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.
The consequences of natural selection can be understood from a purely statistical perspective. In contrast, an explicitly causal approach is required to understand why trait values covary with fitness. In particular, key evolutionary constructs, such as sexual selection, fecundity selection, and so on, are best understood as selection via particular fitness components. To formalize and operationalize these concepts, we must disentangle the various causal pathways contributing to selection. Such decompositions are currently only known for linear models, where they are sometimes referred to as "Wright's rules." Here, we provide a general framework, based on path analysis, for partitioning selection among its contributing causal pathways. We show how the extended selection gradient-which represents selection arising from a trait's causal effects on fitness-can be decomposed into path-specific selection gradients, which correspond to distinct causal mechanisms of selection. This framework allows for nonlinear effects and nonadditive interactions among variables, which may be estimated using standard statistical methods (e.g., generalized linear [mixed] models or generalized additive models). We thus provide a generalization of Wright's path rules that accommodates the nonlinear and nonadditive mechanisms by which natural selection commonly arises.
Extra‐pair paternity within socially monogamous mating systems is well studied in birds and mammals but rather neglected in other animal taxa. In fishes, social monogamy has evolved several times but few studies have investigated the extent to which pair‐bonded male fish lose fertilizations to cuckolders and gain extra‐pair fertilizations themselves. We address this gap and present genetic paternity data collected from a wild population of Variabilichromis moorii, a socially monogamous African cichlid with biparental care of offspring. We show that brood‐tending, pair‐bonded males suffer exceptionally high paternity losses, siring only 63% of the offspring produced by their female partners on average. The number of cuckolders per brood ranged up to nine and yet, surprisingly, brood‐tending males in the population were rarely the culprits. Brood‐tending males sired very few extra‐pair offspring, despite breeding in close proximity to one another. While unpaired males were largely responsible for the cuckoldry, pair‐bonded males still enjoyed higher fertilization success than individual unpaired males. We discuss these results in the context of ecological and phenotypic constraints on cuckoldry and the fitness payoffs of alternative male tactics. Our study provides new insights into how pair‐bonded males handle the trade‐off between securing within‐pair and extra‐pair reproduction.
Sedentary broadcast-spawning marine invertebrates, which release both eggs and sperm into the water for fertilization, are of special interest for sexual selection studies. They provide unique insight into the early stages of the evolutionary succession leading to the often-intense operation of both pre- and post-mating sexual selection in mobile gonochorists. Since they are sessile or only weakly mobile, adults can interact only to a limited extent with other adults and with their own fertilized offspring. They are consequently subject mainly to selection on gamete production and gamete success, and so high gonad expenditure is expected in both sexes. We review literature on gonadosomatic index (GSI; the proportion of body tissue devoted to gamete production) of gonochoristic broadcast spawners, which we use as a proxy for gonad expenditure. We show that such taxa most often have a high GSI that is approximately equal in both sexes. When GSI is asymmetric, female GSI usually exceeds male GSI, at least in echinoderms (the majority of species recorded). Intriguingly, though, higher male GSI also occurs in some species and appears more common than female-biased GSI in certain orders of gastropod molluscs. Our limited data also suggest that higher male GSI may be the prevalent pattern in sperm casters (where only males release gametes). We explore how selection might have shaped these patterns using game theoretic models for gonad expenditure that consider possible trade-offs with (i) somatic maintenance or (ii) growth, while also considering sperm competition, sperm limitation, and polyspermy. Our models of the trade-off between somatic tissue (which increases survival) and gonad (which increases reproductive success) predict that GSI should be equal for the two sexes when sperm competition is intense, as is probably common in broadcast spawners due to synchronous spawning in aggregations. Higher female GSI occurs under low sperm competition. Sperm limitation appears unlikely to alter these conclusions qualitatively, but can also act as a force to keep male GSI high, and close to that of females. Polyspermy can act to reduce male GSI. Higher male than female GSI is predicted to be less common (as observed in the data), but can occur when ova/ovaries are sufficiently more resource-intensive to produce than sperm/testes, for which some evidence exists. We also show that sex-specific trade-offs between gonads and growth can generate different life-history strategies for males and females, with males beginning reproduction earlier. This could lead to apparently higher male GSI in empirical studies if immature females are included in calculations of mean GSI. The existence of higher male GSI nonetheless remains somewhat problematic and requires further investigation. When sperm limitation is low, we suggest that the natural logarithm of the male/female GSI ratio may be a suitable index for sperm competition level in broadcast spawners, and that this may also be considered as an index for internally fertilizing taxa.
Within and across taxa, there is much variation in the mode of fertilization, that is, whether eggs and/or sperm are released or kept inside or on the surface of the parent's body. Although the evolutionary consequences of fertilization mode are far-reaching, transitions in the fertilization mode itself have largely escaped theoretical attention. Here we develop the first evolutionary model of egg retention and release, which also considers transitions between hermaphroditism and dioecy as well as egg size evolution. We provide a unifying explanation for reported associations between small body size, hermaphroditism, and egg retention in marine invertebrates that have puzzled researchers for more than 3 decades. Our model, by including sperm limitation, shows that all these patterns can arise as an evolutionary response to local competition between eggs for fertilization. This can provide a general explanation for three empirical patterns: sperm casters tend to be smaller than related broadcast spawners, hermaphroditism is disproportionately common in sperm casters, and offspring of sperm casters are larger. Local gamete competition also explains a universal sexual asymmetry: females of some species retain their gametes while males release theirs, but the opposite ("egg casting") lacks evolutionary stability and is apparently not found in nature.
The parents' phenotype, or the environment they create for their young, can have long-lasting effects on their offspring, with profound evolutionary consequences. Yet, virtually no work has considered how such parental effects might change the adaptive value of behavioural traits expressed by offspring upon reaching adulthood. To address this problem, we combined experiments on burying beetles (Nicrophorus vespilloides) with theoretical modelling and focussed on one adult behavioural trait in particular: the supply of parental care. We manipulated the early-life environment and measured the fitness payoffs associated with the supply of parental care when larvae reached maturity. We found that (1) adults that received low levels of care as larvae were less successful at raising larger broods and suffered greater mortality as a result: they were low-quality parents. Furthermore, (2) high-quality males that raised offspring with low-quality females subsequently suffered greater mortality than brothers of equivalent quality, which reared larvae with higher quality females. Our analyses identify three general ways in which parental effects can change the adaptive value of an adult behavioural trait: by influencing the associated fitness benefits and costs; by consequently changing the evolutionary outcome of social interactions; and by modifying the evolutionarily stable expression of behavioural traits that are themselves parental effects.DOI: http://dx.doi.org/10.7554/eLife.07340.001
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