Delicate wiry feathers curl behind a male Wilson’s Bird-of-Paradise as it sways back and forth, parading in otherworldly blues, reds, and yellows across the forest floor in Papua New Guinea.
A male Indian Peafowl flaunts hundreds of “eyes”—an array of ocular-looking spheres with blue irises spread across an expansive fan of long tail plumes—in an elaborate display for the brown, unadorned female.
A male Satin Bowerbird decorates his stage with shiny blue objects to lure a brownish female into his forest territory in eastern Australia. As soon as she arrives, he sings a mysterious jangle, a rapid-fire churr that sounds like video-game special effects, while puffing and quivering.
Male birds the world over, with their extravagant plumes, songs, and dances, have puzzled scientists for over a century. Charles Darwin famously wrote in a letter to American botanist Asa Gray in 1860 that “the sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick.” Those plumes sickened Darwin because he could not understand why male birds were so elaborately adorned.
After years of deliberation Darwin proposed that flashy plumage and elaborate song and dance could be explained by female choice—what Darwin termed “sexual selection,” a counterpart to his theory of evolution by natural selection. Males developed showy plumage and elaborate songs in part, Darwin said, to please choosy females.
“It is certain that amongst almost all animals there is a struggle between males for the possession of the female,” Darwin wrote in 1874, in his book The Descent of Man and Selection in Relation to Sex. “Hence the females have the opportunity of selecting one out of several males, on the supposition that their mental capacity suffices for the exertion of a choice.”
Darwin’s theory on sexual selection and female choice set off a cultural explosion. It was fiercely attacked by Victorian society because it put females in control. Females, by a matter of choice, could alter the evolution of their own species.
Darwin’s contemporaries deemed the notion that women had choices as preposterous.
“Seldom or never does the female exert any choice. She is not the awarder of the prize, but rather a hunted creature,” said German philosopher and psychologist Karl Groos in 1898.
English botanist St. George Jackson Mivart, an early supporter of Darwin’s theory of natural selection, viciously criticized Darwin on sexual selection. Mivart went so far as to suggest that women were too amused by passing fancies to have any such exertion on evolution. Even fellow British naturalist (and codiscoverer of natural selection) Alfred Russel Wallace objected to Darwin’s idea of sexual selection.
“Female birds may be charmed or excited by the fine display of plumage by the males; but there is no proof whatever that slight differences in that display have any effect in determining their choice of a partner,” Wallace wrote in 1889.
Wallace focused his critique on female choice and the apparent arbitrariness of beauty as an evolutionary concept, which to Wallace lacked utilitarian value and ran counter to Darwin’s theory of evolution by natural selection. To Wallace, the idea that females choose beauty without function was ridiculous. The long, spotted plumes on the Indian Peafowl, Wallace believed, signaled health and vigor. Male ornaments, Wallace suggested, arose from the “surplus of strength, vitality, and growth-power,” not simply beauty. Those showy plumages meant the male had better genes—natural selection in disguise, the real reason why females choose heavily adorned males.
This idea of beauty is why Richard Prum—an ornithology professor at Yale University and author of the Pulitzer-nominated book The Evolution of Beauty—calls Darwin’s theory “really dangerous.” The danger, Prum suggests, lies with beauty—it flies in the face of the adaptionist view of natural selection that has been the mainstay of evolutionary thought. In his 2017 book, Prum argues that beauty is the driving force behind extravagant adornments. “Animals are agents in their own evolution,” Prum was quoted as saying during an interview with The New York Times Magazine. “Birds are beautiful because they are beautiful to themselves.”
While the critiques of Wallace and others sunk Darwin’s sexual-selection theory into oblivion back in the 19th century, beauty as an evolutionary concept is enjoying a renaissance today. And though Victorian-era societal forces shelved Darwin’s notion of female choice 150 years ago, now in the 21st century societal views are shifting again—as more women become CEOs, members of Congress, and scientists. With a fresh perspective, biologists are reconsidering, and recognizing, the vital role of females in evolution and animal behavior.
“Females,” says Cornell Lab of Ornithology postdoctoral researcher Karan Odom, “play a much larger role than we previously thought.”
Finally, Females Overlooked No Longer
In 1972 Robert Trivers, then a PhD student in biology at Harvard, published a paper entitled “Parental Investment and Sexual Selection” in which he suggested that because females need to provide care for their young to ensure survival, females need to be choosy; they have more to lose than males.Trivers’s theory of parental investment tied female choice to raising their young, not to beauty as Darwin suggested. But Trivers’s work gave legitimacy to female choice for the first time, and what followed was a flurry of research on sexual selection.
“There was definitely a paradigm shift,” says Mike Webster, director of the Cornell Lab’s Macaulay Library multimedia archive of animal behavior. Webster is also a behavioral ecologist who examines questions related to sexual selection. Now, he says, “there have been so many studies on [sexual selection] that they all just blur together.”
Prior to the Trivers paper in 1972, the number of scholarly articles on sexual selection numbered fewer than 40. Post-Trivers, the number of published sexual-selection studies has skyrocketed to more than 19,000. These modern-day studies left out Darwin’s beauty in favor of utility (thanks to Wallace), which many scientists found more palatable.
As it happened, researchers were avidly asking questions about sexual selection right when the women’s liberation movement was picking up steam. In 1972, the U.S. Congress passed the Title IX federal civil rights law that prohibited sex discrimination in educational institutions that receive federal funds. Today more women earn PhDs in biological and biomedical sciences than men.
“I think having more women in science and having a more inclusive scientific community broadens the perspectives available,” says the Cornell Lab’s Karan Odom.
Over the last several decades, more female scientists are asking more questions from the female perspective. One great example is bird song—a breeding behavior that for much of the past 100 years has been almost exclusively studied in male birds.
Some Female Birds Lost Their Songs as They Evolved
“Bird song, according to Darwin, was a textbook example of sexual selection,” says Jordan Price, a behavioral ecologist and evolutionary biologist at St. Mary’s College of Maryland.
In the Northern Hemisphere in spring, forests and fields come alive with bird song. Male Blue-winged Warblers loudly proclaim their breeding territory with a bee-buzz; male Common Yellowthroats with a repeating witchety-witchety-witchety. All this bird song is in part, Darwin tells us, to attract and keep a mate. Females, Darwin said, choose the most melodious males.
Most people in the Northern Hemisphere tend to think of bird song as a behavior exclusive to males, because in the Northern Hemisphere many male birds are conspicuous and vociferous. But around the world, in more than 600 songbird species, female birds are known to sing. (Many more female singers likely exist, but they haven’t yet been documented.)
And in tropical regions, female bird song is common, but most bird research has occurred in the Northern Hemisphere. This geographic bias, says Odom, “shapes how we think about bird song.” Price jokes, “if Darwin had grown up in the tropics or if he was Australian, he might have asked why the female birds he saw on his travels in northern climates didn’t sing instead of asking why males have elaborate song.”
Scientists are now starting to tackle this question, and in the process rewriting the way modern science understands female bird song. The Cornell Lab’s Karan Odom started by studying song in Barred Owls in 2004—specifically the duetting performed by male and female Barred Owls. As the male escalates into a series of squawks, the female responds with a low Who-cooks-for-you-all?
The Barred Owl duet made Odom suspect that female bird song was more common than recognized in the scientific literature. Curious, Odom joined up with biologists Michelle Hall from the University of Melbourne; Katharina Riebel from Leiden University in the Netherlands; Kevin Omland from the University of Maryland, Baltimore County; and Naomi Langmore from the Australian National University, to form a research team focused on studying female bird song.
The team’s work was also shaped by new research published in the Proceedings of the National Academy of Sciences that suggested modern songbirds evolved from ancestors in Australia. Female bird song is common in Australia, which made Odom and company wonder: Could singing be a trait among female birds that was lost in North American passerines over time?
To tackle that question, the team scoured the scientific literature looking evidence of the absence or presence of female song and marked which species had or did not have song on a phylogenetic tree—a diagram showing how all songbirds are related, similar to a family tree. Overlaying their data onto this songbird family tree allowed them to reconstruct when female song appeared and disappeared over time.
What they found was startling, and their results, published in Nature Communications in 2014, challenge the way scientists had thought about sexual selection for the last 150 years. Odom and her team found that the females of those Australian ancestors likely sang. In fact, they found that in the distant past female song was the norm among birds. And they found that female bird song is still present in 64% of songbird species that exist in the world today.
Understanding that females sing means that sexual selection isn’t just for males; females, too, may be under pressure to sing. Some female songbirds—such as the Alpine Accentor, a bird of the high mountains in Europe and Asia—sing to attract male mates when they are ready to breed. Others sing to defend resources, such as nesting sites or food for themselves or their young.
“Female birds sing for a number of reasons, and some of them are quite similar to reasons why males sing, but others are different,” says Odom.
Over time, Odom suggests, some female birds stopped singing, especially outside the tropics. But even female birds that currently don’t sing show signs that female birdsong once occurred in their species. Female songbird chicks, for example, still have a brain region for singing, but that region atrophied over time, similar to the appendix in humans.
Loss of song, Odom and colleagues surmise, could be due to the evolution of migratory behavior among some songbirds. Neotropical migratory species (New World warblers, for example) spend only a few short months on their northern breeding grounds in the U.S. and Canada, which means it may be more efficient for these species to divide up tasks between males and females for raising a family. If the male focuses on defending the territory, the female can then focus on nest building and tending young, which doesn’t require song. And, it may be safer for the females to keep quiet both for themselves and their young, so they don’t become somebody’s lunch.
In tropical areas where female birdsong is more common, and where songbird species with female singers are nonmigratory, pairs of birds defend territories year-round. Defending that turf may be easier when both males and females are singing. The Cornell Lab’s Webster says that in tropical areas where there is strong competition for resources such as nesting sites or food, “you’d expect females to evolve whatever trait gives them the competitive edge. And that could be showy plumage or song.”
Do Females “Claim” Their Mates Through Song, Too?
On the campus of the University of California in San Diego, Dark-eyed Juncos are doing something new. Normally Dark-eyed Juncos in southern California are migratory, visiting only during the winter. But in the early 1980s, a small population of juncos decided to stay put on campus year-round. Changing migratory strategies is not too surprising given that warmer temperatures and the provision of year-round resources, such as bird feeders, can tempt a species to stay. What is surprising about this now-sedentary songbird population is that the females may be starting to sing.
Dustin Reichard, an assistant professor at Ohio Wesleyan University, notes that female song in Dark-eyed Juncos has not previously been reported, but his experiments showed that females in San Diego can and do sing. Reichard introduced a captive female junco into a junco breeding territory, played audio of a female junco’s call, and documented how other juncos responded. Territorial male juncos came streaming in to check out the captive female, while female juncos responded aggressively by singing a male-like song, and chasing their male mates away from the captive female, as if to say: “Hands off!”
Reichard’s findings may help elucidate why some female birds sing and others don’t. Nonmigratory behavior coupled with monogamy could influence female song in the now-sedentary San Diego juncos. Females, Reichard’s study suggests, may sing to prevent other females from mating with “their” male.
Song isn’t the only thing females lost over time, says Jordan Price from St. Mary’s College of Maryland. Price, like Odom, built an avian family tree, but this time he looked at plumage coloration, drawing a line back in time to determine what females and male ancestors of 37 different blackbird and grackle species (from Red-winged Blackbirds to Greater Antillean Grackles) might have looked like. Today male Red-winged Blackbirds sport showy red-and-yellow wing epaulets, and male Boat-tailed Grackles are an iridescent glossy black, but females of both species are dull brown. In the past, Price found, both males and females of blackbirds and grackles had brightly colored plumage. Females in these species, says Price, may have evolved duller plumage to help them blend in with their surroundings, when the pressures to hide from predators increased.
The once colorful and boisterous females, according to Odom’s and Price’s research, put a bit of a wrinkle in Darwin’s theory. Underlying Darwin’s theory of sexual selection is an assumption that both males and females once had duller colors and simpler vocalizations. Males then evolved elaborate traits because females started choosing brighter and more eloquent males, according to sexual selection.
Are Odom and Price suggesting that Darwin was wrong?
“Darwin wasn’t wrong,” says Price, “but our findings contradict [scientists’] assumptions.”
Male colors and songs can still be driven by females choosing males with certain traits, à la sexual selection, says Price, but other selective pressures can also act on females, and these pressures can act on males and females differently, and at the same time.
“Maybe it’s not just sexual selection that’s causing elaboration, but maybe it’s a suite of different selection pressures that can act on both males and females,” says Odom.
Those suites of pressures are what researchers call “social selection,” a term first used by Smithsonian Tropical Research Institute scientist Mary Jane West-Eberhard in 1979 as an alternative to sexual selection. Social selection, Odom says, is broader than sexual selection and involves competition not just for mates, but also for resources such as territories, food, or nest sites.
Social selection offers a new way to explain the evolution of female ornamental traits, such as song, that scientists previously assumed evolved only in males through sexual selection. Female bird song, says Odom, “likely evolved to help mediate a range of social behaviors and interactions, including competition for food or defense of territories inside and outside of the breeding season,” and social selection offers an explanation.
Scientists have long been familiar with the song of the male Hooded Warbler. Photo by Ray Hennessey. But it wasn't until the 1990s that scientists discovered that during breeding season, female Hooded Warblers may wander away from the nest and call loudly to nearby males to elicit extra-pair copulations. Photo by Dave Welling.
Secrets of Female Birds Are Revealed
It isn’t just evolutionary biology that had a history of overlooking females; ornithologists, too, have focused primarily on males in the past.
Until the late 1980s, many ornithologists assumed that songbirds were monogamous. Then along came the technology of paternity testing. DNA analysis revealed that sibling chicks in the same nest frequently came from different fathers. Male birds, scientists discovered, often sneak off to mate with additional females, spreading their genes far and wide—what ornithologists call extra-pair copulation.
For males, it was literally better to not put all their eggs in one basket. As for female birds, the prevailing view among ornithologists at the time was that female birds were the victims of extra-pair copulations. In a paper published in the journal Ethology in 1987, British biologist Tim Birkhead surmised that female birds could be expected to alter their behavior to “reduce the risk of suffering of a forced extra-pair copulation.”
Canadian ornithologist Bridget Stutchbury of York University in Toronto fell in line with Birkhead and the prevailing wisdom about female birds being victims—until she started studying Hooded Warblers in the early 1990s. When Stutchbury put radio transmitters on the backs of female Hooded Warblers to track their whereabouts and closely observe their behavior, she discovered that the females weren’t victims at all. In fact, they were calling loudly to other male Hooded Warblers, as if to say: “Hey, I’m over here!”
Female birds were also seeking additional mating opportunities to get a few more good genes for their offspring, Stutchbury concluded. In fact, the females may even be orchestrating the system to get more extra-pair copulations. By coordinating when they breed, a group of female birds can essentially force all of the males to strut their stuff at the same time, making it easier for them to evaluate multiple males and choose one—or more—of the best, says Stutchbury.
“The focus has usually been on what the males have been up to, and that’s why we don’t fully understand what’s going on,” says Stutchbury.
But by looking at female birds, Stutchbury uncovered one previously unknown behavior after another. Stutchbury’s radio-tagged female Hooded Warblers were recorded leaving their nesting territories once every three hours, which contradicted the prior notions that female birds are homebodies that stay on or near their nests.
“I never had a clue that females were doing that,” says Stutchbury.
Stutchbury’s team also discovered that female Blue-headed Vireos wander away from their nesting territory after the eggs hatch to scope out the bachelor scene. As soon as her young fledge the nest, the female vireo “takes off and mates with another male, while her first mate raises the young alone,” says Stutchbury.
Kent McFarland, cofounder of the Vermont Center for Ecostudies, also noticed some odd breeding behavior among the Bicknell’s Thrushes he studies in the Green Mountains. McFarland and his team watched multiple thrushes, not just the parents, bring food to a nest full of hungry chicks; one male brought food to the nest, and then minutes later a different male brought food. “Suddenly,” says McFarland, “what we had been seeing in the field over the last few years all started to make sense when we started paying attention to the females. The females seemed to be the key to the entire system.”
The research of McFarland and colleagues suggests that females can somehow assess how much food is present on their territories in a summer breeding season, and then adjust the number of males they mate with accordingly. If food is scarce, McFarland says, females will mate with multiple males—building connections and enlisting more helpers into foraging for food to feed the hungry chicks in the nest. But if food is abundant, females will mate with only one male—presumably because in good years a female and her mate can easily find enough food to feed their young on their own.
Understanding Bicknell’s Thrushes during the breeding season, McFarland says, “means focusing on and understanding the females.”
Conservation biologists are finding that they, too, need to understand what females are doing. Ruth Bennett is a former Cornell Lab doctoral student who works on conservation strategies for Neotropical migratory songbirds on their wintering grounds in Latin America. She says that among roughly two-thirds of the migratory birds she studies, males and females use different habitats during the nonbreeding season. Males, for example, may overwinter in middle-elevation forests, while females may overwinter in second-growth forest fragments.
That means one conservation strategy won’t work for both sexes, Bennett says. If females tend to overwinter in areas threatened by habitat loss more than males, it may be harder for females to survive, or vice versa.
But few conservation plans account for differences in habitat use by males and females. Bennett says the reason could be, again, that female birds are being overlooked.
“Because many male [Neotropical migratory] birds have brighter plumage and vocalize more than females, they may be easier to detect,” she says, adding that “if biologists don’t specifically account for this, they may overlook female-dominated habitats and landscapes in their conservation planning efforts, which could also lead to disproportionate declines of females.”
Bennett reexamined previous Golden-winged Warbler studies in which males had been detected at 10 times the rate of females. She concluded that researchers were finding vastly more male birds because males vocalize more, and respond more aggressively to audio playback of bird calls. She also determined that survey efforts were biased toward sites dominated by males.
Furthermore, Bennett found a discrepancy between where male and female Golden-winged Warblers occur and where conservation efforts were focused. Bennett used statistical models of where male and female golden-wings occur on their wintering grounds, coupled with assessments of loss of forest cover, and discovered that from Guatemala to Colombia, female Golden-winged Warblers are losing nonbreeding habitat at twice the rate of males. Yet current conservation planning efforts target male-dominated areas.
Bennett calls for more research on nonbreeding habitat use by male and female songbirds to ensure equal protection of habitat.
The bird-survey bias toward males is just one of the topics on the docket at this year’s American Ornithological Societyannual meeting in Alaska, where Odom is helping to host a symposium entitled “Breaking Through Biases: What We’ve Learned From Female Birds.” The event, featuring presentations by six ornithologists, is a review of the ways in which science is beginning to uncover the power of the female in breeding-bird biology, from the prevalence of female bird song to how female choice can affect mating behavior and evolutionary processes.
“This symposium,” says Odom, “highlights what we can learn from research that focuses on the female bird perspective. Instead of asking, ‘Why did a trait evolve in males?’, biologists are now asking, ‘Why don’t we see this trait in certain females, or how and why did a certain behavior evolve in females?’”
A century and a half after the world of biology shunned Darwin’s notion of female choice, this symposium focused on female birds represents a new era of recognizing and respecting female perspectives in biology, says Odom.
“To me, this symposium illustrates how far we have come in recent decades with more women scientists in ornithology,” she says, “and it celebrates the milestones that have been made through this inclusion.”
Kathi Borgmann is the communications coordinator for the Macaulay Library at the Cornell Lab of Ornithology.
Correction: An earlier version of this story attributed the first use of the term “social selection” to Stanford professor Joan Roughgarden in 2012. The actual first use was in 1979 by Smithsonian scientist Mary Jane West-Eberhard. The text of the article has been updated.
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