Adapted from The Evolution of Beauty, How Darwin’s Forgotten Theory of Mate Choice Shapes the Animal World—and Us by Richard O. Prum. Copyright © 2017 by the author. Published in the United States by Doubleday, a division of Penguin Random House LLC.
In On the Origin of Species, Charles Darwin made two transcendent scientific discoveries: the mechanism of evolution by natural selection, and the concept that all organisms are historically descended from a single common ancestor. But despite these successes, Darwin had three gnawing problems after publication of the Origin. The first was the absence of any working theory of genetics, which was fundamental to natural selection. The second was human evolution, which he left unaddressed in the Origin. And the third problem was the origin of impracticable beauty.
If natural selection was driven by the differential survival of heritable variations, what could explain the elaborate beauty of the peacock’s tail? Obviously, the tail did not help the male peacock to survive; if anything, the huge tail would be a hindrance, slowing him down and making him much more vulnerable to predators.
Darwin was especially obsessed with the peacock’s “eyespots.” He had argued that the human eye could be explained as the result of many small, incremental, functional advances over time. Each advance produced slight improvements in the ability of the eye to detect light, to distinguish shadows from light, to focus, to create images, to differentiate among colors, and so forth, all of which would have contributed to the animal’s survival. But what purpose could the intermediate stages in the evolution of the eyespots have served? Indeed, what function do the eyespots on a peacock serve? In 1860, Darwin wrote to his American friend, Harvard botanist Asa Gray: “The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!”
In The Descent of Man, and Selection in Relation to Sex, published in 1871, Darwin boldly addressed both the problem of human origins and the evolution of beauty. In Descent, Darwin proposed a second, distinct, and independent mechanism of evolution—sexual selection. If natural selection results from differential survival of heritable variations, then sexual selection is the result of their differential sexual success (i.e., the success of heritable variations that contribute to obtaining more mates and fertilizing more offspring).
If female birds had been incapable of appre-ciating the beautiful colours, the ornaments, and voices of their male partners, all the labour and anxiety by the latter in displaying their charms before the females would have been thrown away; and this is impossible to admit.
Darwin concluded, “On the whole, birds appear to be the most aesthetic of all animals, excepting of course man, and they have nearly the same taste for the beautiful as we have.” Today, Darwin’s choice of aesthetic language can seem quaint, anthropomorphic, and possibly even embarrassingly silly. Clearly, Darwin did not have our contemporary fear of anthropomorphism. Indeed, he was engaged in breaking down the previously unquestioned barrier between humans and other forms of life. Darwin’s use of aesthetic language was not just a curious manner-ism, or a quaint Victorian affectation, but an integral feature of his scientific argument about the nature of evolutionary process. Darwin used ordinary aesthetic language to make an extraordinary scientific claim: mate choices based on the subjective evaluations of animals drive the evolution of sexual ornaments in nature. By using the words beauty, taste, charm, appreciate, admire, and love, Darwin proposed that mating preferences evolved for displays that had no utilitarian value, other than the pleasure they evoked to the chooser. Darwin wrote:
The case of the male Argus Pheasant is eminently interesting, because it affords good evidence that the most refined beauty may serve as a sexual charm, and for no other purpose.
In this way, Darwin viewed sexual selection as a dis-tinct evolutionary mechanism from natural selection with independent, potentially non-adaptive consequences. Darwin’s theory of mate choice was also coevolutionary. Darwin hypothesized that specific display traits and the “standards of beauty” used to evaluate them evolved to-gether, mutually influencing and reinforcing one another over time. Thus, he wrote:
…the male Argus Pheasant acquired his beauty gradually through the preference of the females during many gener-ations for the more highly ornamented males; the aesthetic capacity of females advanced through exercise or habit just as our own taste is gradually improved.
To Darwin, behind every sexual ornament is an equally elaborate, coevolved sensory/cognitive preference that has driven, shaped, and been shaped by that ornamental trait.
Upon its publication, Darwin’s theory of sexual selection was swiftly and brutally attacked. Or more precisely, part of it was. Darwin’s concept of male-male competition—the Law of Battle—was immediately and almost uni-versally accepted. Clearly, the notion of male-male competition for dominance over female sexuality was not a hard sell in the patriarchal Victorian culture of Darwin’s time. But, immediately after its publication, the confirmed evolutionist St. George Mivart launched an all-out attack on Darwinian mate choice:
Even in Mr. Darwin’s specially-selected instances, there is not a tittle of evidence tending, however slightly, to show that any brute possesses the representative reflective faculties.
In discussing the role of the peahen in the evolution of the peacock’s tail, Mivart wrote:
such is the instability of vicious feminine caprice, that no constancy of coloration could be produced by its selective actions.
To Mivart, female sexual whims were so malleable (i.e., fickle females preferring one thing one minute, and another the next) that they could never lead to the evolution of something as marvelously complex as the peacock’s tail.
Mivart’s language also reveals the deep misogyny and moral judgment that Darwin’s concept of mate choice evoked. At that time, the word “vicious” meant immoral, depraved, or wicked—literally, characterized by vice. Likewise, to Victorians, “caprice” was a “turn of mind made without apparent or adequate motive.” Thus, to Darwin’s critics, female mate choice had overtones not just of fickleness but of immorality and sin.
Mivart was also the first to portray Darwin as a traitor to his own great legacy—a traitor to true Darwinism:
The assignment of the law of “natural selection” to a subordinate position is virtually an abandonment of the Darwinian theory; for the one distinguishing feature of that theory was the all-sufficiency of “natural selection.”
Mivart established an attack on Darwin’s concept of aesthetic evolution that is still in use today—citing the Origin to argue against Descent.
The most consistent and effective critique of sexual selection came from Alfred Russel Wallace. Darwin and Wallace never agreed on sexual selection, but Wallace’s critique was so successful that sexual selection was almost completely marginalized within evolutionary biology until the 1970s.
Wallace’s view of sexual selection was motivated by his religious faith. Wallace believed that humans had been specially created by God, and divinely endowed with cognitive capacities and free will that animals lacked. Animal choices were inconceivable to him. But Wallace was never able to reject evolution by mate choice entirely. When forced to admit the possibility, he insisted that sexual ornaments could only have evolved because they had an adaptive, utilitarian value. In Tropical Nature, and Other Essays, Wallace wrote:
The only way in which we can account for the observed facts is by supposing that colour and ornament are strictly correlated with health, vigor, and general fitness to survive.
Here, Wallace was the first to articulate the idea that sexual displays constitute “honest” indicators of the objective quality and condition of mates—an entirely orthodox view in sexual selection today. But how can it be that Wallace, the man justly credited with having destroyed sexual selection theory for over a century, invented the viewpoint that would be entirely at home in any modern biology textbook? The answer is that contemporary mainstream views of mate choice are as stridently anti-Darwinian as Wallace’s were.
Today, most evolutionary biologists would agree with Wallace that all sexual selection is simply a form of natural selection. But Wallace went further than they do, by rejecting the term sexual selection entirely. If adaptive natural selection is always driving the show, he reasoned, then the concept of sexual selection should be abandoned entirely.
Then, in the introduction to his 1886 book Darwinism, Wallace wrote,
…[I]n rejecting that phase of sexual selection depending on female choice, I insist on the greater efficacy of natural selection. This is pre-eminently the Darwinian doctrine, and I therefore claim for my book the position of being the advocate of pure Darwinism.
Here, Wallace claims to be more Darwinian than Darwin! Just a few years after Darwin’s death, Wallace had begun to reshape Darwinism in his own image. In these passages, we witness the birth of “adaptationism”—the belief that adaptive natural selection is a universally strong force that will always be predominant in the evolutionary process. In this way, Wallace transformed Darwin’s fertile, creative, and diverse intellectual legacy into the monolithic, narrow, and intellectually impoverished theory with which Darwin is almost universally associated today.
The Darwin we have all inherited has been laundered, retailored, and cleaned up for ideological purity. The true breadth and creativity of Darwin’s ideas have been nearly written out of history. Alfred Russel Wallace may have lost the battle for credit over the discovery of natural selection, but he won the war over what evolutionary biology and Darwinism would become in the twentieth century.
According to Fisher, the force that drives the evolution of mating preference is mate choice itself. In an exact reversal of the Wallacean view of natural selection as “neutralizing” sexual selection, Fisher proposes that arbitrary aesthetic choices (per Darwin) will trump choices made for adaptive advantage (per Wallace). Once the trait is attractive, its attractiveness and popularity become ends in themselves. To Darwin and Fisher, ornamental traits are meaningless and arbitrary—merely beautiful and lacking adaptive utility. In nature, the desire for beauty will endure, and undermine the desire for truth.
How can this work? Fisher hypothesized the evolution of a positive feedback loop between the ornament and the preference for it. Because females who prefer mates with longer or shorter tails will choose corresponding males, genetic variation for display traits and preferences will become correlated (i.e., genes for long tails will be found in individuals with genes for preferring long tails, and vice versa). As a consequence, when females exercise their mate choices for particular display traits, they will also be selecting indirectly on genes for mating preference. The result is a positive feedback loop in which mate choice becomes the selective agent in the evolution of mate choice itself. Fisher called this self-reinforcing sexual selection mechanism a “runaway process.”
Like Darwin’s idea, Fisher’s model is coevolutionary. The form of sexual beauty and the desire for it shape each other through a coevolutionary process. In this way, Fisher provided a mechanism of how the display trait and mating preference can “advance together,” as Darwin envisioned.
Later, in the early 1980s, biologists Russell Lande at the University of Chicago and Mark Kirkpatrick at the University of Texas, Austin, developed explicit mathematical models of Fisher’s long-ignored mechanism of trait and preference evolution. However, this renascent interest in Darwinian mate choice was soon overtaken by Neo-Wallacean theories of adaptative mate choice. Of course, contemporary adaptive mate choice theories had to be reinvented from scratch because no one remembered Wallace’s version of honest advertisement. But all these theories shared Wallace’s original logic.
The chief proponent of adaptive mate choice in the 1970s and 80s was Amotz Zahavi, a charismatic and energetic Israeli ornithologist with a fierce independent streak. In 1975, Zahavi published his “handicap principle,” which was a huge stimulus to the adaptive mate choice paradigm. Echoing Wallace, Zahavi wrote that “sexual selection is effective because it improves the ability of the selecting sex to detect quality in the selected sex.”
Zahavi then added his own distinctive twist to Wallacean logic. To Zahavi, the entire point of any sexual display is that it is a costly burden to the signaler—literally, a handicap. By its very existence, the ornamental handicap demonstrates the superior quality of the signaler because the signaler has been able to survive it. Zahavi wrote that “sexual selection is effective only by selecting for a character that lowers the survival of the organism… It is possible to consider a handicap as a kind of test.”
The more elaborate the trait, the greater the costs, the bigger the handicap, the more rigorous the test, and the better the mate. Accordingly, the individual who is attracted to a mate with such a costly trait is responding not to its beauty, which is incidental to its costs, but to what it tells her about that male’s ability to rise above its cost.
In what way was the handicapped male better? To Zahavi, it was clear that he could be better in every imaginable way. However, those who followed Zahavi established that the adaptive benefits of mate choice could be either direct or indirect. The direct benefits of mate choice include any advantages to the health, survival, or fecundity of the choosers themselves, such as a mate with no sexually transmitted diseases, a greater capacity to invest in the feeding offspring, better protection from predators, or a better territory with more food or better nesting sites. Alternatively, the adaptive indirect benefits are in the form of good genes that are inherited by the chooser’s male and female offspring, and contribute to their survival and fecundity.
To understand the logic of Zahavi’s handicap principle, let’s consider a corollary to it that I call the “Smucker’s Principle.” Smucker’s Jelly takes its name from its founder, Jerome Monroe Smucker, who opened a cider press in Orrville, Ohio, in 1897. Since the early 1950s, the company has used the catchy advertising slogan: “With a name like Smucker’s, it has to be good!” The slogan claims that the Smucker’s brand name is so unappealing, so off-putting, so costly, that the fact that the company has survived with this name proves that its jelly is of really superior quality. The Smucker’s slogan embodies the handicap principle.
But what if Smucker’s Jelly were suddenly in competition with another jelly with an even worse, costlier name? Wouldn’t an even worse, more off-putting name indicate a jelly of even higher quality? What limits the possibility of ever worsening and costlier names indicative of ever higher quality jellies? The “Smucker’s Principle” reveals the logical flaw of Zahavi’s “Handicap Principle.” If the sexual benefit of a signal is directly related to its costs, the signaler will never gain an advantage, unless a small increase in cost yields a large increase in sexual benefit. Rather, handicaps will fail under their own costly burden. The “Smucker’s Principle” also reveals that the handicap principle is fundamentally incompatible with the aesthetic nature of sexual display. Sexual displays evolve because they are aesthetically attractive.
The Darwin versus Wallace debate over mate choice remains vital to science today. Unfortunately, it is not a fair fight, because the framework of modern evolutionary biology was designed to make Neo-Wallacean logic inevitable. For example, let’s examine the history of the word “fitness.” To Darwin, fitness had the ordinary language meaning of physical fitness. Fitness meant fit to do a task. Darwinian fitness was the physical capacity to do the tasks necessary to ensure one’s survival and capacity for reproduction. However, during the development of population genetics in the early twentieth century, fitness was redefined mathematically as the differential success of one’s genes in subsequent generations. This broader and more general definition combined differential survival, fecundity, and mating/fertilization success into a single new variable, under the common umbrella of adaptive natural selection. Of course, the redefinition of fitness was accomplished in the early twentieth century when sexual selection by mate choice had been rejected as irrelevant to evolution.
The effect of redefining fitness was to flatten and eliminate the original, subtle, Darwinian distinction between natural selection on traits that ensured survival and fecundity, and sexual selection on traits that resulted in differential mating and reproductive success. Ever since, this mathematically convenient but intellectually muddled new concept of fitness has shaped how people think evo-lution works, and made it difficult to even articulate the possibility of a distinct, independent, non-adaptive mech-anism of sexual selection.
To restore the promise of Darwin’s insights to contemporary evolutionary biology, we need to recognize sexual selection as a distinct mechanism of evolution, alongside the classic mechanisms of mutation, recombination, drift, and natural selection. This conceptual change will require us to realize that mate choice is not always an adaptive process, and that adaptive mate choice—whenever it occurs—requires a specific and special interaction between sexual and natural selection.
Adaptation by natural selection is justly considered to be among the most successful and influential scientific ideas in history. Because of its profound impact on science and culture despite the persistent resistance to it, the philosopher Daniel Dennett referred to natural selection as “Darwin’s Dangerous Idea.” However, Darwin’s really dangerous idea is the concept of aesthetic evolution by mate choice. Why so dangerous? Because Darwinian mate choice establishes that there are limits to the power of natural selection as an evolutionary force, and as a scientific explanation of the origin of diversity in the living world. Natural selection cannot be the only mechanism at work in evolution, Darwin reasoned, because it fails to fully account for the extraordinary diversity of sexual ornaments we see in the biological world. Darwin’s really dangerous idea is his insight that natural selection is not the only source of design in nature. We are still awaiting the full impact of this revolutionary idea on science and human culture.