Coming Out Darwinian. Is It Time To Rewrite The Story Of Sex?

All coming-out stories are members of the same genus, if not the same species. Mine, however, has one distinguishing trait: along my path to understanding and accepting that I was gay, the obstacle of my religious upbringing was aided and abetted by none other than Charles Darwin. That is, there was a time when I told myself that the uncomfortable feelings I had for male friends and classmates could not possibly be real, because they would be wrong and sinful, and also because they were impossible in a world shaped by natural selection.

I was pulled into this mental tangle by the peculiar tensions of life in a family that was, on the whole, more liberal than the church we attended. When I brought home my first library book about evolution — I picked it up for the dinosaurs, of course — Mom and Dad encouraged me to read more, but also warned me not to discuss it casually at church. Meanwhile, mention of men who fell in love with other men prompted awkward silence from my parents whenever it came up on Public Radio. In Sunday School the people who mentioned the topic at all did so to condemn it.

By the time I began attending my private, church-run high school, I was fully subscribed to the evolutionary view of life. It explained the tremendous and fascinating diversity of the natural world through the elegant principle that traits passed down from one generation to the next become more or less common in proportion to how they help or hinder the reproduction of those who carry them. I enthusiastically defended this logic in lunchroom debates against classmates who were sure that God had personally assembled the world one atom at a time.

But I said nothing about my other difference with orthodoxy. Christianity as I knew it was firmly opposed to romantic love between two men. On the other hand, the best alternative I had found seemed to hold that, even if same-sex attraction was not wrong, it certainly was not natural. Natural selection should have long ago eliminated any gene promoting a desire for sex that had no reproductive purpose, I reasoned. If  there was no genetic basis to those unthinkable thoughts — well, then I could stop thinking them if I tried hard enough, right?

In that weird transitional time, I knew of one story: natural selection eliminates anything that reduces reproduction. My problem was not that I knew this story, but that I did not know how many other stories evolution can tell.

Genetic drift – the random fluctuation of gene variants in small populations – can make natural selection less efficient. A variant that creates a disadvantage when carried by some people may be advantageous for others. Perhaps the same gene variant that makes men gay also makes women more fertile? In humans, the cost or benefit of a particular variant can also change with cultural context: gay men probably had more children when their only socially safe option was marriage to women, and might have more in a future when legal marriage and surrogacy are easily available. Sexuality may even have a biological basis without a genetic cause, if it is influenced by the conditions a developing fetus experiences in the womb. The little solid data we have on the genetics and evolution of human sexuality lends various support to each of these stories. The truth could be any of them, or more than one of them, or none of them; some still unwritten text, perhaps entitled How the Homosexual Got His Fey.

Among evolutionary biologists, stories have a bad reputation. When an argument about an evolutionary cause is grounded not in evidence but a circular argument about what we already see in front of us — it must be favored by natural selection because if it wasn’t it wouldn’t be here — we call this a “just-so story,” after the fanciful explanations from Rudyard Kipling’s book for children. Yet evolutionary biologists tell stories every day. We have to when trying to reconstruct how the living world came to be as we see it now. Some of these stories are purely speculative. Others are elaborately buttressed with experiments and observations. We learn by drawing connections between facts, and what are stories but the sum total of those connections? Once upon a time, things were this way; but then something changed, and now things are that way instead.

The trouble with stories is not simply that they are stories, but that they can be told badly. We can distort the narrative to end the way we find more pleasing, or to confirm what we assume is already true. In trying to understand how whales or giraffes or oak trees or humans came to be the way they are, we run the risk of telling a story about how life ought to be. For whatever reason, the stories that seem to run this risk most often are the stories involving sex.

As with many aspects of evolutionary biology, the stories we tell about the evolution of sex and gender roles can be traced to Charles Darwin. Darwin proposed that traits important for successfully attracting a mate, but with no obvious function in survival—an elk’s antlers or a peacock’s tail—are shaped not by natural selection, but by sexual selection. Echoing Victorian ideas about human gender differences and roles, Darwin assumed that females were weaker, less intelligent, and “coy,” while the stronger, more intelligent males actively pursued them or competed amongst themselves for the chance to mate. These ideas were later formalized by the geneticist A.J. Bateman who reasoned that because it takes fewer resources to make a sperm cell than an egg, males can “afford” to mate with many partners while females should invest more cautiously. Bateman tested Darwin’s assumptions on fruit flies, but the results were interpreted much more broadly (and were likely wrong to begin with).

It is probably not a coincidence that Bateman’s story closely parallels human cultural norms, in which men are expected to have many partners but women are expected to be chaste until marriage. At the intersection of biology and modern Western marriage law, men can more easily evade the physical or financial costs of raising children than women can. This does not necessarily make sexual selection a false story, but it should make us more careful about when and how we decide to tell it. Today, sexual selection is probably best understood as one of many evolutionary stories that can be told about animal mating systems. We know of mammals, birds, fish, reptiles, and insects that reverse the gender roles assumed by Darwin and Bateman, and even species that make things more complicated still.

The implications of sexual selection in humans are much more problematic than for other species. Because the story of sexual selection begins with an analogy from human society, it is hard to apply it to humans without creating circular reasoning. Darwin and Bateman thought human males were naturally “ardent” and females “coy,” other scientists have found that kind of behavior in some animals, so therefore human gender roles are naturally what Darwin and Bateman thought. In the history of human evolutionary biology, individual researchers have extended this logic to propose that the dichotomy of sexual selection makes women less capable of abstract reasoning than men, or that that men may have some genetic urge to rape, or that women may be less interested in sexual variety than men, or that men are less capable than women of monogamous commitments — the list could go on.

These are, at best, incomplete evolutionary stories. They miss the true diversity of human behavior and experience. Even if they are told as a first step to finding factual evolutionary stories, they can appear to justify women’s underrepresentation in scientific and technical careers, or write systematic social disparities into biological fact, or provide one more reason for a gay teenager to be sure that he is utterly alone and unwanted.

Many years after a scientific education that began with a library book full of dinosaurs, I now study the evolution of plants. Plants do not  have sexual orientations, or gender identities, or culture. In most flowering plant species, individuals are hermaphrodites with both male and female sex organs, either within the same flowers, or in separate flower types on the same individual. You might think, therefore, that our understanding of plants’ reproductive biology would be entirely free of human assumptions about gender. But, in fact, the sexual selection story has also been retold with flowering plants in the leading roles. That retelling has shaped almost half a century of research on the evolution of plant mating systems.

Why would anyone think to apply sexual selection to hermaphroditic plants? In a brief 1977 paper in The American Naturalist, the ecologist Dan Janzen laid out the case for that conceptual leap. Janzen pointed out that even when individual flowering plants have both male and female reproductive organs, rather different evolutionary forces might shape these different reproductive functions. He explicitly proposed a parallel between plant and animal reproduction:

[quoted]As with animals, the male portion of the genome differs from the female genome in that the investment per pollen grain (analogous to sperm) is much smaller, and further, once the pollen grain has been donated, there are no further costs to the male parent. This suggests that the male should be much more generous or sloppy per pollen grain than the female per ovule.[/quoted]

Janzen inferred that features of the flower that make male reproduction — pollen export — more effective might not be the same features that make female reproduction — reception of pollen — more effective. Indeed, in many plants that bear male and female organs in separate flowers, or in which individuals are only male or female, the flowers with different sexual functions often look quite different.

This offered the possibility that plants might be subject to evolutionary processes previously thought to be reserved for animals. Janzen proposed that plants’ female organs might have evolved to accept pollen only selectively, perhaps by matching up with one species of animal pollinator over another if these different animals delivered pollen from donors of higher or lower quality. Plants might also abort developing fruits that were fertilized by lower-quality pollen, or evolve biochemical barriers to restrict fertilization in the first place. Plants’ male reproductive organs might also evolve countermeasures: in Janzen’s terms, “the male plant may well wish to effectively rape certain females in the area,” by massively over-producing pollen, manipulating pollinators, and bypassing physiological filters.

This retelling of a classic evolutionary story proved highly influential. Two years after Janzen’s brief on the concept, Mary Willson followed in the same journal with a more detailed argument in favor of applying sexual selection to plants. Willson noted that plant species with separate male and female flowers would often produce more male than female flowers – a finding consistent with Janzen’s claim that male flowers had evolved to saturate their environment with pollen. Willson also argued that the competition created by male flowers for pollen production and dispersal would be more intense than the competition among female flowers for pollen donations. She noted in particular that environmental conditions – from how densely plants were spaced in a population to the availability of nutrient and water resources – might change the relative advantages as well as the investment that an individual plant would make in male versus female reproduction.

Over the following decade this became a widely accepted story about the evolutionary forces shaping plants’ reproduction: male functions were shaped by competition for the services of pollinators and access to female organs, but female functions were mostly limited by the availability of nutrients, water, and sunlight needed to produce fruit fertilized by overabundant pollen. Colorful, showy flowers were like the peacock’s tail, the result of competition for the attention of birds and bees and other animals that would carry off cheaply produced pollen to reluctant, choosy female flowers.

However, this story failed to explain everything that biologists observed in populations of flowering plants. Many botanists tested the idea that female reproduction was resource-limited by artificially dosing plants’ female organs with excessive pollen. If plants given this treatment produced fewer seeds than plants allowed to receive natural pollination it would be evidence that the environment, not pollen, was the factor limiting female reproduction. This would add further support to the idea that sexual selection was at play in flowering plants, just as in Bateman’s fruit flies. Yet, surprisingly, in many cases plants that received this supplemental pollen produced seeds, suggesting that they were not resource-limited but pollen-limited.

Reviewing the available research in 1994, Paul Wilson, James Thomson, Maureen Stanton, and Lisa Rigney called for evolutionary biologists to look “beyond floral Batemania.” They proposed that, under many conditions, flowers might be under stronger selection to acquire pollen than to donate it. More research followed, and in 2004 Tia-Lynn Ashman and a large group of collaborators collected results from 85 pollen-supplementation experiments in which 73% supported pollen limitation. In other words, for three out of any four studies, plants violated the gender roles that Darwin and Bateman described.

Does this mean Janzen and Willson were wrong to extend the sexual selection story to plants? Not at all. They were repurposing the old story to tell a new, speculative one. This is one way that scientific stories are developed in the first place. In a retrospective essay written for the 150th anniversary of The American Naturalist, James Thomson, one of the coauthors on the “Batemania” paper, credited Janzen and Willson with inaugurating a new era of thinking about plants’ reproductive biology, in which different sexual functions must be tracked carefully, even in hermaphrodites. The decades-long back and forth of emphasis on male or female function is a natural consequence of many people thinking seriously about a common scientific question.

But there is one thing that sets evolutionary stories about plants apart from those we tell about humans: the story does not, in any real sense, matter to the plants. Ironically, the living creatures we are best equipped to understand using the scientific process — those we can grow in experiments, or manipulate the reproductive success of, or force into mated pairs under perfectly controlled conditions — are also the ones least likely to suffer any ill effect from a bad or incomplete evolutionary story.

With humans, the situation is reversed. The limitations of good conscience prevent us from doing experiments that can directly determine how natural selection works; but which stories we decide are most credible have real implications for the lives of individual people. Politicians may latch on to the idea that women’s bodies “naturally” reject the sperm of rapists and argue that abortion services are unnecessary as a result. Teachers may decide that some of their students can never be expected to learn as well as others, and redirect their efforts accordingly. Religious leaders — many of whom oppose the very idea of evolution in any other context — can argue in all seriousness that allowing same-sex couples to marry will put our society at some sort of selective disadvantage

All of these stories are described, with various degrees of speculation, in the scholarly literature concerning human evolution. For humans as for plants, this is exactly the forum for such speculative storytelling. Speculation is the first step toward scientific discovery and refutation. Scientists should seriously consider all possible stories, even if we find them unsettling or unpalatable or simply silly. But if the story of gender roles in plants tells us anything, it is that evolutionary stories are almost always more complicated than we can imagine, and we should tell them with caution. If science has struggled for decades to answer the apparently simple question of how the lilies of the field got their colorful petals, how much longer will it take us to truly understand the history of how we got our humanity?

Evolutionary biologists are scientific storytellers and we must acknowledge the power in the stories we tell. We must clearly identify the evidence that supports, or refutes, each story. And we must, I think, hold stories about humans to a higher standard of evidence than mere internal consistency. Even though we are governed by the same natural laws and descended from the same primordial ancestor, human beings are the one organism in all the diversity of life who care about what the stories say.