The Fisher King

It was several decades later that the novelty of breeding mutated fruit flies wore off, and some biologists rediscovered Darwin's ideas. One of these young thinkers was Ronald Fisher, whose career spanned the first half of the 20th century. Fisher was a polymath whose insights shaped many fields. To biologists, he was an architect of the "modern synthesis" that used mathematical models to integrate Mendelian genetics with Darwin's selection theories. To psychologists, Fisher was the inventor of various statistical tests that are still supposed to be used whenever possible in psychology journals. To farmers, Fisher was the founder of experimental agricultural research, saving millions from starvation through rational crop breeding programs. In each case, Fisher brought his powerful mathematical brain to bear on questions that had previously been formulated only vaguely and verbally.

Fisher considered Darwin's theory of mate choice to be one vague idea worth trying to formalize. In his first paper on sexual choice in 1915, Fisher enthused that "Of all the branches of biological science to which Charles Darwin's life-work has given us the key, few if any, are as attractive as the subject of sexual selection." Fisher understood that to make sexual selection scientifically respectable, he had to explain the origins of sexual preferences. In particular, Darwin failed to offer any explanation for female choice. Why should females bother to select male mates for their ornaments? Fisher's breakthrough was to view sexual preferences themselves as legitimate biological traits that can vary, that can be inherited, and that can evolve. In his 1915 paper he faced the problem squarely: "The question must be answered 'Why have the females this taste? Of what use is it to the species that they should select this seemingly useless ornament?'" Later, in a 1930 book, Fisher emphasized that "the tastes of organisms, like their organs and faculties, must be regarded as the product of evolutionary change, governed by the relative advantages which such tastes confer." While Darwin had left sexual preferences as mysterious causes of sexual selection, Fisher asked how sexual preferences themselves evolved.

In thinking about the evolution of sexual preferences, Fisher developed the two major themes of modern sexual selection theory. The first idea is the more intuitive, and concerns the information conveyed by sexual ornaments. In the 1915 paper, Fisher speculated thus:

Consider, then, what happens when a clearly marked pattern of bright feathers affords ... a fairly good index of natural superiority. A tendency to select those suitors in which the feature is best developed is then a profitable instinct for the female bird, and the taste for this "point" becomes firmly established ... Let us suppose that the feature in question is in itself valueless, and only derives its importance from being associated with the general vigor and fitness of which it affords a rough index.

Fisher proposed that many sexual ornaments evolved as indicators of fitness, health, and energy. Suppose that healthier males have brighter plumage. Females may produce more and healthier offspring if they mate with healthier males. If they happen to have a sexual preference for bright plumage, their offspring will automatically inherit better health from their highly fit fathers. Over time, the sexual preference for bright plumage would become more common because it brings reproductive benefits. Then, even if bright male plumage is useless in all other respects, it will become more common among males simply because females prefer it. Fisher understood that preferences for fitness indicators could hasten the effect of natural selection, and could potentially affect both sexes. Unfortunately, Fisher's fitness-indicator idea was forgotten until the 1960s.

Fisher's other idea, the concept of runaway sexual selection, attracted more interest because it sounded much stranger. In fact, it was so strange that Thomas Hunt Morgan had first aired the idea in 1903 as a counter argument against sexual selection. Morgan asked what would happen if female birds had a tendency to prefer plumage slightly brighter man the males of their species currently possess. He realized that the males would evolve brighter plumage under the pressure of female choice, but that the females would still not be satisfied. They would just move the goal posts, demanding still more extreme ornamentation. Morgan mocked, "Shall we assume that . . . the two continue heaping up the ornaments on one side and the appreciation of these ornaments on the other? No doubt an interesting fiction could be built up along these lines, but would anyone believe it, and, if he did, could he prove it?" To Morgan, the possibility of an endless arms rate between female preferences and male ornaments was an evolutionary impossibility that exposed the whole idea of sexual selection as a fallacy. But Fisher was used to integrating equations for exponential growth, and understood the speed and power of positive-feedback processes. He realized that an arms race between female preferences and male ornaments, far from undermining the theory of sexual selection, could offer an exciting possibility for explaining sexual ornamentation.

The idea of runaway sexual selection appeared in Fisher's masterpiece of 1930, The Genetical Theory of Natural Selection. Whenever attractive males can mate with many females and leave many offspring, the sexual preferences of females can drive male ornaments to extremes. Fisher suggested that when this happens, female preferences will evolve to greater extremes as well. This is because a female who prefers a super-ornamented male will tend to produce super-ornamented sons, who will be super-attractive to other females, and who will therefore produce more grandchildren. Evolution will favor super-choosy females for this reason. Yet the choosier the females become, the more extreme the male ornamentation will become in response. Both sexes end up on an evolutionary treadmill. The female preferences and male ornaments become caught up in a self-reinforcing cycle, a positive-feedback loop.

Fisher speculated that whenever the most ornamented individuals gain a large reproductive advantage, there is "the potentiality of a runaway process, which, however small the beginnings from which it arose, must, unless checked, produce great effects, and in the later stages with great rapidity." This runaway process, Fisher claimed, could make ornaments evolve with exponentially increasing speed. They would evolve until the ornaments become so cumbersome that their massive survival costs finally outweigh their enormous sexual benefits: "both the feature preferred and the intensity of preference will be augmented together with ever-increasing velocity, causing a great and rapid evolution of certain conspicuous characteristics, until the process can be arrested by the direct or indirect effects of Natural Selection." I shall explore the runaway process more thoroughly in the next chapter.

Like many mathematical geniuses presenting startling ideas, Fisher thought that runaway sexual selection was so obviously plausible that he did not need to present a detailed proof that it could work. He left that as an exercise for the reader. However, most mathematically talented scientists of the 1930s probably took up the challenge of quantum physics rather than evolutionary biology, and of those who went into biology, nobody took up Fisher's challenge.

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