Book Reviews - Spring 2009

The Peacock Problem

Does sexual selection really explain enough?

By Priscilla Long | March 1, 2009

The Genial Gene: Deconstructing Darwinian Selfishness, by Joan Roughgarden, University of California Press, 256 pp., $24.95

In The Genial Gene, Joan Roughgarden does not challenge Darwin’s theory of evolution or its explanation for how species evolve mainly through natural selection. In­stead she opposes “sexual selection,” the standard explanation (frequently stated simply as fact, as in, the earth is round) for the me­ch­­anism through which natural selection works. Roughgarden points to an impressive catalog of biological studies of particular species that show, for the case under consideration, that the facts do not support the ideas of sexual selection. In her words, “Continuously widening sexual-selection theory converts it into a system that becomes increasingly hard to test and possibly easier to falsify, and so sexual selection slowly morphs from a scientific theory into a doctrine or ideology.” She proposes that we discard sexual-selection theory, and she exhaustively details an alternative hypothesis—“social selection”—which, she insists, nevertheless falls firmly under the umbrella of evolutionary biology.

You don’t have to be a scientist to know—in the year marking Darwin’s 200th birthday and the 150th anniversary of his On the Origin of Species by Means of Natural Selection (1859)—that natural selection is nature’s breeding program. Creatures possessing characteristics best suited to survive and reproduce within their particular pond or wood will tend to pass these characteristics on to their offspring. Through the generations, genes mutate and environments change. Mutations that improve chances for survival and reproduction within the given environment tend to multiply through successive generations, whereas mutations that make survival and reproduction more difficult tend to die out along with the creatures that carry them. The tricky part is that the environment is locally in a state of flux (and sustains an occasional worldwide wallop, as in the extraterrestrial hit that wiped out the din­osaurs 65 million years ago). A good gene this year might hit the wall next year. Nevertheless, natural selection is the chief way life on earth evolved into its diverse zillions of species.

Sexual selection proposes the mechanism for how this works: it holds that, in nature, drab and coy females choose highly ornamented or well-armored males in order to improve the genes of their offspring. (Darwin himself, of course, worked before genes were discovered.) The drab peahen chooses the peacock with the most dazzling train because the dazzling train advertises dazzling genes and these, combined with her own, will best enable her genes to spread into future generations.

The sexual-selection “narrative,” as Roughgarden calls it, contains the idea that males tend to promiscuity and females to monogamy in order for each sex to maximally perpetuate his or her genes. Roughgarden quotes geneticist Jerry Coyne, who wrote (in a review of Roughgarden’s previous book): “Males, who can produce many offspring with only minimal investment, spread their genes most effectively by mating promiscuously. . . . Female reproductive output is far more constrained by the metabolic costs of producing eggs or offspring, and thus a female’s interests are served more by mate quality than by mate quantity.” (Mate quality meaning, Roughgarden explicates, genetic quality.)

The English philosopher Herbert Spencer, not Darwin, politicized natural selection by coining the phrase “survival of the fittest” a few years after Darwin published On the Origin of Species, and Roughgarden terms the philosophy of sexual selection neo-Spencerism rather than neo-Darwinism. (Actually all sides in this debate can easily claim Darwin.) Roughgarden writes, “This book invites debate about whether Spencer and his ideological descendants today correctly describe and explain biological nature. This book focuses on the scientific accuracy of claims that evolution rests on competition, selfishness, and conflict.”

She counterposes her “genial gene” hypothesis to sexual-selection proponent Richard Dawkins’s “selfish gene.” His book The Selfish Gene, published in 1976, puts forth the grim view that “we are survival machines—robot vehicles blindly programmed to preserve the selfish molecules known as genes.” In his 2003 book, A Devil’s Chaplain, Dawkins continues, “Blindness to suffering is an inherent consequence of natural selection.” As Dawkins’s rhetoric illustrates, sexual selection has enormous social and philosophical implications, holding that selfishness, competition, stereotypical sex roles, rape, war, family fights, feuds among scientists, and so forth, are based in biology—they are natural.

In The Genial Gene, Roughgarden repeatedly states that if sexual selection is true, then the consequent conflict, competition, and cruelty, even if repugnant (to some), are natural. So be it. Nothing to be done. But, Roughgarden says, sexual selection is not true.

Take the peacock. A seven-year study of feral Indian peahens and peacocks in Japan [by Mariko Takahashi et al.] titled “Peahens Do Not Prefer Peacocks with More Elaborate Trains” notes that these peahens disregard plumage in making their mating choices. The study further observes that variations in male plumage do not reflect anything in particular about the male’s physiological condition. Most strikingly, this 2008 study finds that a high level of female hormones dulls a bird’s coloration, suggesting there has been selection on females with dull plumage. These scientists propose that both sexes started brightly colored. Females evolved dull coloration, which increases survival chances for this ground-nesting bird, since there is little male involvement in parenting and since the female is vulnerable to predation while incubating eggs on the ground. (The scientists also reviewed the literature on peacocks, found it contradictory in terms of supporting or refuting sexual-selection theory except in the sexual-selection field, and suggested that researchers take care to publish negative as well as positive results.)

Sexual selection intends to explain sexual dimorphism (different forms within a species for male and female, usually the duller, smaller female and the brighter, bigger male). But, Roughgarden asks, what of species in which only the careful inspection of genitals reveals the sex of the animal? (Guinea pigs, penguins.) What of species in which it is the male that is drab and the female that is brightly ornamented? (Sea horses, pipefish, some birds.)

Sexual selection also intends to explain female reticence and male promiscuity. In 1948 the English geneticist Angus Bateman published a study that, according to Roughgarden, “has long been regarded as experimentally confirming Darwin’s theory of sexual selection.” Bateman’s widely cited study found male fruit flies (D. melanogaster) to be possessed of “undiscriminating eagerness” in their sexual relations with the ladies and female flies to have “discriminating passivity” in their relations with their rogue gentlemen. Roughgarden devotes several pages to recent critiques of Bateman’s data, and to his followers’ use of his data, and suggests that Bateman’s conclusions are suspect and discredited. Bateman’s work is one of the pieces of this complex debate that will surely have to be reviewed—whether for defense, deconstruction, or some of each.

Also on the eagerness versus reticence question, Roughgarden asks, what of species in which the females aggressively solicit the coy males for mating? (Alpine accentors, a small bird of the Pyrenees.) What of species in which different males have different roles to play, what Roughgarden calls “template multiplicity”? (Among Euro­­pean ruffs—a sandpiper—black-collared males defend small territories called courts within a communal display area called a lek, while white-collared males accompany the females on feeding expeditions. Then the white-collared males return to the communal display area where black-collared males solicit them to join and become a pair of males within a court. Upon their return to the lek, females prefer mating with a pair of males, one black-collared and one white-collared.)

What of species in which some of the males are dull colored like the females (including a third subgroup of the above-mentioned male ruffs) and some of the females are bright colored like the males? (The South American sunangel hummingbird.) What of homosexual relations, observed in some 300 species of vertebrates? (Perhaps, Roughgarden suggests, fertilizing eggs is not the sole function of sexuality. Perhaps it is to “sustain bonds between animals, bonds comprising the social system within which offspring are reared.”)

Proponents of sexual selection explain kindness and altruistic behaviors as motivated by selfishness—by the creature’s drive to perpetuate its own genes. In kin selection, an animal spreads its own genes into the next generation by helping a close relative. In reciprocal altruism, one animal assists another in expectation of a return assist.

Kin selection is illustrated by bees, wasps, ants, and termites where worker insects have a close genetic relationship to the queen and thus can perpetuate their own genes most efficaciously by assisting Her Majesty. This, Roughgarden states, is certainly true in some cases. The problem for sexual-selection theory is that in some species of social insects, some workers serving the queen are not related to her. One such species is the red wood ant of a supercolony on Hokkaido (Japan) with more than a million queens and 306 million workers living in 45,000 interconnected nests with “often unrelated multiple queens and cohorts of workers with differing parentage.” Kin selection, Roughgarden asserts, “is not incorrect, merely inadequate.”

Reciprocal altruism is illustrated by two robins building a nest together. Sexual-selection theory sees this as “I help you, You help me.” In this view males and females have different interests. The social-selection hypothesis sees it as teamwork: two birds working together toward a common goal. The nest results from the relationship developed by the male and female during courtship. In a disquisition on birds too elaborate to summarize here, Roughgarden attributes intrafamilial squabbling to disagreements that occur later over such things as the division of labor.

For sexual-selection theory there is also the problem of species in which individuals are poorly defined, such as fungi whose bodies can intermingle in strange (to me) ways so that where Millicent ends and Milton begins is an open question. Or take a grove of poplar trees where many trunks arise from one seed; or the Portuguese man-o-war jellyfish, in which separate polyps clump together and “float around together like a spaceship in the ocean.” In the man-o-war jellyfish clump, it’s all for one and one for all. Survival of the fittest means survival of the fittest clump, which then accrues to the benefit of each card-carrying clump member. Sexual-selection proponents, Roughgarden says, generally omit discussion of such species.

Roughgarden spends roughly half her book scrutinizing and questioning sexual-selection theory, point by point, species by species. She devotes most of the second half to building a hypothesis of social selection, with its central idea that members of species relate in order to create a stable infrastructure for raising offspring to reproductive age, a focus that differs considerably from the sexual-selection focus on mating alone.

In consideration of whether “successful gene” means the same thing as “selfish gene,” Roughgarden writes, “To stipulate that evolutionary success equals selfishness means we can’t ask the question of which, cooperation or competition, is the more common route to evolutionary success.” The Genial Gene is crawling with species illustrations, detailed accounts of studies, and arguments critical of supposed evidence for sexual selection. Its social-selection hypothesis, which doesn’t deny competition and conflict but gives it a more peripheral role in natural selection, is built point by point through chapters on the gene, the cell, the body, behavior, evolution, and a detailed chapter on family cooperation and conflict among birds. Many of the ideas are tentative: social selection will have to be tested and retested, with negative results published along with the positive.

This debate has already produced sparks and minor explosions based on Roughgarden’s previous work and that of others. The Genial Gene cannot but escalate the fireworks. The arguments and counterarguments will most certainly generate a good deal of heat, but also, let’s hope, in Darwin’s honor, even more light.

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