The measure and significance of Bateman's principles

Bateman''s principles explain sex roles and sexual dimorphism through sex-specific variance in mating success, reproductive success and their relationships within sexes (Bateman gradients). Empirical tests of these principles, however, have come under intense scrutiny. Here, we experimentally show that in replicate groups of red junglefowl, Gallus gallus, mating and reproductive successes were more variable in males than in females, resulting in a steeper male Bateman gradient, consistent with Bateman''s principles. However, we use novel quantitative techniques to reveal that current methods typically overestimate Bateman''s principles because they (i) infer mating success indirectly from offspring parentage, and thus miss matings that fail to result in fertilization, and (ii) measure Bateman gradients through the univariate regression of reproductive over mating success, without considering the substantial influence of other components of male reproductive success, namely female fecundity and paternity share. We also find a significant female Bateman gradient but show that this likely emerges as spurious consequences of male preference for fecund females, emphasizing the need for experimental approaches to establish the causal relationship between reproductive and mating success. While providing qualitative support for Bateman''s principles, our study demonstrates how current approaches can generate a misleading view of sex differences and roles.     

OVERCOMING STATISTICAL BIAS TO ESTIMATE GENETIC MATING SYSTEMS IN OPEN POPULATIONS: A COMPARISON OF BATEMAN'S PRINCIPLES BETWEEN THE SEXES IN A SEX‐ROLE‐REVERSED PIPEFISH

The genetic mating system is a key component of the sexual selection process, yet methods for the quantification of mating systems remain controversial. One approach involves metrics derived from Bateman's principles, which are based on variances in mating and reproductive success and the relationship between them. However, these measures are extremely difficult to measure for both sexes in open populations, because missing data can result in biased estimates. Here, we develop a novel approach for the estimation of mating system metrics based on Bateman's principles and apply it to a microsatellite‐based parentage analysis of a natural population of the dusky pipefish, Syngnathus floridae. Our results show that both male and female dusky pipefish have significantly positive Bateman gradients. However, females exhibit larger values of the opportunity for sexual selection and the opportunity for selection compared to males. These differences translate into a maximum intensity of sexual selection () for females three times larger than that for males. Overall, this study identifies a critical source of bias that affects studies of mating systems in open populations, presents a novel method for overcoming this bias, and applies this method for the first time in a sex‐role‐reversed pipefish.     

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.     

Greater opportunities for sexual selection in male than in female obligate brood parasitic birds

Females are expected to have evolved to be more discriminatory in mate choice than males as a result of greater reproductive investment into larger gametes (eggs vs. sperm). In turn, males are predicted to be more promiscuous than females, showing both a larger variance in the number of mates and a greater increase in reproductive success with more mates, yielding more intense sexual selection on males vs. females (Bateman's Paradigm). However, sex differences in costly parental care strategies can either reinforce or counteract the initial asymmetry in reproductive investment, which may be one cause for some studies failing to conform with predictions of Bateman's Paradigm. For example, in many bird species with small female‐biased initial investment but extensive biparental care, both sexes should be subject to similar strengths of sexual selection because males and females are similarly restricted in their ability to pursue additional mates. Unlike 99% of avian species, however, obligate brood parasitic birds lack any parental care in either sex, predicting a conformation to Bateman's Paradigm. Here we use microsatellite genotyping to demonstrate that in brood parasitic brown‐headed cowbirds (Molothrus ater), per capita annual reproductive success increases with the number of mates in males, but not in females. Furthermore, also as predicted, the variance of the number of mates and offspring is greater in males than in females. Thus, contrary to previous findings in this species, our results conform to predictions of the Bateman's Paradigm for taxa without parental care.     

Multiple paternity is a shared reproductive strategy in the live‐bearing surfperches (Embiotocidae) that may be associated with female fitness

According to Bateman's principle, female fecundity is limited relative to males, setting the expectation that males should be promiscuous, while females should be choosy and select fewer mates. However, several surfperches (Embiotocidae) exhibit multiple paternity within broods indicating that females mate with multiple males throughout the mating season. Previous studies found no correlation between mating success and reproductive success (i.e., a Bateman gradient). However, by including samples from a broader range of reproductive size classes, we found evidence of a Bateman gradient in two surfperch species from distinct embiotocid clades. Using microsatellite analyses, we found that 100% of the spotfin surfperch families sampled exhibit multiple paternity (Hyperprosopon anale, the basal taxon from the only clade that has not previously been investigated) indicating that this tactic is a shared reproductive strategy among surfperches. Further, we detected evidence for a Bateman gradient in H. anale; however, this result was not significant after correction for biases. Similarly, we found evidence for multiple paternity in 83% of the shiner surfperch families (Cymatogaster aggregata) sampled. When we combine these data with a previous study on the same species, representing a larger range of reproductive size classes and associated brood sizes, we detect a Bateman gradient in shiner surfperch for the first time that remains significant after several conservative tests for bias correction. These results indicate that sexual selection is likely complex in this system, with the potential for conflicting optima between sexes, and imply a positive shift in fertility (i.e., increasing number) and reproductive tactic with respect to the mating system and number of sires throughout the reproductive life history of females. We argue that the complex reproductive natural history of surfperches is characterized by several traits that may be associated with cryptic female choice, including protracted oogenesis, uterine sac complexity, and sperm storage.     

batemanater: a computer program to estimate and bootstrap mating system variables based on Bateman's principles

Bateman's principles continue to play a major role in the characterization of genetic mating systems in natural populations. The modern manifestations of Bateman's ideas include the opportunity for sexual selection (i.e. I_s – the variance in relative mating success), the opportunity for selection (i.e. I – the variance in relative reproductive success) and the Bateman gradient (i.e. β_ss – the slope of the least‐squares regression of reproductive success on mating success). These variables serve as the foundation for one convenient approach for the quantification of mating systems. However, their estimation presents at least two challenges, which I address here with a new Windows‐based computer software package called batemanater . The first challenge is that confidence intervals for these variables are not easy to calculate. batemanater solves this problem using a bootstrapping approach. The second, more serious, problem is that direct estimates of mating system variables from open populations will typically be biased if some potential progeny or adults are missing from the analysed sample. batemanater addresses this problem using a maximum‐likelihood approach to estimate mating system variables from incompletely sampled breeding populations. The current version of batemanater addresses the problem for systems in which progeny can be collected in groups of half‐ or full‐siblings, as would occur when eggs are laid in discrete masses or offspring occur in pregnant females. batemanater has a user‐friendly graphical interface and thus represents a new, convenient tool for the characterization and comparison of genetic mating systems.     

Mating systems and predictors of relative reproductive success in a Cutthroat Trout subspecies of conservation concern

Mating systems and patterns of reproductive success in fishes play an important role in ecology and evolution. While information on the reproductive ecology of many anadromous salmonids (Oncorhynchus spp.) is well detailed, there is less information for nonanadromous species including the Yellowstone Cutthroat Trout (O. clarkii bouvieri), a subspecies of recreational angling importance and conservation concern. Using data from a parentage‐based tagging study, we described the genetic mating system of a migratory population of Yellowstone Cutthroat Trout, tested for evidence of sexual selection, and identified predictors of mating and reproductive success. The standardized variance in mating success (i.e., opportunity for sexual selection) was significantly greater for males relative to females, and while the relationship between mating success and reproductive success (i.e., Bateman gradient) was significantly positive for both sexes, a greater proportion of reproductive success was explained by mating success for males (r ² = 0.80) than females (r ² = 0.59). Overall, the population displayed a polygynandrous mating system, whereby both sexes experienced variation in mating success due to multiple mating, and sexual selection was variable across sexes. Tests for evidence of sexual selection indicated the interaction between mating success and total length best‐predicted relative reproductive success. We failed to detect a signal of inbreeding avoidance among breeding adults, but the group of parents that produced progeny were on average slightly less related than adults that did not produce progeny. Lastly, we estimated the effective number of breeders (N _b) and effective population size (N _e) and identified while N _b was lower than N _e, both are sufficiently high to suggest Yellowstone Cutthroat Trout in Burns Creek represent a genetically stable and diverse population.     

Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid

Kin selection can explain the evolution of cooperative breeding and the distribution of relatives within a population may influence the benefits of cooperative behaviour. We provide genetic data on relatedness in the cooperatively breeding cichlid Neolamprologus pulcher. Helper to breeder relatedness decreased steeply with increasing helper age, particularly to the breeding males. Helper to helper relatedness was age‐assortative and also declined with age. These patterns of relatedness could be attributed to territory take‐overs by outsiders when breeders had disappeared (more in breeding males), between‐group dispersal of helpers and reproductive parasitism. In six of 31 groups females inherited the breeding position of their mother or sister. These matrilines were more likely to occur in large groups. We conclude that the relative fitness benefits of helping gained through kin selection vs. those gained through direct selection depend on helper age and sex.     

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.     

Selection on multiple sexual signals in two Central and Eastern European populations of the barn swallow

Variation in intensity and targets of sexual selection on multiple traits has been suggested to play a major role in promoting phenotypic differentiation between populations, although the divergence in selection may depend on year, local conditions or age. In this study, we quantified sexual selection for two putative sexual signals across two Central and East European barn swallow (Hirundo rustica rustica) populations from Czech Republic and Romania over multiple years. We then related these differences in selection to variation in sexual characters among barn swallow populations. Our results show that tail length and ventral coloration vary between populations, sexes, and age classes (first‐time breeders vs. experienced birds). We found that selection on tail length was stronger in first‐time breeders than in experienced birds and in males than in females in the Romanian population, while these differences between age groups and sexes were weak in Czech birds. We suggest that the populational difference in selection on tail length might be related to the differences in breeding conditions. Our results show that ventral coloration is darker (i.e., has lower brightness) in the Romanian than in the Czech population, and in experienced birds and males compared with first‐time breeders and females, respectively. The sexual difference in ventral coloration may suggest sexual selection on this trait, which is supported by the significant directional selection of ventral coloration in first‐time breeding males on laying date. However, after controlling for the confounding effect of wing length and tarsus length, the partial directional selection gradient on this trait turned nonsignificant, suggesting that the advantage of dark ventral coloration in early breeding birds is determined by the correlated traits of body size. These findings show that ventral coloration may be advantageous over the breeding season, but the underlying mechanism of this relationship is not clarified.     

Temporal but not spatial environmental variation drives adaptive offspring sex allocation in a plural cooperative breeder

Cooperatively breeding birds have been used frequently to study sex allocation because the adaptive value of the sexes partly depends upon the costs and benefits for parents of receiving help. I examined patterns of directional sex allocation in relation to maternal condition (Trivers-Willard hypothesis), territory quality (helper competition hypothesis), and the number of available helpers (helper repayment hypothesis) in the superb starling, Lamprotornis superbus, a plural cooperative breeder with helpers of both sexes. Superb starlings biased their offspring sex ratio in relation to prebreeding rainfall, which was correlated with maternal condition. Mothers produced relatively more female offspring in wetter years, when they were in better condition, and more male offspring in drier years, when they were in poorer condition. There was no relationship between offspring sex ratio and territory quality or the number of available helpers. Although helping was male biased, females had a greater variance in reproductive success than males. These results are consistent with the Trivers-Willard hypothesis and suggest that although females in most cooperatively breeding species make sex allocation decisions to increase their future direct reproductive success, female superb starlings appear to base this decision on their current body condition to increase their own inclusive fitness.     

Sexual selection and sexual size dimorphism in animals

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.     

Sex-specific costs of reproduction on survival in a long-lived seabird

Costs of reproduction on survival have captured the attention of researchers since life history theory was formulated. Adults of long-lived species may increase survival by reducing their breeding effort or even skipping reproduction. In this study, we aimed to evaluate the costs of current reproduction on survival and whether skipping reproduction increases adult survival in a long-lived seabird. We used capture–mark–recapture data (1450 encounters) from two populations of Bulwer''s petrel (Bulweria bulwerii), breeding in the Azores and Canary Islands, North Atlantic Ocean. Using a multi-event model with two different breeding statuses (breeders versus non-breeders), we calculated probabilities of survival and of transitions between breeding statuses, evaluating potential differences between sexes. Females had lower survival probabilities than males, independent of their breeding status. When considering breeding status, breeding females had lower survival probabilities than non-breeding females, suggesting costs of reproduction on survival. Breeding males had higher survival probabilities than non-breeding males, suggesting that males do not incur costs of reproduction on survival and that only the highest quality males have access to breeding. The highest and the lowest probabilities of skipping reproduction were found in breeding males from the Azores and in breeding males from the Canary Islands, respectively. Intermediate values were observed in the females from both populations. This result is probably due to differences in the external factors affecting both populations, essentially predation pressure and competition. The existence of sex-specific costs of reproduction on survival in several populations of this long-lived species may have important implications for species population dynamics.     

Evolutionary inevitability of sexual antagonism

Sexual antagonism, whereby mutations are favourable in one sex and disfavourable in the other, is common in natural populations, yet the root causes of sexual antagonism are rarely considered in evolutionary theories of adaptation. Here, we explore the evolutionary consequences of sex-differential selection and genotype-by-sex interactions for adaptation in species with separate sexes. We show that sexual antagonism emerges naturally from sex differences in the direction of selection on phenotypes expressed by both sexes or from sex-by-genotype interactions affecting the expression of such phenotypes. Moreover, modest sex differences in selection or genotype-by-sex effects profoundly influence the long-term evolutionary trajectories of populations with separate sexes, as these conditions trigger the evolution of strong sexual antagonism as a by-product of adaptively driven evolutionary change. The theory demonstrates that sexual antagonism is an inescapable by-product of adaptation in species with separate sexes, whether or not selection favours evolutionary divergence between males and females.     

Terminal Investment Strategies and Male Mate choice: Extreme Tests of Bateman

Bateman's principle predicts the intensity of sexual selectiondepends on rates of increase of fecundity with mating successfor each sex (Bateman slopes). The sex with the steeper increase(usually males) is under more intense sexual selection and isexpected to compete for access to the sex under less intensesexual selection (usually females). Under Bateman and modernrefinements of his ideas, differences in parental investmentare key to defining Bateman slopes and thus sex roles. Othertheories predict sex differences in mating investment, or anyexpenditures that reduce male potential reproductive rate, canalso control sex roles. We focus on sexual behaviour in systemswhere males have low paternal investment but frequently mateonly once in their lifetimes, after which they are often killedby the female. Mating effort (=terminal investment) is highfor these males, and many forms of investment theory might predictsex role reversal. We find no qualitative evidence for sex rolereversal in a sample of spiders that show this extreme maleinvestment pattern. We also present new data for terminally-investingredback spiders (Latrodectus hasselti). Bateman slopes are relativelysteep for male redbacks, and, as predicted by Bateman, thereis little evidence for role reversal. Instead, males are competitiveand show limited choosiness despite wide variation in femalereproductive value. This study supports the proposal that highmale mating investment coupled with low parental investmentmay predispose males to choosiness but will not lead to rolereversal. We support the utility of using Bateman slopes topredict sex roles, even in systems with extreme male matinginvestment.     

Bateman–Trivers in the 21st Century: sexual selection in a North American pitviper

Assessment of sexual selection in organisms with cryptic life histories is challenging, although accurate parentage assignments using genotypic markers, combined with behavioural observations and a method to account for open population bias, allow for robust estimation of metrics. In the present study, we employed 22 tetranucleotide microsatellite DNA loci to interpret mating and reproductive success in a population of Copperhead (Viperidae, Agkistrodon contortrix) in Connecticut, USA. We sampled DNA from 114 adults (56 males, 58 females) and 137 neonates from known mothers to quantify Bateman gradients (β_ss), as well as sex‐specific opportunities for selection (I) and sexual selection (I_s). We also estimated selection on male size [snout‐to‐vent length (SVL)], a trait important for successful combat and subsequent copulations. Estimates of male I and I_s differed significantly from those of females when estimated with four different methods and only males had a significant Bateman gradient. As predicted, male reproductive success was positively correlated with increasing SVL. These results contrast with those derived in another study investigating the same population but based solely on observational data and without correction for open population bias. We thus argue that molecular approaches to quantifying reproductive success and strength of sexual selection provide more accurate results than do behavioural observations alone. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 436–445.     

Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds

In cooperatively breeding species, restricted dispersal of offspring leads to clustering of closely related individuals, increasing the potential both for indirect genetic benefits and inbreeding costs. In apostlebirds (Struthidea cinerea), philopatry by both sexes results in the formation of large (up to 17 birds), predominantly sedentary breeding groups that remain stable throughout the year. We examined patterns of relatedness and fine-scale genetic structure within a population of apostlebirds using six polymorphic microsatellite loci. We found evidence of fine-scale genetic structure within the study population that is consistent with behavioural observations of short-distance dispersal, natal philopatry by both sexes and restricted movement of breeding groups between seasons. Global F(ST) values among breeding groups were significantly positive, and the average level of pairwise relatedness was significantly higher for individuals within groups than between groups. For individuals from different breeding groups, geographical distance was negatively correlated with pairwise relatedness and positively correlated with pairwise F(ST). However, when each sex was examined separately, this pattern was significant only among males, suggesting that females may disperse over longer distances. We discuss the potential for kin selection to influence the evolution and maintenance of cooperative breeding in apostlebirds. Our results demonstrate that spatial genetic structural analysis offers a useful alternative to field observations in examining dispersal patterns of cooperative breeders.     

Operational sex ratio predicts the opportunity and direction of sexual selection across animals

The operational sex ratio (OSR) has long been assumed to be a key ecological factor determining the opportunity and direction of sexual selection. However, recent theoretical work has challenged this view, arguing that a biased OSR does not necessarily result in greater monopolisation of mates and therefore stronger sexual selection in the mate‐limited sex. Hence, the role of the OSR for shaping animal mating systems remains a conundrum in sexual selection research. Here we took a meta‐analytic approach to test whether OSR explains interspecific variation in sexual selection metrics across a broad range of animal taxa. Our results demonstrate that the OSR predicts the opportunity for sexual selection in males and the direction of sexual selection in terms of sex differences in both the opportunity for sexual selection and the Bateman gradient (i.e. the selection differential of mating success), as predicted by classic theory.     

The evolution of sex-specific immune defences

Why do males and females often differ in their ability to cope with infection? Beyond physiological mechanisms, it has recently been proposed that life-history theory could explain immune differences from an adaptive point of view in relation to sex-specific reproductive strategies. However, a point often overlooked is that the benefits of immunity, and possibly the costs, depend not only on the host genotype but also on the presence and the phenotype of pathogens. To address this issue we developed an adaptive dynamic model that includes host–pathogen population dynamics and host sexual reproduction. Our model predicts that, although different reproductive strategies, following Bateman''s principle, are not enough to select for different levels of immunity, males and females respond differently to further changes in the characteristics of either sex. For example, if males are more exposed to infection than females (e.g. for behavioural reasons), it is possible to see them evolve lower immunocompetence than females. This and other counterintuitive results highlight the importance of ecological feedbacks in the evolution of immune defences. While this study focuses on sex-specific natural selection, it could easily be extended to include sexual selection and thus help to understand the interplay between the two processes.     

Does operational sex ratio influence relative strength of purging selection in males versus females?

According to theory, sexual selection in males may efficiently purge mutation load of sexual populations, reducing or fully compensating ‘the cost of males’. For this to occur, mutations not only need to be deleterious to both sexes, they also must affect males more than females. A frequently overlooked problem is that relative strength of selection on males versus females may vary between environments, with social conditions being particularly likely to affect selection in males and females differently. Here, we induced mutations in red flour beetles (Tribolium castaneum) and tested their effect in both sexes under three different operational sex ratios (1:2, 1:1 and 2:1). Induced mutations decreased fitness of both males and females, but their effect was not stronger in males. Surprisingly, operational sex ratio did not affect selection against deleterious mutations nor its relative strength in the sexes. Thus, our results show no support for the role of sexual selection in the evolutionary maintenance of sex.