The idea that animal evolution is shaped by males boasting and fighting to win female favor is a central biological dogma.

Females pick males whose exaggerated traits suggest virility, thus producing peacock feathers and sage grouse struts. Males compete for female favor, hence a stag's antlers and fights for territorial domination. These are the main engines of sexual selection, the default explanation for differences between the sexes.

Under closer scrutiny, however, the dogma doesn't seem to hold. A new replication of English geneticist Angust Bateman's foundational mid-20th century mate-choice study, a study that reinforced sexual selection assumptions and shaped decades of research, came to very different conclusions than the original.

Bateman's refutation may be an exclamation point for critics who say the evolutionary dance between sexes is far richer and more complicated than a male-dominated two-step.

"Our expectations have been so strongly affected by Bateman," said evolutionary biologist Patricia Gowaty of the University of California, Los Angeles, who led the study's replication, published in June in Proceedings of the National Academy of Sciences. "It's almost as though our imaginations were limited."

The original study, published in 1948, followed on a line of thinking that originated with Charles Darwin, who saw in the fantastically colorful feathers of male peafowl a trait that made no evolutionary sense except as an advertisement to prospective mates. Peacocks and peahens had resembled each other long ago, he surmised, but hens learned that bright, spotted feathers signified fitness. Magnified over evolutionary time, their preference produced the peacocks' otherwise impractical plumage.

For Darwin, this demonstrated a universal principle: Males benefit by mating frequently and indiscriminately, with each successful copulation representing an extra chance to pass on their traits, while females mate infrequently, invest energy in rearing offspring and generally benefit by being choosy about mates. From that dynamic would emerge physical and behavioral differences between sexes.

Bateman tested the principle using what were, for his time, cutting-edge genetic tools. He bred fruit flies that each contained a single pronounced trait, such as tiny heads or shriveled wings or slit-shaped eyes. By looking for these traits in offspring, it was possible to identify their parents.

Tests affirmed Darwin's ideas and were codified into what became known as Bateman's principles, which mathematically described how between-sex differences in mating benefits and reproductive fitness could be measured. The paper has been cited nearly 2,000 times and its ideas became assumptions with cultural resonance. “The word excess has no meaning for a male,” wrote Richard Dawkins in The Selfish Gene.

Over time, however, rumblings of discontent grew. A few biologists, Gowaty among them, suggested that mating patterns measured by Bateman could have been explained by chance or environment. Yet nobody put Bateman's study to the ultimate test – until now.

In the replication, Gowaty and geneticists Wyatt Anderson and Yong-Kyu Kim of the University of Georgia duplicated Bateman's study design, even breeding fresh generations of fruit flies with the same exaggerated physical traits. They noticed something that Bateman didn't consider important: Flies with pronounced traits from two parents, such as shriveled wings and tiny heads, were unfit and died before hatching.

Bateman only counted adult flies, but Gowaty and Anderson included the deceased juveniles. Their results show that Bateman's approach was skewed, causing him to overestimate the number of adults that hadn't mated at all, underestimate the number who mated multiple times, and to under-count mothers. In short, there was no evidence for indiscriminately mating males and finicky, seldom-mating females.

"Bateman's ideas … have helped to define what we mean by sexual selection and how best to measure it," wrote Zuleyma Tang-Martínez, a biologist at the University of Missouri-St. Louis, in a separate commentary in PNAS. She said the new results are "likely to lead to a paradigm shift in the study of sexual selection and related topics."

A contrary interpretation was offered by evolutionary biologist Adam Jones of the University of Texas. "This study, while interesting, is not paradigm challenging," he said. "We now have studies from many other systems other than Drosophila (fruit flies) confirming the main conclusions of Bateman's original study. Thus, even if Bateman's study was flawed, as it certainly was by today's standards, the impact of his study on the field of evolutionary biology is secure."

Jones' own research has demonstrated that classic, Bateman-style sexual selection does explain sexual differences in animals like the rough-skinned newt, and it unquestionably applies to many species.

But Martinez and Gowaty say that traditional views on sexual selection have skewed science. "Bateman’s ideas and conclusions ... have helped to define what we mean by sexual selection," wrote Martinez. "It is fairly common for studies of Bateman gradients to disregard alternative explanations."

Gowaty said her work in the 1980s on female bluebirds, who mate frequently with multiple males, was originally greeted with incredulity. "I had colleagues say that it couldn't happen, that it was rape," she said.

Since then, research has painted a picture of animal reproduction more colorful than Darwin or Bateman ever surmised. Male competition and female choosiness only sometimes describe the variety of reproductive habits influencing animal evolution.

Gowaty hopes that revisiting Bateman's study will encourage people to see "alternative" mating strategies as unexceptional, though she said the fundamental implication is less about animal behavior than the importance of challenging received wisdom. "We believed the results so thoroughly, it didn't occur to people to replicate the study," Gowaty said.

"I wonder if we shouldn't all be a little more self-skeptical," she continued. "If we missed for so long that Bateman was inadequate to his task, what might we be missing in more modern studies?"

Image: 1) Juan David Castillo/Flickr 2) lowjumpingfrog/Flickr

Citations: "No evidence of sexual selection in a repetition of Bateman’s classic study of Drosophila melanogaster." By Patricia Adair Gowaty, Yong-Kyu Kim and Wyatt W. Anderson. Proceedings of the National Academy of Sciences, June 11, 2012.

"Replication of Bateman challenges the paradigm." By Zuleyma Tang-Martínez. Proceedings of the National Academy of Sciences, July 3, 2012.