04/02/2013 07:44 am ET Updated Dec 06, 2017

Evolution, Sex And Monogamy (EXCERPT)

Adapted from Paleofantasy: What Evolution Really Tells Us About Sex, Diet, and How We Live by Marlene Zuke. Copyright © 2013 by Marlene Zuk. Used with permission of the publisher, W.W. Norton & Company.

Our behavior is slippery stuff, with men and women acting differently in different societies and under different circumstances. And without preserved footage of Neandertal dating sites, we are left to speculate about the sexual proclivities of our ancestors. Or are we? Behavior may not fossilize, but bodies do, and we can infer a surprising amount about behavior from those remains. For instance, we are reasonably sure that some dinosaurs cared for their young, because of the discoveries of eggs or young dinosaurs associated with an adult.

We can also draw conclusions about how natural and sexual selection have acted on the sexes in the past, simply by looking at the kind and magnitude of differences between male and female bodies today, as well as by comparing those differences across species. Along with the rest of his focus on sex, Darwin was extremely interested in these differences, and he drew a distinction between what he called primary and secondary sexual characteristics. The primary sexual characteristics are what define us as male or female—the plumbing, so to speak, with human (and other mammal) males having testes and females having ovaries, for example. All animals have primary sexual characteristics, and they can be very obvious or quite subtle; in many rodents, for instance, males and females are difficult to tell apart even after inspection of the nether regions, at least by a nonexpert.

The secondary sexual characteristics are even more variable, and they were also of much interest to Darwin. These are all the other differences between the sexes—the ones that aren’t directly required for reproduction but are still sex-specific, such as the peacock tail or the songs of male frogs, crickets, or birds. Human secondary sexual characteristics include enlarged breasts in women, facial hair in men, and—most germane to our quest for the ancestral mating system—differences in body size, with men being on average 15 centimeters (about 6 inches) taller than women.

This body size difference is mirrored to greater or lesser degrees in many other species, though in some, including whales and many insects, it is the female that is the larger sex. (Larger females are believed to be favored when they can lay more eggs or otherwise provide more for the offspring.) Larger males are thought to be the result of sexual selection for better fighters, and the fighting is generally over access to mates. The general idea is that species with more male competition, and more polygyny, are likely to show a greater difference in body size between the sexes.

Among our primate relatives, the gorillas, which live in groups with a single male that mates with several females, have the most pronounced sexual size difference, with males about twice the size of females; similar sex differences are seen in orangutans. Males and females in the monogamous gibbons, by contrast, are roughly equal in size, as are the two sexes in the muriqui monkeys of Brazil, which have a polygamous mating system in which both males and females have several sexual partners during a season.

Humans, along with chimps and bonobos, have a much more modest difference, which has led many researchers to conclude that we were only moderately to slightly polygynous in our evolutionary history. Fossil evidence also indicates that human sex differences in size have decreased over the last several hundred thousand years, though it can be difficult to draw conclusions, because skeletal remains are sometimes classified as male or female in the first place by comparing the size of the bones.

Owen Lovejoy, an anthropologist at Kent State University in Ohio, extended this idea to suggest that human monogamy arose at least 4.5 million years ago, when the bipedal human ancestor Ardipithecus ramidus lived, and furthermore that it was facilitated by bipedalism, with men making use of the freeing up of their arms to hold tools, going off to hunt and bringing back meat for the women. Women, in turn, would reward their mates for the food with fidelity.

Of course this sharp division of labor is not upheld in modern hunter-gatherer societies, and furthermore, the similarity in relative sexual size between us and the chimps and bonobos suggests that we need more information before we can explain why we would end up monogamous and they would mate with many partners. Lovejoy also suggests that Ardipithecus was relatively peaceful, like the bonobos, but as Professor Frans de Waal of Emory University notes, “unless the diggers come up with a male and female fossil holding hands and having wedding rings, the idea that these ancestors avoided conflict through pair-bonding remains pure speculation.”

Furthermore, it’s not so clear what it means when the sexes are quite similar. Sometimes being bigger isn’t all that useful, as in hummingbirds or other species with aerial displays of aggression, where a more agile opponent wins the day. Other variables, such as the likelihood of mating within one’s group or outside it, can also influence the strength of selection on male competitiveness.

Even when we find evidence of sexual size differences, the degree of those differences is not necessarily the result of mating competition. Modern cultures vary in how different the sexes are in height, with the Maya Indians of South America differing by nearly 10 percent, while the Taiwanese differ by only 5.5 percent. Claire Holden and Ruth Mace from University College London looked at seventy-six populations around the world for which they could find information on height, degree of polygyny, type of subsistence (hunting or agriculture), and the sexual division of labor during a preindustrial period.

The researchers hypothesized that polygyny might not be the only thing affecting sexual size differences; perhaps the way that men and women live is also a factor. And indeed, the more women contributed to food production in a culture, the smaller the difference in height was between the sexes, perhaps because such contributions meant that the women had more control over food distribution. Whether or not a society was polygynous made no difference, although the authors caution that their sample might not have allowed detection of a contribution by the mating system.

The last piece of evidence about our mating history that we can glean from our bodies is a bit more personal than height. In many mammals, the size of the male testis is correlated with the number of females a male might potentially mate with over a short period of time. The testes, of course, produce sperm, and generally speaking, the larger the testis, the more sperm a male can manufacture. Usually, male animals produce enormous numbers of sperm cells (human ejaculates are 1.5–5.0 milliliters and contain anywhere from 20–150 million sperm per milliliter), but ejaculates need to be replenished, and might not be sufficient to fertilize the available females if a male is mating very frequently. In addition, if a female mates with more than one male in a short period of time, the sperm in her reproductive tract can compete with each other, in which case the male supplying the most competitors is at an advantage.

Where do humans fit into this picture? Human testes are smaller relative to body size than those of chimpanzees and bonobos, but larger than those of either the monogamous gibbons or the gorillas. Although male gorillas are substantially larger than females, because they live in groups where only one male routinely mates with the females, the silverbacks have relatively little need for competition with other males.

Most researchers have concluded that this finding supports our decreasingly polygynous history, although the authors of Sex At Dawn: The Prehistoric Origins of Modern Sexuality, Dr Christopher Ryan and Dr Cacilda Jethá try to make the case that it points to a life of polyamory, with simultaneous multiple partners for both sexes.

More recently, detailed examination of the stretches of DNA that are present in our ape relatives but absent in modern humans revealed a loss that women, at least, have cause to celebrate: the genes coding for “genital tubercles,” or more graphically, penis spines. In many other mammals, including chimpanzees, the penis has hardened growths that may serve to sweep away the sperm of previous mates. These structures are absent in humans because we lack the genes responsible for the hormone signals that would cause them to develop. The relative smoothness of the human penis is thought to be linked to a reduced frequency of sperm competition.

So, is monogamy swimming against an evolutionarily promiscuous tide? I doubt it. Lifetime fidelity to a single partner may be rare among animals, and even among humans, but the sheer variation in mating systems among human societies in both space and time makes it unlikely that we have all been ignoring our true natures. If evolution favored a single marriage or sexual system, why would we not all have converged on that pattern?