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The Mate Selection Trapdoor

Tracing the evolution of hidden sexual preferences.

The evolution of sexual beauty is an ongoing experiment in every species, including our own. Variation in courtship traits arise and…By Michael J. Ryan

The evolution of sexual beauty is an ongoing experiment in every species, including our own. Variation in courtship traits arise and are judged by choosers who quickly relegate most of them to the dustbin of history. But new attempts at beauty that pass muster, that trigger a hidden preference, hit the evolutionary jackpot.

Hidden preferences are often lurking in animals’ sexual aesthetics, masked to others because there are yet no sexual traits to elicit them. But if that trait evolves, one that matches or exploits a particular sexual aesthetic, then it is immediately deemed to be sexually beautiful, and, all else being equal, it should soon evolve to be common among males. This notion of how sexual beauty can evolve was virtually unknown before 1990 until a few other researchers and I developed this theory. Now it is thought to be one of the major factors driving the evolution of sexual beauty.

TOWER OF POWER: Male fiddler crabs erect towers by their burrows to be more easily seen by females. The towers are an extension of their sexual phenotype.Pat Backwell, Panama

To appreciate the evolutionary importance of hidden preferences, it pays to realize there are no free lunches in the sexual marketplace. Regardless of how traits and preferences evolve, they incur costs as well as reap benefits. It is the cost-benefit ratio, and how this changes through time, that determines their legacy. Given the cost-benefit ratio involved in sensory exploitation of hidden preferences, this might be an especially easy process to trigger.

A hallmark of sexually attractive traits is that they are costly. Whether they are the showy tail of a peacock or the bright colors of a guppy, these traits usually take more energy to produce, more time to maintain, and are more conspicuous to predators than other types of traits. Attractive red badges evolve in red-winged blackbirds. Yet a mutation that causes red badges can quickly disappear from the population if it is attractive to predators but not yet attractive to females. This must happen often: A mutation gives rise to a conspicuous sexual trait, but it goes extinct while waiting around for a mutation in the preference gene that will deem this trait attractive and thus beneficial. If there are hidden preferences, however, then when a trait like the red badge arises, it will incur the same cost, but there is not the risk of waiting around for a preference mutation to occur—the benefit is immediately provided by the previously hidden but now-exposed preference. Given the same mutation for an attractive trait, that trait is more likely to evolve if hidden preferences for it already exist.

It seems downright silly and certainly maladaptive for an animal to have sex with a plant.

Hidden preferences influence the evolution of sexual traits, but what causes the evolution of hidden preferences? They often arise from selection based on sensory, perceptual, and cognitive systems in other domains. Evolutionary biologist Helen Rodd and her colleagues pointed out that guppies often feed on orange fruit. The researchers suggested that the preference for food is at the root of the guppies’ preference for orange males. The females are not fooled into thinking the males are fruits, but instead, the researchers hypothesized, the females develop a gestalt attraction to orange that spills over from their food preference into their mating preference. Selection on color preferences related to food—also seen in surf perch and bowerbirds—show how selection on sensory systems in the domain of foraging results in hidden preferences for male courtship colors. In most cases, we expect the origin of the hidden preferences to be an adaptive response to the world around them, with an influence on perceptions of beauty that is incidental rather than the immediate consequence of selection and evolution.

Hidden preferences will nearly always be related to adaptive advantages in other domains. To compute the evolutionary costs and benefits of a hidden preference, we must take into account not only how it impacts the chooser’s mating success but also how it relates to functions in other domains that influence the chooser’s fitness.

Let’s go back to the guppies and imagine that males with more orange attract more parasites, and by courting a more orange male rather than a less orange male, a female is more likely to become parasitized herself. If she gains no other benefits from the more orange male, we might assume that exhibiting this hidden preference for especially orange males is maladaptive, all costs and no benefits. And similar to a new sexual trait without the benefits of a preference, a newly exposed hidden preference with only costs should also go extinct.

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But if preferences for food and mate color are inextricably linked, then to give a fair accounting of the fitness costs and benefits of the hidden preference, we also need to take into account benefits of this bias-toward-orange in the foraging domain. The trait facing costs and benefits is not just “preference for oranger males” but “bias toward orange in general.” This is reminiscent of the behavior of orchid bees mating with orchids. It seems downright silly and certainly maladaptive for an animal to have sex with a plant until we consider this perversion in the context of the bee’s mate-searching strategy. Since female bees are hard to come by, then it is better for the male bee to be too eager to mate, and sometimes mate with flowers, rather than too discriminating, and sometimes pass up real female bees.

Yet tracing the evolution of courtship behavior in terms of traits that exploit hidden preferences might suggest that such inclinations are maladaptive. In fact, there are few, if any, examples of this being the case. Instead, the opposite usually holds: Once hidden preferences are revealed, they deliver benefits rather than costs to the chooser. How is that? Hidden preferences probably reduce search costs to choosers. Courters that exploit these preferences often do so because they are more conspicuous to choosers; for example, they are more easily seen in guppies, surf perch, and fiddler crabs, and more easily heard in many frogs, insects, and songbirds. In the fiddler crab, males that erect towers by their burrows are more easily seen by females, since the structure of her eyes make her especially sensitive to objects protruding vertically from the surface. Besides being an extension of the male’s sexual phenotype, the towers also direct females to shelter from predators.

Not only are exploiting males more easily sensed; their sexual traits can facilitate quicker mating decisions and longer memories of the signals. Female túngara frogs decide on a mate faster when choosing between a whine-chuck call and a whine than when faced with the choice between two whines. In addition, females also remember the location of a whine with multiple chucks over a whine-only or a whine with a single chuck. My colleague Molly Cummings and I recently reviewed hundreds of cases in which males evolved sexual traits to exploit hidden preferences. In most cases, these preferences appear to aid rather than impede finding a mate, thus decreasing the time involved in searching.


The sexual marketplace is a dangerous place, but one that can’t be avoided. It is the only place to shop for a mate, but it is also filled with predators shopping for food and parasites looking for a home. The quicker the sexual consumer can get out of there, the less likely it will become the consumed. So having your hidden preferences exploited might not be all that bad—in fact it might be mostly good.

What I find especially interesting are examples of hidden preferences for traits that are not only lacking in the species of interest but also in any closely related species, traits that researchers rather than evolution have brought into being. These examples give us insights into how the preference landscape is ripe with hidden preferences waiting to be exploited. It is this lability of the preference landscape that affords the chooser’s brain so much creative power in driving the evolution of sexual beauty.

Hidden preferences influence the evolution of sexual traits, but what causes the preferences?

The ornithologist Nancy Burley conducted some early and insightful experiments on hidden preferences. When birds are kept in aviaries, it is hard for researchers to keep track of who is who. One solution is to put bands on their legs, and if the bands are different colors, then researchers can identify the birds without handling them. Zebra finches do not have leg bands in nature, so it was a shock when Burley found that leg bands influence the attractiveness of both sexes. Males are more attracted to females adorned with black and pink leg bands, and they are not attracted to females with light blue or light green leg bands. Females, on the other hand, prefer red-banded males and also avoid males with light blue or light green bands.

Burley’s study was important because it revealed that studies of mating success in captive birds could be biased by the use of leg bands. Burley also pushed the envelope a bit with her experiments. She adorned male grassfinches with what looked like “party hats.” Some species of birds have crests, which are elongated feathers on the head, but there are 120 species of grassfinches, and none of them have crests. Yet when elongated feathers are added to the tops of males’ heads in two grassfinch species, they look ridiculous to us but more sexually appealing to females than the typical males of their species.

Other researchers have taken this approach of adding novel traits to males to search for hidden preferences in females. Mosquito fish have been introduced all over the world as a biocontrol agent. As its name implies, mosquito larvae can constitute a substantial component of the diets of these fish. In Australia, a country that is infamous for failed biocontrol efforts such as introducing cane toads, the introduced mosquito fish experiment failed because these fish outcompeted other natural mosquito predators. Like the cane toads, mosquito fish are now considered pests Down Under. There is nothing colorful or exciting about these fish. The males are small, only a few centimeters long, and they lack any conspicuous courtship traits or behaviors. Males have a sexual organ, a gonopodium, that they use to inseminate females, somewhat like a penis. But in most ways it is nothing like a penis. It is a long, modified fin with a groove on the outside. Sperm travels down this groove and, when the end is inserted into a female, the sperm enters the female’s body. Except for the gonopodium, the males make little investment in sex; they lack the flashy colors of guppies and the sexual ornaments of swordtails. But … what if?

This is the question that the animal behaviorist Jim Gould and his colleagues asked. In 29 separate experiments, they presented to females models of male mosquito fish that had been manipulated in a myriad of ways. Tail fins were stretched out, dorsal fins were morphed to appear sharklike, swords were added, fish were blackened, speckled, and whitewashed. In almost every comparison, females showed preferences for the weird, the novel, and the outlandish males. The real males might be conservative in their approach to sexual beauty, but deep down, below the radar, their females are yearning for anything but conservative; they are teeming with hidden preferences.

The same occurs in túngara frogs. Even though these males have outdone their close relatives by evolving the chuck, an incredibly attractive syllable that when added to their call increases a male’s attractiveness by 500 percent, most of their females’ acoustic desires are unmet. In a series of experiments quite similar to Gould’s, we conducted 31 experiments in which we manipulated calls in varying ways, such as replacing the chuck with blasts of white noise, calls of other species, and even bells and whistles. Like Gould, we also found an astounding promiscuity of preferences. Females found many of these acoustic accouterments attractive, even bells and whistles. When the chuck evolved, it was lucky enough to exploit a hidden preference, but we now see it was not uniquely attractive. Many different kinds of sounds might have worked just as well; the luck of the chuck was being first.

In many species, members of one sex have been part of an age-old evolutionary experiment to come up with sexual traits that elicit preferences from members of the other sex. This is paralleled in human societies by cultural experiments to tap into some of our own hidden preferences. Therein lies a cautionary tale: Many human industries have been designed to capitalize on and exploit hidden sexual preferences for their own monetary gain.

The evolution of sexual beauty is analogous to an artist experimenting with paint on a canvas or a musician tinkering with new combinations of beats and chords. They are probing for what will ring true with the aesthetics of their audience. All three are creative processes. All of them surround us with beauty by probing deep into our brains to find out just what we will consider beautiful.


Michael J. Ryan is the author of A Taste for the Beautiful: The Evolution of Attraction, due in February, 2018. He is the Hubbs Regents Professor in Zoology at the University of Texas and a Senior Research Associate at the Smithsonian Tropical Research Institute in Panama. He lives in Austin, Texas.

Excerpted from A Taste For The Beautiful: The Evolution of Attraction by Michael J. Ryan. Copyright © 2018 by Princeton University Press. Reprinted by permission.

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