benefits of novelty.

Imagine you are an animal who is encountering a new landscape that exposes you to differences in temperature, precipitation, predators, disease, and other environmental factors. Sexual reproduction may enable adaptation in the face of these new environmental pressures. An organism’s genome does not know which genetic contributions would be best suited to a new environment, so the production of a new variety of combinations may yield blends that make one organism better adapted than another. As evidence that this hypothetical scenario describes biological reality, we have the example of some species, such as aphids, that vacillate between sexual and asexual reproduction, reserving sexual reproduction for times when they must cope with greater environmental uncertainty (Roughgarden 2004).

Multicellular organisms can also face eternal back-and-forth challenges wrought by pathogens (Hamilton and Zuk 1982; Zuk 2007). As pathogens reproduce themselves in huge numbers and with rapid generation times, organisms may survive by employing an array of defenses. One major defense takes the form of the adaptive immune system. Sexual reproduction enables the production of novel immune markers that, by chance, may be beneficial when challenged by an unpredictable pathogen. This is why the immune systems in humans and other organisms are among the most rapidly evolving components of our physiology, and why in genomics research we repeatedly find that the immune system changes and adapts rapidly: it must do so to fend off the unending variety of pathogens that use humans and other organisms as resources or way stations on their own route to reproductive success.

ORIGINS OF SEX DIFFERENCES

If adaptive cost-benefit ratios favor sexual reproduction, does that translate into sex differences in the phenotypes, or observable characteristics, of an organism? In other words, how does sexual reproduction lead to distinctly different sexes, such as the males and females around us (and variations on these general two sexes), and to the sex differences in anatomy, physiology, and behavior that we also see around us? To be sure, there are species in which sexual reproduction does not require or produce two distinct sexes (for example, clownfish, like the stars of the animated movie Finding Nemo, are sequential hermaphrodites and can change from male to female during their lives, although the movie ignored this biological reality). There are also species in which sexual reproduction requires and produces more than two sexes (e.g., some slime molds), but these examples are far removed from our human-centered world (Low 2000).

Through classic laboratory experiments conducted with fruit flies in the mid-twentieth century, Angus Bateman (1948) helped lay the theoretical and empirical foundation for an understanding of sex differences. Bateman documented that reproductive success in female fruit flies provided with adequate food differed little whether the flies had one, two, or three male mates. The male who mated with her first apparently provided enough sperm to fertilize the female’s eggs, such that additional sperm from additional males had little reproductive benefit to her (there was no difference in the number of fly hatchlings). In that lab setting, the female’s offspring may not have needed adaptive immune differences or other variations to ward off environmental challenges. While these findings (that a female’s reproductive success did not differ by the number of mates she had) may not seem remarkable, they differ from those observed in male fruit flies. Male fruit fly reproductive success increased when males were allowed access to an increasing number of female mates. Males with three mates had a greater number of offspring than those with two mates, who in turn had more offspring than those with one mate. Perhaps eventually males could run out of sperm—or steam—and thus the marginal fitness benefits to having a greater number of mates would gradually decrease to zero, but that was not the case over the range of mates considered.

These experiments showed that female reproductive success was associated with sufficient resources, such as food, whereas male reproductive success depended on access to females. This result became the basis of what biologists call Bateman’s principle. Research with many organisms, not just fruit flies, suggests that Bateman’s principle applies quite widely in nature, even extending to humans (Andersson 1994; Geary 2010).

Bateman’s (1948) original report suggested that the sex difference in gamete investment is the root of the sex difference in reproductive constraint. Females typically invest more in their gametes (their eggs), than males do in theirs (their sperm), leading to these asymmetric relationships in reproductive constraint (the fact that females tend to be ultimately constrained by access to resources, such as food, and males by reproductive access to females). In the years following Bateman’s initial observation scholars have refined and elaborated on this logic.

Robert Trivers (1972), in a book chapter that has since become a classic in the literature, suggested that reproductive asymmetry traces to relative parental investment (rather than gamete size). The sex that invests more in parental care tends to be the reproductively limiting one, while the other sex tends to exhibit more competition for reproductive access. This insight helped move the basis for sex differences closer to humans’ phylogenetic home, among mammals—where parental care is common—but it also had its limitations. One of these limitations was that it did not easily account for exceptions, such as mouth-brooding frogs, in which males might provide the bulk of parental care but also be more apt to compete among themselves for reproductive opportunities with females. Accordingly, Clutton-Brock and Vincent (1991) advanced the concept that “potential reproductive rate” was the better foundation for reproductive asymmetries; the sex with the lower potential reproductive rate is the one over which competition will occur. Even more recently, Hanna Kokko and colleagues have hearkened to demographic factors such as adult sex ratios that can change the gradient of sexual selection (Kokko and Jennions 2008). In contexts with more females than males, females may compete more among themselves over males, while a sex ratio with more males means more male-male competition over females.

Amid the layers of theory, we find the empirical foundation of sex differences. The sex whose potential reproductive rate is lower tends to be the one whose reproductive success is most closely tied to resources such as food, and the sex whose potential reproductive rate is higher tends to be the one whose reproductive success is most closely tied to competition for reproductive access. Applying this to mammalian sexual behavior, imagine a female investing in gestation, lactation, and other forms of parental care. Compare that with a male investing in sperm that fertilize her egg. The female’s intensive forms of investment will typically mean that female mammals, within a given species, are reproductively limited by access to resources such as food. Males within a given species of mammal are reproductively limited by access to females, placing greater emphasis in their lives on competition with other males in courtship and in access to females.

SEXUAL SELECTION

While Charles Darwin had discussed sexual selection in his classic 1871 book, The Descent of Man, and Selection in Relation to Sex, all of the observations of fruit fly sexual behavior, and the theorizing about potential reproductive rates, came long after his death. Yet these later observations and theories only formalized Darwin’s original theory.

Sexual selection theory arises in part from the observation that many traits seem detrimental to reproductive success. Why does a peacock display a magnificent train (sometimes mistakenly called a peacock “tail”)? Wouldn’t this same train help a predator find it, rather than a less flamboyant peacock or a peahen? Wouldn’t this same train be a curb to efficient walking or flying? Wouldn’t this train be a waste of the energy required to make those beautiful feathers shine? How, in the name of natural selection, could such a trait evolve if it seemed to have such downsides?

As Darwin puzzled over traits such as the peacock’s train, the bird-of-paradise’s coloration and mating dances, female chimpanzees’ sexual swellings, and male deer antlers, he surmised that they were produced by competition for access to mating opportunities. As members of one sex competed with each other for access to the other sex, they might evolve traits that would improve their chances of success. Thus, the male stag beetle’s weapons (large mandibles for fighting other males) are the product of sexual selection; his weapons are not designed to help him find more food or to deter predators, but to improve his chances of reproductive success.

Darwin identified two types of sexual selection: intrasexual selection and intersexual selection. Intrasexual selection refers to selection within members of the same sex, whereas intersexual selection refers to selection between the sexes. Darwin emphasized male-male competition as the main form of intrasexual selection, and female choice as the main form of intersexual selection. He saw many traits, like those horns, antlers, and other armaments in mammalian males, as the product of male-male competition. He suggested that the peacock’s train could have been favored by female choice. If females preferred mating with males possessing more colorful feathers or elaborate trains, then their mating choices could also drive these traits to excess, to the point where they might even be counterproductive to survival. Later scholars built on this idea to demonstrate that many traits, such as a peacock’s train, are “honest indicators” of an individual’s overall health. Such signals indicate presence of disease or unfavorable genetic mutation, they might reflect quality of diet and thus foraging ability, and they might demonstrate the individual’s vigor, its ability to put on a flashy show and still avoid depredation (Zahavi and Zahavi 1997).

Sexual selection can also lead to other patterns of sexual behavior besides male-male competition and female choice. In many species we see female-female competition (Rosvall 2011). The female sexual swellings that Darwin observed can be viewed as one product of female-female competition, with females displaying such vivid mating advertisements in order to benefit from enhanced mating opportunities. Male choice clearly operates too, especially when males provide indivisible, hard-to-obtain resources such as food: in these cases, males may seek to optimize investment of their limited resources in the female or females who will provide the greatest return. And as recent work by scholars such as Hanna Kokko reminds us, the demographic specifics of a population may modulate the specifics of intrasexual and intersexual selection (Kokko and Jennions 2008). Change the sex ratio dramatically, for example, and you can also change the ways in which competition plays out.

Sexual selection can account for many differences between the sexes, or sexual dimorphisms (Andersson 1994; Geary 2010). Although some sexual dimorphisms may be related to differences in behavior that relate to survival (for example, when females and males feed on different resources), the kinds of dramatic ones we have highlighted so far in this chapter—those large male antlers, for example—trace instead to sexual selection. Differences in body size dimorphism in association with mating systems are thus thought to represent, in part, the workings of sexual selection. One-male polygynous species (in which a male has several female mates) tend to have extremes of body-size sexual dimorphism. Multi-male, multi-female species (in which multiple males and females live and mate together) tend to be characterized by lower body-size sexual dimorphism. And monogamous species (with mated pairs of one male and one female), are relatively monomorphic, or lacking in sex differences in body size (Dixson 2009). While other factors may be at play (for example, larger female body sizes may be favored in order to enhance fertility [Ralls 1976]), larger males within a species generally seem to use that extra weight during male-male competition. So for many overt sex differences in anatomy, physiology, and behavior, we wonder whether those differences owe their existence to sexual selection.

As is true of many scientific theories, exceptions can help prove the rule. The exceptions, in cases of sexual selection, are sex-role reversals (Eens and Pinxten 2000). These are scenarios in which typical patterns are reversed, accompanied by changes in the kind of sex differences we would expect to see. Take jacana birds or Wilson’s phalarope as examples. In most species of birds, males and females are similar in their size and coloration; in fewer, males (like male peacocks, or the turkeys served on many Thanksgiving tables) are more colorful and larger than females. But among jacana birds and phalaropes, the females tend to deposit their eggs with males, who subsequently provide the bulk of parental care. Females in these species also tend to be larger and more colorful than males. The interpretation is that males in these sex-role-reversed species are the reproductively limiting ones. Accordingly, females compete more among themselves than do males, and males practice more mate choice, resulting in females evolving the kinds of traits—such as colorful feathers—that enhance their chances of reproductive success.

Are there any sex-role reversals among mammals? No. The more extreme sex differences in potential reproductive rates in mammals seem to have prevented sex-role reversals from evolving. There is no ready mammalian counterpart to jacanas or, for that matter, other well-known sex-role reversers, such as pipefish and sea horses (male sea horses go so far as to become pregnant and give birth). Among mammals, the closest thing to a sex-role reversal is seen in the spotted hyena.

Possessing enlarged clitorises (about the size of hyena penises), which led Aristotle to speculate that they were hermaphrodites, female spotted hyenas are also slightly larger than their male counterparts, and they engage in extreme female-female competition, including over territory and the carcasses of their favorite hunted or scavenged prey (Glickman et al. 2006). Female spotted hyenas give birth through their clitoris. Many ...