Sexual Selection and Mating Systems: Competition, Choice and the Evolution of Reproductive Strategies

Topic: Animal Behaviour & Ethology Subject: Sexual Selection, Mate Choice, and Mating Systems Last verified: 2026-09-23

Why does a male long-tailed widowbird carry a tail around half a metre long, why do peacocks display trains covered in eyespots, and why, in some pipefish, is it the males that become pregnant while the females compete for mates? Charles Darwin's answer, set out in 1871, was sexual selection: a form of selection that "depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction" [Darwin 1871]. Over the following century and a half, biologists have tested how competition for mates and choice of mates shape bodies and behaviour. Field experiments have shown female preferences at work, genetic studies have revealed that many apparently faithful pairs are not genetically monogamous, and comparative work across the animal kingdom has confirmed that sexual selection is usually, though not always, stronger in males [Andersson 1982; Griffith et al. 2002; Janicke et al. 2016].

This article traces the idea from Darwin through Bateman's fruit-fly experiments and Trivers's theory of parental investment, including the modern re-analyses that challenged and then refined them. It then looks at experimental tests of female choice, the ecological classification of mating systems, extra-pair paternity, sex-role reversal, sperm competition and the remarkable genetics of alternative male tactics in the ruff. It closes with the practical relevance of sexual selection for conservation and wildlife management.

Darwin's Two Forces: Competition and Choice

Darwin introduced sexual selection in The Descent of Man, and Selection in Relation to Sex to explain traits that seemed hard to account for by survival alone. He separated it from natural selection: when the sexes differ in structure because of different habits of life, or in the organs used to nourish and protect the young, those differences could be explained by ordinary natural selection. Sexual selection, by contrast, concerned the advantage some individuals gain over rivals of the same sex and species purely in obtaining mates and reproducing [Darwin 1871].

Researchers now usually divide sexual selection into two broad processes that follow Darwin's framework. Intrasexual selection arises from competition between members of one sex, typically males, for access to the other. It favours weapons, large body size and fighting ability, and is closely connected to the contest behaviour described in our article on dominance hierarchies. Intersexual selection arises when members of one sex, typically females, choose among potential partners. It favours ornaments and displays that make an individual more attractive [Darwin 1871; Andersson 1982]. Female choice was long harder to demonstrate: introducing his own field experiment more than a century after Darwin, Malte Andersson noted that the hypothesis was theoretically plausible but that there was still little experimental field evidence that such preferences existed [Andersson 1982].

Why Males Usually Compete: Bateman, Trivers and Their Critics

The first influential attempt to explain why sexual selection usually acts more strongly on males came from the geneticist Angus Bateman. Working with small populations of the fruit fly Drosophila melanogaster in which each fly carried a different dominant genetic marker, he inferred parentage from the offspring and concluded that the contribution of males to the next generation was more variable than that of females [Bateman 1948]. He attributed this to the greater dependence of male fertility on the frequency of insemination, that is, on how many times a male mated [Bateman 1948]. Bateman linked this directly to the primary difference between the sexes, the production of large, immobile eggs versus small, mobile sperm produced in great excess. He argued that it explained what he called "an undiscriminating eagerness in the males and a discriminating passivity in the females" [Bateman 1948].

Robert Trivers extended the argument in 1972 by shifting the focus from gametes to parental investment, defined as any investment by a parent in an individual offspring that increases that offspring's chance of surviving, and hence of reproducing, at the cost of the parent's ability to invest in other offspring [Trivers 1972]. Trivers proposed that the relative investment of the two sexes governs how sexual selection operates. The sex that invests more becomes a limiting resource for the other, and members of the sex that invests less compete among themselves for access to it [Trivers 1972]. Because in most species females invest more, through larger gametes and often more parental care, this predicts the familiar pattern of competitive males and choosy females, but it also predicts that the pattern should reverse when males invest more [Trivers 1972].

Bateman's study later came under close scrutiny. Zuleyma Tang-Martinez and Brandt Ryder re-examined the 1948 paper in detail, including its methodological problems. They argued that an over-reliance on Bateman's predictions had slowed recognition of male mate choice and sperm allocation, of the role of females in initiating extra-pair copulations, and of evidence that females in lekking species may commonly mate with more than one male [Tang-Martinez & Ryder 2005]. Patricia Adair Gowaty and colleagues then repeated Bateman's experiment using his own parentage methods. They found that double-mutant offspring, which Bateman had used to count mates, had reduced viability. As a result, his method overestimated the number of flies with no mates, underestimated those with one or more mates, and produced systematically biased estimates of offspring number by sex. The authors concluded that Bateman's methodology had mismeasured the fitness variances on which his conclusions rested [Gowaty et al. 2012].

These critiques did not settle the matter. The quantity Bateman described, the relationship between the number of mates and the number of offspring, is now known as the Bateman gradient and is measured with modern genetic parentage methods rather than visible markers [Jones et al. 2000]. Tim Janicke and colleagues compiled standard Bateman metrics across the animal kingdom in a meta-analysis. They found that sexual selection was indeed stronger in males than in females, and that it was evolutionarily tied to sex biases in parental care and in sexual dimorphism [Janicke et al. 2016]. The authors presented this as the first comprehensive evidence supporting Darwin's concept of conventional sex roles, and as a refutation of recent criticism of sexual selection theory [Janicke et al. 2016]. The modern picture is therefore more nuanced than the 1948 paper, which had real methodological flaws, but the broad Darwin–Bateman–Trivers pattern has held up when tested with better data [Gowaty et al. 2012; Janicke et al. 2016].

Testing Female Choice: Widowbirds and Peacocks

The first clear field experiment on female choice came from Malte Andersson's study of the long-tailed widowbird (Euplectes progne) on the Kinangop plateau in Kenya, carried out between November 1981 and March 1982 [Andersson 1982]. Breeding males are black with a red wing patch and display over their grassland territories with tails around half a metre long, whereas females are mottled brown and short-tailed. Females build nests on males' territories and raise their young without help from the male [Andersson 1982]. Andersson arranged 36 colour-ringed males into nine matched groups of four. In each group, one male's tail was cut to about 14 cm, and the removed feathers were glued onto a second male, lengthening his tail by an average of 25 cm. The other two males served as controls: one was only ringed, and the other had his tail cut and glued back together so that it stayed almost the same length [Andersson 1982].

Mating success was measured by counting new active nests on each territory after the treatment. Males with experimentally elongated tails attracted more new nests than control males, and males with shortened tails attracted the fewest [Andersson 1982]. Males with shortened tails held their territories as long as other males, so competition between males did not appear to explain the long tail. Andersson concluded that the extreme tail length is maintained by female mating preferences [Andersson 1982]. Because females preferred tails even longer than the natural ones, the result also fitted the idea proposed by Darwin and R.A. Fisher that ornaments stop growing only when their survival costs balance their mating advantage [Andersson 1982].

The peacock (Pavo cristatus) has a more complicated history. Marion Petrie, Tim Halliday and Carolyn Sanders studied a lek of ten males at Whipsnade Park in England. They found large differences in mating success between males, with the most successful male copulating 12 times and the least successful obtaining no copulations [Petrie et al. 1991]. More than half of the variation in mating success could be attributed to differences in train morphology, and the number of eyespots in a male's train was positively correlated with the number of females he mated with [Petrie et al. 1991]. However, Mariko Takahashi and colleagues studied a feral population of Indian peafowl in Japan over seven years and found no evidence that peahens preferred males with more elaborate trains, whether measured as more eyespots, a more symmetrical arrangement or greater length [Takahashi et al. 2008]. They concluded that the train is not the universal target of female choice and that females in their population were probably choosing on other cues [Takahashi et al. 2008]. The contrast illustrates that a preference found in one population cannot be assumed to hold in every population of the same species.

Why Choose? Handicaps and Parasites

If females prefer exaggerated ornaments, what do they gain? Amotz Zahavi proposed the handicap principle: characters that develop through mate preference impose a cost on the survival of their bearers, and that cost is what makes them useful to the choosing sex, because only high-quality individuals can afford them. The ornament therefore acts as a test of the quality of a potential mate [Zahavi 1975].

William Hamilton and Marlene Zuk offered a more specific version linked to disease. They combined seven surveys of blood parasites in North American passerine birds and found a weak but highly significant association across species between the incidence of chronic blood infections and striking display, measured as male brightness, female brightness and male song [Hamilton & Zuk 1982]. They proposed that ongoing evolutionary cycles between hosts and parasites keep genetic resistance heritable, and that animals choose mates for genetic disease resistance by examining traits whose full expression depends on health and vigour [Hamilton & Zuk 1982].

Ecology and the Classification of Mating Systems

Mating systems describe how many partners each sex typically has and how those partnerships are formed. In an influential 1977 paper, Stephen Emlen and Lewis Oring argued that ecology sets the stage. They introduced the idea of the environmental potential for polygamy, the degree to which the environment allows individuals of one sex to monopolise several mates, either directly or by controlling the resources that mates need [Emlen & Oring 1977]. That potential is high when resources or mates are clumped in space and when females become receptive at different times, and low when resources are evenly spread and females breed synchronously [Emlen & Oring 1977]. They also emphasised the operational sex ratio, the ratio of sexually active males to fertilisable females at a given time, as a predictor of the intensity of sexual selection [Emlen & Oring 1977].

On this basis Emlen and Oring classified mating systems into monogamy, several forms of polygyny and polyandry. Polygyny can arise when males defend resources that females need (resource defence polygyny), defend groups of females directly (female defence polygyny), or compete for mates in aggregations where females choose among them (male dominance polygyny, which includes leks) [Emlen & Oring 1977]. The framework shifted the study of mating systems from description towards explanation and remains the starting point for most comparative work [Emlen & Oring 1977].

Leks are the most extreme case of male dominance polygyny. Males gather at communal display sites and compete there for matings, while females visit and choose among them [Emlen & Oring 1977]. In the greater sage-grouse (Centrocercus urophasianus), Robert Gibson and Jack Bradbury found that male mating success was related to lek attendance, display rate and an acoustic component of the strut display, and that display rate and the acoustic component each had significant effects in multivariate analyses [Gibson & Bradbury 1985]. Mating success was not significantly related to territory size, proximity to the lek centre or body size [Gibson & Bradbury 1985]. Displays, not real estate, appeared to be what mattered to females.

Social and Genetic Monogamy

Many birds breed in pairs in which a male and a female raise young together, but molecular parentage testing has shown that this does not mean each pair's young share the same father. Simon Griffith, Ian Owens and Katherine Thuman reviewed more than 150 molecular genetic studies and concluded that birds are only very rarely sexually monogamous. Extra-pair offspring, young fathered by a male other than the social partner, were found in approximately 90% of species, and even among socially monogamous species more than 11% of offspring were, on average, the result of extra-pair paternity [Griffith et al. 2002]. The distinction between social monogamy (a pair that lives and breeds together) and genetic monogamy (all offspring sired by the social partner) is now standard [Griffith et al. 2002].

A later overview by Lyanne Brouwer and Simon Griffith drew on more than 500 studies reporting rates of extra-pair paternity in more than 300 bird species [Brouwer & Griffith 2019]. After accounting for phylogeny, they found no clear evidence that variation in extra-pair paternity across socially monogamous species was explained by broad factors such as latitude, breeding density, migration, generation length, dispersal distance or climatic variability [Brouwer & Griffith 2019]. They suggested that large variation within species makes species averages unreliable, and that particular behaviours and ecological conditions, such as breeding synchrony, may facilitate or constrain extra-pair mating in particular groups [Brouwer & Griffith 2019]. Extra-pair mating means that sexual selection continues to operate even in species that look monogamous, and that a male's apparent breeding success can differ from his genetic success [Griffith et al. 2002].

When the Roles Reverse

Trivers's theory predicts that when males invest more in offspring than females, the usual pattern should reverse, with females competing for mates and males choosing [Trivers 1972]. Emlen and Oring likewise treated polyandry, in which a female mates with several males, as a mating system with its own ecological conditions [Emlen & Oring 1977]. Pipefish and seahorses (family Syngnathidae), in which males carry the developing eggs, are a classic test of this prediction [Jones et al. 2000].

Adam Jones and colleagues used molecular parentage analysis in the broad-nosed pipefish (Syngnathus typhle), a species with male pregnancy. They found that females showed a stronger positive relationship between number of mates and number of offspring than males did, the reverse of Bateman's result in fruit flies [Jones et al. 2000]. The relationship also responded as predicted to changes in the adult sex ratio [Jones et al. 2000]. The authors concluded that the Bateman gradient, the link between mating success and offspring number, is a central feature of the genetic mating system that determines the strength and direction of sexual selection [Jones et al. 2000]. Sex-role-reversed species therefore do not contradict sexual selection theory. Instead, they show that what matters is the relative investment and mating opportunities of each sex, not whether an animal is male or female as such [Trivers 1972; Janicke et al. 2016].

After Mating: Sperm Competition and Alternative Tactics

Sexual selection does not stop once mating has happened. In a landmark 1970 review of insects, Geoff Parker described sperm competition, the competition within a single female between the sperm of two or more males to fertilise her eggs [Parker 1970]. Parker argued that when females mate with more than one male, selection will favour male adaptations that improve the chance of fertilising eggs in competition with rivals and that protect a male's own sperm from being displaced, such as mate guarding and mating plugs [Parker 1970]. Post-mating sexual selection is now studied across the animal kingdom, and relative testis size is widely used as an index of its intensity [Morrow & Pitcher 2003].

Competition among males can also produce several distinct ways of being male. The ruff (Calidris pugnax, formerly Philomachus pugnax), a lek-breeding wading bird, has three male morphs that coexist as a balanced polymorphism: aggressive "independents", semi-cooperative "satellites", and "faeders" that mimic females [Küpper et al. 2016]. The morphs differ greatly in body size, ornamentation and behaviour, and the differences are inherited [Küpper et al. 2016].

Two teams independently revealed the genetic basis in 2016. Clemens Küpper and colleagues showed that development into satellites and faeders is determined by a supergene: divergent, non-recombining, dominant versions of an inversion on chromosome 11 containing 125 predicted genes, while independents carry only the ancestral sequence [Küpper et al. 2016]. One breakpoint of the inversion disrupts an essential gene, CENP-N, and pedigree analysis confirmed that inheriting two copies of the inversion is lethal [Küpper et al. 2016]. Sangeet Lamichhaney and colleagues, using whole-genome sequencing, found that the Satellite and Faeder alleles are both associated with a 4.5-megabase inversion that arose about 3.8 million years ago. They proposed that the Satellite chromosome arose through a rare recombination event about 500,000 years ago [Lamichhaney et al. 2016]. Together, the studies show how a complex set of behavioural and physical differences can be inherited as a single unit when many genes are locked together within an inversion [Küpper et al. 2016; Lamichhaney et al. 2016].

Conservation and Wildlife Management Relevance

Sexual selection matters for conservation because it shapes which individuals breed and how populations respond to human pressure. Edward Morrow and Trevor Pitcher examined whether sexual selection was associated with extinction risk in 1,030 bird species [Morrow & Pitcher 2003]. They found no evidence that threatened species were distributed unevenly by social mating system, and neither sexual size dimorphism nor dichromatism was related to extinction risk after controlling for phylogeny. However, threatened species had larger testes, a measure of post-mating sexual selection, than non-threatened species, and this held after including body size in the analysis [Morrow & Pitcher 2003]. The authors suggested that sexual selection may be double-edged, promoting speciation on one hand but raising extinction risk on the other, while noting that the reasons were not yet clear [Morrow & Pitcher 2003].

Species that breed on leks can be sensitive to disturbance at their display sites. Jessica Blickley, Diane Blackwood and Gail Patricelli played recorded noise from natural gas drilling and roads at greater sage-grouse leks over three breeding seasons [Blickley et al. 2012]. Compared with paired control leks, peak male attendance fell by 29% at leks exposed to drilling noise and by 73% at leks exposed to road noise. Intermittent noise had a greater effect than continuous noise, and there was limited evidence for effects on female attendance [Blickley et al. 2012]. The authors concluded that sage-grouse avoid leks with anthropogenic noise, and that such noise is a threat to population viability for this and other sensitive species [Blickley et al. 2012].

Harvesting can also act as an artificial form of selection on sexually selected traits. David Coltman and colleagues used a partly genetically reconstructed pedigree from a 30-year study of wild bighorn sheep (Ovis canadensis) at Ram Mountain in Alberta, Canada, where trophy hunting targeted rams with rapidly growing horns [Coltman et al. 2003]. Body weight and horn size were highly heritable, and harvested rams had significantly higher genetic breeding values for both traits than rams that were not shot [Coltman et al. 2003]. Because rams of high breeding value were shot young, before achieving high reproductive success, mean breeding values for weight and horn size declined, producing smaller-horned, lighter rams and fewer trophies [Coltman et al. 2003]. Horns are weapons shaped by competition between males, and the study shows that removing the individuals that sexual selection would normally favour can change the direction of evolution in a managed population [Coltman et al. 2003].

These examples point to a calm, practical lesson. Harvest rules based on weapon or ornament size, and development near traditional display sites, both interact with a species' mating system. Understanding who competes, who chooses and who actually fathers offspring gives managers a more accurate picture of a population than headcounts alone [Griffith et al. 2002; Blickley et al. 2012; Coltman et al. 2003].

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