Theoretical aspects of sexual selection: A generalized model of mating behaviour

A model of mate selection is described in which females mate preferentially according to their probability of encounter with the males they prefer. In this model, different thresholds of response to the courtship of different male phenotypes determine the female mating preferences. Females with a lower threshold toward particular males require fewer encounters before mating with these males and more encounters before mating with any of the others. Such females mate preferentially if they encounter a male they prefer before they have been stimulated to the level of the higher threshold. At the higher threshold they mate at random. The number of the extra encounters required to raise the females' level of stimulation from the lower to the higher threshold is a parameter of the model. The frequency of the preferred males then determines the probability that a female encounters and mates with one of them before she has been sufficiently stimulated to mate at random. Sexual selection by differences in male courtship can also be described in terms of this model.The preferred characters may be determined either by dominant and recessive alleles or by each different genotype. When only one extra encounter is required before the females mate at random, the preferred males only gain a slight frequency-dependent advantage: Stable polymorphisms can only be maintained if the heterozygotes have the greater preference in their favor. When more than one extra encounter is required before random mating, the males gain a negative frequency-dependent advantage: Stable polymorphisms are generally maintained.The models are fitted to published data on the mating success of male Drosophila at varying frequencies and provide an explanation of the “rare male” effect in which less common males gain a mating advantage.     

Sexual selection favours male parental care, when females can choose

Explaining the evolution of male care has proved difficult. Recent theory predicts that female promiscuity and sexual selection on males inherently disfavour male care. In sharp contrast to these expectations, male-only care is often found in species with high extra-pair paternity and striking variation in mating success, where current theory predicts female-only care. Using a model that examines the coevolution of male care, female care and female choice; I show that inter-sexual selection can drive the evolution of male care when females are able to bias mating or paternity towards parental males. Surprisingly, female choice for parental males allows male care to evolve despite low relatedness between the male and the offspring in his care. These results imply that predicting how sexual selection affects parental care evolution will require further understanding of why females, in many species, either do not prefer or cannot favour males that provide care.     

Cryptic preference for MHC-dissimilar females in male red junglefowl,Gallus gallus

An increasing number of studies test the idea that females increase offspring fitness by biasing fertilization in favour of genetically compatible partners; however, few have investigated or controlled for corresponding preferences in males. Here, we experimentally test whether male red junglefowl, Gallus gallus, prefer genetically compatible females, measured by similarity at the major histocompatibility complex (MHC), a key gene complex in vertebrate immune function. Theory predicts that because some degree of MHC heterozygosity favours viability, individuals should prefer partners that carry MHC alleles different from their own. While male fowl showed no preference when simultaneously presented with an MHC-similar and an MHC-dissimilar female, they showed a ‘cryptic’ preference, by allocating more sperm to the most MHC-dissimilar of two sequentially presented females. These results provide the first experimental evidence that males might respond to the MHC similarity of a female through differential ejaculate expenditure. By revealing that cryptic male behaviours may bias fertilization success in favour of genetically compatible partners, this study demonstrates the need to experimentally disentangle male and female effects when studying preferences for genetically compatible partners.     

Polymorphism of melanic ladybirds maintained by frequency-dependent sexual selection

Sexual selection, whether by female preference or male competition, is almost inevitably frequency-dependent. Female preference gives rise to a 'rare male effect', by which the rarer male phenotypes gain a relatively greater selective advantage. In addition to this effect, the proportion of females expressing a preference may also be frequency-dependent.
Frequency-dependent expression of mating preference can arise in at least two ways: (1) when females encounter a succession of courting males while searching for a male they prefer; (2) when females chose a male from within a lek. Models of mating behaviour reveal a clear distinction between the frequency dependence in the expression of female preference and the frequency dependence in the consequent selection of the males. When expression of preference is highly dependent on frequency, the selection of males is constant or only slightly frequency-dependent: constant expression of preference produces high frequency dependence of selection. Analysis of general models shows that genetic polymorphisms can be maintained under a wide range of conditions.
The ladybird, Adalia bipunctata , is polymorphic for several melanic and non-melanic phenotypes. Females have a genetically determined preference for melanic males. Non-melanic phenotypes mate assortatively. By estimating the parameters of a detailed model of natural selection, sexual selection and assortative mating, it has been shown that the Adalia bipunctata polymorphism will be maintained at frequencies observed in the wild.     

Frequency-dependent sexual selection

Sexual selection by female choice is expected to give rise to a frequency-dependent sexual advantage in favour of preferred male phenotypes: the rarer the preferred phenotypes, the more often they are chosen as mates. This 'rare-male advantage' can maintain a polymorphism when two or more phenotypes are mated preferentially: each phenotype gains an advantage when it is rarer than the others; no preferred phenotype can then be lost from the population. Expression of preference may be complete or partial. In models of complete preference, females with a preference always mate preferentially. Models of partial preference are more realistic: in these models, the probability that a female mates preferentially depends on the frequency with which she encounters the males she prefers. Two different 'encounter models' of partial preference have been derived: the O'Donald model and the Charlesworth model. The encounter models contain the complete preference model as a limiting case. In this paper, the Charlesworth model is generalized to allow for female preference of more than one male phenotype. Levels of frequency dependence can then be compared in the O'Donald and Charlesworth models. The complete preference model and both encounter models are formulated in the same genetical terms of preferences for dominant and recessive male phenotypes. Polymorphic equilibria and conditions for stability are derived for each of the three models. The models are then fitted to data of frequencies of matings observed in experiments with the two-spot ladybird. The complete preference model gives as good a fit as the encounter models to the data of these and other experiments. The O'Donald and Charlesworth encounter models are shown to produce a very similar frequency-dependent relation. Generally, as females become less choosy, they express their preference with more dependence on male frequency, whereas the resulting selection of the males becomes less frequency dependent. More choosy females are more constant in expressing their preference, producing greater frequency dependence in the selection of the males.     

Does Breeding Ornamentation Signal Genetic Quality in Arctic charr, <Emphasis Type="Italic">Salvelinus alpinus</Emphasis>?

Genetic theories of sexual selection predict that most ornamental secondary sexual traits provide reliable indication of the genetic quality of their bearers. Accordingly, also the offspring of mates with elaborate mating display should perform better than those of less conspicuous counterparts. In this study, we used Arctic charr (Salvelinus alpinus) as a model species to investigate whether the variation in a carotenoid-based red breeding coloration (a sexually dichromatic trait) in different sexes would reflect differences in individual genetic variability, one measure of individual quality, and/or indirectly, be manifested in variation in the offspring’s early viability and growth. We created maternal half-sibling families by artificially fertilizing the eggs with milt from bright- and pale-coloured males and then held the resulting progenies under identical hatchery conditions. The expression of red coloration among parental fish was not associated with their genetic diversity estimates in either sex nor did offspring sired by bright males consistently differ in terms of embryo survival or endogenous growth efficiency from offspring sired by pale males. By contrast, maternal effects were notably strong and, additionally, the degree of female coloration was negatively linked to their reproductive potential. The more intensely coloured females had a smaller relative fecundity and they also produced offspring of lower viability, implying a significant trade-off in resource allocation between ornamentation and offspring. Our results indicate that the red breeding ornamentation of Arctic charr is likely to be informative rather among females than males when the reproductive quality is predicted on grounds of the number of offspring produced. Nevertheless, this study does not support the direct selection hypothesis in explaining the evolution of female ornamentation, but rather suggests that the less intense coloration of female charr compared to males may reflect inter-sexual differences in the trade-off between natural and sexual selection.     

Familiarity breeds progeny: sociality increases reproductive success in adult male ring-tailed coatis (Nasua nasua)

The ring-tailed coati (Nasua nasua) is the only coati species in which social groups contain an adult male year round, although most males live solitarily. We compared reproductive success of group living and solitary adult male coatis to determine the degree to which sociality affects reproductive success. Coati mating is highly seasonal and groups of female coatis come into oestrus during the same 1-2 week period. During the mating season, solitary adult males followed groups and fought with the group living male. This aggression was presumably to gain access to receptive females. We expected that high reproductive synchrony would make it difficult or impossible for the one group living male to monopolize and defend the group of oestrous females. However, we found that group living males sired between 67-91% of the offspring in their groups. This reproductive monopolization is much higher than other species of mammals with comparably short mating seasons. Clearly, living in a group greatly enhanced a male's reproductive success. At the same time, at least 50% of coati litters contained offspring sired by extra-group males (usually only one offspring per litter); thus, resident males could not prevent extra-group matings. The resident male's reproductive advantage may reflect female preference for a resident male strong enough to fend off competing males.     

Sperm competition games: sperm selection by females

We analyse a co-evolutionary sexual conflict game, in which males compete for fertilizations (sperm competition) and females operate sperm selection against unfavourable ejaculates (cryptic female choice). For simplicity, each female mates with two males per reproductive event, and the competing ejaculates are of two types, favourable (having high viability or success) or unfavourable (where progeny are less successful). Over evolutionary time, females can increase their level of sperm selection (measured as the proportion of unfavourable sperm eliminated) by paying a fecundity cost. Males can regulate sperm allocations depending on whether they will be favoured or disfavoured, but increasing sperm allocation reduces their mating rate. The resolution of this game depends on whether males are equal, or unequal. Males could be equal: each is favoured with probability, p, reflecting the proportion of females in the population that favour his ejaculate (the 'random-roles' model); different males are favoured by different sets of females. Alternatively, males could be unequal: given males are perceived consistently by all females as two distinct types, favoured and disfavoured, where p is now the frequency of the favoured male type in the population (the 'constant-types' model). In both cases, the evolutionarily stable strategy (ESS) is for females initially to increase sperm selection from zero as the viability of offspring from unfavourable ejaculates falls below that of favourable ejaculates. But in the random-roles model, sperm selection decreases again towards zero as the unfavourable ejaculates become disastrous (i.e. as their progeny viability decreases towards zero). This occurs because males avoid expenditure in unfavourable matings, to conserve sperm for matings in the favoured role where their offspring have high viability, thus allowing females to relax sperm selection. If sperm selection is costly to females, ESS sperm selection is high across a region of intermediate viabilities. If it is uncostly, there is no ESS in this region unless sperm limitation (i.e. some eggs fail to be fertilized because sperm numbers are too low) is included into the model. In the constant-types model, no relaxation of sperm selection occurs at very low viabilities of disfavoured male progeny. If sperm selection is sufficiently costly, ESS sperm selection increases as progeny viability decreases down towards zero; but if it is uncostly, there is no ESS at the lowest viabilities, and unlike the random-roles model, this cannot be stabilized by including sperm limitation. Sperm allocations in the ESS regions differ between the two models. With random roles, males always allocate more sperm in the favoured role. With constant types, the male type that is favoured allocates less sperm than the disfavoured type. These results suggests that empiricists studying cryptic female choice and sperm allocation patterns need to determine whether sperm selection is applied differently, or consistently, on given males by different females in the same population.     

Leader preference in Neoconocephalus ensiger katydids: a female preference for a nonheritable male trait

Female preferences for males producing their calls just ahead of their neighbours, leader preferences, are common in acoustically communicating insects and anurans. While these preferences have been well studied, their evolutionary origins remain unclear. We tested whether females gain a fitness benefit by mating with leading males in Neoconocephalus ensiger katydids. We mated leading and following males with random females and measured the number and quality of F₁, the number of F₂ and the heritability of the preferred male trait. We found that females mating with leaders and followers did not differ in the number of F₁ or F₂ offspring. Females mating with leading males had offspring that were in better condition than those mating with following males suggesting a benefit in the form of higher quality offspring. We found no evidence that the male trait, the production of leading calls, was heritable. This suggests that there is no genetic correlate for the production of leading calls and that the fitness benefit gained by females must be a direct benefit, potentially mediated by seminal proteins. The presence of benefits indicates that leader preference is adaptive in N. ensiger, which may explain the evolutionary origin of leader preference; further tests are required to determine whether fitness benefits can explain the phylogenetic distribution of leader preference in Neoconocephalus. The absence of heritability will prevent leader preference from becoming coupled with or exaggerating the male trait and prevent females from gaining a ‘sexy‐sons’ benefit, weakening the overall selection for leader preference.     

Positive genetic correlation between female preference and offspring fitness

In many species, females display preferences for extreme male signal traits, but it has not been determined if such preferences evolve as a consequence of females gaining genetic benefits from exercising choice. If females prefer extreme male traits because they indicate male genetic quality that will enhance the fitness of offspring, a genetic correlation will evolve between female preference genes and genes that confer offspring fitness. We show that females of Drosophila serrata prefer extreme male cuticular hydrocarbon (CHC) blends, and that this preference affects offspring fitness. Female preference is positively genetically correlated with offspring fitness, indicating that females have gained genetic benefits from their choice of males. Despite male CHCs experiencing strong sexual selection, the genes underlying attractive CHCs also conferred lower offspring fitness, suggesting a balance between sexual selection and natural selection may have been reached in this population.     

Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia)

Models of sexual selection propose that exaggerated secondary sexual ornaments indicate a male's own fitness and the fitness of his offspring. These hypotheses have rarely been thoroughly tested in free-living individuals because overall fitness, as opposed to fitness components, is difficult to measure. We used 20 years of data from song sparrows (Melospiza melodia) inhabiting Mandarte Island, British Columbia, Canada, to test whether a male's song repertoire size, a secondary sexual trait, predicted overall measures of male or offspring fitness. Males with larger song repertoires contributed more independent and recruited offspring, and independent and recruited grandoffspring, to Mandarte's population. This was because these males lived longer and reared a greater proportion of hatched chicks to independence from parental care, not because females mated to males with larger repertoires laid or hatched more eggs. Furthermore, independent offspring of males with larger repertoires were more likely to recruit and then to leave more grandoffspring than were offspring of males with small repertoires. Although we cannot distinguish whether observed fitness variation reflected genetic or environmental effects on males or their offspring, these data suggest that female song sparrows would gain immediate and intergenerational fitness benefits by pairing with males with large song repertoires.     

Nepotism and brood reliability in the suppression of worker reproduction in the eusocial Hymenoptera

In many eusocial Hymenoptera, workers prevent each other from producing male offspring by destroying worker-laid eggs. Kin selection theory predicts that such 'worker policing' behaviour can evolve by increasing the average relatedness between workers and their male brood. Alternatively, if worker-laid eggs are of low relative viability, their replacement would increase the developmental reliability of the brood. Less colony investment in terms of time and resources would be lost on poor males. This gain is independent of the relatedness of the males. Unfortunately, both nepotistic and group efficiency benefits can simultaneously accrue with the replacement of worker-laid eggs. Therefore, worker behaviour towards eggs cannot completely resolve whether both processes have been equally evolutionarily important. Adequate resolution requires the presentation of worker-produced brood of various ages. The stage at which brood are replaced can discriminate whether worker policing occurs owing to a preference for closer genetic kin, a preference for the more reliable brood or both.     

Can too strong female choice deteriorate male ornamentation?

Competition for limited resources can have fundamental implications for population dynamics. However, the effects of resource depletion have rarely been discussed in the context of sexual selection, even though mate choice typically favours males who outperform others in securing access to some limited resource. Here, we develop a model to investigate the question of resource competition as a form of male-male competition in the context of male sexual displays. We phrase our model in terms of male bowerbirds either searching for or stealing resources (ornamental objects) valued by females, and compare the model findings with published studies of time allocation to various activities in different species of bowerbirds. The basic idea of the model, however, extends to cases where the resource is used less directly for the development of sexual ornamentation, such as males excluding others' access to food. We show that if males compete for resources used in sexual displays, intense female preference for high-quality displays can lead to poorer prospects for efficient choice by females. This is because males benefit from excluding others' access to resources used in displays, damaging the overall efficiency of resource use in the population, and the accuracy with which females can judge male ability to gain such resources. The evolution of female choice may therefore have a self-limiting nature when it poses a selection pressure on male resource acquisition.     

Female differential allocation in response to extrapair offspring and social mate attractiveness

Renewed debate over what benefits females might gain from producing extra‐pair offspring emphasizes the possibility that apparent differences in quality between within‐pair and extra‐pair offspring are confounded by greater maternal investment in extra‐pair offspring. Moreover, the attractiveness of a female''s social mate can also influence contributions of both partners to a reproductive attempt. Here, we explore the complexities involved in parental investment decisions in response to extra‐pair offspring and mate attractiveness with a focus on the female point of view. Adult zebra finches paired and reproduced in a colony setting. A male''s early‐life diet quality and his extra‐pair reproductive success were used as metrics of his mating attractiveness. Females paired with males that achieved extra‐pair success laid heavier eggs than other females and spent less time attending their nests than their mates or other females. Extra‐pair nestlings were fed more protein‐rich hen''s egg than within‐pair nestlings. Females producing extra‐pair offspring had more surviving sons than females producing only within‐pair offspring. Collectively, results show that females differentially allocate resources in response to offspring extra‐pair status and their social mate''s attractiveness. Females may also obtain fitness benefits through the production of extra‐pair offspring.     

Multi-male mating and female choice increase offspring growth in the spiderNeriene litigiosa(Linyphiidae)

The purpose of this controlled-breeding study was to investigate the viability consequences of female choice and sequential polyandry for offspring in a way that would separate the influences of these two aspects of female sexual behaviour. Female sierra dome spiders,Neriene litigiosa(=Linyphia litigiosa) typically mate two to three times before production of their first batch of eggs, although some females (ca 16%) mate only once. Strong fighters are preferred as first mates and principal sires. Large males that give a vigorous performance during copulatory courtship are preferred as sires among a female's secondary mates. In this study, the number of matings by free-living females was experimentally controlled and the size and copulatory vigour of all the females’ mates were recorded. At the end of the breeding season, the females were collected and their broods were obtained in captivity. Randomly chosen subsets of 28 female's offspring were reared under standard conditions during the following spring. The spiderlings were reared for 27 days in the company of siblings under conditions that would encourage the expression of genetic variation in viability, and growth and survivorship were monitored. After controlling for maternal effects (i.e. female size and oviposition date) and variance in feeding opportunities among rearing groups, both mate number and mate size were positively and independently related to offspring growth rates and the size of offspring attained after emergence from the natal cocoon. The results support the hypotheses that the preference for large males yields viability benefits to offspring and that polyandry can augment the benefits of selective mating.     

Mate choice for nonadditive genetic benefits and the maintenance of genetic diversity in song sparrows

The lek paradox asserts that strong directional selection via female choice should deplete additive genetic variation in fitness and consequently any benefit to females expressing the preference. Recently, we have provided a novel resolution to the paradox by showing that nonadditive genetic effects such as overdominance can be inherited from parent to offspring, and populations with females that express a mating preference for outbred males maintain higher genetic variation than populations with females that mate randomly. Here, we test our dynamic model using empirical data previously published from a small island population of song sparrows (Melospiza melodia). The model assumes that fitness and male trait expression display overdominance effects. The results demonstrate that female choice for outbred males mediated by directional selection on song repertoire size provides a heritable benefit to offspring through reduced inbreeding depression. Within the population, we estimate the heritability of the inbreeding coefficient to be 0.18 ± 0.08 (SD). Furthermore, we show that mate choice for outbred males increases fitness‐related genetic variation in the population by 12% and thereby reduces inbreeding depression by 1% per generation in typical years and upwards of 15% in severe years. Thus, mate choice may help to stave off population extinction in this and other small populations.     

Sex-Specific Recruitment and Brood Sex Ratios of Eurasian Kestrels in a Seasonally and Annually Fluctuating Northern Environment

Timing of birth and food availability may select for biased offspring sex ratios when they differentially affect the reproductive value of male and female young. Here we show that early hatching date enhances more the probability of male Eurasian kestrels (Falco tinnunculus) to breed as one-year-old than that of females in a Finnish population. This rarely documented phenomenon has been previously observed in a kestrel population in the Netherlands. As kestrels in the Finnish population are migratory, our results refute the hypothesis that early-fledged males would have an advantage for early breeding only in resident populations. Contrary to the predictions, the Finnish population showed no change in brood sex ratio during the breeding season in a long-term data from 8years. As far as we know, this is the first demonstration that biased sex allocation may not occur even when it would appear to be adaptive. This result is different from the Dutch kestrel population, in which the season began with a bias towards males and ended with a bias in favour of females. We suggest that high inter-annual variation in food abundance in Finland might reduce selection for a sex ratio trend.     

Pape in Panorpa scorpionflies and a general rape hypothesis

The adaptive significance of heterosexual rape is difficult to demonstrate because (1) female coyness is difficult to distinguish from apparent rape, and (2) male fitness must be enhanced by rape. Male Panorpa scorpionflies inseminate unwilling females by securing the female's wings in an abdominal clamp. Panorpa rapists gain fitness through avoidance of risks of predation by web-building spiders associated with the more typical male behaviours of feeding females a dead insect or salivary secretion during copulation. Males should be most strongly selected to rape in species in which males provide resources important for female reproduction. In such species, the strength of selection on males to rape should exceed the strength of selection on females to prevent rape.     

SEXUAL SELECTION IN A WOLF SPIDER: MALE DRUMMING ACTIVITY,BODY SIZE,AND VIABILITY

Females are often believed to actively choose highly ornamented males (males with extravagant morphological signals or intense sexual display), and ornaments should be honest signals of male viability. However, this belief is relying only on some pieces of empirical evidence from birds. Our study reports active female choice on sexual display that indicates male viability in spiders. We established trials in which we studied female choice in relation to male courtship drumming activity and body size. Females chose the most actively drumming males as mating partners, but the body size of the males did not seem to be selected. Male drumming activity turned out to be a good predictor of male viability, whereas male viability was independent of male body mass. Our results suggest that by actively choosing mates according to male drumming performance, but independently of male body mass, females are preferring viable males as mates. Because Hygrolycosa rubrofasciata males do not provide obvious direct benefits to their offspring, females may gain some indirect benefits; offspring may have higher chance of survival, or the offspring may inherit the attractiveness of their father.     

Female preference for dominant males in the Mexican mojarra cichlid fish,Cichlasoma istlanum

It is widely assumed that female preference and male competition operate simultaneously during sexual selection. Dominance is likely an honest indicator of male quality, and females can identify and choose the dominant male to reproduce with individuals with greater competitive abilities, thus improving the quality and competitiveness of their offspring. In this context, few studies have investigated female preference in relation to male fighting ability. The Mexican mojarra, Cichlasoma istlanum, is a cichlid species native to the Balsas River basin. It is territorial during reproduction and provides parental care. Males commonly engage in territorial defence, whereas females care directly for offspring. This study examined whether females prefer dominant males that exhibit more aggressive behaviour. The authors conducted experiments using groups of two males and one female to test competitive ability in males and female preference. They also quantified the time during which the female associated with the dominant male and the subordinate male after observing the outcome of a fight between the two males. They found that Mexican mojarra females preferred dominant males and that the time females spent associating with males was positively related with their aggressive behaviours during competition. These results indicate that dominant males were more attractive than subordinate males to female Mexican mojarra. The relationship between female preference and male dominance in the Mexican mojarra demonstrates the importance of male competitive ability for future parental care in reproduction.