DISENTANGLING PRECOPULATORY AND POSTCOPULATORY SEXUAL SELECTION IN POLYANDROUS SPECIES

Sexual selection operates on a sequence of events, from mating to offspring production. Which stages in this sequence undergo stronger selection, especially the relative importance of pre‐ versus postcopulatory processes, are intensely debated issues. Unequal siring success among mates of polyandrous females is classically taken as evidence for a large contribution of postcopulatory processes to the variance in male reproductive success (var(RS_m)). However, paternity skews also depend on the timing and number of copulations, a source of variation that should be considered precopulatory rather than postcopulatory. We develop a method for decomposing var(RS_m) accounting for copulatory activity and apply it to experimental mating groups of the snail Physa acuta. In our experiment, 40% of var(RS_m) emerges at the precopulatory stage, only half of which depends on variation in mating success (number of partners). Ignoring copulation characteristics can therefore lead to severe underestimation of precopulatory sexual selection. Moreover, although only 36% of var(RS_m) arises at the postcopulatory stage, this is when sexual selection on body weight mostly occurs. Finally, trade‐offs were detected between different components of precopulatory success, whereas pre‐ and postcopulatory success appear independent. Our study opens the way to a detailed quantitative understanding of sexual selection in polyandrous species.     

Validation of Bateman's principles: a genetic study of sexual selection and mating patterns in the rough-skinned newt

Few studies have influenced thought on the nature of sexual selection to the extent of the classic paper of A. J. Bateman on mating patterns in Drosophila. However, interpretation of his study remains controversial, and a lack of modern empirical evidence prevents a consensus with respect to the perceived utility of Bateman's principles in the study of sexual selection. Here, we use a genetic study of natural mating patterns in the rough-skinned newt, Taricha granulosa, to investigate the concordance between Bateman's principles and the intensity of sexual selection. We found that males experienced strong sexual selection on tail height and body size, while sexual selection was undetectable in females. This direct quantification of sexual selection agreed perfectly with inferences that are based on Bateman's principles. Specifically, males (in comparison with females) exhibited greater standardized variances in reproductive and mating success, as well as a stronger relationship between mating success and reproductive success. Overall, our results illustrate that Bateman's principles provide the only quantitative measures of the mating system with explicit connections to formal selection theory and should be the central focus of studies of mating patterns in natural populations.     

HOMAGE TO BATEMAN: SEX ROLES PREDICT SEX DIFFERENCES IN SEXUAL SELECTION

Classic sex role theory predicts that sexual selection should be stronger in males in taxa showing conventional sex roles and stronger in females in role reversed mating systems. To test this very central prediction and to assess the utility of different measures of sexual selection, we estimated sexual selection in both sexes in four seed beetle species with divergent sex roles using a novel experimental design. We found that sexual selection was sizeable in females and the strength of sexual selection was similar in females and males in role‐reversed species. Sexual selection was overall significantly stronger in males than in females and residual selection formed a substantial component of net selection in both sexes. Furthermore, sexual selection in females was stronger in role‐reversed species compared to species with conventional sex roles. Variance‐based measures of sexual selection (the Bateman gradient and selection opportunities) were better predictors of sexual dimorphism in reproductive behavior and morphology across species compared to trait‐based measures (selection differentials). Our results highlight the importance of using assays that incorporate components of fitness manifested after mating. We suggest that the Bateman gradient is generally the most informative measure of the strength of sexual selection in comparisons across sexes and/or species.     

INTERACTION-INDEPENDENT SEXUAL SELECTION AND THE MECHANISMS OF SEXUAL SELECTION

Darwin identified explicitly two types of sexual selection, male contests (combat and displays) and female choice, and he devoted the overwhelming majority of his examples to traits that influence the outcome of these interactions. Subsequent treatments of sexual selection have emphasized the importance of intra- and intersexual interactions as sources of sexual selection. However, many traits that are important determinants of mating success influence mating success without necessarily affecting the outcome of intra- and intersexual interactions. Here, I argue that traits can be subject to sexual selection even if they do not affect the outcome of intra- and intersexual interactions. I distinguish two types of sexual selection, interaction-independent and interaction-dependent selection, based on whether variance in mating success is the result of trait-dependent outcomes of interactions between conspecifics. I then use this distinction to construct a framework for classifying types of sexual selection that unifies and expands previously proposed frameworks. Finally, I outline several implications that the concept of interaction-independent sexual selection has for the general theory of sexual selection.     

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.     

A reappraisal of Bateman's classic study of intrasexual selection

Bateman's (1948) study showing greater variances in number of mates and reproductive success in male than female Drosophila melanogaster is a foundational paper in sexual selection. Here we show for the first time that his methods had flaws, including the elimination of genetic variance, sampling biases, miscalculations of fitness variances, statistical pseudo-replication, and selective presentation of data. We conclude that Bateman's results are unreliable, his conclusions are questionable, and his observed variances are similar to those expected under random mating. Despite our analysis, we do not intend this article as a criticism of Bateman; he accomplished his work without modern computational tools, and his approach was groundbreaking emphasizing the significance of fitness variance for sexual selection. However, this reanalysis has implications for what counts as evidence for sexual selection and we believe that our concerns should be of interest to contemporary students of sexual selection. We call for repetitions of Bateman's study using modern statistical and molecular methods.     

EFFECTS OF SOCIAL AND EXTRA‐PAIR MATING ON SEXUAL SELECTION IN BLUE TITS (CYANISTES CAERULEUS)

The contribution of extra‐pair paternity (EPP) to sexual selection has received considerable attention, particularly in socially monogamous species. However, the importance of EPP remains difficult to assess quantitatively, especially when many extra‐pair young have unknown sires. Here, we combine measurements of the opportunity for selection (I), the opportunity for sexual selection (I_S), and the strength of selection on mating success (Bateman gradient, β_SS) with a novel simulation of random mating tailored to the specific mating system of the blue tit (Cyanistes caeruleus). In a population where social polygyny and EPP are common, the opportunity for sexual selection was significantly stronger and Bateman gradients significantly steeper for resident males than for females. In general, success with the social mate(s) contributed most to variation in male reproductive success. Effects of EPP were small, but significantly higher than expected under random mating. We used sibship analysis to estimate the number of unknown sires in our population. Under the assumption that the unknown sires are nonbreeding males, EPP reduced the variance in and the strength of selection on mating success, a possibility that hitherto has not been considered.     

Molecular parentage analysis in experimental newt populations: the response of mating system measures to variation in the operational sex ratio

Molecular studies of parentage have been extremely influential in the study of sexual selection in the last decade, but a consensus statistical method for the characterization of genetic mating systems has not yet emerged. Here we study the utility of alternative mating system measures by experimentally altering the intensity of sexual selection in laboratory-based breeding populations of the rough-skinned newt. Our experiment involved skewed sex ratio (high sexual selection) and even sex ratio (low sexual selection) treatments, and we assessed the mating system by assigning parentage with microsatellite markers. Our results show that mating system measures based on Bateman's principles accurately reflect the intensity of sexual selection. One key component of this way of quantifying mating systems is the Bateman gradient, which is currently underutilized in the study of genetic mating systems. We also compare inferences based on Bateman's principles with those obtained using two other mating system measures that have been advocated recently (Morisita's index and the index of resource monopolization), and our results produce no justification for the use of these alternative measures. Overall, our results show that Bateman's principles provide the best available method for the statistical characterization of mating systems in nature.     

Quantitative measure of sexual selection with respect to the operational sex ratio: a comparison of selection indices

Despite numerous indices proposed to predict the evolution of mating systems, a unified measure of sexual selection has remained elusive. Three previous studies have compared indices of sexual selection under laboratory conditions. Here, we use a genetic study to compare the most widely used measures of sexual selection in natural populations. We explored the mating and reproductive successes of male and female bank voles, Clethrionomys glareolus, across manipulated operational sex ratios (OSRs) by genotyping all adult and pup bank voles on 13 islands using six microsatellite loci. We used Bateman's principles (Is and I and Bateman gradients) and selection coefficients (s' and beta') to evaluate, for the first time, the genetic mating system of bank voles and compared these measures with alternative indices of sexual selection (index of monopolization and Morisita's index) across the OSRs. We found that all the sexual selection indices show significant positive intercorrelations for both males and females, suggesting that Bateman's principles are an accurate and a valid measure of the mating system. The Bateman gradient, in particular, provides information over and above that of other sexual selection indices. Male bank voles show a greater potential for sexual selection than females, and Bateman gradients indicate a polygynandrous mating system. Selection coefficients reveal strong selection gradients on male bank vole plasma testosterone level rather than body size.     

THE DARWIN-FISHER THEORY OF SEXUAL SELECTION IN MONOGAMOUS BIRDS

Males of monogamous birds often show secondary sexual traits that are conspicuous but considerably less extreme than those of polygynous species. We develop a quantitative-genetic model for the joint evolution of a male secondary sexual trait, a female mating preference, and female breeding date, following a theory proposed by Darwin and Fisher. Good nutritional condition is postulated to cause females to breed early and to have high fecundity. The most-preferred males are mated by early-breeding females and receive a sexual-selection advantage from those females' greater reproductive success. Results show that conspicuous male traits that decrease survival can evolve but suggest that the extent of maladaptive evolution is greatly limited relative to what is possible in a polygynous mating system for two reasons. First, in the absence of direct fitness effects of mate choice on the female, the equilibria for the male trait and female preference form a curve whose shape shows that the maximum possible strength of sexual selection on males (and hence the potential for maladaptive evolution) is constrained. Under certain conditions, a segment of the equilibrium curve may become unstable, leading to two alternative stable states for the male trait. Second, male parental care will often favor the evolution of mating preferences for less conspicuous males. We also find that sexual selection can appear in the absence of the nutritional effects emphasized by Darwin and Fisher. A review of the literature suggests that the assumptions of the Darwin-Fisher mechanism may often be met in monogamous birds and that other mechanisms may often reinforce it by producing additional components of sexual selection.     

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.     

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.     

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.     

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.     

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.     

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.     

One tool, many uses: precopulatory sexual selection on genital morphology in Aquarius remigis

While congruent evidence indicates that sexual selection is the most likely selective force explaining the rapid divergence of male genital morphology in insects, the mechanisms involved in this process remain unclear. In particular, little attention has been paid to precopulatory sexual selection. We examine sexual selection for mating success on male genital components in six populations of Aquarius remigis, a water strider characterized by unique genital morphology. Multivariate selection analysis confirms previous findings that precopulatory sexual selection favours longer external genitalia, and provides new evidence that this selection acts independently on external genital components. In contrast, the size of the major internal genital sclerite is not correlated with mating success. Thus, precopulatory sexual selection acts strongly on the size of the external genitalia, but not on the intromittent organ itself. These results highlight the multiple functions of genital organs and the importance of both precopulatory and post-copulatory sexual selection in shaping the remarkable diversity of male genitalia in insects.     

SEXUAL SELECTION THROUGH FEMALE CHOICE IN LAWES' PAROTIA,A LEK-MATING BIRD OF PARADISE

We studied sexual selection in Lawes' Parotia, a lek-mating bird of paradise, during 1981–1983 in Papua New Guinea. There was a high variance in mating success among males, with fewer than half of the individuals mating in any one year. This variance was independent of male-male interactions and disruptions. A role of female choice in sexual selection was suggested by the patterns of female visitation to courts and statistical correlations across males between phenotypic traits and mating success. Females repeatedly visited most males in their home ranges and began visiting males up to six weeks before mating. In one or more years, six aspects of male behavior and one morphological variable were positively correlated with mating success, but the probability values were not significant using a simultaneous inference test. Calculation of combined probability values across all three years revealed that one aspect of male display behavior, the probability of display, positively and significantly influenced mating status. The probability of display was also significantly correlated with relative mating success among males. Females showed strong fidelity to mates, both within and between seasons. Display sites of male Lawes' Parotia are variably dispersed, but mating success did not differ for grouped and solitary males. These data confirm an important role of female choice in sexual selection in birds of paradise but also suggest that female choice may be unrelated to the process of lek-initiation in this species.     

The Measurement of Sexual Selection Using Bateman's Principles: An Experimental Test in the Sex-Role-Reversed Pipefish Syngnathus typhle

Angus J. Bateman's classic study of sexual selection in Drosophila melanogaster has had a major influence on the development of sexual selection theory. In some ways, Bateman's study has served a catalytic role by stimulating debate on sex roles, sexual conflict and other topics in sexual selection. However, there is still considerable disagreement regarding whether or not "Bateman's principles" are helpful in the study of sexual selection. Here, we test the idea that Bateman's principles provide the basis for a useful method to quantify and compare mating systems. In this study, we focus on the sex-role-reversed pipefish Syngnathus typhle as a model system to study the measurement of sexual selection. We set up artificial breeding assemblages of pipefish in the laboratory and used microsatellite markers to resolve parentage. Three different sex-ratio treatments (female-biased, even and male-biased) were used to manipulate the expected intensity of sexual selection. Measures of the mating system based on Bateman's principles were calculated and compared to the expected changes in the intensity of sexual selection. We also compare the results of this study to the results of a similar study of Bateman's principles in the rough-skinned newt, a species with conventional sex roles. The results of this experiment show that measures of the mating system based on Bateman's principles do accurately capture the relative intensities of sexual selection in the different treatments and species. Thus, widespread use of Bateman's principles to quantify mating systems in nature would facilitate comparative studies of sexual selection and mating system evolution.     

Bateman's Principle and Simultaneous Hermaphrodites: A Paradox

Bateman's principle states that reproductive success is limiteda) in females by the resources available for egg production;and b) in males, only by access to females and/or eggs. Theprinciple has been used to generate predictions for two aspectsof hermaphroditism; a) the advantage of hermaphroditism andb) sexual conflict. Comparing these predictions to the empiricaldata offers tests of Bateman's principle. Charnov's predictionthat hermaphroditism would occur under circumstances where Bateman'sprinciple does not apply is found to be largely correct. However,the prediction as to the association of hermaphroditism andlow fixed costs is inconsistent with the data. Alternative explanationsthat predict that hermaphroditism is a strategy for reducingvariance in reproductive success may better explain the data.Probability theory demonstrates that where two strategies haveequal mean fitness, which must be the case for male and femalefunction, the strategy with the lower variance in reproductivesuccess must have higher fitness (Gillespie's principle). Bateman'sprinciple predicts that this will be the female role in hermaphrodites.However, Charnov, assuming Bateman's principle, predicted thatsexual conflict stemming from a preference for the male rolewould be important in hermaphrodite mating systems, creatinga paradox. Many hermaphrodite mating systems are based on conditionalreciprocity with a preferred sexual role indicating sexual conflict.The data demonstrate that the preferred role varies among taxa,contrary to the predictions of Bateman's principle. It has beensuggested that Bateman's principle can explain cases in whichthe female role is preferred (sperm-trading) as involving energyrather than gamete trading. However, energetic considerationssuggest that energy trading would only be adaptive if Bateman'sprinciple does not apply, paradoxically. The gamete tradingmodel, based on the prediction that the role that offers controlof fertilization will be preferred, is more consistent withthe data. Application of Bateman's principle to hermaphroditesleads to contradictory predictions and does not offer the basisfor a coherent theory of sexual selection, as Bateman proposed.