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Book Spring 2007:Book Winter 2007.Qxd.Qxd Tim Birkhead Promiscuity Darwin’s theory of natural selection miscuity–the fact that, in many ani- is so widely known it is almost a cliché, mals, males achieve high reproductive despite continually being misunder- success by copulating with several dif- stood. His concept of sexual selection ferent females. At the same time as he is less well known but no less impor- accepted male promiscuity as the norm tant. Darwin developed the idea of sex- and as an important component of sex- ual selection to account for the dramat- ual selection, Darwin regarded females ic differences that often exist in the ap- as sexually monogamous and faithful to pearance and behavior of the sexes. The a partner for at least a single breeding reason for these differences, he said, attempt. By doing so he automatically was competition for, or choice of, sex- assumed that sexual selection ceased ual partners. Typically, males compete once an individual of either sex had ac- among themselves for females, hence quired a mating partner. their larger body size and their weapons, But Darwin knew it wasn’t true that such as antlers and spurs. Females, on females were sexually monogamous, for the other hand, typically choose among in his various writings he referred to in- males on the basis of the males’ elabo- stances in which females had received rate coloration, extravagant ornaments, sperm from more than one male. For ex- or remarkable vocal repertoires. ample, in The Descent of Man, and Selec- One integral aspect of Darwin’s con- tion in Relation to Sex (1871), Darwin refers cept of sexual selection was male pro- to a case his cousin William Darwin Fox recounted to him, of a female domestic Tim Birkhead is professor of behavior and ecolo- goose that copulated with both a male gy at the University of Shef½eld and a Fellow of domestic goose and a Chinese goose and the Royal Society of London. His books include hatched a brood of very obvious mixed “Promiscuity: An Evolutionary History of Sperm paternity. Despite such clear evidence Competition and Sexual Conflict” (2000) and to the contrary, though, Charles Darwin “The Red Canary” (2003). He is currently writ- stuck ½rmly to the story of female mo- ing a history of ornithology: “The Wisdom of nogamy. Birds.” There are several reasons for this. First, although it was perfectly respect- © 2007 by the American Academy of Arts able to discuss sexuality, fertilization, & Sciences and promiscuity among plants, it was Dædalus Spring 2007 13 Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 Tim less appropriate for a Victorian gentle- Geoff Parker, then a Ph.D. student, Birkhead man to discuss the sexual habits of fe- studied the mating behavior of yellow on sex male animals, including humans. Sec- dung flies in the meadows around Bris- ond, Darwin’s grandfather, Erasmus tol, England. He watched as male after Darwin, had been enthusiastic about re- male copulated with the same female production, advocating sex for his hypo- in what he recognized might be a ½erce chondriac female patients and himself competition for paternity. Parker re- siring several illegitimate offspring. At ferred to this phenomenon as sperm exactly the time Charles was writing De- competition: the competition between scent another illegitimate descendent of the sperm (or more correctly, the ejacu- Erasmus had been discovered–hardly lates) of different males to fertilize the an opportune time to be discussing pro- eggs of a single female. Female dung miscuity. Third, and most important, flies appeared to be passive or indiffer- Charles did not want to offend the wom- ent, and because males were consider- enfolk in his life, especially his wife Em- ably larger and able to impose them- ma and daughter Henrietta. Etty, as she selves on the females, there was no sug- was known, helped proofread and check gestion of female choice. At Harvard, her father’s writings but also acted as another graduate student, Bob Trivers, his censor, striking out anything she observed the pigeons on his of½ce win- didn’t approve of with her blue crayon. dow ledge as they went to roost, and She did precisely that to Charles’s brief was fascinated by the males’ attempts biography of Erasmus Darwin–delet- to position themselves between their ing the reference to Charles’s grandfa- partner and any other male. Once con- ther’s “ardent love of women.” We get sidered models of monogamy, pigeons a further feel for what Charles was up were–as Trivers noticed–exactly the against when we discover that, in later opposite, with both sexes perpetually life, Etty tried single-handedly to remove on the lookout for extrapair liaisons. the eponymous fungus Phallus impudicus In 1970 Parker produced a citation from the British countryside because she classic with his paper “Sperm Competi- thought it might have a bad influence on tion and its Evolutionary Consequences the maids.1 in the Insects,” and in 1972 Trivers did By stating that females were sexually the same with his paper “Parental In- monogamous, Charles Darwin preclud- vestment and Sexual Selection.”2 The ed the possibility that sexual selection revolution in evolutionary thinking might continue after copulation. For a that Williams had initiated in the mid- hundred years after Descent, sexual se- 1960s3 took as its main premise the idea lection was thought to cease at mating. Then, in the late 1960s, as the sel½sh 2 G. A. Parker, “Sperm Competition and its gene was just beginning to raise its rev- Evolutionary Consequences in the Insects,” olutionary head, due largely to the work Biological Reviews 45 (1970): 525–567; R. L. of George C. Williams, two young re- Trivers, “Parental Investment and Sexual Se- searchers, one on each side of the Atlan- lection,” in Sexual Selection and the Descent of tic, changed our view of reproduction Man 1871–1971, ed. B. Campbell (Chicago: forever. Aldine-Atherton, 1972), 136–179. 3 G. C. Williams, Adaptation and Natural Se- 1 G. Raverat, Period Piece: A Cambridge Child- lection (Princeton, N.J.: Princeton University hood (London: Faber & Faber, 1952). Press, 1966). 14 Dædalus Spring 2007 Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 that individuals (rather than popula- But Trivers deliberately neglected Promiscuity tions or species, as had previously been part of Bateman’s results. Because of assumed) were the target in both natural a glitch in the experiment, some of the and sexual selection. A natural develop- flies had received a different diet, so ment of this evolutionary viewpoint was Bateman had kept the two sets of re- that individuals of either sex had evolved sults separate. Trivers reported only the to maximize their own reproductive suc- results from one set, ignoring the other, cess, even at the expense of members of which showed that females that copulat- their species and even their mating part- ed with more than one male did produce ners. more offspring. The bene½ts of promis- Initially, the focus of research was on cuity were fewer for females than they males, and on sperm competition. Much were for males, but they existed none- has been made of this, especially by fem- theless. But since these results didn’t ½t inists. Undoubtedly there was some in- with Trivers’s preconceived ideas, he tellectual chauvinism, but the reality was disregarded them.6 that male behavior, so often lacking in Had he publicized them, the study of sophistication, was much easier to study. female aspects of reproduction might To Parker, female dung flies appeared have occurred much sooner than it did. merely indifferent to their multiple cop- However, they might also have done ex- ulation partners. Trivers was more obvi- actly the opposite and merely clouded ously sexist and unashamedly told me the issue. Instead, for twenty years fol- that that was how most people (men) lowing Trivers’s paper, researchers fo- thought at that time. cused on male aspects of what we now The clearest evidence for Trivers’s call postcopulatory sexual selection, and chauvinism came from his interpreta- started to consider female aspects only tion of a study that formed the basis of once those male-driven processes were his classic 1972 paper.4 In 1948 Angus reasonably well understood. Bateman published an important study of sexual selection in fruit flies.5 Ignored Geoff Parker recognized that, by as- by almost everyone, Bateman’s paper suming sexual selection ceased at the was noticed by the evolutionary vision- point of copulation, Darwin had missed ary Ernst Mayr, who pushed it in Triv- the immense evolutionary potential of ers’s direction. Bateman had measured sperm competition. If females were in- the reproductive bene½t of each sex cop- seminated by more than one male, he ulating with multiple partners. The way surmised, then sperm from those males Trivers portrayed Bateman’s results was would compete to fertilize a female’s that the more females males copulated eggs–and the males that ‘won’ the com- with, the more offspring they fathered; petition would leave more descendants but for females it made no difference and would pass on their genes for those how many partners they had–after their traits that made them successful. ½rst insemination their reproductive In fact, it is more complex than this. success remained unchanged. When sperm competition occurs, selec- 4 R. Trivers, Natural Selection and Social Theory (Oxford: Oxford University Press, 2002). 6 S. J. Arnold, “Bateman’s Principles and the Measurement of Sexual Selection in Plants 5 A.
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