Directional Sexual Selection Research Articles

On the function of song type repertoires: testing the ‘antiexhaustion hypothesis’ in chaffinches

Why some bird species have evolved elaborate song repertoires has puzzled biologists for a long time. According to the antiexhaustion hypothesis avian song type repertoires have evolved because switching between different songs, involving different patterns of muscle contractions, causes less exhaustion in the singer and thus allows a higher song rate to be maintained. Although it is a classic explanation referred to in many textbooks, this hypothesis is still the subject of debate. We investigated the antiexhaustion idea in the chaffinch, Fringilla coelebs, a species in which males may have only one song type or a repertoire of up to six types. We analysed the song delivery rates of 101 male chaffinches, taking into account various seasonal, ecological and social variables. We found that males with a repertoire of several song types did not sing at a higher rate than males with only one song type, even though single song type males produced longer songs on average. Also, repertoire birds singing at high rates did not switch song types more often. These findings indicate that song type switching is not necessary for the maintenance of high song rates in this species. We conclude that preventing motor fatigue was not important in the evolution of chaffinch song type repertoires. Thus other factors, such as direct sexual selection of repertoire size or the use of song type repertoires for vocal interactions, are much more likely to explain why many bird species have evolved a repertoire of several song types.

Comment: On the consequences of sexual selection for fisheries-induced evolution.

It is becoming increasingly recognized that fishing (and other forms of nonrandom harvesting) can have profound evolutionary consequences for life history traits. A recent and welcome publication provided the first description of how sexual selection might influence the outcome of fisheries-induced evolution (FIE). One of the main conclusions was that if sexual selection generates a positive relationship between body size and reproductive success, increased fishing pressure on large individuals causes stronger selection for smaller body size. Here, we re-evaluate the sexual selection interpretation of the relationship between body size and reproductive success, and suggest it may in fact be representative of a more general case of pure natural selection. The consequences of sexual selection on FIE are likely to be complicated and dynamic, and we provide additional perspectives to these new and exciting results. Selection differentials and trait variance are considered, with density-dependent and genetic effects on the strength and the direction of sexual selection given particular attention. We hope that our additional views on the role of sexual selection in FIE will encourage more theoretical and empirical work into this important application of evolutionary biology.

Sexual dimorphism in chelicerae size in three species of nuptial‐gift spiders: a discussion of possible functions and driving selective forces

AbstractPositive allometric patterns observed for intersexual signalling characters are related to directional sexual selection, and supported by theoretical and empirical data. Recent models have shown that positive allometry may not hold as a rule if the influence of natural selection is added to the model. Here we tested these models applying traditional morphometrical techniques for the analysis of chelicerae sexual dimorphism and allometric patterns within the genus Paratrechalea: Paratrechalea azul, Paratrechalea galianoae and Paratrechalea ornata. Spider chelicerae are basically used for prey capture, but males of Paratrechalea also use the chelicerae to offer a nuptial gift during courtship, also presenting a clear size and colour sexual dimorphism supporting a possible role as a signal. Chelicerae size was male biased for all the variables studied and showed an isometric pattern, while females showed a higher variation. Our findings are in accordance with models of viability‐related function for prey capture, questioning some statements proposed by the positive allometry model.

Love will tear you apart: different components of female choice exert contrasting selection pressures on male field crickets

Female mate choice is a driving force in the evolution of male secondary sexual characters. It can be dissected into several components: discrimination describes the degree to which females distinguish male trait variation, responsiveness indicates the speed or likelihood of females’ reactions to a mate, and preference functions illustrate how the probability of mating relates to male trait variation. Relatively little is known about how these components interact to produce final mating decisions and influence the strength and direction of sexual selection, so I used female field crickets (Teleogryllus oceanicus) to measure interactions between individual preference functions, discrimination, and 2 measures of responsiveness (number of responses and response effort). Preference function shape varied considerably between individual females. Highly discriminating females showed greater numbers of responses to playbacks and were more likely to have stabilizing preference functions. When I constructed 2 population-level preference functions using either response number or response effort, the first yielded a linear, directional function, whereas the second implied a stabilizing function. The clear differences between the 2 imply that different components of female choice can exert contrasting selection pressure on a single male trait. Overall, both response number and discrimination were mutually reinforcing and likely govern the strength of sexual selection in this population. The direction of selection in a wild setting ultimately depends on the relative importance of response number versus response effort, where exogenous factors such as predation risk or density will determine which component of female choice predominates mating decisions. Key words: choosiness, discrimination, mate choice, preference function, sexual selection, Teleogryllus oceanicus. [Behav Ecol]

The ecological basis of unusual sex roles in reverse-dichromatic eclectus parrots

In theory, sex roles are determined by the potential reproductive rates of males and females, which are constrained by parental investment. Thus the sex that invests least in offspring typically competes most for matings and is most subject to sexual selection, whereas the caring sex is most choosy when selecting mates. Here I show that ecological variables, rather than patterns of parental investment, can be influential in determining sex roles and the direction of sexual selection. In the polyandrous eclectus parrot, Eclectus roratus , both sexes care for offspring, yet despite traditional parental care patterns, both sexes are competitive and both are subject to sexual selection. The bright red and blue females compete for scarce nest hollows and the iridescent green males for mates. Using data from an 8-year field study, I show that the major ecological variable driving this system is nest hollow quality. Females with drier hollows had higher reproductive success and more males feeding and competing to mate with them. Females with nest hollows that were prone to flooding had fewer fledglings in years with higher dry season rainfall, confirming that hollow quality was a primary determinant of reproductive success. Comparisons of females before and after they changed hollows during the study provided further evidence that these trends were due to hollow quality rather than individual female quality. Thus competition for a scarce resource can lead to high variance in female reproductive success, and promote competition for high-quality mates among males.

Parasite-mediated sexual selection and species divergence in Lake Victoria cichlid fish

We investigate the role of parasite-mediated sexual selection in the divergence of two species of Lake Victoria cichlids. Pundamilia pundamilia and Pundamilia nyererei represent a common pattern of male nuptial colour divergence between haplochromine sister species: metallic grey–blue in P. pundamilia and bright yellow and red in P. nyererei. Female mating preferences for different male colours maintain the genetic and phenotypic differentiation of the two species in clear water. Previous work indicated that the red coloration of P. nyererei males, which is subject to directional sexual selection, may be a carotenoid-dependent signal of parasite infestation rate. In the present study, we find a parallel result for P. pundamilia: bright blue males are infected with fewer species of parasites. We also find that parasite infestation rates differ quantitatively between the two species in a way that is consistent with species differences in diet and microhabitat. We conclude that parasite-mediated sexual selection may have contributed to the divergence of female mating preferences between P. pundamilia and P. nyererei, and may currently strengthen reproductive isolation between these species. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, 53–60.

Sexual selection on aggressiveness in females: evidence from an experimental test with tree swallows

While much research has focused on the evolution of conspicuous male displays, ornaments and behaviours, less is understood about the evolution of similar traits in females. To determine whether females express these traits as nonadaptive by-products of sexual selection favouring the same traits in males or whether females are directly selected to express such traits, the benefits of these traits must be understood. The prevalence of aggression in female–female competition suggests that females may experience direct sexual selection for aggressiveness, but data are lacking. I used the tree swallow, Tachycineta bicolor, to test the hypothesis that selection directly favours aggressiveness in females during intrasexual competition over nesting sites. After assaying the aggressiveness of a population of tree swallows, I experimentally reduced the number of nesting cavities, a resource required for female reproductive success. More aggressive females were more likely to obtain nesting cavities after the experimental reduction, while female age and male aggressiveness did not predict nesting cavity acquisition. Aggressive behaviour in female tree swallows is therefore beneficial in the context of female–female competition for a critical breeding resource. These results indicate that the processes favouring aggressiveness in intrasexual competition among females may not be very different from the processes shaping aggressive behaviour in males.

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara. This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.

Swingin' in the rain: condition dependence and sexual selection in a capricious world

Signals used in mate attraction are predicted to be highly condition dependent, and thus should be sensitive to environmental contributions to condition. However, the effects of temporal fluctuations in the environment on sexual selection in long-lived animals have been largely ignored. Female superb fairy-wrens, Malurus cyaneus, use the time that males moult into nuptial plumage prior to the onset of the breeding season to distinguish between the extra-group sires that dominate paternity. Although moult varies predictably with age, and shows marked differences between males, the phenotypic distribution also changes radically with climate; so after dry summers few males can attempt early moult. We use the recently introduced de-lifing technique to examine sexual selection gradients over 15 years of selection. Overall, there was strong evidence of directional sexual selection for early moult. However, sexual selection was much stronger when the conditions were favourable (rainfall was high), and selection was undetectable in some years. The contribution of early moulting males to population growth increased when many males moulted early, decreased when early moulting males suffered disproportionate mortality and decreased when females lacked subordinate helpers, forcing them to cede paternity to their social partner. These data suggest that short-term and laboratory studies of mate choice and sexual selection may misrepresent or underestimate the complexity of the sexual selection landscape.

OPERATIONAL SEX RATIO AND DENSITY DO NOT AFFECT DIRECTIONAL SELECTION ON MALE SEXUAL ORNAMENTS AND BEHAVIOR

Demographic parameters including operational sex ratio (OSR) and population density may influence the opportunity for, and strength of sexual selection. Traditionally, male-biased OSRs and high population densities have been thought to increase the opportunity for sexual selection on male sexual traits due to increased male competition for mates. Recent experimental evidence, however, suggests that male-biased OSRs might reduce the opportunity for sexual selection due to increased sexual coercion experienced by females. How OSR, density, and any resultant changes in the opportunity for sexual selection actually affect selection on male sexual traits is unclear. In this study, we independently manipulated OSR and density in the guppy (Poecilia reticulata) without altering the number of males present. We recorded male and female behavior and used DNA microsatellite data to assign paternity to offspring and estimate male reproductive success. We then used linear selection analyses to examine the effects of OSR and density on directional sexual selection on male behavioral and morphological traits. We found that females were pursued more by males in male-biased treatments, despite no change in individual male behavior. There were no differences in sexual behavior experienced by females or performed by males in relation to density. Neither OSR nor density significantly altered the opportunity for sexual selection. Also, Although there was significant multivariate linear selection operating on males, neither OSR nor density altered the pattern of sexual selection on male traits. Our results suggest that differences in either OSR or density (independent of the number of males present) are unlikely to alter directional evolutionary change in male sexual traits.

Polyandry in the wild: temporal changes in female mating frequency and sperm competition intensity in natural populations of the tettigoniid Requena verticalis

Empirical tests of sexual selection theory generally utilize model systems under laboratory settings, and extend conclusions to evolutionary processes occurring in nature. The biological significance of laboratory findings will depend largely on the mating rates of females and patterns of paternity in natural populations, information on which is generally lacking. Here we use microsatellite markers to provide rare estimates of female mating rates and patterns of parentage in a species of tettigoniid, Requena verticalis, which has been used extensively to test theory on the evolution of male parental investment and its influence on the direction of sexual selection. We found that although the number of males having a genetic representation in the female's sperm stores was higher for females collected late in the breeding season than those collected early in the season, overall the female mating rate was lower than that expected from laboratory observations. Analysis of parentage of offspring produced by females at the end of the breeding season revealed that all males represented in the sperm stores fathered offspring, although paternity was biased away from that expected from random sperm utilization. The data show that the complete first male sperm precedence documented in laboratory studies of this species does not persist in natural populations. Our data provide a solid underpinning for conclusions drawn from laboratory studies of this species.

Sexual selection explains Rensch's rule of allometry for sexual size dimorphism.

In 1950, Rensch first described that in groups of related species, sexual size dimorphism is more pronounced in larger species. This widespread and fundamental allometric relationship is now commonly referred to as ‘Rensch's rule’. However, despite numerous recent studies, we still do not have a general explanation for this allometry. Here we report that patterns of allometry in over 5300 bird species demonstrate that Rensch's rule is driven by a correlated evolutionary change in females to directional sexual selection on males. First, in detailed multivariate analysis, the strength of sexual selection was, by far, the strongest predictor of allometry. This was found to be the case even after controlling for numerous potential confounding factors, such as overall size, degree of ornamentation, phylogenetic history and the range and degree of size dimorphism. Second, in groups where sexual selection is stronger in females, allometry consistently goes in the opposite direction to Rensch's rule. Taken together, these results provide the first clear solution to the long-standing evolutionary problem of allometry for sexual size dimorphism: sexual selection causes size dimorphism to correlate with species size.

Male choice generates stabilizing sexual selection on a female fecundity correlate

We know very little about male mating preferences and how they influence the evolution of female traits. Theory predicts that males may benefit from choosing females on the basis of traits that indicate their fecundity. Here, we explore sexual selection generated by male choice on two components of female body size (wing length and body mass) in Drosophila serrata. Using a dietary manipulation to alter female size and 828 male mate choice trials, we analysed linear and nonlinear sexual selection gradients on female mass and wing length. In contrast to theoretical expectations and prevailing empirical data, males exerted stabilizing rather than directional sexual selection on female body mass, a correlate of fecundity. Sexual selection was detected only among females with access to standard resource levels as an adult, with no evidence for sexual selection among resource-depleted females. Thus the mating success of females with the same body mass differed depending upon their access to resources as an adult. This suggests that males in this species may rely on signal traits to assess body mass rather than assessing it directly. Stabilizing rather than directional sexual selection on body mass together with recent evidence for stabilizing sexual selection on candidate signal traits in this species suggests that females may trade-off resources allocated to reproduction and sexual signalling.

Reproductive success of male bank voles (Clethrionomys glareolus): the effect of operational sex ratio and body size

The operational sex ratio (OSR) may influence the intensity of competition for mates and mate choice and is therefore thought to be a major factor predicting the intensity and direction of sexual selection. We studied the opportunity for sexual selection, i.e., the variance in male reproductive success and the direction and intensity of sexual selection on male body mass in bank vole (Clethrionomys glareolus) enclosure populations with experimentally manipulated sex ratios. The opportunity for sexual selection was high among male-biased OSRs and decreased towards female-biased OSRs. Paradoxically, selection for large male body mass was strongest in female-biased OSRs and also considerable at intermediate OSRs, whereas at male-biased OSRs, only a weak relationship between male size and reproductive success was found. Litters in male-biased OSRs were more likely to be sired by multiple males than litters in female-biased OSRs. Our results suggest that the intensity and direction of sexual selection in males differs among different OSRs. Although the direction of sexual selection on male body mass was opposite than predicted, large body mass can be favored by sexual selection. Naturally varying OSRs may therefore contribute to maintain variation in male sexually selected traits.

Condition‐dependent expression of red colour differs between stickleback species

Sexual isolation may arise when male mating traits and female preferences differ between species. Such divergence in mating traits is likely to occur when the strength or targets of sexual selection differ. Therefore, by comparing the traits under sexual selection in closely related species and the nature of preference for those traits, we can gain insight into when sexual selection contributes to sexual isolation and how it does so. Collecting these data is no easy undertaking. To simplify this comparison, I use the presence and extent of condition dependence in traits to determine whether directional sexual selection is acting on them. Condition dependence thus serves as a signature of sexual selection. I investigate differences in sexual selection on red nuptial colour in limnetic-benthic species pairs of three-spined sticklebacks. I evaluate condition dependence by comparing the strength of the relationship between colour and condition, and the magnitude of variance in red nuptial colour to other colour traits and to nonsexual traits. I find that limnetic males have strong condition-dependent expression of red nuptial colour whereas benthic males have at most weak condition-dependent expression. Ancestral anadromous males show no condition dependence. This suggests that colour is under strong directional sexual selection only in limnetics and that this is the derived state. Moreover, I find that the strength of female preference for red is related to the extent of condition dependence. The extent of condition dependence is also associated with the importance of colour differences to mate recognition. These results show that differences between these species in the action of sexual selection underlie their sexual isolation.

SEXUAL SELECTION AND ALLOMETRY: A CRITICAL REAPPRAISAL OF THE EVIDENCE AND IDEAS

One of the most pervasive ideas in the sexual selection literature is the belief that sexually selected traits almost universally exhibit positive static allometries (i.e., within a sample of conspecific adults, larger individuals have disproportionally larger traits). In this review, I show that this idea is contradicted by empirical evidence and theory. Although positive allometry is a typical attribute of some sexual traits in certain groups, the preponderance of positively allometric sexual traits in the empirical literature apparently results from a sampling bias reflecting a fascination with unusually exaggerated (bizarre) traits. I review empirical examples from a broad range of taxa illustrating the diversity of allometric patterns exhibited by signal, weapon, clasping and genital traits, as well as nonsexual traits. This evidence suggests that positive allometry may be the exception rather than the rule in sexual traits, that directional sexual selection does not necessarily lead to the evolution of positive allometry and, conversely, that positive allometry is not necessarily a consequence of sexual selection, and that many sexual traits exhibit sex differences in allometric intercept rather than slope. Such diversity in the allometries of secondary sexual traits is to be expected, given that optimal allometry should reflect resource allocation trade-offs, and patterns of sexual and viability selection on both trait size and body size. An unbiased empirical assessment of the relation between sexual selection and allometry is an essential step towards an understanding of this diversity.

THE FORM OF SEXUAL SELECTION ON MALE GENITALIA CANNOT BE INFERRED FROM WITHIN-POPULATION VARIANCE AND ALLOMETRY?A CASE STUDY IN AQUARIUS REMIGIS

Male genital morphology in insects and arachnids is characterized by static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits. The one-size-fits-all model of genital evolution attributes these patterns to stabilizing sexual selection. This model relies on the assumption that the observed patterns of variation and allometry reflect the form of sexual selection acting these traits. We test this by examining the patterns of scaling and trait variation for a set of genitalic and somatic morphological traits in male water striders (Aquarius remigis). This suite of traits is of particular interest because previous work has shown that the genitalic traits are under strong directional selection whereas the somatic traits are under either weak directional or stabilizing selection. Because the selection regime for these traits is known, we can, for the first time, test the purported relationship between trait variation, scaling, and the form of sexual selection. We show that the patterns of variation and scaling of these traits differ sharply from those predicted for traits experiencing strong directional sexual selection. Specifically, the male genital structures show static hypoallometry and low intrapopulational levels of phenotypic variation relative to other male traits, in spite of consistent, strong, directional sexual selection. These scaling relationships and levels of variation are typical of genital traits in other insect species, where they have been presumed to reflect stabilizing sexual selection. Our data clearly refute the assumption of the one-size-fits-all hypothesis that hypoallometric scaling of genitalic traits implies stabilizing selection. We discuss the implications of this finding and propose future directions for improving our current understanding of genital evolution in arthropods.

Direct and indirect selection in moth pheromone evolution: population genetical simulations of asymmetric sexual interactions

Female moths generally use pheromones to attract males. Normally, all females in a population produce a specific chemical blend with only a limited variance, and the local males are highly attracted to this blend. To better understand the direct and indirect selective forces acting on this communication system, where, unusually, it is the reproductively limited sex that signals for matings, a population genetical model has been constructed and numerically analysed. Basic to the model is the assumption that the pheromone attraction system functions asymmetrically, leading to strong sexual selection between males but no direct sexual selection between females. Evolutionary simulations using the model show that sexual selection in males causes an indirect stabilizing selection on the pheromone blends produced by females. Thus, a more narrow range of pheromone variation is selected for, even in the absence of female sexual selection. The strength of the selection is analysed, and it is suggested that this indirect stabilizing selection becomes particularly important in situations where geographically adjacent populations have evolved different pheromone blends.

Ejaculate size, second male size, and moderate polyandry increase female fecundity in a seed beetle

Several hypotheses have been proposed to explain the evolution of polyandry in species that provide nuptial gifts. When nuptial gifts are in the form of nutritional elements in the ejaculate and ejaculate size is correlated with male body size, females can accrue both direct (nutritional) and indirect (genetic) benefits from multiple mating. We examined remating decisions in females of the seed beetle Stator limbatus and, using path analysis, examined the effects of male body size on the size of his ejaculate, the amount of ejaculate that was successfully transferred to females, and the overall effect of these variables on female fecundity. Larger males produced larger ejaculates and consequently transferred a larger ejaculate to females, but the effects on female fecundity differed between the females' first and second mates. Both larger first and second males were able to transfer more of their ejaculate to females than were smaller males. Both the total amount of ejaculate transferred by these males and polyandry (number of matings) were positively correlated to female fecundity independently of each other. However, larger second males were more successful at stimulating female fecundity independently of how much ejaculate they transferred. We also provide evidence that females are choosy during their second mating opportunity. Both female choosiness and higher female investment after mating with larger second males suggest that females may benefit from both direct and indirect effects from multiple mating. We also conclude that male body size is under both directional fecundity selection and directional sexual selection.

EFFECTS OF NATURAL AND SEXUAL SELECTION ON ADAPTIVE POPULATION DIVERGENCE AND PREMATING ISOLATION IN A DAMSELFLY

The relative strength of different types of directional selection has seldom been compared directly in natural populations. A recent meta‐analysis of phenotypic selection studies in natural populations suggested that directional sexual selection may be stronger in magnitude than directional natural selection, although this pattern may have partly been confounded by the different time scales over which selection was estimated. Knowledge about the strength of different types of selection is of general interest for understanding how selective forces affect adaptive population divergence and how they may influence speciation. We studied divergent selection on morphology in parapatric, natural damselfly (Calopteryx splendens) populations. Sexual selection was stronger than natural selection measured on the same traits, irrespective of the time scale over which sexual selection was measured. Visualization of the fitness surfaces indicated that population divergence in overall morphology is more strongly influenced by divergent sexual selection rather than natural selection. Courtship success of experimental immigrant males was lower than that of resident males, indicating incipient sexual isolation between these populations. We conclude that current and strong sexual selection promotes adaptive population divergence in this species and that premating sexual isolation may have arisen as a correlated response to divergent sexual selection. Our results highlight the importance of sexual selection, rather than natural selection in the adaptive radiation of odonates, and supports previous suggestions that divergent sexual selection promotes speciation in this group.