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The Darwin-Bateman paradigm predicts that females enhance their fitness by being choosy and mating with high-quality males, while males should compete to mate with as many females as possible. In many species, males enhance their fitness by defending females and/or resources used by females. That is, males directly defend access to mating opportunities. However, paternity analyses have repeatedly shown that females in most species mate polyandrously, which contradicts traditional expectations that male defensive behaviours lead to monandry. Here, in an extensive meta-analysis, encompassing 109 species and 1026 effect sizes from across the animal kingdom, we tested if the occurrence of defensive behaviours modulates sexual selection on females and males. If so, we can illuminate the extent to which males really succeed in defending access to mating and fertilisation opportunities. We used four different indices of the opportunity for sexual selection that comprise pre-mating and/or post-mating episodes of selection. We found, for both sexes, that the occurrence of defensive behaviours does not modulate the potential strength of sexual selection. This implies that male defensive behaviours do not predict the true intensity of sexual selection. While the most extreme levels of sexual selection on males are in species with male defensive behaviours, which indicates that males do sometimes succeed in restricting females' re-mating ability (e.g. elephant seals, Mirounga leonina), estimates of the opportunity for sexual selection vary greatly across species, regardless of whether or not defensive behaviours occur. Indeed, widespread polyandry shows that females are usually not restricted by male defensive behaviours. In addition, our results indicate that post-mating episodes of selection, such as cryptic female choice and sperm competition, might be important factors modulating the opportunity for sexual selection. We discuss: (i) why male defensive behaviours fail to lower the opportunity for sexual selection among females or fail to elevate it for males; (ii) how post-mating events might influence sexual selection; and (iii) the role of females as active participants in sexual selection. We also highlight that inadequate data reporting in the literature prevented us from extracting effect sizes from many studies that had presumably collected the relevant data.

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Variance in reproductive success (sk2, with k = number of offspring) plays a large role in determining the rate of genetic drift and the scope within which selection acts. Various frameworks have been proposed to parse factors that contribute to sk2, but none has focused on age-specific values of ϕ=sk2/k¯, which indicate the degree to which reproductive skew is overdispersed (compared to the random Poisson expectation) among individuals of the same age and sex. Instead, within-age effects are generally lumped with residual variance and treated as "noise." Here, an ANOVA sums-of-squares framework is used to partition variance in annual and lifetime reproductive success into between-group and within-group components. For annual reproduction, the between-age effect depends on age-specific fecundity (b x), but relatively few empirical data are available on the within-age effect, which depends on ϕ x. By defining groups by age-at-death rather than age, the same ANOVA framework can be used to partition variance in lifetime reproductive success (LRS) into between-group and within-group components. Analytical methods are used to develop null-model expectations for random contributions to within-group and between-group components. For analysis of LRS, random variation in longevity appears as part of the between-group variance, and effects (if any) of skip breeding and persistent individual differences contribute to the within-group variance. Simulations are used to show that the methods for variance partitioning are asymptotically unbiased. Practical application is illustrated with empirical data for annual reproduction in American black bears and lifetime reproduction in Dutch great tits. Results show that overdispersed within-age variance (1) dominates annual sk2 in both male and female black bears, (2) is the primary factor that reduces annual effective size to a fraction of the number of adults, and (3) represents most of the opportunity for selection. In contrast, about a quarter of the variance in LRS in great tits can be attributed to random variation in longevity, and most of the rest is due to modest differences in fecundity with age estimated for a single cohort of females. R code is provided that reads generic input files for annual and lifetime reproductive success and allows users to conduct variance partitioning with their own data.

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Environmental factors can have profound effects on the strength and direction of selection and recent studies suggest that such environment-dependent selection can be sex-specific. Sexual selection theory predicts that male fitness is more condition dependent compared to female fitness, suggesting that male fitness is more sensitive to environmental stress. However, our knowledge about the effect of environmental factors on sex-specific reproductive performance and on sex differences in the opportunity for selection is still very limited. In the present study, we investigated the sex-specific effects of diet quality (yeast deprivation and flour type) in the red flour beetle Tribolium castaneum. Specifically, we manipulated yeast supplementation in wheat and whole-wheat flour in competition assays allowing us to test for sex-specific effects of food quality (i) on reproductive success and (ii) on the opportunity for selection. Our data show that yeast deprivation in wheat flour had significantly negative effects on body mass and reproductive success of both sexes, while high-quality flour (whole-wheat flour) was able to buffer the negative impact to a large extent. Importantly, our data suggest no sex-specific effect of dietary stress on reproductive success because the magnitude of the negative effect of yeast deprivation was similar for males and females. Moreover, our study demonstrates that low food quality inflated the opportunity for selection and did not differ between sexes neither under benign nor stressful dietary conditions. We discuss the implications of our findings for the adaptation to stressful environments.

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PREMISE: Anthropogenic nitrogen (N) addition alters the abiotic and biotic environment, potentially leading to changes in patterns of natural selection (i.e., trait-fitness relationships) and the opportunity for selection (i.e., variance in relative fitness). Because N addition favors species with light acquisition strategies (e.g., tall species), we predicted that N would strengthen selection favoring those same traits. We also predicted that N could alter the opportunity for selection via its effects on mean fitness and/or competitive asymmetries. METHODS: We quantified the strength of selection and the opportunity for selection in replicated populations of the annual grass Setaria faberi (giant foxtail) growing in a long-term N addition experiment. We also correlated these population-level parameters with community-level metrics to identify the proximate causes of N-mediated evolutionary effects. RESULTS: N addition increased aboveground productivity, light asymmetry, and reduced species diversity. Contrary to expectations, N addition did not strengthen selection for trait values associated with higher light acquisition such as greater height and specific leaf area (SLA); rather, it strengthened selection favoring lower SLA. Light asymmetry and species diversity were associated with selection for height and SLA, suggesting a role for these factors in driving N-mediated selection. The opportunity for selection was not influenced by N addition but was negatively associated with species diversity. CONCLUSIONS: Our results indicate that anthropogenic N enrichment can affect evolutionary processes, but that evolutionary changes in plant traits within populations are unlikely to parallel the shifts in plant traits observed at the community level.

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In socially monogamous species, extra-pair paternity (EPP) is predicted to increase variance in male reproductive success (RS) beyond that resulting from genetic monogamy, thus, increasing the "opportunity for selection" (maximum strength of selection that can act on traits). This prediction is challenging to investigate in wild populations because lifetime reproduction data are often incomplete. Moreover, age-specific variances in reproduction have been rarely quantified. We analyzed 21 years of near-complete social and genetic reproduction data from an insular population of Seychelles warblers (Acrocephalus sechellensis). We quantified EPP's contribution to lifetime and age-specific opportunities for selection in males. We compared the variance in male genetic RS vs social ("apparent") RS (RSap ) to assess if EPP increased the opportunity for selection over that resulting from genetic monogamy. Despite not causing a statistically significant excess (19%) of the former over the latter, EPP contributed substantially (27%) to the variance in lifetime RS, similarly to within-pair paternity (WPP, 39%) and to the positive WPP-EPP covariance (34%). Partitioning the opportunity for selection into age-specific (co)variance components, showed that EPP also provided a substantial contribution at most ages, varying with age. Therefore, despite possibly not playing the main role in shaping sexual selection in Seychelles warblers, EPP provided a substantial contribution to the lifetime and age-specific opportunity for selection, which can influence evolutionary processes in age-structured populations.

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Understanding how environmental change affects genetic variances and covariances of reproductive traits is key to formulate firm predictions on evolutionary responses. This is particularly true for sex-specific variance in reproductive success, which has been argued to affect how populations can adapt to environmental change. Our current knowledge on the impact of environmental stress on sex-specific genetic architecture of fitness components is still limited and restricted to separate-sexed organisms. However, hermaphroditism is widespread across animals and may entail interesting peculiarities with respect to genetic constraints imposed on the evolution of male and female reproduction. We explored how food restriction affects the genetic variance-covariance (G) matrix of body size and reproductive success of the simultaneously hermaphroditic freshwater snail Physa acuta. Our results provide strong evidence that the imposed environmental stress elevated the opportunity for selection in both sex functions. However, the G-matrix remained largely stable across the tested food treatments. Importantly, our results provide no support for cross-sex genetic correlations suggesting no strong evolutionary coupling of male and female reproductive traits. We discuss potential implications for the adaptation to changing environments and highlight the need for more quantitative genetic studies on male and female fitness components in simultaneous hermaphrodites.

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Quantifying the relations between plant-antagonistic interactions and natural selection among populations is important for predicting how spatial variation in ecological interactions drive adaptive differentiation. Here, we investigate the relations between the opportunity for selection, herbivore-mediated selection, and the intensity of plant-herbivore interaction among 11 populations of the insect-pollinated plant Primula florindae over 2 years. We experimentally quantified herbivore-mediated directional selection on three floral traits (two display and one phenological) within populations and found evidence for herbivore-mediated selection for a later flowering start date and a greater number of flowers per plant. The opportunity for selection and strength of herbivore-mediated selection on number of flowers varied nonlinearly with the intensity of herbivory among populations. These parameters increased and then decreased with increasing intensity of plant-herbivore interactions, defined as an increase in the ratio of herbivore-damaged flowers per individual. Our results provide novel insights into how plant-antagonistic interactions can shape spatial variation in selection on floral traits and contribute toward understanding the mechanistic basis of geographic variation in angiosperm flowers.

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Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.

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Competition for limiting resources and stress can magnify variance in fitness and therefore selection. But even in a common environment, the strength of selection can differ across the sexes, as their fitness is often limited by different factors. Indeed, most taxa show stronger selection in males, a bias often ascribed to intense competition for access to mating partners. This sex bias could reverberate on many aspects of evolution, from speed of adaptation to genome evolution. It is unclear, however, whether stronger opportunity for selection in males is a pattern robust to sex-specific stress or resource limitation. We test this in the model species Callosobruchus maculatus by comparing female and male opportunity for selection (i) with and without limitation of quality oviposition sites, and (ii) under delayed age at oviposition. Decreasing the abundance of the resource key to females or increasing their reproductive age was challenging, as shown by a reduction in mean fitness, but opportunity for selection remained stronger in males across all treatments, and even more so when oviposition sites were limiting. This suggests that males remain the more variable sex independent of context, and that the opportunity for selection through males is indirectly affected by female-specific resource limitation.

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Sexual selection studies widely estimate several metrics, but values may be inaccurate because standard field methods for studying wild populations produce limited data (e.g., incomplete sampling, inability to observe copulations directly). We compared four selection metrics (Bateman gradient, opportunity for sexual selection, opportunity for selection, and smax') estimated with simulated complete and simulated limited data for 15 socially monogamous songbird species with extrapair paternity (4%-54% extrapair offspring). Inferring copulation success from offspring parentage creates nonindependence between these variables and systematically underestimates copulation success. We found that this introduces substantial bias for the Bateman gradient, opportunity for sexual selection, and smax'. Notably, 47.5% of detected Bateman gradients were significantly positive for females, suggesting selection on females to copulate with multiple males, although the true Bateman gradient was zero. Bias generally increased with the extent of other sources of data limitations tested (nest predation, male infertility, and unsampled floater males). Incomplete offspring sampling introduced bias for all of the metrics except the Bateman gradient, while incomplete sampling of extrapair sires did not introduce additional bias when sires were a random subset of breeding males. Overall, our findings demonstrate how biases due to field data limitations can strongly impact the study of sexual selection.

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Meta-analysis is increasingly used in biology to both quantitatively summarize available evidence for specific questions and generate new hypotheses. Although this powerful tool has mostly been deployed to study mean effects, there is untapped potential to study effects on (trait) variance. Here, we use a recently published data set as a case study to demonstrate how meta-analysis of variance can be used to provide insights into biological processes. This data set included 704 effect sizes from 89 studies, covering 56 animal species, and was originally used to test developmental stress effects on a range of traits. We found that developmental stress not only negatively affects mean trait values, but also increases trait variance, mostly in reproduction, showcasing how meta-analysis of variance can reveal previously overlooked effects. Furthermore, we show how meta-analysis of variance can be used as a tool to help meta-analysts make informed methodological decisions, even when the primary focus is on mean effects. We provide all data and comprehensive R scripts with detailed explanations to make it easier for researchers to conduct this type of analysis. We encourage meta-analysts in all disciplines to move beyond the world of means and start unravelling secrets of the world of variance.

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It is widely acknowledged that in most species sexual selection continues after mating. Although it is generally accepted that females play an important role in generating paternity biases (i.e. cryptic female choice, CFC), we lack a quantitative understanding of the relative importance of female-controlled processes in influencing variance in male reproductive fitness. Here, we address this question experimentally using the guppy Poecilia reticulata, a polyandrous fish in which pre- and postcopulatory sexual selection jointly determine male reproductive fitness. We used a paired design to quantify patterns of paternity for pairs of rival males across two mating contexts, one in which the female retained full control over double (natural) matings and one where sperm from the same two males were artificially inseminated into the female. We then compared the relative paternity share for a given pair of males across both contexts, enabling us to test the key prediction that patterns of paternity will depend on the extent to which females retain behavioural control over matings. As predicted, we found stronger paternity biases when females retained full control over mating compared with when artificial insemination (AI) was used. Concomitantly, we show that the opportunity for postcopulatory sexual selection (standardized variance in male reproductive success) was greater when females retained control over double matings compared with when AI was used. Finally, we show that the paternity success of individual males exhibited higher repeatability across successive brood cycles when females retained behavioural control of matings compared with when AI was used. Collectively, these findings underscore the critical role that females play in determining the outcome of sexual selection and to our knowledge provide the first experimental evidence that behaviourally moderated components of CFC increase the opportunity for sexual selection.

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Sexual selection is a fundamental evolutionary process but remains debated, particularly in the complexity of polyandrous populations where females mate with multiple males. This lack of resolution is partly because studies have largely ignored the structure of the sexual network, that is, the pattern of mate sharing. Here, we quantify what we call mating assortment with network analysis to specify explicitly the indirect as well as direct relationships between partners. We first review empirical studies, showing that mating assortment varies considerably in nature, due largely to basic properties of the sexual network (size and density) and partly to nonrandom patterns of mate sharing. We then use simulations to show how variation in mating assortment interacts with population-level polyandry to determine the strength of sexual selection on males. Controlling for average polyandry, positive mating assortment, arising when more polygynous males tend to mate with more polyandrous females, drastically decreases the intensity of precopulatory sexual selection on male mating success (Bateman gradient) and the covariance between male mating success and postcopulatory paternity share. Average polyandry independently weakened some measures of sexual selection and crucially also impacted sexual selection indirectly by constraining mating assortment through the saturation of the mating network. Mating assortment therefore represents a key-albeit overlooked-modulator of the strength of sexual selection. Our results show that jointly considering sexual network structure and average polyandry more precisely describes the strength of sexual selection.

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Pollinators are considered primary selective agents acting on plant traits, and thus variation in the strength of the plant-pollinator interaction might drive variation in the opportunity for selection and selection intensity across plant populations. Here, we examine whether these critical evolutionary parameters covary with pollination intensity across wild populations of the biennial Sabatia angularis. We quantified pollination intensity in each of nine S. angularis populations as mean stigmatic pollen load per population. For female fitness and three components, fruit number, fruit set (proportion of flowers setting fruit) and number of seeds per fruit, we evaluated whether the opportunity for selection varied with pollination intensity. We used phenotypic selection analyses to test for interactions between pollination intensity and selection gradients for five floral traits, including flowering phenology. The opportunity for selection via fruit set and seeds per fruit declined significantly with increasing pollen receipt, as expected. We demonstrated significant directional selection on multiple traits across populations. We also found that selection intensity for all traits depended on pollination intensity. Consistent with general theory about the relationship between biotic interaction strength and the intensity of selection, our study suggests that variation in pollination intensity drives variation in selection across S. angularis populations.

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In animal-pollinated plants, the opportunity for selection and the strength of pollinator-mediated selection are expected to increase with the degree of pollen limitation. However, whether differences in pollen limitation can explain variation in pollinator-mediated and net selection among animal-pollinated species is poorly understood. In the present study, we quantified pollen limitation, variance in relative fitness and pollinator-mediated selection on five traits important for pollinator attraction (flowering start, plant height, flower number, flower size) and pollination efficiency (spur length) in natural populations of 12 orchid species. Pollinator-mediated selection was quantified by subtracting estimates of selection gradients for plants receiving supplemental hand-pollination from estimates obtained for open-pollinated control plants. Mean pollen limitation ranged from zero to 0.96. Opportunity for selection, pollinator-mediated selection and net selection were all positively related to pollen limitation, whereas nonpollinator-mediated selection was not. Opportunity for selection varied five-fold, strength of pollinator-mediated selection varied three-fold and net selection varied 1.5-fold among species. Supplemental hand-pollination reduced both opportunity for selection and selection on floral traits. The results show that the intensity of biotic interactions is an important determinant of the selection regime, and indicate that the potential for pollinator-mediated selection and divergence in floral traits is particularly high in species that are strongly pollen-limited.

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Lifetime reproductive output (LRO) determines per-generation growth rates, establishes criteria for population growth or decline, and is an important component of fitness. Empirical measurements of LRO reveal high variance among individuals. This variance may result from genuine heterogeneity in individual properties, or from individual stochasticity, the outcome of probabilistic demographic events during the life cycle. To evaluate the extent of individual stochasticity requires the calculation of the statistics of LRO from a demographic model. Mean LRO is routinely calculated (as the net reproductive rate), but the calculation of variances has only recently received attention. Here, we present a complete, exact, analytical, closed-form solution for all the moments of LRO, for age- and stage-classified populations. Previous studies have relied on simulation, iterative solutions, or closed-form analytical solutions that capture only part of the sources of variance. We also present the sensitivity and elasticity of all of the statistics of LRO to parameters defining survival, stage transitions, and (st)age-specific fertility. Selection can operate on variance in LRO only if the variance results from genetic heterogeneity. The potential opportunity for selection is quantified by Crow's index I , the ratio of the variance to the square of the mean. But variance due to individual stochasticity is only an apparent opportunity for selection. In a comparison of a range of age-classified models for human populations, we find that proportional increases in mortality have very small effects on the mean and variance of LRO, but large positive effects on I . Proportional increases in fertility increase both the mean and variance of LRO, but reduce I . For a size-classified tree population, the elasticity of both mean and variance of LRO to stage-specific mortality are negative; the elasticities to stage-specific fertility are positive.

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The link between biotic interaction intensity and strength of selection is of fundamental interest for understanding biotically driven diversification and predicting the consequences of environmental change. The strength of selection resulting from biotic interactions is determined by the strength of the interaction and by the covariance between fitness and the trait under selection. When the relationship between trait and absolute fitness is constant, selection strength should be a direct function of mean population interaction intensity. To test this prediction, we excluded pollinators for intervals of different length to induce five levels of pollination intensity within a single plant population. Pollen limitation (PL) increased from 0 to 0.77 across treatments, accompanied by a fivefold increase in the opportunity for selection. Trait-fitness covariance declined with PL for number of flowers, but varied little for other traits. Pollinator-mediated selection on plant height, corolla size, and spur length increased by 91%, 34%, and 330%, respectively, in the most severely pollen-limited treatment compared to open-pollinated plants. The results indicate that realized biotic selection can be predicted from mean population interaction intensity when variation in trait-fitness covariance is limited, and that declines in pollination intensity will strongly increase selection on traits involved in the interaction.

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It is well known that sexual selection can target reproductive traits during successive pre- and post-mating episodes of selection. A key focus of recent studies has been to understand and quantify how these episodes of sexual selection interact to determine overall variance in reproductive success. In this article, we review empirical developments in this field but also highlight the considerable variability in patterns of pre- and post-mating sexual selection, attributable to variation in patterns of resource acquisition and allocation, ecological and social factors, genotype-by-environment interaction and possible methodological factors that might obscure such patterns. Our aim is to highlight how (co)variances in pre- and post-mating sexually selected traits can be sensitive to changes in a range of ecological and environmental variables. We argue that failure to capture this variation when quantifying the opportunity for sexual selection may lead to erroneous conclusions about the strength, direction or form of sexual selection operating on pre- and post-mating traits. Overall, we advocate for approaches that combine measures of pre- and post-mating selection across contrasting environmental or ecological gradients to better understand the dynamics of sexual selection in polyandrous species. We also discuss some directions for future research in this area.

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Sexual selection operates through consecutive episodes of selection that ultimately contribute to the observed variance in reproductive success between individuals. Understanding the relative importance of these episodes is challenging, particularly because the relevant postcopulatory fitness components are often difficult to assess. Here, we investigate different episodes of sexual selection on the male sex function, by assessing how (precopulatory) mating success, and (postcopulatory) sperm-transfer efficiency and sperm-fertilizing efficiency contribute to male reproductive success. Specifically, we used a transgenic line of the transparent flatworm, Macrostomum lignano, which expresses green fluorescent protein (GFP) in all cell types, including sperm cells, enabling in vivo sperm tracking and paternity analysis. We found that a large proportion of variance in male reproductive success arose from the postcopulatory episodes. Moreover, we also quantified selection differentials on 10 morphological traits. Testis size and seminal vesicle size showed significant positive selection differentials, which were mainly due to selection on sperm-transfer efficiency. Overall, our results demonstrate that male reproductive success in M. lignano is not primarily limited by the number of matings achieved, but rather by the ability to convert matings into successful fertilizations, which is facilitated by producing many sperm.

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Sexual selection is a cornerstone of evolutionary theory, but measuring it has proved surprisingly difficult and controversial. Various proxy measures--e.g., the Bateman gradient and the opportunity for sexual selection--are widely used in empirical studies. However, we do not know how reliably these measures predict the strength of sexual selection across natural systems, and most perform poorly in theoretical worst-case scenarios. Here we provide a rigorous comparison of eight commonly used indexes of sexual selection. We simulated 500 biologically plausible mating systems, based on the templates of five well-studied species that cover a diverse range of reproductive life histories. We compared putative indexes to the actual strength of premating sexual selection, measured as the strength of selection on a simulated "mating trait." This method sidesteps a key weakness of empirical studies, which lack an appropriate yardstick against which proxy measures can be assessed. Our model predicts that, far from being useless, the best proxy measures reliably track the strength of sexual selection across biologically realistic scenarios. The maximum intensity of precopulatory sexual selection s'max (the Jones index) outperformed all other indexes and was highly correlated with the strength of sexual selection. In contrast, the Bateman gradient and the opportunity for sexual selection were poor predictors of sexual selection, despite their continuing popularity.

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