As the midday sun hangs over the Scandinavian spruce forest, a swarm of hopeful suitors takes to the air. They are dance flies, and it is time to attract a mate. Zigzagging and twirling, the flies show off their wide, darkened wings and feathery leg scales. They inflate their abdomens like balloons, making themselves look bigger and more appealing to a potential partner.
Suddenly, the swarm electrifies with excitement at the arrival of a new fly, the one they have all been waiting for: a male. It’s time for the preening flock of females to shine.
The flies are flipping the classic drama reenacted across the animal kingdom, in which eager males with dazzling plumage, snarls of antlers or other extraordinary traits compete for a chance to woo a reluctant female. Such competitions between males for the favor of choosy females are enshrined in evolutionary theory as “sexual selection,” with the females’ choices molding the evolution of the males’ instruments of seduction over generations.
Yet it’s becoming clear that this traditional picture of sexual selection is woefully incomplete. Dramatic and obvious reversals of the selection scenario, like that of the dance flies, aren’t often observed in nature, but recent research suggests that throughout the tree of animal life, females jockey for the attention of males far more than was believed. A new study hosted on the preprint server biorxiv.org has found that in animals as diverse as sea urchins and salamanders, females are subject to sexual selection — not as harshly as males are, but enough to make biologists rethink the balance of evolutionary forces shaping species in their accounts of the history of life.
The new work turns a spotlight on a lopsidedness in sexual selection research that may have robbed evolutionary studies on about half of all animal species of important context. Scientists have reported scattered evidence of female sexual selection in the past, but more often they haven’t had reason to look for it. That could now be changing.
“We really don’t know very much compared to how much we’ve worked on the male side of things,” said Tommaso Pizzari, an evolutionary biologist at the University of Oxford who was not involved with the new paper. “Sexual selection in females is still relatively unknown. It’s still barely charted territory.”
The concept of sexual selection dates back to Charles Darwin’s first writings on natural selection — briefly mentioned in The Origin of Species, and then covered more extensively in The Descent of Man — where he detailed reproductive preferences between the sexes as potentially driving evolutionary change. Within the framework of conventional natural selection, it makes sense that individuals prefer fit mates. But a key point of sexual selection is that attractiveness to potential mates can be a criterion for selection in itself, independently of how it affects fitness otherwise. Members of one sex can develop traits and behaviors appealing to the other that directly conflict with survival-driven natural selection. Taken to extremes, this can result in the unwieldy, exceptionally elongated display feathers of some male birds, for example, which are only useful in the mating contests that the males stage.
The Victorian View of Females
Yet from its very beginning, the science focused on males as the objects of sexual selection. Darwin saw females as reluctantly picking mates from gaggles of desperate male suitors. He was open to the idea of sexual selection in either direction, but the intensity of the obvious competitions for mates among males fed the idea that sexual selection happened primarily to males; the females were prizes to be won. Females might be setting the terms of the mating competitions, but it was the males who were truly being reshaped through evolution by those choices.
Darwin’s perspective was typical of his time. Theories about sexual selection were born “in the Victorian era, when you had these certain sexual stereotypes about how women should behave,” said Rebecca Boulton, an evolutionary biologist at the University of Exeter in the U.K. “And so, because the field essentially sprung up at that time, it was like, ‘Of course females aren’t mating with multiple males. Of course they’re coy or choosy.”
This viewpoint has contributed to a ubiquitous bias in how sexual selection has been investigated in the last century and a half, the researchers behind the new study argue. They estimate that studies of male-male competition and the phenomenon of female choice are 10 times more common than studies targeting the reverse.
“A lot of people are influenced by the culture that they live in and the things that [they] see,” said Salomé Fromonteil, a graduate student in evolutionary biology now at Uppsala University in Sweden and Ludwig Maximilian University in Munich, and lead author on the study. “It’s influenced by what we read, and what they read is that sexual selection works on males primarily.”
There are undeniable exceptions. Some that have caught researchers’ attention are in species with “sex roles” that are flipped from the conventional arrangement, as in the dance flies. Females of the American tropical wading birds called wattled jacanas (Jacana jacana) keep and defend territories rich in male mates. Among the seahorses and other pipefish, males even take on the job of “pregnancy” by internally incubating their young in a specialized pouch.
Still, scientists studying sexual selection have mostly continued to defer to Darwin’s initial observations in the 19th century. It was generally accepted that males — with their propensity for ornaments and courtship displays — experienced greater sexual selection pressures.
“Of course, that’s not how research should be,” said Tim Janicke, an evolutionary biologist at the Center for Functional and Evolutionary Ecology at the University of Montpellier in France, and senior author of the new study. “If the aim is to describe general patterns in nature, we need data-driven syntheses behind this.”
In 2016, Janicke and his team dove into the published literature measuring the strength of sexual selection acting on a variety of animal species and compared those values between the sexes. That study, published in Science Advances, confirmed that males experience a higher degree of sexual selection than females did.
But as further examples of species likely to be undergoing female sexual selection accumulated, Janicke and his team were struck by a question that their study had not addressed: Just how common is sexual selection among females? They began to wonder whether it was “something rare, or whether it’s actually a general pattern,” Janicke said.
In early 2020, Janicke and Fromonteil were planning to start an empirical study on sexual selection in beetles to probe that question. Then the COVID-19 pandemic and the institutional shutdowns it triggered made laboratory experiments suddenly infeasible. But a meta-analysis of the data from the 2016 study could be done even in “confinement,” as Janicke puts it.
To compare the relative strength of sexual selection in a wide range of species, the scientists needed some way of quantifying that selection intensity. They settled on a method using the Bateman gradient, a measurement named after the 20th-century British geneticist Angus John Bateman.
More Mates, More Sexual Selection
Bateman recognized that while males can produce many sperm at low metabolic cost, females have to make relatively high investments in far fewer eggs. In the 1940s, his research on fruit flies led Bateman to propose that this fundamental divergence in gamete investment drives apart the mating strategies of males and females: To maximize their reproductive capacity, males might routinely seek out and compete for many mating partners, while females might instead evolve to be choosy.
Other researchers built on this idea, developing the Bateman gradient to describe the fitness benefits of having multiple mating partners. The measurement is the slope of the line comparing reproductive output to the number of mating events — in effect, it shows how sharply an organism’s number of offspring increases with more mating. The steeper the positive slope, the greater the fitness benefit of more mating events, which in most species means having more mates. (By mating with multiple males rather than just one, a female can sometimes hedge her bets about which mate will produce the fittest offspring.)
“If there’s positive selection on having more mating partners, this should translate into competition for mating partners,” said Janicke. “And this competition is basically the essence of Darwinian sexual selection.” For this reason, Bateman gradients are a common way of indirectly quantifying sexual selection.
From a sweep of the scientific literature, the team compiled 111 Bateman gradients calculated for females in 72 animal species, ranging from beetles to mollusks to mammals. The gradients varied widely, but they clustered in the positive range. The team also found, as expected, that species with “polyandrous” females who had access to many partners simultaneously had Bateman gradient values considerably greater than those of species with “monandrous” females who mostly mated with one male at a time.
The findings suggest that — as has long been presumed for males — females get a fitness boost from multiple matings, and that opens the door to widespread sexual selection. The positive female Bateman gradients don’t appear to be as large as those for males, Janicke said, but their pervasiveness hints at the importance of sexual selection in the evolution of females, even in species seen as having “typical” sex roles.
While acknowledging that the Bateman gradient is a “powerful measurement to quantify sexual selection,” Janicke noted that it only reflects selection directly related to the act of mating. In species that spawn profusions of eggs, such as many fish as well as corals and other marine invertebrates, there are opportunities for selection after mating, too, with eggs competing for access to sperm, or sperm having choice capabilities that affect fertilization. Janicke’s study did not extend to this kind of post-mating sexual selection. It’s therefore possible that even more female sexual selection occurs than the new study suggests, but future work will need to test that possibility.
For Pizzari, the study “confirms something that I think we have been, as a community, beginning to realize for quite some time now: that sexual selection is potentially quite important in females across a number of species, as well as for males.”
Alternative explanations, however, do still need to be tested. Some of the gradients that Janicke’s team identified may be rooted in certain females’ inherent attractiveness to males due to their reproductive output. “It may well be that the females that have more eggs to produce … happen to attract a lot more males simply because they have a higher reproductive value,” Pizzari said. If so, it wouldn’t be that more matings were more beneficial to females, “it’s that males are more interested in mating with fecund females.”
If that is the case, however, then Jonathan Henshaw, an evolutionary biologist at the University of Freiburg in Germany who was also not involved with the study, thinks that empirical tests could help isolate this effect. “If you really wanted to know what the causal effect of mating on reproductive success is, the best thing would be to do as others have done and actually manipulate the number of mates that are available to individual females,” he said.
Experiments could also help reveal whether sexual selection is playing out in these females in the wild, and how selection might be influencing the traits that females use to compete with one another. “The potential for … different mechanisms of sexual selection is there,” Boulton said. “Whether that’s what’s actually happening is something that is a little bit harder to tease apart.”
Confrontations and Decorations
Now that scientists are becoming more aware that they should look for evidence of female sexual selection, the traits and behaviors it cultivates in females may become more obvious. Black grouse (Tetrao tetrix) were considered a classic example of male sexual selection: The males have distinct, vivid coloration, and they compete for females in elaborate courtship display arenas called leks. But recent evidence suggests that while the males are putting on their show, the females are also aggressively jockeying for their choices. Female Mediterranean fruit flies (Ceratitis capitata) take a very similar approach. Certain dung beetle females have even evolved horns that may be used for battling with other females in contests over access to males.
But such intrasexual combat isn’t likely to develop in most females, Boulton argues. Fighting has an inherent risk of bodily harm — something that males can more easily afford since they just need to survive until copulation. Female reproductive success takes time: They have to live long enough to lay all their eggs, and sometimes to care for the newborns. “Whereas the males, they’ve kind of got less to lose,” she said.
The ornaments and competitions that females use to gain mates may sometimes have been overlooked because they are more subtle and look like pared-down versions of what males sport. For instance, female Malurus fairy wrens are undergoing sexual selection on their bill and plumage coloration independently of similar pressures on the males. Both male and female chickens (Gallus gallus) have fleshy ornamental combs. Hens prefer roosters with bigger combs as mates, but the roosters give more sperm to hens with bigger combs, too.
Such ornamentation traits in females are sometimes viewed as byproducts of sexual selection on a female’s male ancestors — “leaky sexual dimorphism,” Pizzari said. But he argues that males may pay attention to these ornaments, which could give them evolutionary significance in the females. “They might have been the target of adaptive selection in their own right.”
Another trait that males commonly seem to key in on is female body size, Boulton said. Males tend to prefer bigger and heavier females. This preference might be rooted in the value of size as a signal of the females’ overall health and reproductive potential, but it could also be a platform for female competitiveness.
No matter how female animals respond to sexual selection in nature, the new findings help reiterate how much of it went largely undetected by science for many decades. Part of the rigid stereotyping around research into sexual selection was likely informed by culture and patriarchal attitudes.
The stereotype of male-centered sexual selection may also have persisted so stubbornly “because there’s a kernel of truth in it — that in the vast majority of species, males do gain more from additional matings than females do,” Henshaw said. The pitfall is that “it’s sort of easy to go from that truth to an opposite stereotype which says that ‘generally speaking, females don’t gain anything from extra matings.’ But then you’ve kind of gone too far.”
Extreme physical differences between the sexes in some species may also have blunted the search for the more hidden but widespread sexual selection among females. “If you have a species that shows this striking sexual dimorphism, you might not start to study intrasexual selection among females,” Janicke said, because male selection would seem like the default explanation.
And yet, despite the weight of human assumptions and sensory biases, a pattern is beginning to rise to the surface: Female sexual selection is the norm. “Generally speaking, sexual selection operates on females,” Fromonteil said.
Janicke plans to continuously update the database with Bateman gradients as they are published. “This database will grow and grow, and we’ll see what other kinds of questions we can still address with this. But I am very confident that this pattern on sexual selection for females will not change,” he said.
Correction: August 16, 2021
The caption of the photograph of the jacanas incorrectly described it as showing an interaction between two females.