Animal Behaviour 77 (2009) 3–11

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Animal Behaviour

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Reviews Sexual selection in females

Tim Clutton-Brock*

Department of Zoology, University of Cambridge article info Darwin developed the theory of sexual selection to account for the evolution of weaponry, ornamen- Article history: tation and other secondary sexual characters that are commonly more developed in males and which Received 28 April 2008 appeared unlikely to contribute to survival. He argued that these traits had evolved either through Initial acceptance 25 May 2008 intrasexual competition between males to monopolize access to females or through consistent female Final acceptance 27 August 2008 preferences for mating with superior partners. Since 1871, a substantial body of research has confirmed Published online 31 October 2008 his explanation of the evolution of secondary sexual characters in males, although sex differences in MS. number: 08-00267 reproductive behaviour are more diverse and the evolutionary mechanisms responsible for them are more complex than was initially recognized. However, secondary sexual characters are also widespread Keywords: in females but, as yet, their evolution and distribution have received relatively little attention from gender differences evolutionary biologists. Here, I suggest that the mechanisms responsible for the evolution of secondary intrasexual competition sexual characters in females are similar to those operating in males and include intrasexual competition mate choice sex roles between females for breeding opportunities, male mating preferences and female competition to attract sexual selection mates. Unlike males, females often compete more intensely for resources necessary for successful reproduction than for access to mating partners and the development of secondary sexual characters in females may be limited by costs to fecundity rather than to survival. Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

In many animals, males develop elaborate weapons or orna- In the The Descent of Man Darwin (1871/1958) adopted Hunter’s ments and become increasingly aggressive as they reach sexual distinction between primary and secondary sexual differences with maturity. Over 90 years before the publication of the The Descent of an important difference. Instead of using secondary to refer to Man (Darwin 1871/1958), these ‘secondary’ marks or characters of sexually dimorphic traits that develop some time after hatching or sex were a focus of the attention of the anatomist John Hunter birth, Darwin drew a functional distinction: his primary sexual (1780,1837) who distinguished them from the sex organs, which he characters were those connected with the act of reproduction itself, identified as the ‘primary’ characters of males and females. Hunter while his secondary sexual characters were used in intrasexual realized that the development of secondary sexual characters was competition to breed. He termed the evolutionary process gener- related to ecological differences between species. ating them ‘sexual selection’, describing it as selection that ‘depends on the advantage which certain individuals have over The males of almost every class of animals are probably disposed to others of the same sex and species solely in respect of reproduction’ fight, being, as I have observed, stronger than the females; and in (Darwin 1871/1958, page 209). He emphasized the central impor- many of these are parts destined solely for that purpose, as the tance of intrasexual competition in the evolution of secondary spurs of the cock, and the horns of the bull. One of the most sexual characters and described how sexual selection can take two general marks [of sex] is the superior strength of make in the male; distinct forms (Darwin 1871/1958, page 614): ‘sexual selection and another circumstance, perhaps equally so, is this strength depends on the success of certain individuals over others of the being directed to one part more than another, which part is that same sex, in relation to the propagation of the species . . The most immediately employed in fighting. This difference in external sexual struggle is of two kinds; in the one it is between individuals form is more particularly remarkable in the animals whose females of the same sex, generally the males, in order to drive away or kill are of a peaceable nature, as are the greatest number of those their rivals, the females remaining passive; whilst in the other, the which feed on vegetables, and the marks to discriminate the sexes struggle is likewise between individuals of the same sex, in order to are in them very numerous. excite or charm those of the opposite sex, generally the females, (Hunter 1837, page 45) which no longer remain passive, but select the more agreeable partners’. Subsequent developments of Darwin’s theory explained why * Correspondence: T. Clutton-Brock, Department of Zoology, University of Cam- bridge, Downing Street, Cambridge CB2 3EJ, U.K. intrasexual competition and secondary sexual characters are often E-mail address: [email protected] more highly developed in males. Building on empirical studies of

0003-3472/$38.00 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.08.026 4 T. Clutton-Brock / Animal Behaviour 77 (2009) 3–11

Drosophila by Bateman (1948); Trivers (1972) argued that it is the Carey 2001; O’Connor et al. 2002; Sherman & Jarvis 2002; Damman relative expenditure by males and females on gametes plus & Burda 2005). As a result, individual differences in breeding parental care (‘parental investment’) that determines the relative success and the degree of reproductive skew among females can be intensity of competition for breeding partners in the two sexes. Sex unusually large and can exceed the variance in breeding success differences in parental investment affect the time necessary to among males (Hauber & Lacey 2005; Clutton-Brock et al. 2006; complete a successful breeding attempt, which limits the potential Clutton-Brock 2007). Since only a small proportion of females can rate at which males and females can process partners of the breed as dominants, competition for social status can be intense opposite sex (potential reproductive rate; Clutton-Brock & Parker and contests between females can be lethal. 1992; Ahnesjo et al. 2001) and leads to biases in the operational sex Females also commonly compete for access to mates. Female ratio (OSR: the ratio of males and females ready to breed at competition for mates is widespread in polyandrous birds where a particular time; Emlen & Oring 1977; Simmons 1995). OSRs are biased towards females (Emlen & Oring 1977; Oring et al. While secondary sexual characters are usually more highly 1991a, b) as well as in some insects where males produce unusually developed in males than females, females show some development large sperm (Lorch 2002; Bjork & Pitnick 2006) and some mammals of secondary sexual characters (including weaponry, brightly col- where the sperm supplies are depleted by frequent mating oured plumage or pelage and elaborate ornaments) in a substantial (Dewsbury 1982, 2005). Female competition for mating access also number of animals (Andersson 1994; Kraaijeveld et al. 2007). In occurs in species where OSRs are male biased but individual some species, they possess secondary sexual characters that are differences in their ability to invest in offspring or in the number of absent in males and, in a few, they show greater development of eggs or offspring they can care for are large. For example, in the traits that are present in both sexes (Clutton-Brock 2007). The monogamous seahorse, Hippocampus subelongatus, where males presence of secondary sexual characters in females raises impor- brood eggs and adult sex ratios are often biased towards females, tant questions about the evolutionary mechanisms responsible for female competition is common and body size appears to exert them and for their distribution (Isaac 2005; Clutton-Brock 2007; a stronger influence on breeding success in females than in males Kraaijeveld et al. 2007). Although Darwin (1871/1958) was aware of (Kvarnemo et al. 2007). In addition, female competition for mates is the presence of secondary sexual characters in females, he was common where females gain direct or indirect benefits from primarily concerned with explaining the evolution of secondary mating with multiple partners in the course of a single breeding sexual characters in males, noting in passing (page 614), that: ‘in cycle (Tregenza & Wedell 1998; Fisher et al. 2006). Finally, female almost every great class, a few anomalous cases occur, where there competition for mating access is likely to occur when individual has been an almost complete transposition of the characters proper differences in the direct or indirect benefits that males can offer as to the two sexes; the females assuming characters which properly mating partners are large and the most preferred male(s) cannot belong to the males’. Almost all subsequent reviews have main- service all receptive partners (Gowaty 2004; Bro-Jørgensen 2007). tained the same bias (Huxley 1938, 1942; Ghiselin 1974; Andersson In many species, sex roles are flexible and the relative frequency 1994). In this paper, I attempt to redress the balance by reviewing of intrasexual competition in the two sexes varies between stages our existing knowledge of the development and distribution of of the reproductive cycle (Gowaty 2004; Gowaty & Hubbell 2005). secondary sexual characters in females. I first examine the For example, in two-spotted gobies, Gobisculus flavescens, the processes leading to the evolution of secondary sexual characters in relative intensity of intrasexual competition for mating partners in females, then describe their distribution across species with con- the two sexes varies throughout the breeding cycle as the relative trasting breeding systems, and finally I compare the operation of numbers of receptive females and males change (Amundsen & sexual selection in the two sexes. Forsgren 2001; Forsgren et al. 2004). Similarly, in some ungulates where OSRs are generally male biased and males compete intensely REPRODUCTIVE COMPETITION BETWEEN FEMALES for access to females, females that are close to oestrus and need to mate rapidly compete for access to breeding males (Bebie & Both of the forms of sexual selection described by Darwin (see McElligott 2006; Bro-Jørgensen 2007). In bush crickets, Tettigo- above) occur in females as well as males. In a substantial number of niidae, where males bring nuptial gifts to receptive females, animals, females compete between themselves for access to manipulation of food availability to males changes the OSR and breeding territories or other resources necessary for conception or affects the relative frequency of competition for mates in males and rearing offspring (Floody 1983; Heinsohn & Legge 2003; Emlen & females (Simmons & Gwynne 1993; Simmons 1995; Kvarnemo & Wrege 2004; Andersson 2004, 2005). In group-living species where Simmons 1999). several mature females breed each year, females commonly The phenotypic characters that affect the ability of females to compete for social rank, which is often related to their ability to acquire breeding opportunities, high status or mates are often produce or rear offspring (insects: Reeve 1991; birds: Vehrencamp similar to those that affect the acquisition of mating opportunities 1977; Bertram 1992; primates: Fedigan 1983; Silk 1997; ungulates: by males in polygynous species. They include the individual’s age, Clutton-Brock et al. 1982; carnivores: Holekamp & Smale 2000; weight and hormonal status, as well as the rank of her mother Clutton-Brock et al. 2001; Hofer & East 2003; Hodge et al. 2008). In (insects: Reeve 1991; Reeve & Ratnieks 1993; primates: Walters & some cooperative breeders, one dominant female in each group Seyfarth 1986; Silk 1987; carnivores: Holekamp et al. 1996; Engh usually prevents most (and, in some cases, all) other females from et al. 2000; Holekamp & Smale 2000; Clutton-Brock et al. 2006). breeding by a combination of physiological suppression (marmo- The identity of alliances and coalition partners may also be sets: French 1997; mole-rats: Faulkes & Abbott 1997; meerkats: important in species where related females support each other in Clutton-Brock et al. 2001) and infanticide (meerkats: Clutton-Brock competition with members of other matrilines for rank or access to et al. 1998; Young & Clutton-Brock 2006; wild dogs: Creel & Creel resources (Hrdy 1981; Walters & Seyfarth 1986; Chapais 1992). For 2001) and eviction of potential competitors from their group (wild example, in some cercopithecine primates, as well as in some dogs: Malcolm & Marten 1982; Creel & Creel 2001; meerkats: carnivores, females from the same matriline support each other in Clutton-Brock et al. 1998, 2006). In most of these ‘singular’ coop- competitive interactions with members of other matrilines and the erative breeders, dominant females can maintain their status for social rank of individuals, as well as their reproductive success, several years while, in some species where they do not forage for depends on the rank of their matriline (Chapais 1992; Holekamp themselves and the extrinsic risks of mortality are low, they live et al. 1996). The relative rank of matrilines increases with their size substantially longer than helpers or workers (Clark & Faulkes 1997; and, in some species, females from dominant matrilines focus their T. Clutton-Brock / Animal Behaviour 77 (2009) 3–11 5 aggression on female recruits to subordinate matrilines (Dittus and attract the attention of males. For example, in Barbary 1977, 1979; Silk et al. 1981; Clutton-Brock 1991). macaques, Macaca sylvanus, the mating calls of fertile and infertile females differ and calls given by fertile females are more likely both MALE MATING PREFERENCES to stimulate ejaculation by their partners and to attract the atten- tion of other males (Pfefferle et al. 2007). In humans, the voices of In many animals, males also show preferences for mating with women become more attractive when they are fertile (Pipitone & particular individuals or categories of females which often generate Gallup 2008) and studies of female lap dancers show that they earn competition between females to attract mates (Herbert 1968; significantly more in tips from clients during their fertile periods Amundsen 2000a; Kraaijeveld et al. 2007). Male mating prefer- than at other stages of the cycle (Miller et al. 2007). Selection to ences have now been documented in insects (Dewsbury 1982; attract males has probably played an important role in the evolu- Kvarnemo & Simmons 1999; Bonduriansky 2001), fish (Sargent tion of exaggerated female ornaments, such as the scales of empi- et al. 1986; Berglund & Rosenqvist 2001, 2003; Kvarnemo et al. did flies, as several recent studies have shown that their size, 2007), lizards (LeBas & Marshall 2000; Orrell & Jenssen 2002), birds structure or colouring are associated either with temporal variation (Amundsen 2000b; Jones et al. 2001; Schamel et al. 2004; Torres & in fecundity or with individual differences (see next section). Velando 2005; Kraaijeveld et al. 2007) and mammals (Herbert 1968; Berger 1989; Keddy-Hector 1992; Mu¨ ller & Thalmann 2000; BREEDING SYSTEMS AND SECONDARY SEXUAL Domb & Pagel 2001; Craig et al. 2002; Preston et al. 2005; Parga CHARACTERS IN FEMALES 2006). Like female competition for males, the relative choosiness of males varies with the availability of partners and can differ The association between breeding systems and the develop- between local populations (Simmons & Gwynne 1993) and ment of secondary sexual characters in males (Clutton-Brock et al. between stages of the breeding cycle (Amundsen & Forsgren 2001). 1977; Plavcan 2004) suggests that their development in females, Male preferences vary. In some species, males prefer familiar too, should vary between polygynous, monogamous and poly- partners (Huck & Banks 1979) while, in others, they prefer novel androus species. Secondary sexual traits associated with direct partners (Orrell & Jenssen 2002). Sometimes, males prefer older, intrasexual competition should be most highly developed in larger or more dominant partners (Szykman et al. 2001; Werner & females of polyandrous species where OSRs are usually female Lotem 2003; Wong & Jennions 2003; Herdman et al. 2004; Preston biased (Trivers 1972; Emlen & Oring 1977) or where competition et al. 2005; Muller et al. 2006; Kvarnemo et al. 2007) while, in between females for breeding opportunities is unusually strong, as others, they prefer younger partners (Buss 1989; Jones 1996; Orrell in many singular cooperative breeders (Clutton-Brock et al. 2006; & Jenssen 2002; Sugiyama 2005). In several species, males also Clutton-Brock 2007) and least developed in polygynous species show consistent preferences for partners that have not mated where OSRs are biased towards males and females do not defend recently: for example, male Drosophila melanogaster are less likely resources or territories. Among monogamous species, traits asso- to court inseminated than uninseminated females while male rats, ciated with competition for breeding opportunities should be most Rattus norvegicus, prefer unmated oestrous females to ones that highly developed in females in species where females play an have already mated several times (Zucker & Wade 1968). In species important role in the defence of resources or territories (West- where females are ornamented or brightly coloured, males Eberhard 1983), while female ornamentation might be expected to commonly show a preference for brighter or more highly orna- show the greatest development where OSRs vary throughout the mented females (Berglund et al. 1997; LeBas & Marshall 2000; reproductive cycle, where females can gain important benefits from Amundsen & Forsgren 2001; Domb & Pagel 2001; Berglund & mating with multiple partners, or where both sexes can gain Rosenqvist 2003; Torres & Velando 2005; Griggio et al. 2005). In substantial benefits from mate choice and males as well as females addition, like females, males sometimes copy each other’s choice of select partners on the basis of phenotypic characters. Although partners, reinforcing the effects of individual choice (Widemo there has yet to be a systematic quantitative analysis of the distri- 2006). bution of secondary sexual characters in females, their distribution Male mating preferences may often serve to increase their appears to be consistent with these predictions, although incon- reproductive success, as the characteristics of females that they sistencies and surprises are common. prefer are often correlated with individual differences in fecundity or with the proximity of females to conception (McLennan 1995; Polyandrous Species Berglund et al. 1997; Jones et al. 2001; Szykman et al. 2001; Ruscio & Adkins-Regan 2003; see below). Few studies have yet investi- In many birds with polyandrous mating systems, females typi- gated the additional possibility that male mate choice may also cally compete more frequently or intensely for breeding opportu- affect the quality of offspring, but a recent study of house mice, Mus nities than males and are sometimes the larger sex (Jenni 1974; domesticus, suggests that this may be the case: when males were Erckmann 1981, 1983; Berglund et al. 1986; Oring et al. 1991a; experimentally mated with females they did not prefer, they Owens & Thompson 1994; Andersson 1995; Ahnesjo et al. 2001; produced offspring with lower viability and poorer performance Berglund & Rosenqvist 2003). Females are also commonly brighter, than those allowed to mate with preferred females (Drickamer more strikingly marked or highly ornamented than males in poly- et al. 2003; Gowaty et al. 2003). Interspecific contrasts in male androus birds, although this is not the case in all species (Jenni preferences may often be related to variation in the effects of 1974; Trivers 1985; Andersson 1994; Eens & Pinxten 2000; Ahnesjo particular female characteristics on paternity certainty, fecundity or et al. 2001; Houde 2001). Why females are more highly orna- rearing success. For example, in chimpanzees, Pan troglodytes, mented than males in some polyandrous animals but not in others where males do not invest in their offspring and older females have is not well understood (Trail 1990): one possibility is that females higher breeding success than younger ones, males prefer older are more likely to be brightly coloured where males may invest and partners, whereas in humans, where males commonly provide breed with multiple partners, making multiple choices of mate resources for their offspring and paternity uncertainty has high during their breeding lives (Kraaijeveld 2003). In other cases, costs, males commonly prefer younger partners (Symons 1979; variation in female coloration may be related to sex differences in Buss 1989; Jones 1996; Sugiyama 2005; Muller et al. 2006). the roles of the two sexes in territory defence and in the sites at Where females compete for the attention of males, selection which they display. In eclectus parrots, Eclectus roratus, for may favour the evolution of signals that indicate their fecundity example, females are bright red and blue while males are bright 6 T. Clutton-Brock / Animal Behaviour 77 (2009) 3–11 green. Incubating females are tended and provisioned by multiple females as well as males are commonly involved in aggressive males and sex differences in colouring appear to be related to the displays aimed at rivals, suggesting that intrasexual competition is contrasting roles of the two sexes: females do not need to be cryptic involved (West-Eberhard 1983; LeBas 2006). Mutual mate choice and display below the canopy where their bright colouring would also be expected to generate larger benefits where both contrasts with the dark limbs and trunks of the trees they nest in, sexes defend resources or contribute to parental care (Burley 1983; whereas males forage in the canopy and their coloration reflects Kvarnemo et al. 2007). Showy signals in females may also offer a compromise between the need for camouflage from predators larger benefits where males make repeated choices between while foraging and the need for conspicuous displays (Heinsohn multiple alternative partners and, as expected, the degree of et al. 2005). ornamentation in both sexes increases with interspecific differ- Several studies have investigated whether females show ences in annual divorce rates (Kraaijeveld 2003). Female plumage elevated testosterone levels in polyandrous species but there is may also be affected by the risk of predation: for example, in some little evidence that they do so (Fivizzani & Oring 1986; Eens & groups of birds, there is a negative correlation between the Pinxten 2000; Goymann & Wingfield 2004; Voigt & Goymann brightness of females (but not the brightness of males) and the 2007). However, in dunnocks, Prunella modularis, females in frequency of nest predation (Martin & Badyaev 1996). breeding groups that include a single male and more than one female have higher testosterone levels than those in monogamous Cooperative Breeders pairs (Langmore et al. 2002). One possible reason for the absence of elevated testosterone levels in females in polyandrous species is In many cooperative or eusocial vertebrates, one female in each that females may show enhanced sensitivity to testosterone rather group dominates reproduction, breeding principally with a single than elevated testosterone levels. For example in African black male (Clutton-Brock et al. 2001, 2006; Griffin et al. 2003; Cockburn coucals, Centropus grillii, females have a higher mRNA expression of 2004). Although many cooperative breeders are monogamous, androgen receptors than males (Voigt & Goymann 2007) and in their breeding systems differ from those of normal monogamous some fish where reproductive competition between females is species in that only a small proportion of mature females breed and, intense, the brain gene expression of dominant females resembles in some cases, variance in breeding success is larger in females than that of males (Aubin-Horth et al. 2007). males (Hauber & Lacey 2005; Clutton-Brock et al. 2006). In these species, overt competition for breeding opportunities can be more Monogamous Species frequent and more intense in females than in males and traits enhancing competitive ability, such as body size, can exert Females also show pronounced secondary sexual characters in a stronger effect on fitness in females than males (Reeve & Sherman many socially monogamous species. Where secondary sexual 1991; Clutton-Brock et al. 2006). In several cooperative breeders, characters are similar but less highly developed in females than breeding females are often the largest individuals in their group males the traditional explanation is that the presence of secondary and are socially dominant to all group members, playing an sexual characters in females is a consequence of genetic correla- important role in controlling group activities and in preventing tions (Lande 1980; Trail 1990; Amundsen 2000a, b, c). However, subordinate females from breeding (Reeve & Sherman 1991; while selection experiments show that selection on secondary Faulkes & Abbott 1997; Clutton-Brock et al. 1998, 2001; Creel & sexual characters in males can lead to correlated responses in Creel 2001). In meerkats and naked mole-rats, females that acquire females (Harrison 1953; Wilkinson 1993; Price & Birch 1996; the breeding position also show increased levels of circulating Chenoweth & Blows 2003, 2005), their effects are usually weak and testosterone (Faulkes & Abbott 1997; Clutton-Brock et al. 2006)as comparative studies indicate that sex-linked modification of the well as a period of secondary growth that is reduced or absent in expression of ornaments is more common than sex-linked inheri- males (O’Riain & Braude 2001; Russell et al. 2004; Clutton-Brock tance of ornament genes (Wiens 2001; Emlen et al. 2005), sug- et al. 2006). Where females compete intensely for breeding status, gesting that explanations of this kind are unlikely to account for the breeders are likely to possess superior phenotypes, and the maintenance of secondary sexual characters in females. In addition, potential benefits of mate choice to males are likely to be reduced, comparative studies show that evolutionary changes in female which may explain why breeding females rarely compete to attract ornamentation and transitions between dimorphism and mono- males and bright coloration or elaborate ornaments are normally morphism are common (Amundsen 2000b; Kraaijeveld et al. 2007). absent. An alternative explanation is that in monogamous species where both sexes are brightly coloured or carry other ornaments, Polygynous and Promiscuous Species mutual mate choice may often play an important role in the development of secondary sexual characters in both sexes, rein- As expected, secondary sexual characters in females are usually forcing genetic correlations between them (Amundsen 2000a; absent or little developed in polygynous species that breed in Kraaijeveld et al. 2007). Mutual mate choice has now been harem groups. For example, in vertebrate groups where polygyny is demonstrated in a wide variety of species, including fruit flies, highly developed (as in many gamebirds and ungulates), females rotifers, termites, amphipods, fish, amphibians and birds (Kraaije- are commonly smaller and have less-developed weaponry than veld et al. 2007). Female plumage may commonly provide males males (Clutton-Brock et al.1977,1980; Harvey et al.1978; Alexander with an indication of a female’s fecundity or capacity for parental et al. 1979; Plavcan 2004). In some cases where females possess investment (Møller 1993; Blount et al. 2002). For example, in obvious weapons these may be used primarily in defence against northern cardinals, Cardinalis cardinalis, brighter females feed predators or in competition for resources rather than in repro- nestlings more than duller ones (Linville et al. 1998) while female ductive competition: for example, antelope and deer species where zebra finches, Taeniopygia guttata, that have been experimentally females carry horns commonly live in open country where they are fed show enhanced fecundity and are preferred as mating partners easily accessible to predators and form large mixed-sex herds over unfed females, although they are indistinguishable to the where competition for resources between, as well as within, sexes human eye (Monaghan et al. 1996). is common (Clutton-Brock 1982; Packer 1983). In other cases, A wide variety of ecological factors may also affect the evolution female weaponry is used in intrasexual competition. For example, of ornamentation or other secondary sexual characters in females in Soay sheep, Ovis aries, where some females are horned and some in monogamous species. Where both sexes have similar ornaments, are not, females with horns are more likely to initiate and win T. Clutton-Brock / Animal Behaviour 77 (2009) 3–11 7 aggressive interactions with other individuals during the lambing In a number of polygynous or promiscuous animals, females period than females without (Robinson & Kruuk 2007), while in possess striking ornaments that may have evolved as a result of some antelopes, receptive females use their horns when competing male mating preferences. Well-studied examples include the for access to males (Bro-Jørgensen 2007). abdominal sacs and enlarged pinnate leg scales of females in some Although OSRs are usually male biased in polygynous species empidid dance flies (Cumming 1994; LeBas et al. 2003) and the and reproductive competition is often more frequent or intense perineal swellings of females in social primates and some birds among males, intrasexual competition between females can also be (Chiba & Nakamura 2002, 2003; Zinner et al. 2004; Ekstrom et al. intense, especially where they defend resources (Racey & Skinner 2007). In most (if not all) polygynous species where females are 1979; Hawkins et al. 2002) or their social rank affects their breeding ornamented, they have access to multiple males and can gain direct success (Silk et al. 1981; Fedigan 1983; Gilchrist 2001). In some benefits from courtship or mating with multiple partners. For polygynous species where female rank and breeding success are example, in empidid dance flies where females are ornamented, closely correlated, testosterone levels are higher in dominant than males provide females with nuptial gifts, the size of a female’s subordinate females during particular stages of the breeding cycle: ornaments reflects her fecundity and males favour highly orna- for example, in spotted hyaenas, Crocuta crocuta, the rank of mented partners (Cumming 1994; LeBas et al. 2003). Similarly, females is closely related to the survival of their offspring and adult most primates where females show pronounced sexual swellings females show elevated testosterone levels in the later stages of live in multimale groups where females have access to multiple pregnancy (Racey & Skinner 1979; Frank 1997; Holekamp & Smale partners (Clutton-Brock & Harvey 1976; Zinner et al. 2004). In many 2000; East & Hofer 2001; Drea 2007). Heightened androgen levels of these species, females gain support and protection for them- may increase the ability of females to compete or to defend their selves and their offspring from males they consort with (de Waal young and may have evolved in these species for this reason. In 1982; Smuts 1985; Weingrill 2000; Palombit et al. 2001), and breeds of domestic cattle where females have been selected for females compete for the attention of males. The size and colouring their fighting ability, they show higher levels of circulating testos- of female sexual swellings varies throughout the menstrual cycle of terone and are usually dominant to females of breeds where females, providing an approximate indicator of changes in fecun- females have not been selected to compete (Plusquellec & Boussou dity (Plavcan 2004; Zinner et al. 2004). In addition, studies of 2001). In addition, heightened androgen levels in females may baboons, Papio cynocephalus anubis, suggest that individual differ- affect the development of offspring (Staub & de Beer 1997). For ences in the size of swellings may be correlated with individual example, in spotted hyaenas, cubs born to dominant mothers with variation in the fecundity of females and their capacity to rear high concentrations of androgens in late pregnancy show higher offspring (Domb & Pagel 2001). It seems likely that the fat-padded rates of aggression as juveniles than those born to females with breasts, thighs and buttocks of human females may have evolved lower androgen levels (Dloniak et al. 2006). for similar reasons (Mealey 2000), for, in humans, as in other In some species where dominant females show elevated primates, female secondary sexual characters are commonly used testosterone levels during gestation, their genitalia show signs of in displays that serve to attract males (Miller et al. 2007). masculinization (Licht et al. 1992, 1998; Drea et al. 1998; Glickman et al. 1998): spotted hyaenas are the best-known example, but CONTRASTS IN THE OPERATION OF SEXUAL SELECTION genitalia of adult females show evidence of masculinization in IN MALES AND FEMALES a number of other species where females compete intensely, including several lemurs (Ostner et al. 2003; Drea 2007; Drea & While intrasexual competition for breeding opportunities and Weil, in press). Masculinization of female genitalia may be mating preferences in the opposite sex appear to have played an a nonadaptive by-product of elevated testosterone levels or of important role in the evolution of secondary sexual characters in increased sensitivity to androgens (Racey & Skinner 1979; Frank both sexes, there are fundamental contrasts between the opera- 1997). Alternatively, it may allow females to deflect aggression tion of sexual selection in males and females. Because of their directed at them by dominant females or to reduce sexual harass- greater energetic investment in gametes and parental care, ment by males (Hawkins et al. 2002; Hofer & East 2003). For females more commonly compete with each other for access to example, the striking pseudopenis and pseudoscrotum of female resources necessary for successful reproduction (including spotted hyaenas closely mimic male genitalia and may allow breeding sites, parental care and social rank) than for access to subordinate females to mimic males, and to reduce the amount of gametes produced by the opposite sex (LeBas 2006; Clutton-Brock aggression they receive from dominant females (see above, 2007). As a result, the relative intensity of intrasexual competition Reproductive competition between females). In some mammals (and the development of traits that increase competitive success where adult females are frequently aggressive to younger subor- in females) may be more strongly influenced by variation in dinates, younger females show transient masculinization which resource distribution and less by variation in the form of mating diminishes or disappears in adults: for example, in fossas Crypto- systems than in males. The differences in fecundity between procta ferox, juvenile females develop an enlarged spinescent females generated by intrasexual competition for resources may clitoris supported by an os clitoridis and a pigmented secretion on commonly lead to large individual differences in fecundity the fur underparts which, in adults, is confined to adult males (Clutton-Brock et al. 1982, 1988; Owens & Thompson 1994) which (Hawkins et al. 2002). This disappears in mature females and may are likely to strengthen selection on males to identify and prefer help to reduce aggression from territorial females (Hawkins et al. superior partners and, on females, for signals reflecting temporal 2002). This explanation is strengthened by evidence that, in some and individual differences in fecundity (Berger 1989; Reinbold colobine monkeys where adolescent males are the target of intense et al. 2002; Clutton-Brock 2007). aggression from resident males, the genitalia of male adolescents There may also be qualitative differences in the costs of appear to show transient feminization (Kuhn 1972). In other cases, reproductive competition and secondary sexual characters for the female mimicry of males serves to reduce harassment by courting two sexes. While intense reproductive competition and the males. For example, in some damselflies and a number of butter- evolution of increased body size in males is often associated with flies, females occur in two colour phases, one of which closely higher juvenile mortality and reduced longevity in males resembles males and andromorphic females are not harassed as compared to females (Clutton-Brock et al. 1985), there is, as yet, frequently by courting males as normal females (Robertson 1985; no evidence that sex differences in survival are reversed in Van Gossum et al. 1999, 2001). species where reproductive competition is more intense or 8 T. Clutton-Brock / Animal Behaviour 77 (2009) 3–11 secondary sexual characters are more highly developed in females sexual selection in females and the evolution of sex differences (Clutton-Brock 2007). One possibility is that the costs of expen- have yet to be answered. diture by females on reproductive competition or ornamentation depress fecundity or parental investment, constraining the Acknowledgments development of secondary sexual characters below the level at which they have measurable costs to female survival (LeBas I am grateful to Christine Drea, Malte Andersson, Sarah Hodge, 2006). For example, elevated levels of testosterone may have Joan Silk, Justin O’Riain and Andy Russell for comments on this adverse effects on the fecundity of females or on the development paper or related discussion. of their offspring which constrain the evolution of further increases in female competitiveness (Drea et al. 2002; Knick- References meyer & Baron-Cohen 2006). A few studies provide indicators that costs of this kind may occur: for example, in some pop- Ahnesjo, I., Kvarnemo, C. & Merilaita, S. 2001. 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Animal Behaviour

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Commentaries Defining sexual selection as sex-dependent selection

Juan Carranza*

Biology & Ethology Research Group, University of Extremadura article info

Article history: Received 8 August 2008 Initial acceptance 29 September 2008 Final acceptance 2 November 2008 Published online 3 December 2008 MS. number: 08-00516

Keyword: sexual selection

After almost 150 years of research, the very definition of sexual generally been interpreted solely in terms of competition for mates. selection remains unclear. The term sexual selection was coined in Only in some cases have authors extended sexual selection to other 1859 by Darwin (1859), who described it in more detail in his later reproductive events (Møller 1994; Reynolds & Harvey 1994)or book (Darwin 1871), as an explanation for the evolution of those referred to the ‘narrow sense’ when using sexual selection only for characters of males of some species that did not seem to contribute competition for mates (Partridge & Endler 1987, page 272). to survival in the struggle for existence, those features previously Recently, Clutton-Brock (2007) has reviewed sexual selection, referred to by Hunter (1837) as ‘secondary sexual characters’. From focusing especially on the operation of sexual selection in females that date, sexual selection has become a sexy topic that has in the context of the current debate (Roughgarden et al. 2006; attracted huge interest among behavioural ecologists and evolu- Kavanagh 2007), and has proposed a return to Darwin’s initial tionary biologists. However, as Clutton-Brock (2004, page 26) words on sexual selection as the intrasexual competition to breed, stated, ‘one of the problems in writing about sexual selection today rather than the most commonly acknowledged competition for is that the term is used in so many different ways’, and recent mates. debate on the basic structure of sexual selection theory (Rough- When Darwin discussed whether certain reproductive struc- garden et al. 2006; Kavanagh 2007; Clutton-Brock 2007) indicates tures were the products of natural or sexual selection, he that its definition has probably never been clear enough. explained that those directly connected to reproduction such as Darwin himself was ambiguous in the definition of the term, the mammary glands of mammals and abdominal pouches of and was imprecise about what type of elements in the behaviour marsupials in the case of females, or the receptacles for the ova in and life history of individuals should or should not be included in certain male fishes, were selected by natural selection. However, the sexual selection process, and how to differentiate between he also stated ‘in many cases it is scarcely possible to distinguish natural and sexual selection. Darwin initially defined sexual the effects of natural and sexual selection’ (Darwin 1871, page selection on the basis of intrasexual advantages in relation to 257). Darwin adopted the term ‘secondary sexual characters’ reproduction. However, in describing the process he always (Hunter 1837) for those traits not ‘directly’ linked to reproduction, referred to the advantages in relation to access to mating oppor- and used the qualifiers primary and secondary to assign to a given tunities, either by competition with members of the same sex character the natural or sexual selection processes, respectively. (in most cases males) or from the preferences of members of the However, the distinction between primary and secondary sexual other sex (mostly females; Darwin 1871). From the discussions traits was also unclear, and Darwin himself came finally to state shortly after the publication of Darwin’s book (e.g. Wallace 1889)to that: ‘Unless indeed we confine the term ‘primary’ to the repro- more recent reviews (e.g. Andersson 1994), sexual selection has ductive glands, it is scarcely possible to decide which ought to be called primary and which secondary’ (Darwin 1871, pp. 253–254). We already know that even the reproductive glands (Hosken & Stockley 2004) and the gametes (Roldan et al. 1992), at least those * Correspondence: J. Carranza, Unidad de Biologı´a y Etologı´a, Facultad de Veter- inaria, Universidad de Extremadura, 10071 Ca´ceres, Spain. of males, are themselves greatly influenced by mate competition, E-mail address: [email protected] (J. Carranza) which, since Darwin, has been the central component of sexual

0003-3472/$38.00 Ó 2008 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2008.11.001 750 J. Carranza / Animal Behaviour 77 (2009) 749–751 selection. Therefore, distinguishing a type of selection aimed at becomes adequately regulated to be dependent on the male or explaining secondary sexual traits is, from its conception, female environments, as current genome research increasingly imprecise, and so is the distinction between secondary and shows to be the case for many genes affecting the whole primary sexual traits. organism (e.g. Drosophila: Ranz et al. 2003;mice: Yang et al. Returning to Darwin’s wording to define sexual selection as the 2006). Not only ornaments and weapons, but also organs not competition for reproduction is not theoretically consistent previously considered as ‘sexual’, such as liver, adipose, muscle or nowadays. This is not of course to cast doubts on the exceptional brains, experience the effects of sex-differential gene expression importance of Darwin’s legacy but simply to realize that we should (Yang et al. 2006). We may say that natural selection becomes not remain bound by the limitations existing at that time and that sexual selection when the fitness effects of genes change from our understanding has moved on considerably since Darwin’s day. a previous evolutionary stage as a consequence of the strategies To Darwin, one main difference between natural and sexual of one or other sex within a species, thus leading to a situation in selection was that natural selection affected survival in the struggle which the genes have to face different selective scenarios for life, whereas sexual selection arose from the competition with depending on sex. members of the same sex with effects not in survival but in number We might say that, under this definition, almost all selection is of offspring (Darwin 1859, 1871). However, we already know that sexual selection. In fact, once sexual reproduction appeared and survival, like any other elements of an individual’s life history, is the existence of two sexes became the typical situation for many simply part of a general strategy designed to pass copies of one’s species, sexual selection may have become a widespread type of own genes to the next generation. Indeed, we should focus on selection affecting most traits. This is, however, the common comparing the selection pressures operating on males and females situation only for large and familiar animals, especially verte- and their consequences instead of trying to distinguish between brates, and to some extent flowering plants, but not for many natural and sexual selection (Grafen 1987; Clutton-Brock 2004), but other organisms such as ciliates, seaweeds, foraminiferans or an agreement on terminology is still necessary (Arnold 1994; Grant yeasts. Natural selection is universal for living things. However, 1995). sex has become widespread in nature and so has its influences on In 1994, in an edited textbook on ethology in Spanish for selection. University students (Carranza 1994; see also Veiga 1995), Sexual selection as selection related to sex can be identified in I proposed a definition for sexual selection as (page 380; translated all cases when there are two sexes or two sexual functions. The from Spanish): ‘those natural selection forces that operate differ- two sexual functions (and sexual selection) may occur within the ently in males and females because of the strategies of the sexes’. same organism in hermaphrodites (Leonard 2006), either animals This is simply to adopt the concept of sex-dependent selection as or plants (Arnold 1994). In other cases, sexually selected strategies a modern use of the term sexual selection to investigate the may converge into similar patterns in monogamous species. This evolution of differences between the sexes. may indeed hamper the identification of sexual selection but, as Competition for mates is obviously of central importance in for any evolutionary convergence, the key is the evolutionary sexual selection. Sexual reproduction provided the potential for history of the strategy in each sex. If sex strategies were always increasing gene copies by multiple mating (Bateman 1948), so it identical, selection would probably never be related to sex. Sex- seems clear that mating competition was at the origin of the dependent selection may also be a good way of unifying the evolutionary divergence leading to the existence of the two sexes concept of sexual selection for animals and plants (Arnold 1994). (Bulmer & Parker 2002). However, responses to selection acting in Sexual selection cannot be identified as mere differences in each sex produce new selective scenarios, so that the consequences selection intensity between males and females, but rather in the give rise to new components of selection. Female preferences, for nature of the trait–fitness relationships in each sex. Sexual example, might, to a great extent, be regarded as a consequence of selection acting on each sex or sexual functions leads to the sexual selection, as far as such preferences may have been differentiation of phenotypes, producing sex-specific traits or promoted by the pre-existing competition between males for sexual versions of many traits. These sex traits were historically mates, although they are, indeed, elements of sexual selection in classified as primary or secondary, although I believe that this their own right. Similarly, divergent selection fuelled by mating distinction should not be maintained. competition has led to differences between the sexes in many other Although there is only one selection process, we can, indeed, elements of their life histories, such as feeding behaviour and maintain a practical differentiation between natural and sexual habitat use (Clutton-Brock et al. 2001), immune function (Marriott selection. In the evolution of any trait we may identify forces of & Huet-Hudson 2006), growth and mortality (Clutton-Brock 1991) natural selection and then look at how they have been modulated or senescence (Carranza et al. 2004; Carranza & Pe´rez-Barberı´a because of the strategies of the sexes. We may refer to specific 2007; Bonduriansky et al. 2008). Such differences between the selection modes such as signal selection, fecundity selection, mating sexes are not only the consequences of selection but also causes of selection, including intrasexual competition for mates and mate sex-dependent selection since they affect the sex-differential choice, as well as postcopulatory competition including sperm fitness effects of many phenotypic traits. competition and cryptic mate choice, when describing how selection A relevant theoretical basis in support of the view proposed acts in each sex, but use sexual selection as the general term that here is that, under sexual selection, genes successively experi- refers to selection acting differently in each sex or sexual function, ence different selective scenarios when carried by males and favouring adaptations that facilitate the sex-specific differentiation females during the evolution of a lineage. Darwin (1871) and of phenotypes. In conclusion, I suggest that extending sexual selec- Wallace (1889) themselves were already concerned with the tion to sex-dependent selection may help to unify modern research heritability and expression of characters in males and females. In on Darwin’s original idea of ‘selection in relation to sex’. many cases in polygynous species it seems that males and females belong to ‘different species’. What is remarkable is that this different selection takes place despite males and females I Thank T. H. Clutton-Brock, A. Cordero, C. Mateos, J. Pe´rez-Gon- sharing (except for a small part of the sex chromosomes) the za´lez, R. Putman, J. Valencia, Louise Barrett and three anonymous same gene pool. Genes subjected to sexual selection may either referees for discussions and comments on the manuscript. Angela tend to increase or decrease in frequency after being in male or Turner helped with the English style. My research was funded by female bodies (Foerster et al. 2007), unless their expression project CGL2007-63594 of the Spanish Ministry of Science. J. Carranza / Animal Behaviour 77 (2009) 749–751 751

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Animal Behaviour xxx (2009) 1–4

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Animal Behaviour

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Forum Do we need a Sexual Selection 2.0?

Joan Roughgarden a,*, Erol Akçay b,1 a Department of Biology, Stanford University b National Institute for Mathematical and Biological Synthesis, University of Tennessee article info

Article history: Received 30 December 2008 Initial acceptance 25 May 2009 Final acceptance 8 June 2009 Available online xxx MS. number: 08-00834R

Keywords: competition cooperation cooperative game theory evolutionarily stable strategy Nash bargaining solution Nash competitive equilibrium noncompetitive game theory sexual conflict sexual selection social selection two-tiered evolutionary theory

Sexual selection is one of Darwin’s major contributions to render any hypothesis infinitely malleable and thus untestable. evolutionary biology. However, it has been subjected to repeated Overall, we find that replacing the standard theory of sexual controversy, including our own recent challenge (Roughgarden selection with some updated version 2.0 is inadvisable. Instead, we et al. 2006), which has provoked lively debate (Kavanagh 2006; note that our proposal for an altogether new theory to replace Clutton-Brock 2007). In response, Clutton-Brock (2009) proposes to sexual selection avoids compounding existing errors, is testable, extend the theory of sexual selection to females in a manner and is possibly correct. parallel to that for males, and Carranza (2009) proposes to redefine Below, we consider the two papers separately. sexual selection theory. We refer to both of these proposals collectively as ‘Sexual Selection 2.0’. In this paper we show that Clutton-Brock’s extension of the EXTENDING SEXUAL SELECTION TO FEMALES theory to females exacerbates the problems with standard sexual- selection theory, compounding the errors already present when the The crux of the difficulty with Clutton-Brock’s proposal is stated theory is applied specifically to males. We also show that Carranza’s in the abstract in which he writes, ‘Since 1871, a substantial body of redefinition of sexual selection violates the basic canon of science research has confirmed his [Darwin’s] explanation of the evolution that once a hypothesis has been falsified, it shall not be redefined to of secondary sexual characters in males’. This claim, although render it true in light of new data, a process that, if allowed, would widely believed, is not true. Research has not confirmed Darwin’s theory of sexual selection in males. Chapter 2 of The Genial Gene (Roughgarden 2009) details three categories of objections to sexual selection theory. The first category * Correspondence: J. Roughgarden, Department of Biology, Stanford University, consists of the many exceptions to the promiscuous-male and Stanford, CA 94305, U.S.A. choosy-female templates that Darwin stipulates as ‘nearly universal’ E-mail address: [email protected] (J. Roughgarden). 1 E. Akçay is at the National Institute for Mathematical and Biological Synthesis, subject only to ‘rare exception,’ as summarized in 2004 in Evolution’s University of Tennessee, Knoxville, TN 37996, U.S.A. Rainbow (Roughgarden 2004). Sexual selection advocates dismiss

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2 J. Roughgarden, E. Akçay / Animal Behaviour xxx (2009) 1–4 these exceptions because sexual selection is supposedly true in that females might compete more for resources than males do, as a great majority of cases. None the less, the variety and quantity of well as for mates, thus implicitly endorsing the dubious assumption exceptions are now known to be enormous and invite suspicion that that females invariably have the higher parental investment. sexual selection theory was on the wrong track to begin with. Clutton-Brock’s version of Sexual Selection 2.0 amounts to The second category consists of studies that have appeared since saying that there is intra- and intersexual competition simulta- 2004 based on species that were not thought to be exceptional to neously in both sexes. If we add sexual conflict to this mix and the promiscuous-male and choosy-female templates, species that assume that it too operates in both directions, then we are left with possessed what were thought to be typical showy secondary sexual the simple position that every animal is always competing with characters in males. In The Genial Gene, these species are termed every other animal. Such a theory is devoid of any specific meaning. ‘poster-child species.’ For these species extensive data have, Moreover, awarding females parity in the eye of sexual selection according to the studies’ authors, refuted sexual selection predic- transfers to females the problems of the male-based sexual selec- tions or expectations. Failed poster-child species include the tion theory. The paradox of the lek for females (termed ‘the paradox collared flycatcher, Ficedula albicollis (Qvarnstro¨m et al. 2006), the of the cre`che’ in The Genial Gene) is the dilemma of replenishing the blue tit, Cyanistes caeruleus (Hadfield et al. 2006), the barn swallow, bad genes in females that male choice is presumably weeding out Hirundo rustica (Bro-Jørgensen et al. 2007), the lark bunting, each generation. Although data in some species might show a bit of Calamospiza melanocorys (Chaine & Lyon 2008), the peacock, Pavo male choice of females simultaneous with female choice of males, cristatus (Takahashi et al. 2008), swallowtail butterflies (Papil- the rationale that such choice is to acquire genetic benefits has not ionidae; Kunte 2008) and dragon lizards (Agamidae; Ord & Stuart- been shown and is almost surely false. Instead, choice for direct Fox 2006; see also a meta-analysis of extrapair parentage, Akçay & benefits by either sex amounts to the negotiation that underlies Roughgarden, 2007b). Furthermore, the classic studies of Bateman cooperation and bargaining, the very negotiation that our own (1948), cited by both Clutton-Brock and Carranza, have been thor- theory focuses on. oughly discredited by three independent critiques (Tang-Martinez Finally, the Clutton-Brock position unwittingly abandons any & Ryder 2005; Dewsbury 2005; Snyder & Gowaty 2007). It is not an connection between gamete size and sex role, a connection that exaggeration at this time to say that every species studied with sexual selection advocates have taken as fundamental. If both males sufficient care and rigour fails to confirm sexual selection theory and females are equally choosy, as Clutton-Brock proposes, then and that, despite the thousands of papers over the years that invoke gamete size is irrelevant to sexual selection, leading to yet another the sexual selection narrative to explain their results, evidence for logical inconsistency in the standard theory. In sum therefore, we find sexual selection remains inconclusive and sexual selection remains Clutton-Brock’s proposal for a Sexual Selection 2.0 to be untenable. undemonstrated in any single case. The third category consists of logical, often population-genetic, contradictions to the sexual selection story. Notable among these is REDEFINING SEXUAL SELECTION the ‘paradox of the lek’, which can be circumvented only by postulating far-fetched and untested schemes for replenishing the In contrast to Clutton-Brock, Carranza acknowledges difficulties bad genes in males that female choice is presumably weeding out with present-day sexual selection theory. Indeed, his first sentence each generation. Without a continual supply of bad genes in males, states, ‘After almost 150 years of research, the very definition of continual female choice for male genetic quality is pointless. As of sexual selection remains unclear’. The definition of descent through 2007, 10 distinct hypotheses to circumvent the paradox of the lek modification from common ancestors and the definition of natural had been proposed (Miller & Moore 2007). In 2008, two more selection, which together are the bedrock of evolutionary theory, attempts at circumvention appeared as well (Harris et al. 2008; are not unclear; only sexual selection theory suffers conceptual Kotiaho et al. 2008). The growing literature of the past dozen years malaise. Carranza notes that Darwin originally defined sexual aimed at ‘resolving’ the paradox of the lek is itself testimony that selection quite generally as selection in relation to reproduction, to the paradox has not been resolved. It cannot be resolved. The be contrasted with selection in relation to survival. paradox of the lek is a fatal flaw of sexual selection theory. Another Despite this initial generality, Carranza further notes that ‘in population-genetic contradiction detailed in The Genial Gene is that describing the process he [Darwin] always referred to the advan- the fitness difference between a ‘good’ and ‘bad’ male is extremely tages in relation to access to mating opportunities, either by low and undetectable according to the population-genetic theory of competition with members of the same sex (in most cases males) or how weakly deleterious mutations accumulate. from the preferences of members of the other sex (mostly females)’. Still other self-contradictions lurk throughout sexual selection In practice, Darwin’s picture of sexual selection was specifically theory. Recent reviews highlighted logical inconsistencies in the about mating advantages and, as such, offers an explanation for theory that supposedly connects parental investment to the very secondary sexual characters that could be true or false empirically. existence of sexual selection (Queller 1997; Houston & McNamara That is, the secondary characters might relate to mating success, as 2002; Kokko & Jennions 2008). Despite this, Clutton-Brock continues he hypothesized, or could relate to other considerations such as to invoke parental investment theory as the correct theoretical offspring-rearing success, as we hypothesize. explanation for sex roles in sexual selection (Clutton-Brock 2007, The beauty of Darwin’s formulation is that it is a genuine scien- 2009). tific hypothesis subject to falsification. If it is false, then so be it, if Thus, Clutton-Brock’s confident assertion that sexual selection is true, then so be that too. Redefining sexual selection so that it well established for males and therefore ripe for extension to becomes no longer falsifiable disqualifies sexual selection as females is unwarranted. None the less, Clutton-Brock’s review a scientific hypothesis and, if permitted, would undercut the scien- surveys reproductive behaviour in females and proposes to extend tific credibility of behavioural ecology. But Carranza takes this tack. the definition of sexual selection to encompass ‘all selection Carranza writes, ‘Darwin’s wording to define sexual selection as processes operating through intrasexual competition for breeding the competition for reproduction is not theoretically consistent opportunities in either sex’ (Clutton-Brock 2009, page 6). Clutton- nowadays’. So Carranza defines ‘sexual selection as ‘‘those natural Brock argues that even in non-sex-role-reversed species, sexual selection forces that operate differently in males and females selection in females mirrors that in males, operating through male because of the strategies of the sexes’’’. He writes that natural mate choice and intrasexual contests. The only major distinction is selection becomes sexual selection when ‘genes have to face

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J. Roughgarden, E. Akçay / Animal Behaviour xxx (2009) 1–4 3 different selective scenarios depending on sex’ and goes on to state consensus, but by the facts. And it is the facts that are sinking sexual that ‘under this definition, almost all selection is sexual selection’. selection. The enormous and still growing evidence against sexual Carranza does sexual selection no favour. In an effort to render it selection is what motivates our call for a new theory and our efforts always true by definition, he destroys sexual selection’s standing as to provide one. Yet, sexual selection advocates routinely ignore or a scientific hypothesis. Thus, we do not find Carranza’s proposal for misinterpret our findings. As an example, our meta-analysis that a Sexual Selection 2.0 to be tenable either. Instead, we retain the casts serious doubt upon the validity of good-genes or compatible- original statement of Darwin’s theory of sexual selection and find genes benefits in avian extrapair paternity (Akçay & Roughgarden the data available today sufficient to regard it as having been 2007b) is either ignored entirely (Griffith & Immler 2009) or worse, falsified. cited as supporting these hypotheses (Gangestad & Thornhill 2008). Thus, our position may be far more consistent with available data COMPETITION, COOPERATION AND SOCIAL SELECTION than the ‘consensus’ appreciates. Instead of engaging in continuing polemic, our lab has been Our position is that the greatest scientific progress will now be developing a new theory for sexual reproduction that we term social made by offering alternative hypotheses in place of sexual selection. Concerning the genetic system, Iyer & Roughgarden selection. (2008b) have shown that the basic difference between male and We conceive of a reproductive social group as the biological female gamete sizes (anisogamy) can evolve to maximize the equivalent of a firm in economics, a firm whose product is offspring. contact rate between gametes and represents a mutually beneficial Thus, our focus is not on mating success, but on offspring- state with regard to the male and female functions. This result producing success. Members of a reproductive social group must counters the established theory attributed to Parker et al. (1972) that work as a team, and we see reproductive social behaviour, including anisogamy results from males reducing investments in gametes and mate choice and reproductively relevant traits such as secondary thus parasitizing female investment, which is the source of claims sexual characters, as revolving around what must be done by that sexual conflict must underlie all sexual reproduction (Parker individuals to join a team, to coordinate actions in the team and to 2006). Similarly, Iyer & Roughgarden (2008a) show that the evolu- discern and pursue a team goal. tion of male and female bodies (dioecy) may reflect a specialization Central to our proposed theory to replace sexual selection is to increase fertilization rates. These papers show that nonconflicting a conceptualization of social evolution with two ‘tiers’, one behav- selection on the sexes can potentially explain the most basic features ioural and the other population genetic. In contrast, the theory of the genetic system for sex. Another study investigates the origin behind sexual selection conceives of social evolution in a single tier, of alternation of generations in plants as a mechanism to increase as exemplified by the evolutionary game theory started by Maynard fertilization rates (Iyer & Roughgarden 2009). Smith (1982). This requires that behavioural dynamics coincide Concerning behaviour, as already mentioned, we introduced with gene-pool dynamics, which precludes using modelling tools a two-tier approach to modelling social behaviour (Roughgarden such as cooperative game theory to describe behaviour because the et al. 2006) in place of the single-tier ESS framework from Maynard gene-pool dynamics are purely competitive, culminating in an Smith (1982). The two-tier framework allows cooperative game evolutionarily stable strategy (ESS). Instead, splitting the overall theory, including Nash bargaining, to be used in the behavioural process into two tiers allows the lower (behavioural) tier to be tier. Our work also explores how cooperative dynamics can explain governed by cooperative outcomes such as the Nash bargaining why bird species often have extrapair paternity. The canonical solution (Nash 1950), as well as by the familiar Nash competitive explanation for extrapair paternity, namely that females have equilibrium, whereas the upper (population-genetic) tier remains extrapair copulations with genetically superior males, has failed in governed by purely competitive dynamics leading to the ESS. We empirical tests (Arnqvist & Kirkpatrick 2005; Akçay & Roughgarden have termed this approach ‘social selection’, which is different from 2007b). We propose instead that extrapair parentage might other uses of the phrase by Crook (1972) and West-Eberhard (1979). represent reproductive transactions between males in exchange for Because our original proposal for a new theory to replace sexual pairing with females that have higher breeding success (Akçay & selection (Roughgarden et al. 2006) drew much criticism at the Roughgarden 2007a). Similarly, in species with biparental care, time, and still does, two anonymous referees have requested that experiments that manipulate parental effort fail to confirm the we address the criticisms to our theory. In the absence of answers predictions of competitive parental care theory (Hinde 2006). We to our critics, the referees suggest that attempts to revise sexual have shown that this discrepancy can be explained by modelling selection into version 2.0 would be preferable to its wholesale the parents as working together as a team to maximize nest replacement, or even that the standard version should be consid- production (Akçay & Roughgarden 2009). In a model that combines ered OK as it currently stands. Of our proposal for a new theory, one both the behavioural and the evolutionary tiers, we have shown referee notes ‘how widely the scientific community disagreed with that even with strict payoff–conflict between individuals, indi- it’ and another referee wonders what could produce a ‘shift in the vidual-level natural selection can lead to other-regarding motiva- consensus view of sexual selection towards the views of the tions (Akçay et al. 2009). Manuscripts soon to be submitted include authors [us]’. Well, we responded to the criticisms when they studies of the evolution of ornaments, sexual dimorphism and appeared (Kavanagh 2006; see also our online responses on the sexual polymorphism (P. Iyer & J. Roughgarden, unpublished data); Science Web site and other venues). For the most part, the criticisms the evolution of the payoff matrices for behavioural-tier dynamics have been emotional and less than useful in contributing to (E. Akçay & J. Roughgarden, unpublished data); and the evolution of constructive discourse. Today, our most recent overall position, parent–offspring relations using management science theory for including our response to critics, is summarized in The Genial Gene the optimal incentive policy in a conglomerate (J. Roughgarden & (Roughgarden 2009; cf. book reviews in Belden 2009, Odling-Smee Z. Song, unpublished data). 2009, Pruett-Jones, in press and video-blog interview with Robert Wright on 19 April 2009 at http://bloggingheads.tv/diavlogs/ CONCLUSION 19126). We note also that consensus is a ‘lagging indicator’, describing what people have thought in the past, whereas criticism In conclusion, we appreciate the contributions by Clutton-Brock is a ‘leading indicator’, describing what people might think in the and Carranza to the debate on the future of sexual selection theory. future. The truth of sexual selection will not be decided by vote or Few people apprehend how grave the deep, broad difficulties are for

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4 J. Roughgarden, E. Akçay / Animal Behaviour xxx (2009) 1–4 sexual selection, and we interpret the Clutton-Brock and Carranza Hinde, C. A. 2006. Negotiation over offspring care? A positive response to partner- proposals as implicitly acknowledging this situation. However, we provisioning rate in great tits. Behavioral Ecology, 17, 6–12. Houston, A. I. & McNamara, J. M. 2002. A self-consistent approach to paternity and also think that neither Clutton-Brock nor Carranza resolves the parental effort. Philosophical Transactions of the Royal Society of London, Series B, problems sexual selection theory is facing because the problems are 357, 351–362. simply unsolvable. Rather than issue a new version of sexual Iyer, P. & Roughgarden, J. 2008a. Dioecy as a specialization promoting sperm delivery. Evolutionary Ecology Research, 10, 867–892. selection, Sexual Selection 2.0, alternatives to the entire theoretical Iyer, P. & Roughgarden, J. 2008b. Gametic conflict versus contact in the evolution approach may be preferable. We invite readers to consider the of anisogamy. Theoretical Population Biology, 73, 461–472. alternative approach we have proposed, social selection. Iyer, P. & Roughgarden, J. 2009. Alternation of haploid and diploid generations: evolution by gamete amplification. Evolutionary Ecology Research, 11, 57–77. Kavanagh, E. E. 2006. Debating sexual selection and mating strategies. Science, 312, 689–697. References Kokko, H. & Jennions, M. D. 2008. Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology, 21, 919–948. Akçay, E. & Roughgarden, J. 2007a. Extra-pair parentage: a new theory based on Kotiaho, J. S., LeBas, N. R., Puurtinen, M. & Tomkins, J. L. 2008. On the resolution transactions in a cooperative game. Evolutionary Ecology Research, 9, of the lek paradox. Trends in Ecology & Evolution, 23, 1–3. 1223–1243. Kunte, K. 2008. 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Animal Behaviour xxx (2009) 1–4

Contents lists available at ScienceDirect

Animal Behaviour

journal homepage: www.elsevier.com/locate/anbehav

Forum We do not need a Sexual Selection 2.0dnor a theory of Genial Selection

Tim Clutton-Brock*

Department of Zoology, University of Cambridge article info

Article history: Received 31 July 2009 Initial acceptance 18 August 2009 Final acceptance 9 October 2009 Available online xxx MS. number: 09-00509

SEXUAL SELECTION IN MALES a stronger effect on fitness in males than females and variance in breeding success is higher and selection for traits that improve We have no need of a Sexual Selection 2.0 and, despite Rough- access to breeding partners is stronger in males (Clutton-Brock garden and Akçay’s assertions (Roughgarden & Akçay 2010), I 1988; Jones et al. 2000, 2002; Lorch 2002, 2005; Becher & have never suggested that we did. Roughgarden and Akçay believe Magurran 2004; Rios-Cardenas 2005; Mills et al. 2007; Webster that the theory of sexual selection is fundamentally flawed and et al. 2007; Lorch et al. 2008). should be abandoned. Their attack on sexual selection rests on The third plank of their case against sexual selection rests on three main planks, all of them shaky. First, they point to irregu- criticisms of sexual selection operating through female mating larities, inconsistencies and anomalies in relationships between the preferences. Here, they argue that female mating preferences are characteristics of females and males and sex differences in invest- bound to remove genetic variance in male fitness although there is ment in gametes and offspring (Trivers 1972), in potential rates of extensive evidence that this need not be the case (Andersson 2004; reproduction (Clutton-Brock & Parker 1992), and in variance in Miller & Moore 2007), ignoring many of the most comprehensive breeding success (Wade & Arnold 1980; Clutton-Brock 1988; studies of pre- and postcopulatory female choice (Andersson 1982; Clutton-Brock et al. 1988). While these certainly exist, they have Hoglund et al. 1990; van Rhijn 1991; Wilkinson & Dodson 1997). been recognized for many years (Campbell 1972; Clutton-Brock They review five empirical studies of birds where they suggest that 1983; Andersson 1994; Gowaty 2004; Kappeler & van Schaik 2004) evidence fails to support the predictions of sexual selection theory. and are an integral part of the modern theory of sexual selection, Of the five species, three are biparental, monogamous species showing us how sexual selection operates in different systems. where the magnitude of sex differences in breeding competition They are refinements not flaws and do not undermine sexual and mate choice is likely to be relatively small. In one of the selection theory. remaining two (lark buntings) they suggest that evidence that Second, Roughgarden and Akçay attack evidence of sex differ- sexual selection on male phenotypic traits varies between years is ences in reproductive variance, exaggerating criticisms of Bate- incompatible with the theory of sexual selection, which is not the man’s original study of sexual selection in Drosophila. Bateman case. In the other (peacocks) they cite the results of a recent study (1948) argued that mating with multiple partners had no effect on that failed to find evidence of consistent female preferences for the reproductive success of females but a strong effect on repro- train (tail) size in males but fail to mention the results of other ductive success in males whereas subsequent work has shown that studies of the same species that have provided evidence of female mating with two or three partners increases the reproductive preferences for males’ elaborate plumage (Petrie et al. 1991; Yasmin success of females (Tang-Martinez & Ryder 2005; Snyder & Gowaty & Yahya 1996; Loyau et al. 2005a, b, 2007, 2008). 2007). However, Bateman’s fundamental principle remains intact. Even if we accept Roughgarden and Akçay’s critical assessment In many species, the number of mating partners typically has of the evidence of sexual selection operating through precopula- tory female choice (which I don’t), there remains the first mode of sexual selection, Darwin’s ‘law of battle’. What about the classical examples of the operation of sexual selection through intrasexual * Correspondence: T. Clutton-Brock, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB3 9EJ, U.K. competition? Do Roughgarden and Akçay believe that males do not E-mail address: [email protected] regularly compete in horned beetles and water spiders, bullfrogs,

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Please cite this article in press as: Clutton-Brock, T., We do not need a Sexual Selection 2.0dnor a theory of Genial Selection, Animal Behaviour (2009), doi:10.1016/j.anbehav.2009.10.018 ARTICLE IN PRESS

2 T. Clutton-Brock / Animal Behaviour xxx (2009) 1–4 pheasants, lions, seals and elephants and that intrasexual compe- of sexual selection restrict it to evolutionary processes operating tition has played no part in the evolution of male characteristics through competition for mates (Andersson 2004), while intra- in these species (Le Boeuf 1974; Borgia 1979; Eberhard 1979; sexual competition between females is often over breeding Alexander et al. 1979; Clutton-Brock et al. 1979, 1988; Harcourt et al. opportunities or resources rather than mates or mating opportu- 1981; Davison 1985; Conner 1988; Le Boeuf & Reiter 1988; Kruuk nities (West-Eberhard 1979; Clutton-Brock 2007, 2009). To solve et al. 2000, 2002)? There is enormous evidence to the contrary this problem, it is sometimes suggested that we need an additional (Andersson 2004). And how do they account for consistent rela- category of ‘social’ selection to include cases where individuals tionships between the development of competitive traits in males compete with members of the same sex for resources necessary for and the degree of polygyny (Clutton-Brock et al. 1977, 1980; Harvey reproduction rather than for mates (West-Eberhard 1975, 1979). et al. 1978; Alexander et al. 1979; Harcourt et al. 1981)? However, this has the disadvantage that it can lead to similar traits that have evolved through fundamentally similar processes being SEXUAL SELECTION IN FEMALES attributed to sexual selection if they occur in males and to social selection if they occur in females. A further problem is that males as In the first part of their article, Roughgarden and Akçay focus well as females often compete for resources that are necessary to their criticisms on my unremarkable suggestion that, to understand rear offspring (including breeding sites, feeding territories and the evolution of sex differences in behaviour and morphology, we parental care). In addition, in many systems where females need to understand the operation of sexual selection in females as compete for access to males, they are probably competing for well as in males (Clutton-Brock 2009). They argue that the recog- resources in the form of parental care rather than for access to nition of sexual selection in females leaves a theory that is ‘devoid gametes. Distinguishing clearly between sexual and social selection of any specific meaning’, but do not say why. If sexual selection is seldom easy in either sex. does not operate in females, how do they explain the evolution To avoid these difficulties, my own preference is to abandon any of elaborate plumage in females in many polyandrous birds formal attempt to distinguish between natural and sexual selection (Erckmann 1983; Davison 1985; Amundsen 2000a) or the and to focus on contrasts in the components, intensity and targets conspicuous perineal swellings found in females in a number of of selection between males and females (Clutton-Brock 1983, 2004, primates and birds where females have access to more than one 2009). Another solution is to define sexual selection as operating potential partner (Clutton-Brock & Harvey 1976; Zinner et al. 2004), through individual differences in breeding success generated either or the breasts of human women (Caro 1987; Caro & Sellen 1990)? by intrasexual competition or by intersexual mate choice, so that it Roughgarden and Akçay appear to believe that the idea that encompasses the consequences of reproductive competition and sexual selection operates in females is novel and represents a new mate choice in both sexes (Clutton-Brock 1983, 2004, 2009). Views version of the theory of sexual selection. It isn’t and doesn’t. Darwin differ and I recognize that there is a discussion to be had over this was well aware that sexual selection operates in both sexes, but these are not grounds for dismissing the operation of sexual although he was principally concerned with its operation in males. selection in females. Here he is on the evolution of sex differences in button quail: ‘Taking as our guide the habit of most male birds, the greater size GENIAL SELECTION and strength as well as the extraordinary pugnacity of the females of the Turnix and emu must mean that they endeavour to drive If we have no need of a Sexual Selection 2.0, still less do we need away rival females, in order to gain possession of the male; and on to replace the theory of sexual selection with Roughgarden and this view, all the facts become clear; for the males would probably Akçay’s vague and amorphous concept of social selection. As they be most charmed or excited by the females which were most are using the term to refer to a very different concept to West- attractive to them by their bright colours, other ornaments or vocal Eberhard (1979, 1983) and social selection has been used in several powers. Sexual selection would then do its work, steadily adding to other ways (Tanaka 1996; Moore et al. 2002), I shall follow the attractions of the females; the males and young being left not at Roughgarden’s practice of giving a convenient label to arguments all or but little modified.’ (Darwin 1871, page 480). that she is commenting on and shall refer to the processes she Research over the last 10 years has greatly extended our describes as Genial Selection, in line with the title of her recent knowledge of the operation of sexual selection in females book, The Genial Gene (Roughgarden 2009). (Amundsen 2000a; Domb & Pagel 2001; Houde 2001; LeBas et al. Genial Selection has recently been described by Michael Ruse in 2003; Heinsohn et al. 2005; LeBas 2006; Wright et al. 2008). There his review of Roughgarden’s book as a ‘warmer and friendlier way is now extensive empirical evidence that females as well as males of thinking’ (Ruse 2009). It consists of an explanation of repro- often compete intensively for breeding opportunities (Erckmann ductive behaviour and the evolution of sex differences based on 1983; Simmons 1995; Holekamp et al. 1996; Kvarnemo & Simmons two-tier models of selection involving mutualistic interactions 1999; Berglund & Rosenqvist 2003); that males, as well as females, between individuals that maximize their reproductive output can show persistent preferences for breeding with particular (Roughgarden et al. 2006; Roughgarden 2009). When Roughgarden categories of partners (McLennan 1995; Amundsen & Forsgren originally presented Genial Selection as an alternative to sexual 2001; Pizzari et al. 2003; Wong & Jennions 2003; Herdman et al. selection (Roughgarden et al. 2006), her claims provoked 40 2004; Griggio et al. 2005); and that both these processes affect the evolutionary biologists to write in to take issue with her arguments evolution of behaviour and morphology in females (Davison 1985; (Kavanagh 2006). Their criticisms were detailed, closely reasoned Amundsen 2000a, b; Amundsen & Forsgren 2001; Heinsohn et al. and extensive and there is no space to repeat them here: anyone 2005; Rubinstein & Lovette, in press). interested should read the original commentaries. The theoreti- Although we now understand more about the operation of cians argued that her theoretical arguments were not novel and sexual selection in females, it has still received much less attention what was new was wrong. The empiricists objected to criticisms of than sexual selection in males and there are still basic conceptual sexual selection, the selective use of examples and the distortion of issues to be sorted out. One of them concerns which evolutionary arguments and evidence. Here, Roughgarden and Akçay repeat processes operating in females should be regarded as examples of their original arguments and dismiss the responses of Rough- sexual selection and which should be treated as examples of garden’s original critics as ‘emotional’, but make no attempt to natural selection. The problem here is that many recent definitions answer them.

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The principal problem with Genial Selection lies in Rough- Caro, T. M. & Sellen, D. W. 1990. The reproductive advantage of fat in women. garden’s claim that it provides an alternative to the theory of sexual Ethology and Sociobiology, 11, 51–66. Clutton-Brock, T. H. 1983. Selection in relation to sex. In: Evolution from Molecules selection rather than in the detailed structure of her models. to Men (Ed. by B. J. Bendall), pp. 457–481. Cambridge: Cambridge University Mutualistic interactions between the sexes are not uncommon, Press. especially in monogamous, biparental species, and are capable of Clutton-Brock, T. H. 1988. Reproductive success. In: Reproductive Success (Ed. by T. H. Clutton-Brock), pp. 472–486. Chicago: University of Chicago Press. generating strong selection for cooperation between breeding Clutton-Brock, T. H. 2004. What is sexual selection? 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Hinde), pp. 195–237. common, too, and sexual selection theory provides ways of estab- Cambridge: Cambridge University Press. lishing the extent to which intersexual interactions are mutualistic Clutton-Brock, T. H. & Parker, G. A. 1992. Potential reproductive rates and the or antagonistic (Parker 1979, 2006; Pizzari & Snook 2003, 2004; operation of sexual selection. Quarterly Review of Biology, 67, 437–456. Clutton-Brock, T. H., Harvey, P. H. & Rudder, B. 1977. Sexual dimorphism, socio- Shuster & Wade 2003). While Genial Selection may add to our nomic sex ratio and body weight in primates. Nature, 269, 797–800. understanding of the behaviour of males and females in particular Clutton-Brock, T. H., Albon, S. D., Gibson, R. M. & Guinness, F. E. 1979. The logical circumstances, unlike the theory of sexual selection, it provides no stag: adaptive aspects of fighting in red deer (Cervus elaphus L.). 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Animal Behaviour

journal homepage: www.elsevier.com/locate/anbehav

Forum Sexual selection and the evolution of evolutionary theories

Juan Carranza*

Biology and Ethology, University of Extremadura article info

Article history: Received 18 July 2009 Final acceptance 4 August 2009 Available online xxx MS. number: 09-00480

Keywords: Darwin evolution theory males and females natural selection sex-dependent selection sexual selection

Evolutionary theory has experienced big changes since Darwin problem of the lek paradox (e.g. Kotiaho et al. 2008). Notable published his book on the origin of species (Darwin 1859). New advances such as sexual selection in plants (Shuster 2009) and elements such as the development of genetic theory (Fisher 1930; postcopulatory sexual selection (Eberhard 2009) have helped fill Wright 1931; Haldane 1932; Dobzhansky 1937), recognition of early gaps. However, it is remarkable that the basic concept of selection at the level of genes (Williams 1966) and kin selection sexual selection has scarcely been revised after the revolution in (Hamilton 1964) have been incorporated to refine and adapt the our understanding of natural selection. new natural selection theory. As a consequence, when we now use In a recent opinion article (Carranza 2009) I proposed we should the term natural selection in an academic context we refer to return to Darwin’s initial idea of ‘selection in relation to sex’ but, processes resulting in changes in gene frequencies rather than because our understanding has moved on considerably since ‘preservation of favoured races in the struggle for life’ or ‘survival of Darwin’s day, we should not feel trapped by the details of his the fittest’. original suggestions of the processes involved. I suggested that Darwin also appreciated a distinctive form of selection, which what is remarkable in the light of current knowledge is that under he invoked to explain sexual dimorphism, referring to it as ‘selec- sexual selection, genes successively experience different selective tion in relation to sex’ (Darwin 1871). He was, however, ambiguous scenarios when carried by males and females during the evolution when describing the process, initially considering that it derived of a lineage, and that these different scenarios are what actually from competition for reproduction, but later recognizing the shape sexual dimorphism. Thus, I proposed ‘sex-dependent selec- process as mediated through competition for mates, which has tion’ as a modern use of the term sexual selection to focus on the become the most widely accepted definition for sexual selection selection pressures operating differently on males and females and (e.g. Andersson 1994). their consequences. I do not see this interpretation different By contrast to our understanding (and revision) of the theory of enough to Darwin’s description to deserve differentiation from his natural selection, it seems that sexual selection has been little theory; rather it is an updating of it, in exactly the same way as our updated. Considerable empirical and theoretical effort has focused understanding of Darwin’s theory of natural selection has been on studying trait evolution through mate choice (e.g. Mays & Hill refined and revised. I agree that intrasexual competition for mates 2004; Andersson & Simmons 2006), or explaining the recurrent (including broad-sense mate choice and postcopulatory selection) is a very important component of sexual selection (and it is perhaps at the root of the whole process). Also, my proposal includes competition for breeding opportunities (Clutton-Brock 2007, 2009) * Correspondence: J. Carranza, Ungulate Research Unit, CRCP, University of Co´ rdoba, 14071 Co´ rdoba, Spain. as far as it differs in males and females. However, competition for E-mail address: [email protected] mating or breeding commonly affects many aspects of life history

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2 J. Carranza / Animal Behaviour xxx (2009) 1–2 that were traditionally regarded as not being sexual selection (Ranz Finally, I would like to stress that my proposal was not designed et al. 2003; Marriott & Huet-Hudson 2006; Yang et al. 2006). As for as an alternative to R&A’s work, as they seem to suggest. R&A are natural selection, the conceptual boundary that I propose is at the free to propose a replacement if they want, but the view I propose level of genes, that is, using sexual selection as ‘selection in relation for sexual selection is not meant to solve any potential problem of to sex’ or ‘sex-dependent selection’ to refer to the differences in sexual selection theory that they might have raised, as I think that selective scenarios that any gene of a sexual species may face in the problems with the theory R&A present do not exist. Never- being carried by one or other sex during evolution, since this is theless, I acknowledge that R&A have criticized my proposal on what actually shapes the differences between male and female sexual selection, because I believe that discussion is not only phenotypes within a species. enriching but also essential to the advancement of scientific ideas. Roughgarden & Akçay (2010; hereafter R&A) criticize this posi- I thank C. Mateos, J. Pe´rez-Gonza´lez and R. Putman for tion by making two points. On the one hand they defend their comments on the manuscript. A. Turner helped with the English proposal (Roughgarden et al. 2006) of replacing sexual selection by style. My research was funded by project CGL2007-63594 of the social selection. This idea may need discussion in the scientific Spanish Ministry of Science. community (as has already begun: Kavanagh 2007). However, although I do not myself concur with this suggestion, it is not my objective in this short note to provide arguments against it. On the References other hand, R&A worry about the proposals by Clutton-Brock Andersson, M.1994. Sexual Selection. Princeton, New Jersey: Princeton University Press. (2009) and myself (Carranza 2009) because they do not accept any Andersson, M. & Simmons, L. W. 2006. Sexual selection and mate choice. Trends in development of the original Darwinian theory of sexual selection Ecology & Evolution, 21, 296–302. from what was originally described. To defend their position they Carranza, J. 2009. Defining sexual selection as sex-dependent selection. Animal Behaviour, 77, 749–751. have gone too far by saying that my proposal of updating sexual Clutton-Brock, T. H. 2007. Sexual selection in males and females. Science, 318, selection ‘violates the basic canon of science that once a hypothesis 1882–1885. has been falsified, it shall not be redefined’. Sexual selection theory Clutton-Brock, T. H. 2009. Sexual selection in females. Animal Behaviour, 77, 3–11. Darwin, C. 1859. On the Origin of Species by Means of Natural Selection, or the (note that R&A prefer to rate it as a hypothesis when rejecting my Preservation of Favoured Races in the Struggle for Life. London: J. Murray. proposal) has not been falsified but greatly supported in its Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. London: essentials. R&A seem not to admit that any theory may need J. Murray. refinement by the addition of new elements as scientific knowledge Dawkins, R. 1982. The Extended Phenotype. Oxford: Oxford University Press. Dobzhansky, T. 1937. Genetics and the Origin of Species. New York: Columbia advances. Rather, they prefer to maintain the theory as it was University Press. almost 150 years ago and try to rebut it today. With the same Eberhard, W. E. 2009. Postcopulatory sexual selection: darwin’s omission and its procedure, we could falsify the 150-years-old natural selection consequences. Proceedings of the National Academy of Sciences, U.S.A., 106, 10025–10032. theory, because Darwin’s original conception that it was the Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford: Oxford survival of the fittest that caused evolutionary change offered an University Press. inaccurate and incomplete explanation of a more complex process. Haldane, J. B. S. 1932. The Causes of Evolution. London: Longmans. Hamilton, W. D. 1964. The genetical theory of social behaviour I-II. Journal of However, the essentials of Darwinian description of natural selec- Theoretical Biology, 7, 1–52. tion are not only still valid but also constitute the basis for all Kavanagh, E. 2007. Debating sexual selection and mating strategies. Science, 312, modern evolutionary biology, although it is also true that our 689–697. Kotiaho, J. S., Lebas, N. R., Puurtinen, M. & Tomkins, J. L. 2008. On the resolution understanding of the process has been repeatedly updated and of the lek paradox. Trends in Ecology & Evolution, 23, 1–3. redefined (Fisher 1930; Haldane 1932; Dobzhansky 1937; Hamilton Marriott, I. & Huet-Hudson, Y. M. 2006. Sexual dimorphism in innate immune 1964; Williams 1966; Dawkins 1982). Sexual selection, as an responses to infectious organisms. Immunologic Research, 34, 177–192. Mays, L. M. & Hill, G. E. 2004. Choosing mates: good genes versus genes that are element of natural selection, deserves the same treatment, a good fit. Trends in Ecology & Evolution, 19, 554–559. although R&A might surprisingly think that this ‘would undercut Ranz, J. M., Castillo-Davis, C. I., Meiklejohn, C. D. & Hartl, D. L. 2003. the scientific credibility of behavioural ecology’. Sex-dependent gene expression and evolution of the Drosophila transcriptome. R&A also made an out-of-context citation of my phrase ‘under Science, 300, 1742–1745. Roughgarden, J. & Akçay, E. 2010. Do we need a Sexual Selection 2.0? Animal this definition, almost all selection is sexual selection’. They omit Behaviour, doi:10.1016/j.anbehav.2009.08.010. the previous part of the sentence ‘We might say that,’. I used this Roughgarden, J., Oishi, M. & Akcay, E. 2006. Reproductive social behavior: coop- rather extreme statement to introduce the reasons why I think that erative games to replace sexual selection. Science, 311, 965–969. Shuster, S. M. 2009. Sexual selection and mating systems. Proceedings of the this is not the case for many species and that it may be accurate in National Academy of Sciences, U.S.A., 106, 10009–10016. cases when sexual selection has affected most life history traits. Williams, G. C. 1966. Adaptation and Natural Selection. A critique to Some Current Rather than doing ‘sexual selection no favour’, as R&A state, this is Evolutionary Thought. Princeton, New Jersey: Princeton University Press. Wright, S. 1931. Evolution in mendelian populations. Genetics, 16, 97–159. simply to realize the power of sexual selection in influencing so Yang, X., Schadt, E. E. & Wang, S. 2006. Tissue-specific expression and regulation of many elements of life histories. sexually dimorphic genes in mice. Genome Research, 16, 995–1004.

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Animal Behaviour xxx (2009) 1–7

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Animal Behaviour

journal homepage: www.elsevier.com/locate/anbehav

Forum Sexual selection: endless forms or tangled bank?

David M. Shuker*

School of Biology, University of St Andrews article info

Article history: Received 5 August 2009 Initial acceptance 18 August 2009 Final acceptance 20 October 2009 Available online xxx Ms. number: 09-00518

Keywords: Darwin, Charles female choice male–male competition mating systems natural selection sexual selection

Few people apprehend how grave the deep, broad difficulties are for natural selection. Second, the collection of theory (which I will term sexual selection ‘mating systems theory’) used in part to predict patterns of sexual Roughgarden & Akçay 2010 selection is not the same as sexual selection itself; mating systems theory attempts to predict how aspects of a species’ biology (from For some biologists sexual selection is in trouble. For the first its physiology through to ecology) determine what patterns of time since the reinvigoration of sexual selection in the 1970s competition for mates occurs, and whether or not this differs following the effective rediscovery of mate choice (Bateson 1983; between the sexes (if ‘sexes’ even exist). Mating systems theory is Bradbury & Andersson 1987), the validity of sexual selection as therefore conceptually analogous to aspects of population ecology a central component of modern evolutionary theory is being theory that predict how organisms compete for other resources, challenged (Roughgarden et al. 2006). That paper, in which thereby driving natural selection. Third, the action of sexual Roughgarden and colleagues baldly stated that sexual selection was selection does not depend on whether or not behavioural interac- ‘wrong’, caught evolutionary biologists on the hop (Kavanagh tions between mating partners during reproductive episodes are 2006). Since then renewed versions of the challenge to sexual considered cooperative or selfish. Fourth, whether or not there is selection have appeared (e.g. Roughgarden 2007; Roughgarden & sexual selection does not depend on what ‘roles’ different repro- Akçay 2010), and, as will be obvious from the companion pieces to ductive classes (mating types or sexes) take during reproductive this article, resolution is still some way off. In addition, core aspects interactions. Fifth, the claim that there is no evidence for sexual of the theory of sexual selection, including its definition, have also selection is false. To make these points, I will describe a view of received renewed attention (Clutton-Brock 2007, 2009; Carranza sexual selection that I consider a consensus view, and use this to 2009). Here I consider the current status of sexual selection and consider what should best not be considered sexual selection. First attempt to make five points. First, sexual selection is best consid- though, I will consider natural selection and why behavioural and ered as a useful subset of the overall process of natural selection, evolutionary ecologists choose to go beyond the evolution of fitness with which biologists seek to understand the evolution of traits to look at individual traits at all. associated with competition for mates. As such, sexual selection shares the logical framework and coherence of its twin sister, Natural Selection and Need for Sexual Selection

* Correspondence: D. M. Shuker, School of Biology, University of St Andrews, Harold Mitchell Building, St Andrew, Fife KY16 9TH, U.K. Evolution by natural selection is driven by competition, be it E-mail address: [email protected] competition for resources or competition to avoid death, as

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2 D.M. Shuker / Animal Behaviour xxx (2009) 1–7 ultimately something limits population growth (Darwin 1859). selection’ (Endler’s ‘nonsexual selection’, or ‘narrow-sense natural Competition among organisms can take a bewildering array of selection’), often in the context of viability selection (competition forms, the identification of which forms the basis of much of for resources and so on such that an organism lives long enough to modern population ecology. The resulting evolutionary adaptations engage in competition for mates). For instance, sexual selection is to competition are themselves equally bewildering, but include often talked of as being ‘balanced’ by natural selection, as in some some rather satisfyingly paradoxical traits such as cooperative models of exaggerated displays or ornaments (Andersson 1994). It behaviour and the sacrificing of individual reproduction (West et al. probably would be more precise to say that sexual selection may be 2007). In the end though, all these various forms of competition balanced by other ‘components’ of natural selection, but use of the boil down to competition among individuals in a population to term natural selection also to mean viability selection is now leave the most offspring. If individuals vary genetically in their familiar and well entrenched. ability to leave offspring in the face of the biotic and abiotic envi- Additionally, Endler (1986) pointed out that statistical descrip- ronment they occur in, natural selection has to result in the genetic tions of genetic change derived from the breeder’s equation parti- change to the population that we think of as evolution (Endler tion ‘selection’ from ‘heredity’ (i.e. separating selection from 1986). This is the syllogism at the heart of Darwinian evolution: if genetics). Natural or sexual selection (measured or modelled as individuals differ in their ability to leave offspring, and if these selection differentials or gradients) is then no longer synonymous differences are partly heritable, then evolution has to occur. with ‘evolution by natural/sexual selection’. Selection can occur but Evolution by natural selection is therefore a population genetic there will not be genetic change unless there is heritable variation process. If the Darwinian syllogism holds we will see a relationship for the trait. As above, this partition has proved very useful (it is the form between genotype and fitness. As such, it is not necessary to basis of quantitative genetics modelling for example), but it is again specify how this relationship forms, that is, to make the links a conceptual tool, as nature is not an animal breeder. Consider again between genotype and phenotype, and then phenotype and fitness, the trait of interest to be fitness itself. A term denoting the additive explicit (e.g. Brookfield 2009). Put another way, the only trait that genetic variance in fitness among individuals in fact encapsulates matters for evolution is fitness. However, the population genetic both the necessary genetic variation required for a genetic response perspective leaves untouched many aspects of organism biology we and also the definition of selection itself (fitness differences among might care about, in particular the nature of phenotypes. Animal individuals), thereby collapsing the partition between selection and behaviour of course is all about these phenotypes, and from Darwin heredity, and giving us Fisher’s Fundamental Theorem (Fisher onwards animal behaviour researchers interested in evolution have 1930). In this article I will consider sexual selection as a component used conceptual tools to explore phenotypic evolution. One such of an overall natural selection process, and inclusive of both tool, often used implicitly, is to try to partition how selection has selection and heredity. ‘acted’ on different aspects of the phenotype, including across Competition for mates can occur in very many forms (Darwin different stages of an organism’s life cycle. This tool is distinctly 1871; Andersson 1994), and cooperation between individuals is Darwinian, in the sense that Darwin himself used it when talking again not precluded (e.g. DuVal 2007), but it is useful to consider about selection for particular traits (Darwin 1859). In some cases, competition over quantity and competition over quality. In terms of we have given names to these components of the overall natural quantity of mates, the most basic and familiar form of competition selection process, when it has proved useful to focus on certain for many of us arises over ‘none’ versus ‘some’. It is well known that aspects of phenotypes and consider how selection has acted on in some species some individuals of a given class may fail to obtain them. One of the most influential has of course been sexual a mate because of competition (for instance, male elephant seals selection. and female meerkats: Haley et al. 1994; Clutton-Brock et al. 2006). Alternatively, individuals in a population may for the most part all What is Sexual Selection? succeed in finding a reproductive partner, in which case competi- tion may become focused on the quality of that partner. If certain Sexual selection describes the selection of traits associated with individuals represent a better reproductive resource (there will be competition for mates. As such we can say that sexual selection a greater number of offspring produced by that partnership), it is arises from competition for mates (Andersson 1994). To avoid clear that competition can arise for access to those individuals as confusion, I define ‘mate’ as a reproductive partner with which one reproductive partners, as it can in any other ecological context. How or more zygotes are formed (thereby allowing postcopulatory those partners are obtained may vary, from out and out coercion processes). Despite the work of Roughgarden and colleagues, and (Clutton-Brock & Parker 1995) to taking advantage of being indeed the recent commentaries by Carranza (2009) and Clutton- a limited resource and choosing only to mate with the most Brock (2009), I consider this to be the standard definition of sexual appropriate partner(s) (Bateson 1983). It is for this reason that selection. More formally, sexual selection is the relationship sexual selection is not precluded in strictly monogamous species between a trait and its effect on fitness through sexual competition. (Darwin 1871), and mutual mate choice where both members of As such, many traits can be thought of as being both naturally and reproductive pairs make mate choices is now well established sexually selected, although from a population genetic viewpoint it (Kraaijeveld et al. 2007; Clutton-Brock 2009). For sexual selection is all ‘natural selection’. The debate about the distinctions between not to occur in a population, there either has to be no scope for natural and sexual selection has a long history (e.g. see Endler 1986; competition (partners as resources are not limiting, and all partners Andersson 1994), but a few words might be useful here. One can are of equal quality), or the outcome of any competition for mates is view evolution by natural selection in its simplest form if fitness totally random with respect to the traits expressed by individuals, itself is the trait under selection. Components of this process can be such that successful partnerships represent a random sample of identified and considered separately though, which becomes pairs of individual phenotypes (and thus genotypes). While we extremely useful when we turn our attention (out of desire or cannot claim that competition for reproductive partners, and thus necessity) to the evolution of certain phenotypic traits, rather than sexual selection, is ubiquitous (and as Roughgarden & Akçay 2010 just fitness. Such a view is given by Endler (1986) in his Figure 1.2. note, not all sexual selection processes act in all populations at all Sexual selection is then a component of natural selection. Unfor- times), it has been abundantly clear since Darwin that sexual tunately, evolutionary biologists then tend to lump all other selection describes something that commonly occurs in nature, components of natural selection together and call this ‘natural with effects that are nontrivial at the phenotypic level. And to make

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D.M. Shuker / Animal Behaviour xxx (2009) 1–7 3 this point extremely clear, for sexual selection to be ‘wrong’ and not attention from behavioural ecologists (a point also made by Clut- to occur at all (as suggested by Roughgarden et al. 2006), we have to ton-Brock 2009). That lack of attention is historical and it does not show that one or both of the premises of the syllogism underlying in itself represent a statement of what sexual selection ‘is’. For sexual selection are always untrue in natural populations. As such, example, sexual selection can occur in isogamous species (e.g. either there would never be variation among individuals in their Rogers & Greig 2009) even though the seminal monograph of success at obtaining (potentially high-quality) mates, and/or there Andersson (1994) is not full of such examples. In a similar vein, both would never be additive genetic variation among individuals in isogamous and anisogamous gametes can compete for reproduc- traits that influence this success. Male guppies have pigmentation tive partners in order to create a zygote. In this case, the quantity of that influences their success in mate competition. Male guppies partners for a gamete over which competition arises is (usually) have heritable differences in pigmentation. There is sexual selec- zero or one. Gametes may also vary in quality (for instance in terms tion in guppies (Brooks & Endler 2001). One could go on, but I hope of resources provided by the parent) and gametes of the comple- it is sufficient just to note here that, like its twin sister natural mentary sort may compete for access to each other. The role of selection, sexual selection happens (Andersson 1994). sexual competition in gamete evolution is now well established Viewing sexual selection as competition for mates is to define (Birkhead et al. 2009). sexual selection in broad terms. In their commentary in response to Competition for mates has the potential to arise among all Clutton-Brock (2009), Roughgarden & Akçay (2010) suggest that classes of organisms in a population, and Darwin (1871) famously any such broad definition of sexual selection is ‘devoid of any pointed out the two forms it would take: intraclass competition specific meaning’. I find this unconvincing, not least because and interclass choice, where ‘choice’ refers to aspects of the natural selection, which is of course a description of an overall phenotype that bias the probability that an individual of one class process that is even broader and subsumes all forms of competition will become the reproductive partner of an individual of the other among organisms for future genetic representation, seems to have class (as such, ‘choice’ may sometimes seem an unfortunate term). both a pretty clear meaning and great intellectual utility. Why In terms of isogamous species, there may therefore be intramating sexual selection should then be singled out for being overly broad is type competition and intermating type choice. In terms of anisog- not clear. If we look for similar examples in ecology, do we find that amous gametes, we can envisage intragamete type competition the concept of density dependence is too broad and therefore (among sperms and among ova) and intergamete choice (including meaningless because of the almost innumerable ways in which it passive attraction to gametes of certain phenotypes, or by making can be manifested? Sexual selection, like density dependence, may fertilization for one class of gamete difficult for the other class). encompass a lot of processes but the logic at its heart is simple and However, it is in anisogamous species at the organismal level, with the premises refutable. sperm-producing male tissues and ova-bearing female tissues, that Other definitions of sexual selection have made attempts to sexual selection has been most thoroughly conceptualized and make explicit just what it is that is being competed over, including studied. fecundity and resource acquisition that increases fecundity (see Clutton-Brock 2007, 2009). Fecundity (which entails how energy to How Controversial is this View of Sexual Selection? be invested in reproduction is spread among ova) may be both naturally and sexually selected from a phenotypic point of view. In The extent to which this view of sexual selection is controversial terms of sexual selection, fecundity may be selected if by being will be in part measured by the number of readers that have already more fecund one attracts an individual who is a better reproductive got bored and stopped reading. My perception is that the above partner in some way. Such sexual selection may of course in turn represents the consensus among evolutionary biologists of what increase the competition for mate quality (highly fecund partners). sexual selection is (and is at the heart of the view of sexual selection However, fecundity can be fixed in a population and sexual selec- given by Andersson 1994). But clearly controversy is in the air. Of tion still act. In contrast to Clutton-Brock (2007, 2009), I would course, researchers can call whatever they like sexual selection, but argue that fecundity by itself, when not associated with competi- in doing so a clear conceptual framework is needed. I contend that tion for mates, is best considered as only being naturally selected we already have one, and that the ‘conceptual malaise’ identified by (even if it leads to sexual dimorphism). Otherwise sexual selection Roughgarden & Akçay (2010) will come as a big surprise to the vast comes to equate itself with natural selection. Clutton-Brock (2009) majority of evolutionary biologists. Using the above framework, I considered female–female competition for resources as a possible will suggest some things that should not be called sexual selection candidate for a sexual selection process, but going down this route or confused with sexual selection, highlighting where possible the of course means that all foraging behaviours (and indeed all conceptual consequences of ignoring these suggestions. behaviours that mean an individual does not die before managing to become reproductively mature) become associated with differ- What Sexual Selection Should Not Be ences in fecundity (or sperm load say, if we switch attention to males). At this point, the benefit of a conceptual tool that partitions Sexual selection should not be a description of the difference in (and names for convenience) different aspects of the population how selection has acted on males and females (as suggested by genetic natural selection process becomes moot, and we might as Carranza 2009). While that phenomenon is currently of great well revert to just thinking about natural selection, a point made by interest, and likely to be pervasive in nature, we already consider it Clutton-Brock (2009). I do not think we need to go that far though. sufficiently under the umbrella of sexually antagonistic selection Viewing sexual selection as competition for mates, while general in and sexual conflict (Chapman et al. 2003; Arnqvist & Rowe 2005). A the sense of covering a wonderfully diverse range of phenotypes, is difference in selection on traits in males and females (or the actually an excellent focus for researchers: is there competition for influence of sex on selection, to paraphrase Carranza) is not mates, and does a given trait influence that competition? If a trait Darwinian sexual selection, not least because these differences may does not, then there are plenty of other drivers of ecological be unrelated to reproduction (ecological selection on dimorphism competition (for resources, enemy-free space and so on) that may for example: Shine 1989), and this means that what Carranza have left their evolutionary mark on a trait. would call sexual selection might influence traits not associated Although competition for mates can occur in many different with reproduction. This seems a long way from how sexual selec- contexts (Andersson 1994), some have received rather little tion is currently used. Moreover, the fact that isogamous organisms

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4 D.M. Shuker / Animal Behaviour xxx (2009) 1–7 with sexual reproduction, but no ‘sexes’, can experience sexual but that is a different story) with no effect at all on the logical basis selection pretty much seals the case. I therefore concur with of sexual selection detailed above. Understanding why leks form, Roughgarden & Akçay (2010) that the attempt by Carranza to why harems form, why resource defence evolves, while impacting change the definition of sexual selection is less helpful than it might our ability to predict forms of sexual selection present in a pop- be. Of course, sexual selection as currently understood may well ulation, does not impact on whether or not sexual selection is have contributed to traits having different fitness effects in males actually happening. For that, we just have to test the validity of our and females, but turning the logic around is problematic. two logical premises: variation in success in competition for mates; Sexual selection is also not just intersexual choice, let alone just a heritable component to that variation. This may seem a facile female choice. As already explained, intra- and interclass processes point, but trying to understand the criticisms of Roughgarden and co-occur within the framework of sexual selection. It seems of little colleagues leads more to mating systems theory than it does to conceptual relevance to use sexual selection exclusively to refer to sexual selection per se. one aspect of competition for mates, whether or not a topic such as Ecological analogies with respect to natural selection abound. female choice has been popular and/or controversial (reviewed in For instance, we might be completely wrong about how trait- Clutton-Brock 2009). Likewise, just because female–female mediated or density-mediated competition impacts fitness in competition for mates has perhaps not received the attention (or a focal population (i.e. their contribution to natural selection), but been as overt) as male–male competition or female choice does not we can still test evolution by natural selection in our focal pop- mean it is not a part of sexual selection (Clutton-Brock 2007, 2009). ulation by examining the relationship between fitness and geno- The same is of course true for male mate choice (e.g. Bonduriansky type: failure of one does not demand failure of the other. The 2001). Claims by Roughgarden & Akçay (2010) that this makes phenotypes and the components of selection we try to ascribe as sexual selection too broad are misplaced (see above). One aspect of important to those phenotypes are typically what interest us most, interclass choice that might need clarifying though is how but our ability to identify selection correctly is irrelevant to the ‘competition’ (as in ‘competition for mates’) fits in. From the point underlying evolutionary process. (Because of this, one could argue of the class being chosen (in sexual species, males say), we can that one perhaps shouldn’t bother trying to measure selection easily see that males may compete via displays or some such to be ‘acting’ on individual traits at all: Grafen 1987.) We must remember the chosen one (Darwin 1871; Andersson 1994). This competition to separate tests of natural or sexual selection from tests of things need not ‘look’ like competition, as the males could all just stand we think might influence natural or sexual selection. They are not around showing off their morphology, but they are competing to be the same thing. Of course, in reality we want to be able to make chosen (in the way flowering plants may compete to be pollinated). predictions about when different forms of competition for mates What about the class doing the choosing though (females for occur, and in which sex or mating type. But how good we are at that example)? As mentioned above (and reviewed in Clutton-Brock is a test of our understanding of mating systems, not a test of the 2009), there could be active competition among females to be able fundamental process of sexual selection. I reiterate this point to choose the best mating partner. However, the competition need because clearly our grasp of mating systems is not as complete as not be overt and some choices might just lead to more offspring or we perhaps thought (a point made very clearly by Clutton-Brock fitter offspring (if we allow indirect genetic benefits) than others. 2007, 2009), but to use that to demolish sexual selection is wrong. Thus it needs to be kept in mind that these mate preferences evolve Now I am aware that this separation may seem a little convenient, via intrasexual selection (while having intersexual selection effects a nice way of hiding sexual selection away from some inconvenient on males). This has not always been clear because the evolution of truths about our knowledge of the true roles of operational sex ornaments and the preferences for them is often (and partly ratio, parental investment and the like. But I hope I have stressed correctly) bundled together as intersexual selection. But the clearly enough, especially through analogy with natural selection, selection on the choosers arises because some female choices mean that our difficulty in always correctly predicting when ‘something’ access to higher quality or more attractive mates than others should happen is not the same as saying that the ‘something’ (Kirkpatrick & Ryan 1991; Maynard Smith 1991). Remember that if therefore never happens. all females made the same choice, there would be no variation in Perhaps most importantly, sexual selection is not dependent on preference and sexual selection on female preference would stop. If what have been termed ‘sex roles’ (who chooses, who competes in the next generation all the males displayed the preferred and so on). This is clear from again considering competition for phenotype, all selection would stop on them as well. Thus intra- reproductive partners in organisms without sexes, and is also sexual selection (i.e. intrasexual competition for mates) is part and abundantly clear from the many natural systems where both sexes parcel of mate choice, and therefore I do not believe we have engage in mate choice (Kraaijeveld et al. 2007). It is true that Dar- a definition of sexual selection that largely confines sexual selection win (1871) did not belabour this point, and that most of his writing to males (see Clutton-Brock 2007). on sexual selection proscribed male and female sex roles in a rather Sexual selection is also not the same as what I will call mating ‘traditional’ way (most, but not all: see below). It is also true that systems theory (Trivers 1972; Emlen & Oring 1977; Davies 1991; behavioural ecologists may seem to drop by default into assuming Clutton-Brock & Parker 1992; Shuster & Wade 2003). Mating that sexual selection comprises ‘male–male competition’ and systems theory seeks to address why particular mating (or ‘female choice’. However, one really does not have to go very far to breeding) systems form, and has included what consequences appreciate that behavioural ecologists have not actually been that particular kinds of mating system might have for competition for stupid (reading Andersson 1994 will suffice). One of the most mates, and thus what forms of sexual selection may occur. Broadly curious aspects of the challenge to sexual selection put forward by speaking then, mating systems theory takes the biology of an Roughgarden and colleagues has been their contention that the organism (from its physiology, through to its life history and existence of ‘sex role-reversed’ species are in some way fatal to ecology) and tries to predict how and when individuals come sexual selection. Rather, such species have long been taken to together to reproduce, and what opportunities there are for support our ideas of how mating systems work and evolve, espe- competition for mates. At its fullest extent, it is a theory base of cially when we manipulate ‘sex role’ by manipulating which sex is when we expect sexual selection to act, not a theory of sexual the more limiting (e.g. Gwynne & Simmons 1990; Simmons & selection. For example, all sorts of aspects of mating systems theory Bailey 1990; Simmons 1992). The fact that individuals of a given could be wrong (and the lack of experimental work is surprising, class can sometimes be competitive, and sometimes choosy, all

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D.M. Shuker / Animal Behaviour xxx (2009) 1–7 5 depending on how different aspects of the environment and been developed from only one strand of game theory as originally species’ biology influence competition for mates as a whole, fits developed by economists such as Nash (Roughgarden & Akçay, mating systems theory rather nicely. The problem is we do not yet 2010). In particular, they argue that Maynard Smith introduced have all the answers. This may be simply because aspects of ‘competitive’ game theory to biology, but failed to introduce a species’ biology and ecology that would allow us to make better ‘cooperative’ game theory, which is based on between-actor predictions are poorly known for all but a few species. In any case negotiations (although this interpretation of what constitute though, our ability to understand and predict the causation of sex different strands of game theory is contested: e.g. Dall et al. 2006). roles is the purview of mating systems theory; sexual selection At one level it might not seem a particularly important point, not does not need males or females to have one sex role or another, it least because much of the sexual selection theory developed just needs competition for mates. (especially in terms of mate choice) has been avowedly population Sexual selection is not the same thing as sexual conflict. The genetic in nature (Kokko et al. 2006). However, clearly game theory, shift in the way we have viewed reproductive interactions over the in the guise of evolutionarily stable strategies (ESSs), has pene- last century or so has been well documented (e.g. the well-known trated the psyche of behavioural ecology. Has it done so to the change in moral status of the dunnock: Davies 1992; Arnqvist & detriment of our understanding of sexual selection? I suggest not Rowe 2005). This reinterpretation continues, as it should, to this for three reasons. First, game-theoretical models in behavioural day. Over the last 15 years or so, driven by empirical observations ecology have actually developed over the years to consider (most notably in insects), the idea of conflict between males and behavioural negotiation (e.g. Houston et al. 2005; Johnstone & females over reproductive ‘decisions’ has become a dominant Hinde 2006). These models generated useful predictions and did so theme (Arnqvist & Rowe 2005). While it is clear that males and without creating a crisis in evolutionary ecology. Second, much of females have to cooperate to some extent in order to mate, espe- the context given for this alternative modelling framework sits cially in internally fertilizing species, both theory and (to a lesser firmly in the field of the evolution of parental care, not sexual extent) experiment have moved us to view the context in which selection at all. Parental care, or more generally the patterns of reproductive behaviour evolves as one primarily driven by sexual parental investment within and among the sexes, has been an conflict rather than sexual cooperation. The key of course is the important component of mating systems theory, from Trivers phrase ‘to some extent’. In some insect species, male–female (1972) onwards. However, parental investment need have no reproductive interactions may be brief, with much of the interac- a priori link to the pattern of sexual selection since a whole array of tion dominated by a mating struggle as males try to force mating ecological factors may influence how individuals of a class compete (as in seaweed flies or water striders: Rowe et al. 1994; Shuker & for mates (see above). Third, a rigorous critique of sexual selection Day 2001). In these species, ‘to some extent’ is not very much. In that calls for a major redefining of what we mean by sexual many other taxa, on the other hand, such as socially monogamous selection and how we model it surely needs to be one that is birds, reproductive interactions include significant investment in broadly applicable across taxa. As an insect behavioural ecologist, it parental care by both parents, male and female alike (reviewed in is not at all clear to me how the inclusion of behavioural negotia- Clutton-Brock 1991). In these cases, ‘to some extent’ may actually tions in some form of new sexual selection theory could have be quite a lot. anything other than a marginal impact on most reproductive That said, behavioural ecologists will probably need to continue interactions in insects. Of course, one could frame any interaction in to explore the relationship between sexual selection and sexual terms of a ‘negotiation’ if one wanted, but it is not clear this would conflict. For instance, given the current re-emergence of the ‘good be much more than a semantic gesture in many cases. I could genes’ sexual selection debate (as mentioned by Roughgarden & repeatedly punch someone and say it was a negotiation, but Akçay, 2010) and some of the important structural weaknesses members of the local constabulary may consider the interaction underlying existing models of intersexual choice (outlined by less than harmonious. Is it really helpful therefore to reimagine Arnqvist & Rowe 2005), there is a current enthusiasm for sexual vigorous mating struggles and acts that look like rejection behav- conflict models of the evolution of mate preferences (Holland & iour as ‘negotiations’ (Rowe et al. 1994)? The same of course is likely Rice 1998; Gavrilets et al. 2001; Cameron et al. 2003). In these to be true for sexual selection in plants, if one wishes to look models, mate preferences (behaviours that bias the mating success outside animals. of the opposite sex) are in fact the outcome of attempts to limit Perhaps the most important point to remember though, which (implicitly) costly mating interactions, thus ‘choosing’ individuals is in fact implicit in the work of Roughgarden and colleagues, is that that are able to overcome or subvert those attempts (but this is still behavioural negotiations do not ‘remove’ conflict from mating sexual selection, only ‘chase-away’ sexual selection in terms of interactions, because they could only exist and be relevant if there competition among the ‘choosy’ sex to limit matings to the is conflict present in the first place. Rather, negotiations may minimum necessary: Holland & Rice 1998). These models are provide a strategy to ameliorate the expression of conflict, and attractive and have rightfully received a lot of attention (although ‘resolve it’ even, such that cooperative outcomes result. These not necessarily in terms of experimental tests). However, the fact outcomes will only arise though if cooperation, be it reached via that a sexual conflict over mating can lead to sexual selection does real-time negotiation or as part of a genetically programmed not mean that sexual conflict is sexual selection (or vice versa). The behavioural repertoire, has a higher inclusive fitness. Organisms two are definitely at risk of being conflated by the unwary though. will not negotiate just to be ‘nice’. In summary, the behavioural tier introduced by Roughgarden and colleagues may prove useful in Sexual Reproduction as a Cooperative Venture certain circumstances, but these models cannot redefine sexual selection. One of the main criticisms voiced by Roughgarden & Akçay, in the current article and others, is that the emphasis on sexual What did Darwin Think? competition and conflict fundamentally misunderstands how evolution has shaped reproductive behaviour in animals. Part of One aspect of the sustained critique of sexual selection by this critique is motivated by the use of certain game-theoretical Roughgarden and colleagues has been that various societal biases tools, and in particular the impact of the work of Maynard Smith associated with gender have detrimentally influenced how scien- (1982). Their main contention is that evolutionary game theory has tists have thought about sexual selection. Moreover, it is argued

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6 D.M. Shuker / Animal Behaviour xxx (2009) 1–7 that this goes right back to Charles Darwin himself (e.g. Rough- and an extremely useful organizing tool. We should be wary of garden 2007). The problem of what Darwin really meant has also giving it away too cheaply. cropped up in the recent commentaries by Carranza (2009) and I thank the editors for the invitation to write this article, and Clutton-Brock (2009). One could easily devote many pages to this, Angela Turner for her patience in my getting it ready. I am also very but here are two points perhaps worth briefly considering. First, of grateful to Louise Barrett, Dave Hosken and an anonymous referee course scientific interpretations are not immune from the societies for their extremely thoughtful and generously given comments. My in which they are made (sexual selection provides a nice case study research is supported by the Natural Environment Research Council after all: Cronin 1992). What matters though is how enlightening and the Biotechnology and Biological Sciences Research Council. those interpretations remain in the face of new data and new interpretations. The fact we are still all thinking about sexual selection is testament to the lasting value of Darwin’s insight, even References if we may wish he had left us with a clearer sound-bite of a defi- nition. Second, just what did Darwin think? The answer depends on Andersson, M. 1994. Sexual Selection. Princeton, New Jersey: Princeton University where you look. In their recent biography, Desmond & Moore Press. (2009) detail how Darwin’s thoughts on sexual selection developed Arnqvist, G. & Rowe, L. 2005. Sexual Conflict. Princeton, New Jersey: Princeton University Press. over time (especially in terms of its relationship with human Bateson, P. (Eds). 1983. Mate Choice. Cambridge: Cambridge University Press. evolution), and that development was not straightforward. For Birkhead, T. R., Hosken, D. J. & Pitnick, S. S. 2009. Sperm Biology: An Evolutionary instance, in a notebook from 1837 Darwin was able to make notes Perspective. Oxford: Academic Press. Bonduriansky, R. 2001. The evolution of male mate choice in insects: a synthesis of on female–female competition for males (Desmond & Moore 2009), ideas and evidence. Biological Reviews, 76, 305–339. a long way from the classic view of Darwin and his coy, choosy Bradbury, J. W. & Andersson, M. (Eds). 1987. Sexual Selection: Testing the Alterna- females ‘selecting. males, according to their standard of beauty’ tives. Chichester: J. Wiley. Biology Letters The Descent of Man Brookfield, J. 2009. Evolution and evolvability. , 5, 44–46. (Darwin 1859). And similarly, while (Darwin Brooks, R. & Endler, J. A. 2001. Direct and indirect sexual selection and quantitative 1871) is undoubtedly home to much of what we now would genetics of male traits in guppies (Poecilia reticulata). Evolution, 55, 1002–1015. consider gender-role stereotyping, he was also able to assert that Cameron, E., Day, T. & Rowe, L. 2003. Sexual conflict and indirect benefits. Journal sexual selection ‘depends on the advantage which certain indi- of Evolutionary Biology, 16, 1055–1060. Carranza, J. 2009. Defining sexual selection as sex-dependent selection. Animal viduals have over others of the same sex and species solely in Behaviour, 77, 749–751. respect of reproduction’, a definition notably devoid of explicit Chapman, T., Arnqvist, G., Bangham, J. & Rowe, L. 2003. Sexual conflict. Trends in gender roles. However, with thoughts developing nonlinearly over Ecology & Evolution, 18, 41–47. Clutton-Brock, T. H. 1991. Parental Care. Princeton, New Jersey: Princeton Univer- time, coupled with the (very frustrating!) 19th Century practice of sity Press. making often substantial revisions to books for new editions across Clutton-Brock, T. 2007. Sexual selection in males and females. Science, 318, many years, trying to ascribe to Darwin a definitive view of sexual 1882–1885. Clutton-Brock, T. 2009. Sexual selection in females. Animal Behaviour, 77, 3–11. selection must ultimately be somewhat unsatisfactory (as indeed it Clutton-Brock, T. H. & Parker, G. A. 1992. Potential reproductive rates and the would be for anyone; see Reeves 2007 for a similar discussion of operation of sexual selection. Quarterly Review of Biology, 67, 437–456. attempts to claim the thought processes of Darwin’s equally bril- Clutton-Brock, T. H. & Parker, G. A. 1995. Sexual coercion in animal societies. Animal Behaviour, 49, 1345–1365. liant contemporary John Stuart Mill). Thus, trying to say whether Clutton-Brock, T. H., Hodge, S. J., Spong, G., Russell, A. F., Jordan, N. R., Darwin got it right or wrong on sexual selection is a bit like trying to Bennett, N. C. & Manser, M. B. 2006. Intrasexual competition and sexual claim Darwin for religion or atheism: you pay your money and take selection in cooperative meerkats. Nature, 444, 1065–1068. Cronin, H. 1992. The Ant and the Peacock. Cambridge: Cambridge University Press. your choice (of quotations). Dall, S. R. X., McNamara, J. M., Wedell, N. & Hosken, D. J. 2006. Debating sexual selection and mating strategies. Science, 312, 689. Do We Need a New Sexual Selection? Darwin, C. 1859. The Origin of Species. London: J. Murray. Darwin, C. 1871. The Descent of Man. London: J. Murray. Davies, N. B. 1991. Mating systems. In: Behavioural Ecology: An Evolutionary Do we need sexual selection version 2.0? Given the fall and rise Approach (Ed. by J. R. Krebs & N. B. Davies), pp. 263–294, 3rd edn. Oxford: of the popularity of intersexual selection since Darwin (Andersson Blackwell. 1994), the discovery of postcopulatory sexual selection (Parker Davies, N. B. 1992. Dunnock Behaviour and Social Evolution. Oxford: Oxford University Press. 1970; Eberhard 1996), the change in our understanding of the role Desmond, A. & Moore, J. 2009. Darwin’s Sacred Cause: Race, Slavery and the Quest females more typically play in mating systems (Reynolds 1996; for Human Origins. London: Allen Lane. Clutton-Brock 2009), and a broader appreciation of sexual conflict DuVal, E. H. 2007. Social organization and variation in cooperative alliances among male lance-tailed manakins. Animal Behaviour, 73, 391–401. (Arnqvist & Rowe 2005), it is clear that we are already well past Eberhard, W. G. 1996. Female Control: Sexual Selection by Cryptic Female Choice. version 2.0. But do we need a fundamental redefining of sexual Princeton, New Jersey: Princeton University Press. selection? I argue not. All of these discoveries change our under- Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–223. standing of when and through what mechanism sexual selection Endler, J. A. 1986. Natural Selection in the Wild. Princeton, New Jersey: Princeton might be said to act on individuals (we know there are more ways University Press. for individuals to compete for mates than Darwin did), but they do Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon Press. Gavrilets, S., Arnqvist, G. & Friberg, U. 2001. The evolution of female mate choice not change (or demand a change of) the fundamental definition of by sexual conflict. Proceedings of the Royal Society B, 268, 531–539. sexual selection. Studying the behavioural underpinnings of sexual Grafen, A. 1987. Measuring sexual selection: why bother? In: Sexual Selection: selection has revealed endless forms of reproductive diversity, Testing the Alternatives (Ed. by J. W. Bradbury & M. B. Andersson), pp. 263–294. a diversity we are still only at the beginning of trying to come to New York: J. Wiley. Gwynne, D. T. & Simmons, L. W. 1990. Experimental reversal of courtship roles in terms with. The fact that traits are, in phenotypic terms, both an insect. Nature, 346, 172–174. naturally and sexually selected, and that the evolution of traits Haley, M. P., Deutsch, C. J. & Le Boeuf, B. J. 1994. Size, dominance and copulatory associated with the mating system feed back into the evolutionary success in male northern elephant seals, Mirounga angustirostris. Animal Behaviour, 48, 1249–1260. mix, means that disentangling these selection pressures can be Holland, B. & Rice, W. R. 1998. Perspective: chase-away sexual selection: antago- a formidable task (indeed one worth avoiding if one is only inter- nistic seduction versus resistance. Evolution, 52, 1–7. ested in the population genetic consequences of evolution). Houston, A. I., Szekely, T. & McNamara, J. M. 2005. Conflict between parents over care. Trends in Ecology & Evolution, 30, 33–38. However, the conceptual structure we have inherited from Darwin, Johnstone, R. A. & Hinde, C. A. 2006. Negotiation over offspring care: how should with a few adjustments here and there, is strong in its simplicity parents respond to each other’s efforts? Behavioral Ecology, 5, 818–827.

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Animal Behaviour xxx (2010) 1–6

Contents lists available at ScienceDirect

Animal Behaviour

journal homepage: www.elsevier.com/locate/anbehav

Forum Final response: sexual selection needs an alternative

Joan Roughgarden a,*, Erol Akçay b,1 a Department of Biology, Stanford University b National Institute for Mathematical and Biological Synthesis, University of Tennessee article info

Article history: Received 20 November 2009 Initial acceptance 30 November 2009 Final acceptance 14 December 2009 Available online xxx MS. number: 09-00740

Keywords: behavioural ecology competition density dependence game theory genial gene mating systems theory Nash bargaining solution selfish gene sexual selection social selection

Shuker (in this issue) enumerates five points and we organize is understood as the product of fertility with survival. Conferring our response accordingly. a higher fitness by this definition is sufficient for a gene to fix in the First, we agree that sexual selection (and social selection) are gene pool without reference to competition for resources. A higher subsets of natural selection, and therefore share the same logical fitness could be attained with higher efficiency under unlimited framework of natural selection. We do not agree that natural resources. selection is ‘driven by competition, be it competition for resources To say that natural selection is always driven by competition or competition to avoid death, as ultimately something limits widens the meaning of competition beyond common usage in population growth’. It is true that in Chapter 3 of The Origin of ecology. For example, the colonization phase of community Species, Darwin (1859) wrote of natural selection as a struggle for succession, which lacks competition, is distinguished from the existence caused by resource limitation, as ‘the doctrine of Malthus climax phase in which competition occurs. Similarly, the r-selection applied with manifold force to the whole animal and vegetable phase of population dynamics during density-dependent evolution kingdoms’ (page 63), and wrote, ‘There is no exception to the rule involves natural selection for efficiency and productivity whereas that every organic being naturally increases at so high a rate, that if the K-selection phase involves natural selection resulting from not destroyed, the earth would soon be covered by the progeny of competition. To be sure, evolutionary writers sometimes view all a single pair’ (page 64). This framing of natural selection as natural selection as resulting from competition regardless of resulting from resource competition was superseded by the neo-- whether resources are limiting. Bell (2008, page 15), for example, Darwinian formulation of early population genetics in which fitness refers to ‘competition’ as occurring when ‘variants with greater exponential growth rates are selected’ during density-independent population growth (i.e. during r-selection), saying that ‘the nature * Correspondence: J. Roughgarden, Department of Biology, Stanford University, of competition changes’ when the population dynamics transition Stanford, CA 94305, U.S.A. from density-independent selection to density-dependent selec- E-mail address: [email protected] (J. Roughgarden). 1 E. Akçay is at the National Institute for Mathematical and Biological Synthesis, tion (i.e. from r-selection to K-selection). We do not consider University of Tennessee, Knoxville, TN 37996, U.S.A. r-selection, that is, differential density-independent growth, as

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2 J. Roughgarden, E. Akçay / Animal Behaviour xxx (2010) 1–6

‘competition’. If competition and natural selection are synony- of males fighting with one another for access to and/or control of mized, saying that competition ‘drives’ natural selection is empir- females, of females choosing males whose good genes are revealed ically meaningless because this is then true by definition and could though displays, ornaments or armaments, and of an evolutionary not be falsified, and moreover imparts the ideological connotation rationale for such behaviours that traces to sperm being cheap and that competition enjoys a logical priority and universality in bio- eggs expensive. Most biologists are then surprised to hear that this logical evolution. Instead, competition for resources, that is, archetypal narrative may often be incorrect, and they are especially crowding in the original Darwinian and Malthusian sense, is merely surprised when an archetypal example such as the peacock needs one of many mechanisms that can cause natural selection, and it is reinterpretation. Shuker relegates this archetypal sexual selection not always present. Even though natural selection is indeed ubiq- narrative to the domain of ‘mating systems theory’, many parts of uitous, it does not follow that competition is ubiquitous too, and in which Shuker allows ‘could be wrong’ and which he also particular, it does not follow that competition for mates is ubiqui- acknowledges show a ‘lack of experimental work’. He states further tous either. that, ‘clearly our grasp of mating systems is not as complete as we Second, we agree that what Shuker terms ‘mating systems perhaps thought’. But relocating the archetypal narrative of sexual theory’ is not the same as sexual selection itself. We recognize selection to mating systems theory so that its failure can be dis- a distinction between core and peripheral issues pertaining to missed as having ‘no effect at all on the logical basis of sexual sexual selection by referring to a ‘central narrative’ within the selection’ is evasive, or as Shuker himself recognizes, very ‘conve- sexual selection ‘system’ of theories. Our terminology draws nient’. If one is serious about placing mating systems theory, attention to the logical connections among these theories. Mating including the archetypal narrative of sexual selection, at arms systems theories expand upon the sexual selection narrative and length from ‘core’ sexual selection, then textbook writers and other sexual selection theory relies on mating systems theory to make decision makers who influence biology curricula worldwide should concrete predictions. Take, for example, extrapair copulation (EPC). be informed so that the present widely taught accounts of sexual By any definition of core sexual selection, the explanation of EPCs selection can be revised. lies beyond the core. If one views the core of sexual selection as We do not feel strongly about how sexual selection is defined, being about females selecting males for good genes, then EPCs provided that the definition allows sexual selection to be falsified follow logically as a tactic for females to secure a genetic upgrade with data and acknowledges that alternatives exist. We object over their pair male. So, failure to confirm that extrapair males have when the definition is slippery, infinitely malleable, and continually better genes than pair males reflects back on the truth of core revised in light of contrary data, making the theory unfalsifiable. In sexual selection that was the premise from which this particular our own work, we typically employ a definition of the ‘central EPC theory was derived. Such a failure to confirm would at least narrative’ that is closer to Darwin’s original statement than is provoke a restatement of what can be derived from the core Shuker’s definition, namely, that sexual selection is ‘Natural selec- specifically concerning EPC, and if many such theories were found tion from differences in mating success. Males compete for mating to be unconfirmed, a reexamination of the truth of core sexual opportunities, females are a ‘limiting resource’ for males, and selection. The point is, any definition of core sexual selection is females choose males for genes’ (Roughgarden, 2009, Table 1, page logically connected to the peripheral theories pertaining to it, 62). We argue that sexual selection in this sense does not occur, and including all of mating systems theory as well as many other issues we accept Shuker’s observation that ‘the criticisms of Roughgarden such as the evolution of anisogamy (cf. Roughgarden 2009, Table and colleagues lead more to mating systems theory than they do to 19, pp. 237–238), all of which unite as one of evolutionary biology’s sexual selection per se’, according to his definition. In this light, the master narratives. Thus, sexual selection and mating systems reservations Shuker has expressed about the correctness of theory are logically interdependent, and falsifying either of these present-day mating systems theory are an important concession. components within the sexual selection system has repercussions Still, for the present exchange we are happy to work with Shuker’s for the other components. broad definition of sexual selection, namely, as any selection Shuker defines core sexual selection as ‘the selection of traits resulting from competition for mates, which we do accept as associated with competition for mates’. Moreover, he defines concrete and falsifiable. However, by this definition too, the a mate as ‘a reproductive partner with which one or more zygotes evidence for sexual selection is weak, as discussed further in point are formed’ thereby ruling out the ample variety of known same- five below. sex matings, even though same-sex matings might carry out the Third, we disagree with the claim that ‘the action of sexual same social functions as between-sex matings. This definition selection is unaffected by whether the behavioural interactions allows that much sexual activity, both hetero- and homosexual is between mating partners during reproductive episodes are not about mating, and is not part of mating systems theory, but of considered cooperative or selfish’. By the letter of Shuker’s own some other topic, such as the emerging subject area of animal definition of sexual selection, namely selection associated with friendships. Moreover, as stated, Shuker’s definition refers solely to competition for mates, if the interactions between potential or behaviour. However, Shuker also requires that the traits involved actual mates are anything other than competitive, say cooperative, must be heritable, and Shuker describes ‘sexual selection as then manifestly, sexual selection is not taking place. a component of an overall natural selection process, and inclusive Still, the text of Shuker’s comment dwells on what he feels is the of both selection and heredity’. We agree that sexual selection importance of competitive game theory in behavioural ecology and pertains to behaviour with evolutionary consequence, and not to the sufficiency of Maynard Smith’s (1982) evolutionarily stable the behavioural act of mate selection itself. strategy (ESS) concept in particular. He also remarks that our Shuker considers that his definition of sexual selection ‘repre- alternative modelling framework pertains to ‘the evolution of sents the consensus among evolutionary biologists of what sexual parental care, not sexual selection at all’, and as such is banished to selection is’. We think this perception of consensus requires careful the hinterland of mating systems theory. picking of the sample population. In our experience, most biolo- We suspect the discussion here is at crossed purposes. Our gists, including evolutionary biologists, together with present and position is that sexual selection theory misconceptualizes the former biology students, not to mention social scientists such as reproductive process. Sexual selection focuses entirely on mating, evolutionary psychologists and anthropologists, think of a specific both the act of mating and the identity of the mating partner, and narrative when queried about what sexual selection is. They think relegates what happens next to a distinct topic of ‘parental care’.

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Instead, we focus on the integrated and indivisible social process ‘mating systems theory’. Hence, sex role-reversed species are now, that yields offspring who are counted in the next generation. by fiat, no longer problematic for sexual selection itself, because Mating is an instrumental part of this process, perhaps not so much either sex can do anything and still count as sexual selection so long because of the exchange of gametes, but because of the social bonds as competition for mates is taking place. But, as Shuker notes, that mating and other affiliative behaviour produces. In the social Darwin (1871) prescribed male and female sex roles in a ‘tradi- selection perspective, courtship and mating behaviour are part of tional’ way, as near-universal generalizations (‘with the rarest of an extended view of how parental and social investments are exceptions’). Shuker notes too that ‘behavioural ecologists may allocated. And a reproductive social group, from a monogamous seem to drop by default into assuming that sexual selection pair to an extended family, is a ‘firm’ whose product is offspring. comprises ‘male–male competition’ and ‘female choice’’, although We have further argued that a theory of social selection must the cognoscenti are assumed never to commit this ‘stupid’ error, to depart from the game-theoretical framing introduced by Maynard quote Shuker’s adjective. Still, many leaders in behavioural ecology, Smith (1982) because we need to introduce a wider variety of now and in the past, continually adopt the cheap-sperm/expensive- game-theoretical solution concepts than that corresponding to the egg narrative as integral to sexual selection, as even a contributor to ESS because we think the ESS is not sufficient. We feel the most this Forum exchange illustrates. convenient taxonomy of solution concepts distinguishes what we The step from assuming that sperm are cheap and eggs expen- have termed competitive game theory from cooperative game sive to concluding that males are naturally promiscuous and theory, as illustrated by the distinction between playing chess females naturally choosey is quickly taken, inviting the hasty where the players cannot communicate and playing monopoly dismissal of copious exceptions. Although a solely competition- where the players can communicate to make deals. We do not deny for-mates definition of sexual selection is not challenged by sex that others might prefer other taxonomies. All in all, we advocate role-reversed species, the many narratives that incorporate the the wider use of game theory. cheap-sperm/expensive-egg premise are challenged. In sex role- One of the new solution concepts that seems interesting with reversed pipefish, males make sperm each of which is much smaller respect to intimate animal friendships, including both within- and than an egg, and yet they provide the parental care, and may between-sex pair bonds, is the Nash bargaining solution (NBS). therefore be in the better bargaining position relative to females None the less, we freely use competitive solution concepts as who are seeking partners to care for their eggs. Thus, gamete size appropriate. For example, we envision parents who, as ‘owners’ of does not predict or explain sex role. Therefore, even if sexual a firm (or ‘conglomerate’, Groves 1973) that produces offspring, set selection is defined to remain intact in the face of sex role-reversed incentives for offspring participation as helpers in the group’s species, a central tenet of commonly taught sexual selection reproductive activity: an approach consistent with, and synthe- narratives is false, and, instead, one cannot derive sex role from sizing, Alexander’s (1974) view of parental control, Vehrencamp’s gamete size. We would applaud any systematic effort to publicize (1983) concept of staying incentive, as well as extensions to skew the disconnect between sexual selection and sex roles, so that even theory such as social queuing (Kokko & Johnstone 1999) and if sexual selection does turn out to occur, it cannot be used to parental imposition of costs (Crespi & Ragsdale 2000). The offspring naturalize traditional sex roles, which brings us to the last point. serve as members of their parent’s reproductive firm because each Fifth, we disagree that compelling evidence presently exists for maximizes its own fitness by doing so, which represents a nonco- sexual selection in nature. We accept that sufficient (although not operative solution, given that the parent can set the incentive necessary) conditions for sexual selection not to occur in a pop- structure. Accomplishing the introduction of a wider array of ulation are (1) that ‘all partners are of equal [genetic] quality’, or (2) solution concepts requires splitting the modelling into two tiers, as that the outcome of mate selection is that ‘successful partnerships compared with the original single population-genetic tier formu- represent a random sample of pairs of individual phenotypes (and lation of Maynard Smith because these other solution concepts do thus genotypes)’. By these very criteria, the existing empirical case not arise in gene-pool dynamics. for sexual selection is lacking. We have stated many times that an apparently cooperative The paradox of the lek pertains precisely to the question of outcome can indeed be achieved with solely competitive dynamics, whether all partners are of equal genetic quality. In the absence of as illustrated by the division of space into territories through an external source to resupply continually the bad genes in males competitive engagements between neighbours (e.g. Roughgarden that female choice is supposedly pruning every generation, all 2009, pp. 151–154). But are all cooperative outcomes the result of males wind up genetically equal in fitness, thereby defeating the competitive dynamics? Animal friendships, and the evolution of value of continued female choice. Although untested proposals other-regarding preferences, raise the possibility that cooperative exist for mechanisms that might generate an endless supply of bad outcomes can also be realized through cooperative means. We have genes to merit making it worthwhile for females to continue proposed the NBS as a possible criterion to predict the outcome of screening males for genetic quality, the evidence argues that males a cooperative path to a cooperative end. And we can only take are in fact of equal genetic quality. The 24-year collared flycatcher advantage of an extended set of solution concepts when we study on Gotland Island in Sweden by Qvarnstro¨m et al. (2006) consider the possibility that social-behavioural dynamics do not shows exactly what is expected if the paradox of the lek is indeed march in lock step with gene-pool dynamics because these are true. Fitness differences between male collared flycatchers are not governed solely by the ESS. heritable, even though the badge size is heritable, so it is a waste of We respect that insect ecologists find animal negotiations more time for females to bother selecting males on the basis of badges in implausible for insects than, say, for vertebrates. Still, many have hopes of endowing their sons with fitness-enhancing good genes. witnessed intimate contact between insects, and we are not aware And these investigators in fact found that female choice for badge that the possibility of friendships has been investigated in insects, size had nothing to do with genetic quality. Hence there is no sexual especially today, when sexual conflict is so much in vogue. selection in collared flycatchers by Shuker’s criterion. Fourth, we agree that whether sexual selection exists ‘does not Instead, Shuker offers the interesting study on male guppies by depend on what ‘roles’ the different reproductive classes (mating Brooks & Endler (2001) as a clear-cut case establishing the reality of types or sexes) take during reproductive interactions’, assuming, sexual selection: ‘Male guppies have pigmentation that influences that is, that sexual selection is defined solely as competition for their success in mate competition. Male guppies have heritable mates. The question of who competes for whom is then relegated to differences in pigmentation. [Therefore,] There is sexual selection

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4 J. Roughgarden, E. Akçay / Animal Behaviour xxx (2010) 1–6 in guppies’. QED? Invoking this ‘Darwinian syllogism’ would seem theory’ is useless when the specifics all claim to derive their to settle the matter. But is mating success the same as fitness, in legitimacy from the narratives of sexual selection. Getting the nature or the laboratory? Do the attractively ornamented males in explanations of social behaviour right inevitably requires deter- nature reliably leave more offspring in the next generation than the mining whether sexual selection itself is true: always, often, rarely unattractive males, thereby offering grounds for females to choose or never. attractive males as mates to acquire their good genes? If not, then The comparison with density dependence is instructive. Ecolo- sexual selection is absent by Shuker’s criterion. Brooks & Endler gists do not assume that density dependence inevitably exists. They present data solely on attractiveness and mating success in the once did, but not now. During the 1950s and later, Andrewartha & laboratory, not on fitness itself in natural populations. So we do not Birch (1954, cf. Ehrlich & Birch 1967) explored mechanisms for the know whether the ornamented males differ in genetic fitness from density-independent persistence of a population. Now, for anyone the unornamented males. Compare with the collared flycatcher studying population regulation, a necessary first step is to reject case. In this species too, the background information seemed a density-independent null hypothesis, prior to fitting a density- clearly to implicate sexual selection in maintaining the male dependent model such as a logistic or Ricker equation. Alterna- ornament. Yet, sexual selection was absent, after all. The male tively, a population might in fact not possess any effective density guppy case, while possibly offering an example of sexual selection, dependence, such as marine populations with no detectable stock is not conclusive, and the continuing failure of sexual selection’s recruitment relation or butterfly populations whose abundance other poster-child species to withstand scrutiny invites scepticism always remains too low to effect defoliation and whose annual here too. fluctuations in abundance depend on diapause rates controlled It has been argued to us that ‘whether or not attractive males only by the timing of the winter’s final rainfall. Similarly, commu- have high fitness in terms of fitness components outside of repro- nity ecology in the 1980s saw the beginnings of ‘neutral theory’ ductive competition can be irrelevant to the action of sexual (Hubbell & Foster 1986; cf. Hubbell 2001) that has been effective in selection’. No. According to sexual selection, female choice is accounting for community patterns in Panamanian rainforest as an supposed to use the ornament to identify males with whose genes alternative to the earlier ‘community matrix’ species-interactive she should endow her sons. If some genes promote mating success view of community structure from MacArthur & Levins (1967) and at a cost to other fitness components resulting in no net fitness Hutchinson (1959). And even natural selection has genetic drift as advantage, then seeking out such males as mates is pointless. A its principal alternative hypothesis. marker for those genes should be selectively neutral. What about sexual selection? Where is the alternative? A null Shuker also mentions the interesting recent study by Rogers & model for the reproductive skew expected by a Poisson process of Greig (2009) of mate competition in yeast, an isogamous species. mate selection has been presented by Sutherland (1985) and These investigators set up an experimental scheme in the labora- Hubbell & Johnson (1987). By and large though, no extensive alter- tory whereby a gene conferring success in mate competition could native hypothesis exists for sexual selection that potentially evolve to fixation. Yet the authors clearly discuss morphological matches its scope ranging from core sexual selection through its and cellular mechanisms that minimize sexual selection in nature, derivative mating systems theories. Sexual selection needs to be and their innovative experimental set-up circumvents these tested against a fully fledged alternative before it can be accepted as obstacles. Although the experimental set-up that results is likely to having been demonstrated. We anticipate that sexual selection be a valuable tool to test evolutionary hypotheses, the evidence for cannot withstand such a test based on our reading of the evidence sexual selection in nature remains inconclusive. so far. For those who already accept sexual selection, the available Shuker’s second criterion for the absence of sexual selection is data seem to fall nicely into place, whereas through the eyes of those that successful partnerships represent a random sample of genetic who still need to be convinced, the case is far from compelling. pairings. This situation results when the bad genes consist of We applaud Shuker for stating, at last, that the premises of accumulated weakly deleterious mutations. Byers & Waits (2006) sexual selection are indeed ‘refutable’ even though he defines assert that mating behaviour in pronghorn antelopes demonstrates sexual selection so as to be at a seemingly safe distance from data selection for good genes because female choice of male prowess that might contradict it. We have received mixed messages from supposedly weeds out males who have accumulated a load of sexual selection advocates in regard to the falsifiability of sexual weakly deleterious mutations. But the fitness difference between selection. Shuker, like other participants in this Forum exchange, a genetically good male and a genetically bad male is less than 1%, often writes as though sexual selection is simply inevitable, and according to population-genetic theory for how weakly deleterious that the task of field research is to show how sexual selection is genes accumulate. (cf. Roughgarden 2009, pp. 51–54.) This differ- playing out in various species and ecological circumstances. To the ence is surely undetectable by females in any conceivable natural contrary, we continue to point out that sexual selection, even in the setting. Therefore, mating pairs of antelopes probably represent broad definition that Shuker prefers, is still undemonstrated, and random pairings with respect to their genetic quality, rendering the mating systems theory that derives from sexual selection’s sexual selection absent according to Shuker’s second criterion. definition keeps running afoul of the data. Byers & Waits’s conclusion which states, in effect, that sexual Finally, we have been asked to comment on the studies of selection endows all species with a natural system of eugenics to Andersson (1994) and Hoekstra et al. (2001) that summarize weed out bad genes is unwarranted by the evidence they supply. positive evidence for sexual selection. Accordingly, we hope it does In conclusion, Shuker asks why sexual selection should be not seem churlish to criticize work that was state-of-the-art when ‘singled out for being overly broad’? He writes, ‘If we look for the truth of sexual selection was not being challenged and the task similar examples in ecology, do we find that the concept of density was to consolidate the available information that seemed to dependence is too broad and therefore meaningless because of the confirm sexual selection. In the present context, however, these almost innumerable ways in which it can be manifested? Sexual summaries are insufficient as evidence that sexual selection exists selection, like density dependence, may encompass a lot of or is widespread. processes but the logic is simple and its premises are refutable’. We Andersson reports that his survey of 232 species from studies up single out sexual selection because it is logically central to an entire to 1990 found 186 species that showed a ‘statistical relationship system of explanation for animal social behaviour. Challenging between some character and mating success’, including traits such dubious specifics within what Shuker terms ‘mating systems as ‘song and display, body size, visual ornaments, and territory or

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J. Roughgarden, E. Akçay / Animal Behaviour xxx (2010) 1–6 5 other resources’ (Andersson & Iwasa 1996, page 56). Andersson also females are not choosing males because of those genes: the reports that this mating success results from ‘female choice’ for correlation is incidental to what is actually happening, which is such traits in 167 species and from ‘male contests’ in 58 species. female choice of safe egg-laying sites. This is not sexual selection Two difficulties prevent our regarding this summary as conclusive, because the female is not choosing the male, but is choosing egg- difficulties acknowledged by Andersson himself, but that seem laying sites, nor is it competition between males for mates, but more significant in the present context than previously. simply natural selection for signalling clarity. First, Andersson notes that ‘studies vary in their criteria for Thus, we respect the positive evidence for sexual selection mating success; some do not follow success to copulation. Least summarized by Andersson (1994) and Hoekstra et al. (2001), among complete in this respect are the tests that measure female attrac- others, but do not find it compelling. As a counterpoint to their tion to isolated male traits, for instance loudspeaker tests broad- positive evidence, we emphasize the growing number of exceptions casting natural or synthetic calls’ (Anderson 1994, page 124). and discrepancies to sexual selection’s predictions. Citing only Females can be attracted to males for social reasons other than positive information on behalf of sexual selection is picking the copulation, such as protection, foraging efficiency and thermoreg- literature with as much bias as picking only negative information ulation, and therefore some unknown number of studies observed would be. A future research programme should test sexual selection social attraction and not mating success. against alternatives, not seek merely to confirm sexual selection. Second, Andersson comments that ‘Mating is far from synony- In ecology, when alternatives to dominant theories have been mous with fertilization. genetic analysis of paternity is therefore called for in the past, the prevailing opinion was as confident as desirable to ensure that mate attraction and copulation are reflec- today’s is for the generality of sexual selection. In the 1950s density ted in production of offspring; few studies have yet done so’ dependence was thought to be inevitable and ubiquitous, in the (Andersson 1994, page 124). Andersson continues with an impor- 1960s the limiting similarity between adjacent niches in niche tant further quotation, ‘even a measure of success based on fertil- space was thought to underlie community structure, and in the ization is incomplete: what happens to offspring before or at 1970s benthic species interactions rather than pelagic larval- adulthood may depend strongly on rearing conditions and recruitment processes were thought to determine marine pop- phenotypic or genetic aspects of the parents’. These postmating ulation and community dynamics. Today the consensus has shifted considerations lie in the area of parental care, a topic Shuker places on these topics in population and community ecology. We do not in mating systems theory, not sexual selection. From our perspec- know whether the consensus will similarly shift on the inevitability tive, these offspring-raising considerations are precisely what and generality of sexual selection in behavioural ecology, and we social selection theory emphasizes: the formation of social groups will never know unless the need for alternative theories is recog- that act as firms to produce offspring. By our theory, mating per se nized, and alternatives developed and tested. Therefore, we may be a small, although instrumental, component of the overall continue to point out grounds for suspecting that sexual selection reproductive process. Thus, Andersson conceptualizes ‘mating will never be substantiated in nature. And we continue to develop success’ as including what we would consider as part of social and to offer alternative framings and formulations for reproductive selection, namely all activities that lead to increasing the number social behaviour in place of sexual selection and its corollaries and (rather than the genetic quality) of offspring raised. Hence, extensions. evidence Andersson regards as favouring sexual selection might be We offer no further response to Clutton-Brock (in this issue) and mixed in with evidence that actually supports social selection. Carranza (in this issue). Hoekstra et al. (2001) provide a quantitative database of selec- tion gradients in the wild that indicate correlations between We thank Noa Pinter-Wollman and Zhiyuan Song for valuable mating success and various traits. They report that ‘Sexual selection comments on the draft of this response. A reviewer’s comments led (measured by mating success) appeared stronger than viability to some clarifications. We also thank the editors of Animal Behav- selection (measured by survival)’ (page 9157). iour, Louise Barrett and Angela Turner, for their time, care and As in Andersson’s (1994) compilation, the first difficulty is that impartiality in supervising this exchange in what is often a painful the term ‘mating success’ includes a variety of variables such as dispute. E.A. is a postdoctoral fellow at the National Institute for pairing date, territory tenure or number of pollen per flower. Some Mathematical and Biological Synthesis (NIMBioS), an Institute of these variables are likely to be more related to other aspects of sponsored by the National Science Foundation, the U.S. Department the breeding system, such as parental care, and thus not be of Homeland Security, and the U.S. Department of Agriculture representative of sexual selection (competition for mates) but of through NSF Award number EF-0832858, with additional support social selection (behaviour to maximize number of offspring). from The University of Tennessee, Knoxville. A second difficulty lies in assuming that mating success is the main determinant of fitness. As before, one might find that some References trait such as, say, red colour in males is correlated with higher mating success of males. However, the same trait might be negatively Andersson, M. 1994. Sexual Selection. Princeton, New Jersey: Princeton University correlated with the male’s survival, or with the survival of the Press. 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Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution, 55, 1002–1015. such locations will sire offspring because females choose to lay eggs Byers, J. A. & Waits, L. 2006. Good genes sexual selection in nature. Proceedings of at the locations these males specify. So genes evolve in males to the National Academy of Sciences, U.S.A., 103, 16343–16345. improve signalling clarity, thereby hitchhiking on female choice for Carranza J. Sexual selection and the evolution of evolutionary theories. Animal Behaviour, in this issue, doi:10.1016/j.anbehav.2009.08.010. safe egg-laying sites. Males with such genes will then appear to Clutton-Brock, T. We do not need a sexual selection 2.0 – nor a theory of genial enjoy a higher mating success than ineffective signallers, but the selection. Animal Behaviour, in this issue, doi:10.1016/j.anbehav.2009.10.018.

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