Iconic sexual selection study “fatally flawed”

A classic study from more than 60 years ago that suggested males are more promiscuous and females more choosy in selecting mates has informed and influenced evolutionary biology for decades, but a modern day repeat of the experiment indicates the original work may have been fatally flawed. The new work calls into question many of the fundamental tenets of female mating habits and sexual selection in general.

Sexual selection emerged as a scientific discipline following Charles Darwin’s publication of The Descent of Man, and Selection in Relation to Sex. Darwin argued that while the unwieldy, colorful tails of peacocks hindered flight and made males easy targets for hungry tigers, the flamboyant plumage served a vital role in attracting potential mates. The overdressed birds had an unexpected evolutionary advantage that did not help when it came to escaping predators but did help when it came to producing offspring through sexual selection.

The original experiment, carried out in 1948 by English geneticist Angus John Bateman, indicated that male fruit flies gain an evolutionary advantage from having multiple mates, while their female counterparts do not. “Bateman’s 1948 study is the most-cited experimental paper in sexual selection today because of its conclusions about how the number of mates influences fitness in males and females,” said Patricia Adair Gowaty, a distinguished professor of evolutionary biology at the University of California – Los Angeles (UCLA). “Yet despite its important status, the experiment has never been repeated with the methods that Bateman himself originally used, until now.

Gowaty’s team of researchers repeated Bateman’s experiment and found that what was previously accepted as scientific bedrock may actually be quicksand. “It is possible that Bateman’s paper should never have been published,” said Gowaty. Her findings appear in the Proceedings of the National Academy of Sciences .

The original experiment on the common fruit fly (Drosophila melanogaster) was performed by creating multiple, isolated populations with either five males and five females or three of each gender in a jar. The insects mated freely in the experimental populations, and Bateman examined the children that made it to adulthood. To count the number of adult offspring engendered by each of his original insect subjects, Bateman needed a reliable way to match parents with children.

Nowadays, modern geneticists would use molecular evidence to determine the genetic parentage of each child, but DNA analysis was not available in the 1940s. Instead, Bateman chose his initial specimens carefully, selecting fruit flies that each had a unique, visible mutation that could be transferred from parent to child.

The mutations he chose were extreme. Some of the flies had curly wings, others thick bristles, and still others had eyes reduced in size to narrow slits. The outward differences in each breeding subject allowed Bateman to work backward to determine the parentage of some of the fly progeny and to document each mating pair among the original insects. A child with curly wings and thick bristles, for example, could only have come from one possible pairing.

Yet Bateman’s method, which was cutting-edge for its time, had a “fatal flaw,” according to Gowaty. “Imagine the child of a curly-winged mother and an eyeless father. The child has an equal chance of having both mutations, only the father’s mutation, only the mother’s mutation or no mutation at all. In order to know who mated with whom, Bateman used only the children with two mutations, because these were the only ones for which he could specifically identify both the mother and father. But by counting only the children with two mutations, Bateman probably got a skewed sample,” Gowaty explained. In repeating Bateman’s experiment, she and her colleagues found that the flies with two severe mutations are less likely to survive into adulthood.

Flies use their wings not only to hover but also to sing during courtship, which is why curly wings present a huge disadvantage. Specimens with deformed eyes might have an even tougher time surviving. The 25 percent of children born with both mutations were even more likely to die before being counted by Bateman. “It’s not surprising that the kids died like flies when they got one dramatic mutation from mom and another dramatic mutation from dad,” Gowaty observed.

Her team found that the fraction of double-mutant offspring was significantly below the expected 25 percent, which means Bateman would have been unable to accurately quantify the number of mates for each adult subject. Further, Gowaty argues, his methodology resulted in more offspring being assigned to fathers than mothers, something that is impossible when each child must have both a father and a mother.

Bateman concluded that male fruit flies produce many more viable offspring when they have multiple mates but that females produce the same number of adult children whether they have one mate or many. But Gowaty and her colleagues, by performing the same experiment, found that the original data were decidedly inconclusive.

In the repeated experiment – and possibly in Bateman’s original study – the data failed to match a fundamental assumption of genetic parentage assignments. Specifically, explained Gowaty, the markers used to identify individual subjects were influencing the parameters being measured (the number of mates and the number of offspring). When offspring die from inherited marker mutations, the results become biased, indicating that the method is unable to reliably address the relationship between the number of mates and the number of offspring. Nonetheless, Bateman’s figures are featured in numerous biology textbooks, and the paper has been cited in nearly 2,000 other scientific studies.

“Bateman’s results were believed so wholeheartedly that the paper characterized what is and isn’t worth investigating in the biology of female behaviour,” said Gowaty. “Those who blindly accept that females are choosy while males are promiscuous might be missing a big piece of the puzzle. Our worldviews constrain our imaginations. For some people, Bateman’s result was so comforting that it wasn’t worth challenging. I think people just accepted it.”

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Source: University of California – Los Angeles

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