Lifetime reproductive success,selection on lifespan,and multiple sexual ornaments in male European barn swallows

Natural and sexual selection arise when individual fitness varies according to focal traits. Extra‐pair paternities (EPPs) can affect the intensity of selection by influencing variance in fitness among individuals. Studies of selection require that individual fitness is estimated using proxies of lifetime reproductive success (LRS). However, estimating LRS is difficult in large, open populations where EPPs cause reallocation of biological paternity. Here, we used extensive field sampling to estimate LRS in a population of barn swallows (Hirundo rustica) to estimate selection on lifespan and ornamental traits of males. We found selection on lifespan mediated both by within‐ and extra‐pair fertilization success and selection on tail length mediated by within‐ but not extra‐pair fertilization success. In addition, we found selection on tail white spots via extra‐pair fertilization success after controlling for selection on other traits. These results were not confounded by factors that hamper studies of LRS, including nonexhaustive sampling of offspring and biased sampling of males. Hence, natural and sexual selection mediated by LRS operates on lifespan, tail length, and size of the tail white spots in barn swallows.     

Geographical and seasonal variation in the intensity of sexual selection in the barn swallow Hirundo rustica: a meta‐analysis

Sexual selection arises from competition among individuals for access to mates, resulting in the evolution of conspicuous sexually selected traits, especially when inter‐sexual competition is mediated by mate choice. Different sexual selection regimes may occur among populations/subspecies within the same species. This is particularly the case when mate choice is based on multiple sexually selected traits. However, empirical evidence supporting this hypothesis at the among‐populations level is scarce. We conducted a meta‐analysis of the intensity of sexual selection on the largest database to date for a single species, the barn swallow (Hirundo rustica), relying on quantitative estimates of sexual selection. The intensity of sexual selection was expressed as the strength (effect size) of the relationships between six plumage ornaments (tail length, tail asymmetry, size of white spots on tail, ventral plumage colour, throat plumage colour and throat patch size) and several fitness proxies related to reproduction, parental care, offspring quality, arrival date from spring migration, and survival. The data were gathered for four geographically separated subspecies (H. r. rustica, H. r. erythrogaster, H. r. gutturalis, H. r. transitiva). The overall mean effect size (Z_r = 0.214; 95% confidence interval = 0.175–0.254; N = 329) was of intermediate magnitude, with intensity of sexual selection being stronger in males than in females. Effect sizes varied during the breeding cycle, being larger before egg deposition, when competition for access to mates reaches its maximum (i.e. in the promiscuous part of the breeding cycle), and decreasing thereafter. In addition, effect sizes from experiments were not significantly larger than those from correlative studies. Finally, sexual selection on different sexually dimorphic traits varied among subspecies. This last result suggests that morphological divergence among populations has partly arisen from divergent sexual selection, which may eventually lead to speciation.     

Measurement of concurrent selection episodes

Current methods for measuring selection with longitudinal data have been developed with the assumption that episodes of selection are sequential. However, a number of empirical examinations have demonstrated that natural and sexual selection may act concurrently and in opposing directions. Other recent work has highlighted the difficulty of assigning fitness values for survival when reproduction and mortality within a population temporally overlap. I treat these as facets of a single problem; how to analyze selection where mortality and reproduction are concurrent. To address this problem, I formalize a method to estimate total fitness of individuals over a period of time utilizing longitudinal data. I then show how the fitness may be partitioned to provide two separate estimates of fitness for reproductive opportunity and reproductive success. In addition, another total fitness estimate for the period can be obtained from the two partitioned estimates. This procedure will allow calculation of total fitness where there are some missing datapoints for reproductive success of an individual. A simulation indicates that bias is generally low for the various fitness estimates. These methods should expand our ability to understand the interaction of different selection episodes.     

COMPARING STRENGTHS OF DIRECTIONAL SELECTION: HOW STRONG IS STRONG?

The fundamental equation in evolutionary quantitative genetics, the Lande equation, describes the response to directional selection as a product of the additive genetic variance and the selection gradient of trait value on relative fitness. Comparisons of both genetic variances and selection gradients across traits or populations require standardization, as both are scale dependent. The Lande equation can be standardized in two ways. Standardizing by the variance of the selected trait yields the response in units of standard deviation as the product of the heritability and the variance-standardized selection gradient. This standardization conflates selection and variation because the phenotypic variance is a function of the genetic variance. Alternatively, one can standardize the Lande equation using the trait mean, yielding the proportional response to selection as the product of the squared coefficient of additive genetic variance and the mean-standardized selection gradient. Mean-standardized selection gradients are particularly useful for summarizing the strength of selection because the mean-standardized gradient for fitness itself is one, a convenient benchmark for strong selection. We review published estimates of directional selection in natural populations using mean-standardized selection gradients. Only 38 published studies provided all the necessary information for calculation of mean-standardized gradients. The median absolute value of multivariate mean-standardized gradients shows that selection is on average 54% as strong as selection on fitness. Correcting for the upward bias introduced by taking absolute values lowers the median to 31%, still very strong selection. Such large estimates clearly cannot be representative of selection on all traits. Some possible sources of overestimation of the strength of selection include confounding environmental and genotypic effects on fitness, the use of fitness components as proxies for fitness, and biases in publication or choice of traits to study.     

Sexual selection and speciation: the comparative evidence revisited

The spectacular diversity in sexually selected traits in the animal kingdom has inspired the hypothesis that sexual selection can promote species divergence. In recent years, several studies have attempted to test this idea by correlating species richness with estimates of sexual selection across phylogenies. These studies have yielded mixed results and it remains unclear whether the comparative evidence can be taken as generally supportive. Here, we conduct a meta‐analysis of the comparative evidence and find a small but significant positive overall correlation between sexual selection and speciation rate. However, we also find that effect size estimates are influenced by methodological choices. Analyses that included deeper phylogenetic nodes yielded weaker correlations, and different proxies for sexual selection showed different relationships with species richness. We discuss the biological and methodological implications of these findings. We argue that progress requires more representative sampling and justification of chosen proxies for sexual selection and speciation rate, as well as more mechanistic approaches.     

How to quantify (the response to) sexual selection on traits

Natural selection operates via fitness components like mating success, fecundity, and longevity, which can be understood as intermediaries in the causal process linking traits to fitness. In particular, sexual selection occurs when traits influence mating or fertilization success, which, in turn, influences fitness. We show how to quantify both these steps in a single path analysis, leading to better estimates of the strength of sexual selection. Our model controls for confounding variables, such as body size or condition, when estimating the relationship between mating and reproductive success. Correspondingly, we define the Bateman gradient and the Jones index using partial rather than simple regressions, which better captures how they are commonly interpreted. The model can be applied both to purely phenotypic data and to quantitative genetic parameters estimated using information on relatedness. The phenotypic approach breaks down selection differentials into a sexually selected and a “remainder” component. The quantitative genetic approach decomposes the estimated evolutionary response to selection analogously. We apply our method to analyze sexual selection in male dusky pipefish, Syngnathus floridae, and in two simulated datasets. We highlight conceptual and statistical limitations of previous path‐based approaches, which can lead to substantial misestimation of sexual selection.     

An analysis of continent-wide patterns of sexual selection in a passerine bird

Patterns of selection are widely believed to differ geographically, causing adaptation to local environmental conditions. However, few studies have investigated patterns of phenotypic selection across large spatial scales. We quantified the intensity of selection on morphology in a monogamous passerine bird, the barn swallow Hirundo rustica, using 6495 adults from 22 populations distributed across Europe and North Africa. According to the classical Darwin-Fisher mechanism of sexual selection in monogamous species, two important components of fitness due to sexual selection are the advantages that the most attractive males acquire by starting to breed early and their high annual fecundity. We estimated directional selection differentials on tail length (a secondary sexual character) and directional selection gradients after controlling for correlated selection on wing length and tarsus length with respect to these two fitness components. Phenotype and fitness components differed significantly among populations for which estimates were available for more than a single year. Likewise, selection differentials and selection gradients differed significantly among populations for tail length, but not for the other two characters. Sexual selection differentials differed significantly from zero across populations for tail length, particularly in males. Controlling statistically for the effects of age reduced the intensity of selection by 60 to 81%, although corrected and uncorrected estimates were strongly positively correlated. Selection differentials and gradients for tail length were positively correlated between the sexes among populations for selection acting on breeding date, but not for fecundity selection. The intensity of selection with respect to breeding date and fecundity were significantly correlated for tail length across populations. Sexual size dimorphism in tail length was significantly correlated with selection differentials with respect to breeding date for tail length in male barn swallows across populations. These findings suggest that patterns of sexual selection are consistent across large geographical scales, but also that they vary among populations. In addition, geographical patterns of phenotypic selection predict current patterns of phenotypic variation among populations, suggesting that consistent patterns of selection have been present for considerable amounts of time.     

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.     

Antagonistic pleiotropy in species with separate sexes,and the maintenance of genetic variation in life‐history traits and fitness

Antagonistic pleiotropy (AP)—where alleles of a gene increase some components of fitness at a cost to others—can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex‐specific phenotypic selection estimates—many of which are based on single fitness components.     

Sexual conflicts along gradients of density and predation risk: insights from an egg-trading fish

In principle, the intensity of sexual conflict is best measured as a loss of fitness associated with the expression of conflict-related traits. But because the relevant traits may be difficult to manipulate and fitness difficult to assess, proxy variables linked to conflict intensity may provide important tools for empirical measurement. Here we identify two common types of sexual conflict—one within mating pairs over the less expensive male role, and one between mating pairs and intruders seeking to obtain fertilizations—and consider how they vary in intensity along gradients of population density and predation risk. To do this, we develop and analyze a model of mating dynamics in the chalk bass, an egg-trading simultaneous hermaphrodite that lives on Caribbean coral reefs. In this species, within-pair sexual conflict leads each female-role partner to provide in each mating episode only a subset (parcel) of its egg clutch to its mate for fertilization. Pair-intruder sexual conflict (i.e., sperm competition) increases the proportion of the gonad allocated to male function. In the model, more parceling and greater male allocation both resulted in lower fitness at the ESS, our measure of conflict intensity. Male allocation increased along the density gradient but decreased along the predation-risk gradient, reflecting shifts in intrusion frequency. Parcel number sharply increased and then decreased more gradually along a gradient of increasing local density, initially responding to increased availability of alternative mates across low densities and then to diminishing clutch size toward higher densities. Parcel number decreased with predation risk as each mating episode became more dangerous. Conflict intensities were usually greatest at intermediate positions along the two environmental gradients, and each conflict ameliorated the intensity of the other. Overall, parceling and sex allocation may be good though imperfect proxies for intensities of within-pair and pair-intruder sexual conflicts among chalk bass.     

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.     

Quantifying sexual selection: a comparison of competing indices with mating system data from a terrestrially breeding salamander

Calculations for quantifying the potential for sexual selection remain controversial. Many indices have been promoted in the literature, but each has unique sets of advantages and disadvantages. Using marbled salamanders, I evaluated the performance of several measures by manipulating intensity of sexual selection in experimental breeding replicates of varying operational sex ratio. Theory predicts that sexual selection among males will be higher when sex ratio is male‐biased and lower when female‐biased. I used microsatellite data to assign hatchling parentage, estimate adult fitness, and calculate several indices of inequality for quantifying sexual selection. Opportunity for selection and Morisita index always conformed to theoretical expectations, which was not the case for index of resource monopolization, standardized Morisita index, or binomial skew index. Although I conclude that opportunity for selection is advantageous in sexual selection studies because of its link to formal theory, this should be tested against the null hypothesis of random variation in ambiguous cases. In the present study, although variation in both reproductive and mating success was high when quantified using opportunities for selection, it was only significantly greater than random expectations for reproductive success. This study provides further empirical support for the continued use of opportunity for selection in sexual selection studies. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 73–83.     

Phenology of scramble polygyny in a wild population of chrysolemid beetles: the opportunity for and the strength of sexual selection

Recent debate has highlighted the importance of estimating both the strength of sexual selection on phenotypic traits, and the opportunity for sexual selection. We describe seasonal fluctuations in mating dynamics of Leptinotarsa undecimlineata (Coleoptera: Chrysomelidae). We compared several estimates of the opportunity for, and the strength of, sexual selection and male precopulatory competition over the reproductive season. First, using a null model, we suggest that the ratio between observed values of the opportunity for sexual selections and their expected value under random mating results in unbiased estimates of the actual nonrandom mating behavior of the population. Second, we found that estimates for the whole reproductive season often misrepresent the actual value at any given time period. Third, mating differentials on male size and mobility, frequency of male fighting and three estimates of the opportunity for sexual selection provide contrasting but complementary information. More intense sexual selection associated to male mobility, but not to male size, was observed in periods with high opportunity for sexual selection and high frequency of male fights. Fourth, based on parameters of spatial and temporal aggregation of female receptivity, we describe the mating system of L. undecimlineata as a scramble mating polygyny in which the opportunity for sexual selection varies widely throughout the season, but the strength of sexual selection on male size remains fairly weak, while male mobility inversely covaries with mating success. We suggest that different estimates for the opportunity for, and intensity of, sexual selection should be applied in order to discriminate how different behavioral and demographic factors shape the reproductive dynamic of populations.     

The group-level consequences of sexual conflict in multigroup populations

In typical sexual conflict scenarios, males best equipped to exploit females are favored locally over more prudent males, despite reducing female fitness. However, local advantage is not the only relevant form of selection. In multigroup populations, groups with less sexual conflict will contribute more offspring to the next generation than higher conflict groups, countering the local advantage of harmful males. Here, we varied male aggression within- and between-groups in a laboratory population of water striders and measured resulting differences in local population growth over a period of three weeks. The overall pool fitness (i.e., adults produced) of less aggressive pools exceeded that of high aggression pools by a factor of three, with the high aggression pools essentially experiencing no population growth over the course of the study. When comparing the fitness of individuals across groups, aggression appeared to be under stabilizing selection in the multigroup population. The use of contextual analysis revealed that overall stabilizing selection was a product of selection favoring aggression within groups, but selected against it at the group-level. Therefore, this report provides further evidence to show that what evolves in the total population is not merely an extension of within-group dynamics.     

Genetic versus census estimators of the opportunity for sexual selection in the wild

Abstract The existence of a direct link between intensity of sexual selection and mating-system type is widely accepted. However, the quantification of sexual selection has proven problematic. Several measures of sexual selection have been proposed, including the operational sex ratio (OSR), the breeding sex ratio (BSR), and the opportunity for sexual selection (I(mates)). For a wild population of pronghorn (Antilocapra americana), we calculated OSR and BSR. We estimated I(mates) from census data on the spatial and temporal distribution of receptive females in rut and from a multigenerational genetic pedigree. OSR and BSR indicated weak sexual selection on males, but census and pedigree I(mates) suggested stronger sexual selection on males than on females. OSR and BSR correlated with census but not pedigree estimates of I(mates), and census I(mates) did not correlate with pedigree estimates. This suggests that the behavioral mating system, as deduced from the spatial and temporal distribution of females, does not predict the genetic mating system of pronghorn. The differences we observed between estimators were primarily due to female mate sampling and choice and to the sex ratio. For most species, behavioral data are not perfectly accurate and therefore will be an insufficient alternative to using multigenerational pedigrees to quantify sexual selection.     

SOME PROBLEMS IN ESTIMATING THE INTENSITY OF SELECTION THROUGH FERTILITY DIFFERENCES IN NATURAL AND EXPERIMENTAL POPULATIONS

We used empirical data from a laboratory population of Heterandria formosa (Pisces, Poeciliidae) and simulations based on those data to examine methods of estimating the intensity of phenotypic selection through fertility differences when generations overlap. The correct intensity was known because we knew the history of every female, as well as the rate at which the population was growing. The net reproductive rate, which is an appropriate measure of fitness when generations do not overlap, underestimated the true intensity of selection. This measure of fitness did not provide a rank order of individuals that agreed significantly with the correct rank order. Simulated schemes of vertical sampling of females, using number of offspring produced during the sampling window as a measure of fitness, provided no consistently useful information about the direction or intensity of selection. Weighting the number of offspring by female age, to give more value to offspring of younger females, produced only a slight improvement in accuracy. Other data indicated that fertility differentials are closely tied to particular environmental conditions. When generations overlap, estimates of fertility differentials will have to be based on horizontal studies of lifetime performance of a cohort coupled with demographic information on the entire population.     

Natural selection in the tropical treehopper <Emphasis Type="Italic">Alchisme grossa</Emphasis> (Hemiptera: Membracidae) on two sympatric host-plants

The pronotum is the most distinctive and representative structure in treehoppers. Although several functions have been proposed for this structure, its involvement in fitness has not been formally evaluated. Given the high degree of maternal investment exhibited by the subsocial membracid Alchisme grossa (Hoplophorionini), the pronotum has been suggested as a shield for offspring protection. We performed selection gradient analyses on A. grossa in order to evaluate how natural selection is acting upon two traits associated with this structure considering three different fitness proxies: (1) number of eggs, (2) the ratio between the number of first-stage nymphs and the number of eggs (early survival), and (3) the number of third-stage nymphs (late survival). Since A. grossa feeds, oviposits and mates on two alternative host-plants (Brugmansia suaveolens and Solanum ursinum, both Solanaceae), we also evaluated and compared selection gradients between these host-plants. We found positive linear selection acting upon pronotum length considering the number of eggs and the late survival fitness proxies and positive linear selection acting on the distance between the suprahumeral horns considering the early survival proxy on females ovipositing on both host-plants. These results highlight the importance of the pronotum in treehoppers females’ fitness and suggest that maternal care appears to have a greater importance in the way that natural selection is operating than the host-plant where oviposition occurs.     

The roles of natural and sexual selection during adaptation to a novel environment

The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.     

Sexual selection: harem size and the variance in male reproductive success

Sexual selection is potentially stronger than natural selection when the variance in male reproductive fitness exceeds all other components of fitness variance combined. However, measuring the variance in male reproductive fitness is difficult when nonmating males are absent, inconspicuous, or otherwise difficult to find. Omitting the nonmating males inflates estimates of average male reproductive success and diminishes the variance, leading to underestimates of the potential strength of sexual selection. We show that, in theory, the proportion of the total variance in male fitness owing to sexual selection is approximately equal to H, the mean harem size, as long as H is large and females are randomly distributed across mating males (i.e., Vharem=H). In this case, mean harem size not only provides an easy way to estimate the potential strength of sexual selection but also equals the opportunity for sexual selection, I(mates). In nature, however, females may be overdispersed with VharemH. We show that H+(k-1) is a good measure of the opportunity for sexual selection, where k is the ratio Vharem/H. A review of mating system data reveals that in nature the median ratio for Vharem/H is 1.04, but as H increases, females tend to become more aggregated across mating males with V(harem) two to three times larger than H.     

Environmental context drives seed predator-mediated selection on a floral display trait

Linking trait selection to environmental context is necessary to move beyond the simple recognition that selection is spatially variable and to understand what ultimately drives this variation. Natural selection acts through differences among individuals in lifetime fitness and information about effects on fitness components is therefore often not sufficient to gain such an understanding. We investigated how environmental context influenced intensity of seed predation, flower abortion and selection on floral display traits in 44–52 populations of the perennial herb Primula veris over 2 years. Phenotypic selection on both inflorescence height and flower number varied among populations and was mediated partly by pre-dispersal seed predation and flower abortion in one of the years. Among-population variation in selection on inflorescence height, but not flower number, was linked to variation in canopy cover via its effects on seed predation. Lifetime fitness was less sensitive to seed predator damage in shaded environments but estimates of selection based on lifetime fitness agreed qualitatively with those based on seed output. Our results demonstrate that seed predators constitute an important link between environmental conditions and trait evolution in plants, and that selection on plant traits by seed predators can depend on environmental context.