Tim Birkhead

Promiscuity

Darwin’s theory of 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 ferent females. At the same time as he is less well known but no less impor- accepted male 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, 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 ” (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. .” 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

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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 . 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 , 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 . 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, and Natural Se- 1 G. Raverat, Period Piece: A Cambridge Child- lection (Princeton, N.J.: Princeton University hood (London: Faber & Faber, 1952). Press, 1966).

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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. J. Bateman, “Intrasexual Selection in Dro- and Animals,” American Naturalist 144 (1994): sophila,” Heredity 2 (1948): 349–368. S126–S149.

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Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 Tim tion simultaneously favors males that him that males must have some chance Birkhead on successfully fertilize previously insem- of fertilizing these females’ eggs–other- sex inated (but not yet fertilized) females, wise there would be no advantage to this and those males that prevent other behavior. And without an evolutionary males from inseminating or fertilizing advantage such behavior would soon females they have just inseminated. disappear. Typically what happens in dung flies is There is an important point of biolog- after a male has ½nished transferring his ical information here. First, like many sperm to a female, he remains attached other animals, female dung flies store to, but not in genital contact with, the sperm before using it to fertilize their female, in what Parker called ‘the pas- eggs. Any male that could somehow dis- sive phase’ of mating and what we now pose of, or disable, these stored sperm refer to as ‘mate guarding.’ Guarding and replace them with his own would provides time for the guarding male’s be at a huge selective advantage. sperm to fertilize at least some of the Parker tested this idea using the only female’s eggs. Other males attempt to technology then available to determine usurp the guarding male, in what Park- the paternity of a female’s offspring: he er called a ‘takeover.’ allowed females to copulate sequential- As we’ll see, selection favors males ly with two males, one of which was that successfully achieve a takeover. Se- sterilized via a dose of radiation. Strictly lection, however, also favors guarding speaking, the sterile males had function- males that prevent takeovers; that is, it al sperm, but any eggs fertilized by their favors males that protect their paternity. sperm failed to develop. As he predicted, Parker realized that these opposing se- regardless of whether the sterile male lection pressures on males would result copulated ½rst or second, the second (or in the rapid evolution of to last) male to copulate fertilized the ma- sperm competition. Mate guarding is an jority of a female’s eggs, a phenomenon adaptation, and takeover a counteradap- he called “last male sperm precedence.” tation, to sperm competition. Aristotle had noticed the same thing in These are just two of a multitude of chickens in 300 bc, and many studies adaptations and counteradaptations to conducted in the last thirty years have sperm competition that spans behavior, con½rmed it in domestic birds.7 physiology, and anatomy. Indeed, sperm Last male sperm precedence explains competition provides a good evolution- why it is always worthwhile for a male ary explanation for many previously to copulate with a previously inseminat- unexplained reproductive phenomena: ed female, and why, in Bateman’s study, huge , spiny , vast quan- male fruit flies that copulated more sired tities of sperm, toxic , excessively more offspring. prolonged or frequent copulation, and Working out how last male sperm pre- many others. cedence occurs in the yellow dung fly proved to be dif½cult. Initially, Parker This brings us to the actual mecha- assumed that incoming sperm flushes nism of sperm competition itself: how out or displaces any existing sperm in do sperm compete? As Geoff Parker no- ticed, male dung flies were always very 7 T. R. Birkhead, “Sperm Competition in keen to copulate, even with females that Birds,” Reviews of Reproduction 3 (1998): 123– were already inseminated, suggesting to 129.

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Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 the female’s storage structures, but in combination of sperm quality and quan- Promiscuity fact the process appears to be largely fe- tity. male driven. In response to new insemi- What is surprising is that there should nation, the female dung fly dumps the be any individuals at all with slow majority of previously stored sperm. sperm. If sperm competition is intense, In birds, last male sperm precedence one might expect selection for sperm occurs in a different way. Female birds velocity to be so strong that all males release sperm from their sperm-storage possess fast sperm. But it isn’t quite that structures continually over the several simple. Dominant cockerels have prefer- days they are ovulating (typically each ential access to females (who want to egg is fertilized twenty-four hours before copulate with them) and, as a result, can it is laid). If two inseminations are suf- achieve reasonable ½ciently well separated in time, most of with low-velocity sperm. Subordinate the sperm from the ½rst insemination males, on the other hand, who might have been used by the time the second only rarely get a chance to copulate, have insemination occurs, and the second (or to make the most of any opportunity last) male ‘wins’ simply by having more and tend to have high-velocity sperm. sperm in the female’s reproductive tract Amazingly, a change in social status is at the time of fertilization. followed by a corresponding change in Sperm numbers are important and ex- sperm velocity. plain why, in species where sperm com- So far we have ignored the effect of petition is intense (and females highly females on male fertilization success. promiscuous), males tend to have rel- Are females really just passive conduits atively large testicles. Larger testicles for male gametes? This was the view make more sperm per unit time, and back in the 1970s, but it has slowly be- more sperm (larger ejaculates) outcom- come apparent that females play an pete smaller ones–all else being equal. important role in the way sperm per- Across much of the animal kingdom, in- form. The change in outlook was slow cluding butterflies, birds, amphibians, because it was remarkably dif½cult to reptiles, and mammals, relative testis establish unequivocally whether females size is an excellent predictor of the in- could influence fertilization. The pro- tensity of sperm competition. cess is referred to as ‘cryptic female All else is rarely equal, however, not choice’–cryptic because it takes place least in terms of the quality of sperm. out of sight inside the female’s repro- As well as favoring large numbers of ductive tract. sperm, promiscuity also favors high- reproductive biologists ½rst quality sperm. In species where females proposed the idea as long ago as the are promiscuous, sperm need to be fast 1940s, but since it lacked evidence, the and effective. In our studies of domes- idea slipped quietly into obscurity. With tic and feral fowl, in which sperm com- the birth of , the idea petition is rife, faster-swimming sperm reemerged in the 1980s, but again was outcompete slower sperm–all else be- ignored, probably because researchers at ing equal.8 Paternity is decided by a

the Outcome of Sperm Competition in the Do- 8 T. R. Birkhead, J. G. Martinez, T. Burke, and mestic Fowl,” Proceedings of the Royal Society B: D. P. Froman, “Sperm Mobility Determines Biological Sciences 266 (1999): 1759–1764.

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Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 Tim that time were still struggling to demon- conducted paternity tests on the chicks. Birkhead on strate precopulatory female choice and If the pattern of paternity was similar sex didn’t want to be distracted by the tech- across all ten hens there would be no nically much more dif½cult question of evidence for any female effect. But, in cryptic female choice. There was anoth- fact, each time we did the experiment, er problem. Most of those interested in a small number of females showed a pat- these questions were behavioral ecolo- tern of paternity very different from that gists, ½rst and foremost ½eld biologists of the others, suggesting that those par- with little knowledge or experience of ticular females preferred the sperm of what was going on inside the female re- one male over that of the other.9 How productive tract. Eventually, however, they do this remains a mystery–but we in the 1990s they started to devise inge- suspect that they must be able to recog- nious experiments to see whether fe- nize (physiologically) proteins on the males did have any control over whose surface of the sperm that either facilitate sperm fertilized their eggs. or hamper (unconsciously, of course) The ½rst of these studies looked at the sperm’s progress through the ovi- whether females showed any preference duct. for the sperm of close relatives (broth- Because sperm competition is so in- ers) or that of nonrelatives, on the as- tense in domestic fowl (and in their wild sumption that females would want to ancestor, the red jungle fowl), females avoid . But these investiga- have additional ways to control paterni- tions were dif½cult to design and to exe- ty. Females prefer to be inseminated by cute: to be certain that a female effect the dominant cockerel. Subordinate had occurred researchers had to be ab- males, however, do not accept celibacy solutely sure they had eliminated, or lightly, and seduce females whenever controlled for, all possible male effects. the dominant male is absent. On being An example will make this clearer. Imag- approached by a subordinate male, fe- ine we were unaware of the differences males typically run away, but sometimes in sperm quality in the domestic fowl a subordinate male will capture a hen, mentioned earlier. We might inseminate holding her by the feathers on her nape. hens with a mixture comprising equal When this happens, the female shrieks numbers of sperm from two cockerels for help, uttering a distinctive distress and ½nd that one male fertilized most of call that causes the dominant male to the eggs. Super½cially it would appear intervene hurriedly. We tested the ef½- that all females ‘preferred’ the sperm of cacy of this distress call by playing re- one of the males (i.e., a female effect), cordings of it: If the dominant male when in fact it could have been due to a was within earshot, he never failed to male effect–sperm quality. respond. If, however, the dominant was My colleagues and I designed an ex- too far away, a subordinate could coerce periment to examine whether female a female into copulation and successful- fowl could discriminate between the ly inseminate her. When this occurs, the sperm of different males. We made a female has one last trick up her sleeve: sperm mixture with equal numbers of live sperm from each of two males 9 T. R. Birkhead, N. Chaline, J. D. Biggins, and then inseminated an appropriate T. A. Burke, and T. Pizzari, ”Nontransitivity amount into each of ten females. We of Paternity in a ,” Evolution 58 (2004): collected and hatched the eggs, and 416–420.

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Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 she can eject the unwanted sperm. Even the previous winter when they foraged Promiscuity before the subordinate has dismounted together in small mixed-sex flocks. By from the female’s back, she often squirts providing the ½rst clear evidence that out most of his ejaculate.10 females might bene½t from their choice of extrapair copulation partner, Susan Most of what I have discussed so far Smith’s study launched a revolution in has been concerned with the mecha- behavioral ecology. Within a short time nisms of sperm competition: how sperm other researchers were reporting females compete, how females bias paternity, of ‘their’ species looking for promiscu- and how sperm and the female repro- ous copulations, with the implication ductive tract interact. Traditionally, that doing so had an evolutionary bene- however, behavioral ecologists have fo- ½t.11 cused on questions relating to the adap- What did females stand to gain? There tive signi½cance of particular behaviors were two possibilities: direct bene½ts or anatomical traits, asking how they for themselves or indirect (genetic) ben- enhance an individual’s reproductive e½ts for their offspring. A direct bene½t success. might be food–females might trade sex The question of whether promiscuity for food. Some birds and insects, for ex- is adaptive for males seemed at one time ample, perform courtship feeding, in self-evident: more copulations meant which males present females with a pre- more offspring, as in Bateman’s fruit-fly copulatory gift of some sort. Another di- study. It was more dif½cult to show that rect bene½t might be paternal care–the this was true in nature, but the develop- females of some species trade sex for ment of molecular paternity tests during assistance in raising offspring. By ‘sex’ the mid-1980s made such ½eld studies here, I mean paternity and increased more tractable. Based on such paternity reproductive success for the extra-pair analyses, the few suf½ciently detailed male. studies that have been conducted (main- Direct bene½ts may also accrue from ly on birds) con½rm that male promiscu- sperm itself. For many insect species ity pays. It need not have done; any ben- that lay large numbers of eggs, the pos- e½ts of extrapair paternity could easily sibility of a female running out of sperm have been offset by cuckoldry. is real. To avoid this they remate and re- The one major unanswered question plenish their sperm supplies at regular is whether promiscuity is adaptive for intervals. It would be too risky to wait females. As mentioned earlier, females until all their stored sperm has been were initially ignored. But then in the used before remating, so females may mid-1980s, in a study of a small North routinely carry the sperm from different American bird, the black-capped chick- males. So, for many insects, a plentiful adee, Susan Smith noticed that females supply of sperm may be the main bene- went looking for extrapair copulations. ½t of copulating with several different Not only that, they seemed to go upmar- males. ket–seeking out males that were social- ly dominant to their partner–during 11 S. A. Smith, “Extra-Pair Copulations in Black-Capped Chickadees: The Role of the Fe- male,” Behaviour 107 (1988): 15–23; B. Kempe- 10 T. Pizzari and T. R. Birkhead, “Female Fowl naers et al., “Extra-Pair Paternity Results from Eject Sperm of Subdominant Males,” Nature, Female Preference for High Quality Males in London 405 (2000): 787–789. the Blue Tit,” Nature 357 (1992): 494–496.

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Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 Tim For most other animals, females do which males congregate to display. Fe- Birkhead on not seem to acquire any direct bene½ts males visit the lek, choose a partner, sex from being promiscuous. That leaves copulate, and then leave to rear their genetic bene½ts, but the concept of ge- offspring entirely alone. There are (ap- netic bene½ts has a number of theoreti- parently) no direct bene½ts from her cal problems. Let’s start by considering choice of male, only genetic ones, since the main potential genetic bene½ts. The all a male provides are sperm. The males ½rst possibility is that some males are of lekking species are often elaborately genetically superior (that is, they possess adorned, like birds of paradise, because genes that confer greater longevity or sexual selection is intense and a few reproductive success) compared to oth- males fertilize the majority of females. ers and females compete for them. Some A similar situation involving genetic females get to pair with superior males, bene½ts–in which females, like Susan but some have little choice but to accept Smith’s chickadees, seek extrapair cop- a mediocre or inferior male in order to ulations–also occurs among socially reproduce at all. In those cases females monogamous birds.13 can modify their initial choice of partner Here is the resolution to the lek para- by seeking extrapair copulations with a dox: if the expression of sexually select- genetically superior male. ed traits is dependent on an animal’s By doing so it is assumed that females body condition or health, as seems to will produce genetically superior sons. be the case (individuals in good condi- It has also been presumed that females tion produce bigger and better displays), identify these genetically superior males and if there are large numbers of genes from their sexually selected displays– influencing condition, then mutations large tails, flashy colors, wonderful song. in condition may arise just as quickly The theoretical snag is that if all females as they are eroded through selection by have their offspring fathered by these females. The theory relating to this reso- superior males the variation in genetic lution of the lek paradox remains to be quality would be quickly used up. An fully tested, but the results so far are en- analogy will make this clearer: if an ani- couraging. mal breeder selects for a trait such as A second possible advantage to pro- body size in cattle, the ½rst few genera- miscuity is genetic compatibility– tions will exhibit a rapid increase in size, whether your genes mesh well with but as time goes on increases in size will those of your partner. A good genetic become less and less as the genetic varia- combination results in vigorous, healthy tion in size is used up. offspring; a bad one generates genetical- A possible solution to this erosion of ly defective offspring. A clear example genetic variation and the question of in humans is the Rhesus factor (Rh): a what maintains genetic diversity in sex- Rh-negative mother and a Rh-positive ually selected traits involves a somewhat father can result in hemolytic disease convoluted but nonetheless plausible ar- in the newborn (hdn). Another almost gument. It is referred to as ‘the paradox obvious example of genetic incompati- of the lek.’12 A lek is a breeding arena in

13 A. Johnsen, V. Andersen, C. Sunding, and 12 M. Kirkpatrick and M. J. Ryan, “The Evolu- J. T. Lifjeld, “Female Bluethroats Enhance Off- tion of Mating Preferences and the Paradox of spring Immunocompetence Through Extra-Pair the Lek,” Nature 350 (1991): 33–38. Copulations,” Nature 406 (2000): 296–299.

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Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 bility is inbreeding–something Darwin, Females in the breeding season are Promiscuity whose wife Emma was his cousin, won- primed for copulating, and may–as in dered might explain the sickly natures Geoff Parker’s dung flies–½nd it easier and early deaths of some of his children. to acquiesce rather than waste a lot of The problem with the genetic-compati- time and energy avoiding male atten- bility idea, however, is that it isn’t clear tion. Even if this is true, though, there how a male would signal his compatibil- are many other species where females ity (or otherwise) to a potential partner. are overtly promiscuous and produce On the other hand, he might not have broods or litters with multiple fathers– to. If females are routinely promiscuous, and where we still have no idea why. then they could let physiological mecha- nisms in their reproductive tract sort out I want to conclude with two addition- the compatible from the incompatible al points: genuine monogamy and hu- sperm–using the ’ surface pro- mans. There appears to be a small num- teins as their guide. ber of species in which females are usu- Despite several possible genetic ben- ally faithful to their partner. e½ts to , the evidence (several species of them) provide the is far from compelling. Some published classic example. Since it is the male sea- studies–probably a biased subset–pro- horse that cares for the eggs inside his vide support for the idea of genetic ben- brood pouch (transferred there by an e½ts, but many studies fail to detect any egg tube from the female), and since effect at all. To date, we simply do not the eggs are fertilized as they go into the know why the females of many species brood pouch (or inside it), the opportu- apparently seek copulations with ad- nity for another male to introduce his ditional males. There is an interesting sperm is extremely limited. The one sea- twist to this: Susan Smith’s study horse-paternity study con½rms that all launched a new wave of research that the offspring in a single brood have but showed that female birds in particular a single father. As predicted, male sea- sought extra copulation partners. As horses also have very small testes–so often occurs in science, enthusiasm for small, in fact, that they are extremely this particular idea probably led to a dif½cult to ½nd. With no sperm compe- publication bias, overemphasizing how tition and complete control over where active females were in initiating promis- their sperm go, males can afford to have cuous matings. With hindsight, it now tiny testes producing a small number seems that the evidence for female ini- of sperm. A rather different form of mo- tiative is limited.14 nogamy occurs in Hamadryas baboons: Where does that leave us? With birds, males are much larger than females and which is what I know most about, I won- ferociously bully females into ½delity. der whether, in those species that typi- Among birds, there is a handful of spe- cally have around 10 to 15 percent extra- cies, including the mute swan, where no pair paternity, extrapair paternity may extrapair paternity has been detected, simply be accidental and not adaptive. but the reasons for this are currently un- known. 14 D. F. Westneat and I. R. K. Stewart, “Extra- Finally, what about sperm competition Pair Paternity in Birds: Causes, Correlates and and cryptic female choice in humans? Conflict,” Annual Review of Ecology and Systemat- As one might expect, this is a topic close ics 34 (2003): 365–396. to the hearts of researchers and nonre-

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Downloaded from http://www.mitpressjournals.org/doi/pdfplus/10.1162/daed.2007.136.2.13 by guest on 01 October 2021 Tim searchers alike, and while there has been tellectual pathway. The nuts and bolts Birkhead on a great deal of speculation there is very of reproduction were still poorly known sex little hard evidence. Obviously, some fe- at that time, which may have made it males are promiscuous, but the impor- dif½cult to imagine postcopulatory sex- tant question is whether female promis- ual selection. On the other hand Dar- cuity is adaptive or suf½ciently frequent win was no prude–he joked about the to result in the evolution of speci½c ad- barnacle’s enormous in a book aptations. While the level of extrapair he knew the public (and his wife and paternity might be a useful measure of daughter) wouldn’t read. My guess is promiscuity in birds and a good starting that he would say the same thing Thom- point for thinking about the evolution of as Henry Huxley did on having natural promiscuity, equivalent data for human selection explained to him: why didn’t societies are, I believe, much less inform- I think of that? ative. Cultural circumstances have so dramatically changed human sex lives that it is dif½cult to infer anything from contemporary data. The best indication of our inclination toward promiscuity is relative testis size. Compared with other primates, human testes are neither as large as those of the highly promiscuous , nor as small as those of the monogamous goril- la, suggesting that humans have evolved to cope with only a moderate degree of female promiscuity. Other morphologi- cal features further suggest that human males are poorly adapted to sperm com- petition: the rate of sperm production is relatively low, and ejaculate quality is abysmal, with many dead or deformed sperm. On the other hand, we do have a long penis for our body size (an indica- tor of sperm competition in some other animal groups–longer is better for plac- ing sperm closer to the eggs). Evolution- ary psychologists are also persuaded of the ubiquity of sperm competition by our powerful sexual jealousy and obses- sion with paternity, but, despite this, my overall impression is that sperm compe- tition in humans has always been rela- tively modest. What would Darwin have made of all this? Despite knowing, but not writing, about female promiscuity, Darwin never allowed himself to venture down this in-

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