Should females prefer dominant males? Anna QvarnströmaA and Elisabet Forsgrenb Trends in Ecology and Evolution 1998, 13:498-501 a Dept of Zoology, Uppsala University, Villavägen 9, S-75236 Uppsala, Sweden b Dept of Marine Ecology, Göteborg University, Kristineberg Marine Research Station, S-45034 Fiskebäckskil, Sweden. A anna.qvarnstrom@zoologi.uu.se

Abstract

It is generally believed that success in male–male competition genuinely reflects high quality and that female preference for dominant males should therefore be widespread. However, recent studies suggest that male dominance is not always attractive and that it does not necessarily predict superior parental quality, better genes or other forms of benefit to females. In fact, the costs of choosing a dominant male can sometimes outweigh the benefits. When traits selected by male–male competition do not reflect overall mate quality, females are expected to use other choice cues and might occasionally prefer subordinate males. Thus, male–male competition and female choice can sometimes work in different, or even opposing, directions.

The evolution of sexually selected traits is driven by contests over mating opportunities and/or by mate choice. In most species, males can increase their reproductive success by increasing their number of mating partners, whereas females increase their reproductive success mainly by improving the quality of their mates. Consequently, females are usually more selective about their mates than are males. In this article we will, for simplicity, discuss only female choice and male–male competition, although males occasionally constitute the more choosy sex and females the more competitive one. The issues we discuss will, however, apply to either case.

It is generally thought that winners of male–male competition are of superior quality and that it would be in the females' interest to mate with these males 123. Thus, dominance per se or traits reflecting it, such as large body size, heavy weaponry and intense signals of fighting ability (such as status badges; Box 1), are expected to be important cues in female choice. Indeed, female preference for dominant males has been found in many species and, occasionally females even incite competition between males and then mate with the winner3. However, although it is often assumed that females gain by mating with dominant males, few studies have actually investigated the fitness consequences. Furthermore, it is important to bear in mind that there are several possible ways in which the two processes of sexual selection can interact (Fig 1). An increasing number of studies are showing that dominant males are not always preferred by females (1). Here, we summarize some of the present evidence of the main benefits and costs of choosing dominant males.

Figure 1. The possible ways in which male–male competition and female choice can interact in determining male mating success. Here, we assume that dominant males are successful at intimidating rivals. Pathway `a' applies only when females prefer traits that are negatively correlated with dominance.

Table 1. Examples of species where females have been found not to prefer dominant males
Species	Ref.
Pheasant (Phasianus colchicus)	40
Sharp-tailed grouse (Tympanuchus phasianellus)	41
Pintail duck (Anas acuta)	42
Yellow-browed leaf warbler (Phylloscopus inornatus)	43
House sparrow (Passer domesticus)	a
Tiger salamander (Ambystoma t.tigrinum)	44
Field cricket (Gryllus bimaculatus)	31b
Wax moth (Achroia grisella)	45
Sand goby (Pomatoschistus minutus)	10b
Three-spined stickleback (Gasterosteus aculeatus)	c

Direct benefits and costs

Do dominant males provide high quality resources?

In many species where males compete for resources necessary for attracting females (e.g. suitable breeding sites), dominant males monopolize high quality resources and consequently enjoy a mating advantage2. However, in polygynous species, dominance per se can be a poor predictor of the breeding situation for a specific female because she might have to share resources with other females. In such cases, other cues, such as territory quality and number of females already settled, can be important for female mating decisions4. Thus, when resources provided by males are crucial for female reproductive success, females should base their mate choice on the quality of the resource provided directly, rather than on male dominance position (i.e. the ability to monopolize resources). Several experimental studies have shown that females seem to base their mate choice mainly on the quality of the territory or nest site567 rather than on male traits. Although female attraction to essential resources could be the reason why males compete for access to such resources, male dominance per se need not necessarily be used as an important cue in female choice.

Do dominant males provide better parental care?

In organisms with paternal or biparental care, the quality of male care can be important for the number and quality of offspring produced. Females might therefore increase their fitness by selecting good parents8. It is often assumed that dominant males are of higher overall quality and that they can consequently provide superior parental care, as was demonstrated in a freshwater goby (Padogobius martensi)9. However, the results of a recent study show that in the closely related sand goby (Pomatoschistus minutus), winners of male–male competition did not provide better parental care than losers10. Furthermore, in the sand goby, females did not prefer winners of male contests, but instead preferred males that provided good paternal care. As a result, these females managed to bring a larger proportion of their eggs to hatching10. Therefore, traits important in male–male competition might not always be the same as those that are important to females selecting a mate.

Dominance could even have negative effects on parental abilities if males have to trade the effort spent in male contest against parental effort, as suggested in studies of three-spined sticklebacks (Gasterosteus aculeatus)11 and collared flycatchers (Ficedula albicollis)12. Such a tradeoff could be mediated by male sex hormones promoting dominance while having negative effects on parental care13. In any case, there is the possibility of a tradeoff between the effort spent on achieving dominance and on providing parental care, which suggests a number of interesting scenarios relating to sexual selection.

For example, the tradeoff between resources expended on obtaining high dominance positions, relative to that expended on paternal effort, could vary depending on differences in life history traits between species and/or differences in environmental conditions experienced by populations (Box 2). If highly competitive males feed the offspring less, the optimum mate choice of a female might vary depending on her own quality, residual reproductive value and/or environmental factors, such as food abundance. A female of high quality might, for example, be able to increase her maternal care at a lower cost than a female of low quality. If these costs are outweighed by a genetic benefit of choosing dominant males, females might be willing to increase their investment in offspring14. Another possibility is that females have different mate preferences when selecting a social mate (who will contribute to offspring provisioning) than when selecting an extrapair mate (who provides nothing but genes)—thus, dominant males might be preferred as extrapair mates but not as social mates. Extrapair paternity is common in socially monogamous birds and is most often suggested to result from females actively seeking `good genes'15.

In conclusion, dominance might not always reflect the male's contribution to paternal care. Further studies considering the links between sexually selected traits and life history traits, such as offspring number and quality, are needed to clarify which factors determine the balance between male investment in dominance and in parental care. Another interesting question concerns the optimal response from females when dominance and paternal care are in conflict. Do females still prefer dominant males and accept the cost of increased maternal care, or do they use other cues to predict paternal quality? There remain many questions to be answered.

Do matings with dominant males reduce female copulation costs?

There are several direct costs of copulation that can vary in magnitude according to the copulatory partner. Females might be expected to try to minimize such costs when selecting their partner, and the question then becomes what are the relationships between these costs and male dominance? These costs include the following:

Risk of injury or death caused by males

In species where males are larger than females or where the sex ratio is strongly male biased, females can be injured and occasionally killed during mating, typically by several competing males16. Thus, by selecting a dominant male, who by definition is successful at excluding rivals, a female could reduce the risk of being injured.

Disease transmission

It has been suggested that the outcome of male–male competition reliably reflects a male's disease state because infection will prevent a male from becoming dominant, as observed in mice17. Consequently, females could avoid infection by parasites by mating with dominant males. However, high androgen levels not only increase male dominance, but also suppress the immune system, which means that dominant males could actually be more susceptible to diseases and parasites. However, dominant males might be able to bear the cost of this immunocompetence handicap18. Consequently, there is no a priori expectation for the relationship between dominance and health state in any particular species.

Sexually transmitted diseases are exclusively transferred during copulation. For species with mating systems in which male mating success is strongly skewed, such as in lekking species or in species where single males defend harems of females, top-ranking males are likely to be highly exposed to such diseases. Because the costs of exposure to these diseases are higher for females than for males19, a sexual conflict could arise. In the presence of a virulent sexually transmitted disease, a dominant male might still benefit from monopolizing several females (by excluding other males from matings), whereas it may be in the females' interest to seek private mates even if that would mean accepting subdominant individuals. Thus, whether females face an increased or a reduced risk of disease transmission by mating with dominant males is still unclear.

Fertilization failure caused by sperm depletion

Given that males do not have a superabundance of sperm, increased mating frequency will lead to reduced sperm provision per mating20, which might lower female fertilization probabilities. Consequently, if dominant males monopolize many females, their fertilization efficiency may be reduced.


Indirect benefits and costs

Do dominant males sire offspring of superior genetic quality?

Success in male contests probably depends on male condition and overall health. It has therefore been suggested that females gain genetic benefits in terms of more viable offspring by mating with dominant males1. Some studies have shown that the size of male secondary sexual characters, used in both male–male competition and female choice, can predict offspring survival212223. However, dominance might not always be a reliable indicator of high genetically determined viability. If the direct energy cost of aggressiveness (e.g. caused by increased metabolic rates24) is sensitive to foraging conditions and/or if traits indicating dominance—such as large body size—impose energy stress, dominant individuals could be more liable to starvation. Thus, during harsh conditions, the survival of dominant individuals might be reduced, and so the optimal mate choice for the female might vary with environmental conditions. It has been shown, for example, that female yellow dung flies (Scathophaga stercoraria), which can store sperm from several males, can choose to lay eggs of different genotypes in different environments, thereby producing the greatest number of viable offspring25. A variable environment might therefore cause shifts in female preferences from dominant to subordinate males.

Similarly, female preferences can be frequency dependent. For example, several arthropod and fish species display a within-population dimorphism in male morphology and/or behaviour26, which could represent alternative genetically determined strategies. One of the morphs typically has larger size, larger weapons or is more aggressive and therefore successful in fights over mates, whereas the other morph is less aggressive but might, for example, have higher survival probability. Both strategies can therefore be maintained in the population. Frequency-dependent costs of `dominance' might result in a relative fitness shift between dominant and subordinate males, depending on the frequency of dominants in the population. Therefore, when traits indicating dominance are at least partly genetically determined, it might pay for females to choose subordinate males when dominant males are most common, whereas the reverse would be true when submissiveness is the most common strategy in the population. Indeed, in the side-blotched lizard (Uta stansburiana), the subordinate morph was shown to have a sexually selected advantage when occurring at low frequency27.

To produce viable offspring a female needs not only to assess the quality of male genes, but also to take into account how well they complement her own genes. It is well known that combinations of genes from close relatives can result in the expression of deleterious recessive genes, which causes inbreeding depression28. Therefore, females should avoid mating with dominant males if they are likely to be close relatives. In several mammalian species where philopatric females form stable nuclei of groups, some females prefer to mate with immigrant subordinate males rather than with resident dominant males, probably to avoid inbreeding2930. Similarly, female preference for unrelated males was shown to override the dominance rank of the male in determining male reproductive success in the field cricket (Gryllus bimaculatus)31. Possible cues female mammals can use to avoid genome-wide inbreeding, or improve the immune system of their offspring, are major histocompatibility complex (MHC)-dependent odours. It has been shown in both mice and humans that females prefer mates with an MHC genotype different from their own323334. Therefore, the optimal mate choice might vary between females. Furthermore, intragenomic conflicts can result in certain combinations of male and female genes being incompatible35. In this case, females might be expected to mate with several males, a behaviour that minimizes the risk of fertilization failure caused by sperm depletion or genetically incompatible sperm36.

Empirical evidence showing that heritable mate quality is reflected by male dominance is scarce. It is also largely unknown whether the balance between genetic benefits and costs of dominance is frequency dependent or varies with environmental conditions (i.e. results from gene×environment interactions). This is a research area that has the potential to yield interesting and important new findings.


Conclusions

Both male–male competition and female choice have recently been subject to considerable research, and understanding of both processes is well developed. By contrast, their interaction has received little attention and is poorly understood. Recent studies suggest that caution should be exercised before assuming that traits selected in male–male competition are also preferred by females. In some situations, the costs of dominance could outweigh the benefits, and females might therefore use other cues to assess male quality. Future studies investigating how choice cues are correlated, how females weigh different cues against each other and whether their relative importance varies with, for example, life history patterns and/or environmental conditions are needed. Such studies will provide new insights not only into the evolution of multiple secondary sexual traits but also into male reproductive tactics, sexual conflicts and female preferences in general.



Acknowledgements

We thank Ingrid Ahnesjö, Trond Amundsen, Anders Berglund, Tomas Pärt, Ben C. Sheldon, Staffan Ulfstrand and three anonymous referees for their constructive comments on earlier drafts of this article. Thanks also to Christer Hemborg for spotting typing errors.