[This is the last post for Sex Week]

The animal kingdom is filled with wild extravagances, and a lot of them have something to do with sex. Hermit crabs wave their claws, swordtail fish flash their swordtails, manakins leap and buzz their wings. Darwin considered these displays so important and so puzzling (”the sight of a feather in a peacock’s tail, whenever I gaze at it, makes me feel sick!” he wrote to a colleague), that he dedicated half of a book to the subject.

Darwin argued that many extravagant displays in male animals were the result of a special kind of evolution he called sexual selection. Females preferred males with certain traits over other males, and so those males had more offspring, which inherited their traits. In recent decades, scientists have documented many cases in which females do indeed prefer males with certain traits over others. As I mentioned in my post on electric fish, for example, female bulldog fishes are more attracted to long electric pulses than short ones.

But why should females have any particular desire? For many scientists, the most compelling explanation is that there’s some meaning in the displays that attract them. One possible meaning is that the male who sports a particularly extreme version of a trait has good genes. As I wrote in my post on the love songs of yeast (sic), the amount of pheromones a yeast cell produces is a reliable clue to the quality of its genes. Other scientists have found similar links between the length of tail feathers and the quality of male birds.

There are other possible meanings, though. Some scientists have argued, for example, that female of some birds species prefer bright feathers on males simply because they’re easy to spot. A female with such a preference will be able to mate more efficiently than a female attract to drab, harder-to-find males. She’ll be less likely to get killed by a predator and can spend her time and energy on more useful things than hunting for a mate. Wham, bam, thank you, sir.

All of these explanations share something in common: sexual signals evolve because they signify something. Many scientists see little evidence to think that sexual displays evolved for no good reason.

And yet in other realms of evolution, biologists have come to accept that some patterns can emerge without the help of selection. Each of us is born with around 70 new mutations in our DNA. In a few cases, a mutation will cause a lethal disease and will not be able to be passed down to the next generation. In a few cases, a mutation will boost a person’s reproductive success and will gradually spread. In both these cases, natural selection is at work. It’s the reason why the harmful mutation is rare, and the beneficial one is widespread. But the spread of mutations is also governed by chance. A mutation that has no benefit or risk at all can spread throughout an entire species thanks to a fortunate roll of the genetic dice.

There was a time when most biologists did not believe that neutral genetic variation even existed. It all had to be the product of selection. Now, however, biologists generally agree that neutral genetic variation is rampant. In fact, netural evolution has taken on an important role in the study of natural selection. Scientists who want to know if a particular stretch of DNA has experienced natural selection must reject the null hypothesis that it is simply the result of neutral evolution. If you can show that neutral evolution couldn’t have produced a particular sequence of DNA, then you can be fairly confident that selection was responsible. Once you do that, you can start to investigate what sort of selection was at work. (For more on the underappreciated role of neutral evolution, check out Larry Moran’s periodic posts on the subject on his blog, Sandwalk.)

The phrase null hypothesis was first coined in the early 1900s by a British mathematician named Ronald Fisher. Fisher did some of the most important work to put Darwin’s theory of evolution on a sound mathematical footing–figuring out how to represent things like natural selection as equations and graphs, rather than just verbal arguments. Fisher showed, for example, how natural selection could proceed through the spread of lots of mutations with tiny effects. But Fisher also developed an idea that’s not so well remembered these days. Like Darwin, he pondered how sexual displays could evolve through female preferences. One idea he came up with is that a display–and a female’s preference for it–could both be completely arbitrary.

It’s fair to say that most evolutionary biologists today don’t find Fisher’s idea very useful. Nevertheless, some important thinkers have embraced and updated it. And in a new review in the journal Evolution, the Yale evolutionary biologist Richard Prum makes a bold case for taking Fisher seriously. Prum argues that it’s quite reasonable to expect sexual signals to be totally arbitrary, signifying nothing deeper about the animals who show them off. In fact, he argues, it should be the null hypothesis for scientists studying sexual displays.

I’ve known Prum for a few years now, having written some articles on his work and having had him talk to my writing class. Many of our conversations have gravitated to this big idea, which he’s been mulling for some time. So it’s good to finally see this argument in print at last.

The idea that something like a courtship dance or a song can evolve with no help from selection is a tricky one to grok. Here’s a simple version of the model. Imagine a population of birds. The males have genetic variation in the size of a red spot on their breast. Some have a bright red spot, and others have a dull one. The females, on the other hand, have genetic variation in their preference for the trait. Some only mate with males with bright red spots, and some will mate with any males. The extravagant males will have more offspring than the plain ones, because they can mate with all the choosy females and some of the non-choosy ones. The plain males only mate with the non-choosy ones. What’s more, the males with the bright red spot and the choosy females combine their genes in their offspring. The population increasingly is made up of males with an extravagant trait and females with a preference for it. And so the extravagant display spreads quickly through the population–even though the trait doesn’t signify anything.

Mark Kirkpatrick of the University of Texas, Russell Lande of Imperial College London, and their colleagues have developed much more sophisticated mathematical models of Fisher’s idea. They have found that even if the variations in male traits and female preferences are subtle, they can still get swept up into all sorts of complex evolutionary changes. Yet many others have been skeptical. One scientist declared that excepting this runaway process as an explanation for sexual selection without a lot of proof was “methodologically wicked.”

One objection was that sexual displays often impose such a big cost that they have to have some major benefit. Yet Kirkpatrick and Lande have shown that female preference and male displays can drive each other’s evolution so hard that males may end up with traits that are a major burden. They’re just so sexy that the males still continue to spread their genes. In fact, Prum argues, this runaway process is much more powerful and flexible than sexual selection based on an honest signal. If sexual displays are just relaying honest information about males, then why are closely related species so different in what they find attractive?

In his review, Prum looks at a series of studies in which scientists tried to figure out the reason that birds have extravagant traits, such as complex songs. He notes how the scientists always go into the studies assuming that there must be some meaning to the trait, so that its evolution can be driven by selection. Sometimes they fail to find that meaning, and when they do, they conclude that there must be another meaning they haven’t found yet. All they’re doing is trying to confirm a foregone conclusion, Prum argues, when they out to be trying to reject the null hypothesis.

If they can’t reject the null hypothesis, they should conclude that the best explanation for a bird song or a dance or some other display is that it’s just arbitrary. Prum doesn’t think that every sexual display will turn out to be arbitrary, but he expect that a lot of them will.

“I do not claim that the ‘Emperor has no clothes,’” he writes in his conclusion. “I would predict that the ‘Emperor wears a loincloth.’”

I’d be curious to know what evolutionary biologists who work on sexual selection think of Prum’s manifesto (paging Marlene Zuk). It’s certainly provocative, evoking not just Stephen Jay Gould’s attacks on Dawkins and other adaptationists, but even the Dadaists, who toyed with the arbitrariness of beauty in pieces such as Marcel Duchamp’s Fountain, shown here. And it’s also a good way to end Sex Week, as we leave biologists continuing to argue and marvel over the mysteries of sex.

[Image: Wikipedia]