THE EVOLUTION OF SEXUAL DIMORPHISM BY SEXUAL SELECTION: THE SEPARATE EFFECTS OF INTRASEXUAL SELECTION AND INTERSEXUAL SELECTION

Libellula luctuosa, a pond dragonfly found in eastern North America, is apparently sexually dimorphic. Previous studies of the mating behavior in this species suggested that both male-male competition and female mate choice are important influences. Males compete for territories, where they attract females and where mating occurs. Female behavior influences both the copulation success and the fertilization success of males. Because of temporal and spatial separation of these episodes of sexual selection, multivariate and nonparametric statistical techniques could be used to investigate the influence of components of sexual selection on various sexually dimorphic traits. Sexual dimorphism in L. luctuosa was first quantified; then the direct effects and the form of selection were estimated. Sexually dimorphic wing size, body size, wing coloration, and body coloration are distributed either continuously or discontinuously between the sexes in L. luctuosa. These traits have apparently diverged between the sexes as a result of directional sexual selection. Body size is further influenced by stabilizing selection. Intrasexual selection (success in gaining access to a territory) and intersexual selection (success in copulation and fertilization) can influence the same or different sexually dimorphic characters. Body size is influenced by directional selection during the intrasexual phase of sexual selection and is also influenced by stabilizing selection during intersexual selection. The size of the brown wing patch is influenced by directional selection, primarily during the intersexual phase of sexual selection. There is directional selection on the white wing patch during both phases. Thus, the different proximate mechanisms of sexual selection may jointly or separately affect the evolution of sexually dimorphic characters. Further empirical and theoretical investigations into the differences in the effects of intrasexual selection and intersexual selection are needed to clarify the circumstances leading to separate consequences of these two mechanisms of sexual selection.     

SEXUAL SELECTION,SPACE, AND SPECIATION

A Fisherian model of sexual selection is combined with a diffusion model of mate dispersal to investigate the evolution of assortative mating in a sympatric population. Females mate with one of two types of polygynous males according to a male's display of one of two sex-limited, autosomal traits; these male traits may be associated with differential phenotypic mortalities. Through a Fisherian runaway process, female preferences and male traits can become associated in linkage disequilibrium, leading to patterns of assortative mating. Dispersing males, whose rate of movement is dependent on mating success, carry female preference genes with them, and displaced males thereby produce daughters with preference genes for their respective traits in locally higher than average frequencies. The reduced diffusion of the more preferred males permits the success of other male types in adjacent areas. Thus, mating-success dependent diffusion, when coupled with the rapid divergence in phenotypes possible under the Fisher process, can lead to the coexistence of two female preferences and two male traits in sympatry. We argue that many existing approaches to sympatric speciation fail to explain observed male polymorphisms because they exclude explicit spatial structure from their speciation models.     

SEXUALLY TRANSMITTED DISEASE AND PARASITE-MEDIATED SEXUAL SELECTION

Few studies have investigated the consequences of parasite-mediated sexual selection on the parasites involved. In some cases parasite-mediated sexual selection could lead to increased virulence, but I develop a simple model that shows that, if a parasite is sexually transmitted (i.e., is a sexually transmitted disease, or STD) and if mating success of the host is adversely affected by the parasite, then less virulent STDs will be selected for because transmission of the STD depends on the mating success of the host. This selection for reduced virulence could have important consequences for the role of STDs in sexual selection.     

DIRECT AND INDIRECT SEXUAL SELECTION AND QUANTITATIVE GENETICS OF MALE TRAITS IN GUPPIES (POECILIA RETICULATA)

Abstract.— The ornamentation and displays on which sexual attractiveness and thus mating success are based may be complex and comprise several traits. Predicting the outcome of sexual selection on such complex phenotypes requires an understanding of both the direct operation of selection on each trait and the indirect consequences of selection operating directly on genetically correlated traits. Here we report the results of a quantitative genetic analysis of the ornamentation, sexual attractiveness, and mating success of male guppies (Poecilia reticulata). We analyze male ornamentation both from the point of view of single ornamental traits (e.g., the area of each color) and of composite measures of the way the entire pattern is likely to be perceived by females (e.g., the mean and contrast in chroma). We demonstrate that there is substantial additive genetic variation in almost all measures of male ornamentation and that much of this variation may be Y linked. Attractiveness and mating success are positively correlated at the phenotypic and genetic level. Orange area and chroma, the area of a male's tail, and the color contrast of his pattern overall are positively correlated with attractiveness and/or mating success at the phenotypic and genetic levels. Using attractiveness and mating success as measures of fitness, we estimate gradients of linear directional sexual selection operating on each male trait and use equations of multivariate evolutionary change to predict the response of male ornamentation to this sexual selection. From these analyses, we predict that indirect selection may have important effects on the evolution of male guppy color patterns.     

PURGING THE GENOME WITH SEXUAL SELECTION: REDUCING MUTATION LOAD THROUGH SELECTION ON MALES

Healthy males are likely to have higher mating success than unhealthy males because of differential expression of condition‐dependent traits such as mate searching intensity, fighting ability, display vigor, and some types of exaggerated morphological characters. We therefore expect that most new mutations that are deleterious for overall fitness may also be deleterious for male mating success. From this perspective, sexual selection is not limited to influencing those genes directly involved in exaggerated morphological traits but rather affects most, if not all, genes in the genome. If true, sexual selection can be an important force acting to reduce the frequency of deleterious mutations and, as a result, mutation load. We review the literature and find various forms of indirect evidence that sexual selection helps to eliminate deleterious mutations. However, direct evidence is scant, and there are almost no data available to address a key issue: is selection in males stronger than selection in females? In addition, the total effect of sexual selection on mutation load is complicated by possible increases in mutation rate that may be attributable to sexual selection. Finally, sexual selection affects population fitness not only through mutation load but also through sexual conflict, making it difficult to empirically measure how sexual selection affects load. Several lines of enquiry are suggested to better fill large gaps in our understanding of sexual selection and its effect on genetic load.     

PERSPECTIVE: CHASE-AWAY SEXUAL SELECTION: ANTAGONISTIC SEDUCTION VERSUS RESISTANCE

A model of sexual selection that leads to the evolution of exaggerated male display characters that is based on antagonistic coevolution between the sexes is described. The model is motivated by three lines of research: intersexual conflict with respect to mating, sensory exploitation, and the evolution of female resistance, as opposed to preference, for male display traits. The model generates unique predictions that permit its operation to be distinguished from other established models of sexual selection. One striking prediction is that females will frequently win the coevolutionary arms race with males, leaving them encumbered with costly ornaments that have little value except that their absence understimulates females. Examples from the literature suggest that the model may have broad application in nature. The chase-away model is a special case of the more general phenomenon of Interlocus Contest Evolution (ICE).     

ON THE OPPORTUNITY FOR SEXUAL SELECTION, THE BATEMAN GRADIENT AND THE MAXIMUM INTENSITY OF SEXUAL SELECTION

Bateman's classic paper on fly mating systems inspired quantitative study of sexual selection but also resulted in much debate and confusion. Here, I consider the meaning of Bateman's principles in the context of selection theory. Success in precopulatory sexual selection can be quantified as a "mating differential," which is the covariance between trait values and relative mating success. The mating differential is converted into a selection differential by the Bateman gradient, which is the least squares regression of relative reproductive success on relative mating success. Hence, a complete understanding of precopulatory sexual selection requires knowledge of two equally important aspects of mating patterns: the mating differential, which requires a focus on mechanisms generating covariance between trait values and mating success, and the Bateman gradient, which requires knowledge of the genetic mating system. An upper limit on the magnitude of the selection differential on any sexually selected trait is given by the product of the standard deviation in relative mating success and the Bateman gradient. This latter view of the maximum selection differential provides a clearer focus on the important aspects of precopulatory sexual selection than other methods and therefore should be an important part of future studies of sexual selection.     

SPATIAL VARIATION IN SELECTIVE REGIMES: SEXUAL SELECTION IN THE WATER STRIDER,GERRIS ODONTOGASTER

Studies of phenotypic selection in natural populations are often concerned with simply detecting selection. In adopting a more mechanistic approach, this study compares the sexual selection regimes in natural populations of the water strider Gerris odontogaster with a priori predictions of selection, based on a number of previous field and laboratory studies of the behavioral mechanisms of selection. In this species, a general reluctance of females to mate allows for intersexual selection for ability to subdue reluctant females in males. Female reluctance to mate has been shown to decrease with increasing population density, suggesting that sexual selection should be weaker in high density populations. Three different populations with large differences in population density were studied. A number of traits including parasite load, body mass, body size and male abdominal process length were found to experience significant sexual selection. The investigated populations differed considerably with regard to the total strength of selection on the measured traits and the form of selection on single traits. In general, males in the population with the highest density experienced the weakest selection for grasping ability. This pattern is ascribed to density-related alterations of female mating behavior. Selection for male grasping ability, as reflected by selection on male abdominal process length, is reduced in high-density populations where reluctant females are more easily subdued. Further, the studied populations differed significantly in mean phenotype and phenotypic variance for male abdominal process length. It is suggested that interpopulational differences in selective regimes may generate local adaptations with respect to male abdominal process length, and that gene flow may contribute to the maintenance of the high genetic variation in this trait. It is further suggested that more empirical effort should be made in quantifying and understanding spatial and temporal variation in selection in natural populations, since this may provide information on the prevalence of local adaptations in metric traits and on the mechanisms of selection.     

SEXUAL SELECTION AND THE EVOLUTION OF SEXUAL SIZE DIMORPHISM IN THE WATER STRIDER,AQUARIUS REMIGIS

Sexual size dimorphism (SSD) is often attributed to sexual selection, particularly when males are the larger sex. However, sexual selection favoring large males is common even in taxa where females are the larger sex, and is therefore not a sufficient explanation of patterns of SSD. As part of a more extensive study of the evolution of SSD in water striders (Heteroptera, Gerridae), we examine patterns of sexual selection and SSD in 12 populations of Aquarius remigis. We calculate univariate and multivariate selection gradients from samples of mating and single males, for two sexually dimorphic traits (total length and profemoral width) and two sexually monomorphic traits (mesofemoral length and wing form). The multivariate analyses reveal strong selection favoring larger males, in spite of the female-biased SSD for this trait, and weaker selection favoring aptery and reduced mesofemoral length. Selection is weakest on the most dimorphic trait, profemoral width, and is stabilizing rather than directional. The pattern of sexual selection on morphological traits is therefore not concordant with the pattern of SSD. The univariate selection gradients reveal little net selection (direct + indirect) on any of the traits, and suggest that evolution away from the plesiomorphic pattern of SSD is constrained by antagonistic patterns of selection acting on this suite of positively correlated morphological traits. We hypothesize that SSD in A. remigis is not in equilibrium, a hypothesis that is consistent with both theoretical models of the evolution of SSD and our previous studies of allometry for SSD. A negative interpopulation correlation between the intensity of sexual selection and the operational sex ratio supports the hypothesis that, as in several other water strider species, sexual selection in A. remigis occurs through generalized female reluctance rather than active female choice. The implications of this for patterns of sexual selection are discussed.     

MODE OF SEXUAL SELECTION DETERMINED BY RESOURCE ABUNDANCE IN TWO SAND GOBY POPULATIONS

We used field observations and experiments to show that sexual selection in two populations of sand gobies, Pomatoschistus minutus (Pisces, Gobiidae), was affected by differences in resource availability. Male sand gobies rely on empty mussel shells for nest building and spawning. The two populations differed considerably in nest-site abundance and sexual-selection regimes. In one population nest sites were scarce, leading to stronger male-male competition over nests, a higher nest site colonization rate and reduced potential for female choice compared with the other population that had a surplus of nests. In the high-competition population, males were larger than females, perhaps as a response to selection, whereas the other population was not sexually size dimorphic. The results from the field were confirmed in a pool experiment that demonstrated the effect of nest abundance on nest occupancy and male reproductive success. Larger males were more successful in obtaining nest sites in both high and low nest availability treatments. Larger males were also favored by females as mating partners, but only in the treatment with surplus nest sites. Nest shortage was associated with an increased potential for intrasexual selection (measured as the coefficient of variation), whereas the potential for intersexual selection was increased when nests were common. In conclusion, nest-site abundance can influence the relative contribution of intrasexual competition and mate choice in a population. Hence, resource availability can contribute to within-species variation in mating patterns.     

SIGNALING EFFICACY DRIVES THE EVOLUTION OF LARGER SEXUAL ORNAMENTS BY SEXUAL SELECTION

Why are there so few small secondary sexual characters? Theoretical models predict that sexual selection should lead to reduction as often as exaggeration, and yet we mainly associate secondary sexual ornaments with exaggerated features such as the peacock's tail. We review the literature on mate choice experiments for evidence of reduced sexual traits. This shows that reduced ornamentation is effectively impossible in certain types of ornamental traits (behavioral, pheromonal, or color‐based traits, and morphological ornaments for which the natural selection optimum is no trait), but that there are many examples of morphological traits that would permit reduction. Yet small sexual traits are very rarely seen. We analyze a simple mathematical model of Fisher's runaway process (the null model for sexual selection). Our analysis shows that the imbalance cannot be wholly explained by larger ornaments being less costly than smaller ornaments, nor by preferences for larger ornaments being less costly than preferences for smaller ornaments. Instead, we suggest that asymmetry in signaling efficacy limits runaway to trait exaggeration.     

SEXUAL SELECTION AND MALE CHARACTERISTICS IN THE BLUEHEAD WRASSE,THALASSOMA BIFASCIATUM: MATING SITE ACQUISITION,MATING SITE DEFENSE,AND FEMALE CHOICE

Through a series of replacement experiments with the bluehead wrasse, Thalassoma bifasciatum, we have identified male morphological characteristics that appear to be under phenotypic sexual selection. We were particularly interested in whether the various sources of sexual selection (male-male competition for unoccupied mating sites, defense of mating sites against small males, and female choice of males) were (1) independently associated with different phenotypic characteristics; (2) jointly affected the same characteristic in the same way; or (3) jointly affected the same characteristic in an antagonistic fashion. We replaced the resident large, brightly colored Terminal Phase (TP) males on a reef with the same number of TP males from other reefs. When transplanted, these males contest with each other to take over mating sites. The transplanted group of males were then scored for three components of fitness: (1) the quality of the site obtained through competition with other large males; (2) the male's ability to defend arriving females from small intruding males; and (3) changes in female visits to the site once the new male takes over. The first and second components are part of intrasexual selection; the third represents intersexual selection. We measured the opportunity for selection by partitioning variance in mating success, and measured the direct effects of sexual selection by estimating the covariance between morphology and fitness components. Opportunities for selection: Because females generally remain faithful to particular mating sites, most (54%) of the explainable variation in male mating success is due to the acquisition of a particular mating territory, which is the outcome of competition among TP males. There was less variation in mating success due to shifts in site use by females and defense of females against the intrusions of smaller males, but all components were significant. Effects of selection: Success in male–male competition among TP males, estimated by the quality of the territory acquired, was positively associated with body length and the relative length of the pectoral fin. Success in territorial defense against small males was primarily related to body length, with lesser contributions from body depth and the area of a white band on the flank. Contribution to fitness through female choice of males was positively associated with white band area. In the two instances where a character was associated with two fitness components, the direction of selection was the same. While body length was positively associated with winning intrasexual contests, it was not correlated to any behavioral measures of aggression. Similarly, the white band associated with attractiveness was not correlated with any aspect of courtship or aggression. Parasite load was uncorrelated with other morphological characters, and did not appear to affect any aspect of sexual selection. There was no evidence for stabilizing selection or significant additional contributions from second-order effects to the fitness surfaces. Fitness functions calculated using cubic splines were generally linear except for body length, which appeared sigmoid in its effect on site acquisition ability; this same feature tended to plateau in its effect on site defense. Analyses of the interactions of selection gradients with reef or experiment indicated that the effect of particular male characters on estimates of fitness was generally homogeneous in both time and space.     

SEXUAL SELECTION AND BUTTERFLY DESIGN—A COMPARATIVE STUDY

Temperate butterflies of 44 species were examined to determine if their mating system (perching and patrolling) affected flight design. To control for spurious effects due to ancestry, 25 of these species were assigned to eight contrasts within which a change in mating system had occurred. In perching species sexual selection was predicted to favor traits associated with high acceleration ability and speed, while in patrolling species traits associated with flight endurance were predicted. In conformance with these expectations males of perching species had larger thorax/body mass ratios, higher wing loadings, and higher aspect ratios than patrolling species. The male mating system affected females in the same direction in the same variables as males. This could be explained by a genetic correlation with males. When removing the covariance between the sexes, only male design was explained by the mating system. The mating system was also associated with different degrees of sexual dimorphism in wing size. This supported the hypothesis that male design was affected by the mating system.     

OPERATIONAL SEX RATIO BUT NOT DENSITY AFFECTS SEXUAL SELECTION IN A FISH

The operational sex ratio (OSR) and density are considered important factors affecting the strength of sexual selection. Although there is increasing evidence that OSR and density affect the potential for sexual selection, few studies have addressed whether this is realized in phenotypic selection and how the two factors interact. We manipulated OSR (three levels) and male density (two levels) in 36 experimental breeding populations of Gobiusculus flavescens—a fish with paternal care. We measured mating competition behavior, the opportunity for selection (I), and selection on four morphological traits in males. We found sexual selection on two male traits, with the strongest selection being 20% of I. As predicted from OSR theory, increasing female scarcity caused males to become more competitive, concomitant with an increase in I and selection on morphological traits. Model simulations of I based on random mating (I_min) and maximum mate monopolization (I_max) demonstrated that the potential for sexual selection was close to its theoretical maximum across the range of OSRs. However, male density and its interaction with the OSR did not affect sexual selection. We argue that a multifaceted approach, combining mating behavior and selection analyses, can help us to understand how ecological factors affect sexual selection.     

SEXUAL SELECTION AGAINST HYBRIDS BETWEEN SYMPATRIC STICKLEBACK SPECIES: EVIDENCE FROM A FIELD EXPERIMENT

Sexual selection against viable, fertile hybrids may contribute to reproductive isolation between recently diverged species. If so, then sexual selection may be implicated in the speciation process. Laboratory measures of the mating success of hybrids may underestimate the amount of sexual selection against them if selection pressures are habitat specific. Male F₁ hybrids between sympatric benthic and limnetic sticklebacks (Gasterosteus aculeatus complex) do not suffer a mating disadvantage when tested in the laboratory. However, in the wild males choose different microhabitats and parental females tend to be found in the same habitats as conspecific males. This sets up the opportunity for sexual selection against male hybrids because they must compete with parental males for access to parental females. To test for sexual selection against adult F₁ hybrid males, we examined their mating success in enclosures in their preferred habitat (open, unvegetated substrate) where limnetic males and females also predominate. We found significantly reduced mating success in F₁ hybrid males compared with limnetic males. Thus, sexual selection, like other mechanisms of postzygotic isolation between young sister species, may be stronger in a wild setting than in the laboratory because of habitat-specific selection pressures. Our results are consistent with, but do not confirm, a role for sexual selection in stickleback speciation.     

EVOLUTION OF DIVERGENT FEMALE MATING PREFERENCE IN RESPONSE TO EXPERIMENTAL SEXUAL SELECTION

Sexual selection is predicted to drive the coevolution of mating signals and preferences (mating traits) within populations, and could play a role in speciation if sexual isolation arises due to mating trait divergence between populations. However, few studies have demonstrated that differences in mating traits between populations result from sexual selection alone. Experimental evolution is a promising approach to directly examine the action of sexual selection on mating trait divergence among populations. We manipulated the opportunity for sexual selection (low vs. high) in populations of Drosophila pseudoobscura. Previous studies on these experimental populations have shown that sexual selection manipulation resulted in the divergence between sexual selection treatments of several courtship song parameters, including interpulse interval (IPI) which markedly influences male mating success. Here, we measure female preference for IPI using a playback design to test for preference divergence between the sexual selection treatments after 130 generations of experimental sexual selection. The results suggest that female preference has coevolved with male signal, in opposite directions between the sexual selection treatments, providing direct evidence of the ability of sexual selection to drive the divergent coevolution of mating traits between populations. We discuss the implications in the context sexual selection and speciation.     

SEXUAL SELECTION CAN REMOVE AN EXPERIMENTALLY INDUCED MUTATION LOAD

Sexual selection is argued to be important for the removal of deleterious mutations, promoting population fitness, accelerating adaptation, and compensating for the two‐fold cost of sex. Here we induced mutations in the dung beetle Onthophagus taurus using ionizing radiation, and tested the efficacy of sexual selection in their removal. Mutations reduced male precopulatory (strength) and postcopulatory (testes mass) sexual traits. Two generations of sexual selection were sufficient to remove mutations that affected male strength, but not testes mass. Induced mutations did not affect female productivity, which was elevated by sexual selection. Our results provide empirical support for the hypothesis that condition‐dependent traits offer a large target for mutational variation, and that sexual selection can purge the genome of deleterious mutations and promote population fitness.     

MULTI‐LEVEL SEXUAL SELECTION: INDIVIDUAL AND FAMILY‐LEVEL SELECTION FOR MATING SUCCESS IN A HISTORICAL HUMAN POPULATION

Precopulatory sexual selection is the association between fitness and traits associated with mate acquisition. Although sexual selection is generally recognized to be a powerful evolutionary force, most investigations are limited to characters belonging to individuals. A broader multilevel perspective acknowledges that individual fitness can be affected by aspects of mating success that are characters of groups, such as families. Parental mating success in polygynous or polyandrous human societies may exemplify traits under group‐level sexual selection. Using fitness measures that account for age‐structure, I measure multilevel selection for mate number over 55 years in a human population with declining rates of polygyny. Sexual selection had three components: individual‐level selection for ever‐mating (whether an individual mated) and individual‐ and family‐level selection for polyandry and polygyny. Family‐ and individual‐level selection for polygyny was equally strong, three times stronger than family‐level selection for polyandry and more than an order of magnitude stronger than individual‐level selection for polyandry. However, individual‐level selection for polyandry and polygyny was more effective at explaining relative fitness variance than family‐level selection. Selection for ever‐mating was the most important source of sexual selection for fitness; variation for ever‐mating explained 23% of relative fitness variance.     

Determinants of male fitness: disentangling intra- and inter-sexual selection

Both intra- and inter-sexual selection may crucially determine a male's fitness. Their interplay, which has rarely been experimentally investigated, determines a male's optimal reproductive strategy and thus is of fundamental importance to the understanding of a male's behaviour. Here we investigated the relative importance of intra- and inter-sexual selection for male fitness in the common lizard. We investigated which male traits predict a male's access to reproduction allowing for both selective pressures and comparing it with a staged mating experiment excluding all types of intra-sexual selection. We found that qualitatively better males were more likely to reproduce and that sexual selection was two times stronger when allowing for both selective pressures, suggesting that inter- and intra-sexual selection determines male fitness and confirming the existence of multi-factorial sexual selection. Consequently, to optimize fitness, males should trade their investment between the traits, which are important for inter- and intra-sexual selection.     

VARIATION IN ACOUSTIC SIGNALLING TRAITS EXHIBITS FOOTPRINTS OF SEXUAL SELECTION

Phenotypic variation is ubiquitous in nature and a precondition for adaptive evolution. However, theory predicts that the extent of phenotypic variation should decrease with increasing strength of selection on a trait. Comparative analyses of trait variability have repeatedly used this expectation to infer the type or strength of selection. Yet, the suggested influence of selection on trait variability has rarely been tested empirically. In the present study, I compare estimates of sexual selection strength and trait variability from published data. I constricted the analysis to acoustic courtship traits in amphibians and insects with known variability and corresponding results of female binary choice experiments on these traits. Trait variability and strength of sexual selection were significantly correlated, and both were correlated with signal duration. Because traits under stronger selection had lower variation even after the effect of signal duration was eliminated, I conclude that traces of the strength of selection can be observed with respect to variation of acoustic signaling traits in insects and amphibians. The analysis also shows that traits under stabilizing selection have significantly lower phenotypic variability than traits under directional selection.