Bateman's principle and immunity: phenotypically plastic reproductive strategies predict changes in immunological sex differences

The sexes often differ in the reproductive trait limiting their fitness, an observation known as Bateman's principle. In many species, females are limited by their ability to produce eggs while males are limited by their ability to compete for and successfully fertilize those eggs. As well as promoting the evolution of sex-specific reproductive strategies, this difference may promote sex differences in other life-history traits due to their correlated effects. Sex differences in disease susceptibility and immune function are common. Two hypotheses based on Bateman's principle have been proposed to explain this pattern: that selection to prolong the period of egg production favors improved immune function in females, or that the expression of secondary sexual characteristics reduces immune function in males. Both hypotheses predict a relatively fixed pattern of reduced male immune function, at least in sexually mature individuals. An alternative hypothesis is that Bateman's principle does not dictate fixed patterns of reproductive investment, but favors phenotypically plastic reproductive strategies with males and females adaptively responding to variation in fitness-limiting resource availability. Under this hypothesis, neither sex is expected to possess intrinsically superior immune function, and immunological sex differences may vary in different environments. We demonstrate that sex-specific responses to experimental manipulation of fitness-limiting resources affects both the magnitude and direction of sex differences in immune function in Drosophila melanogaster. In the absence of sexual interactions and given abundant food, the immune function of adults was maximized in both sexes and there was no sex difference. Manipulation of food availability and sexual activity resulted in female-biased immune suppression when food was limited, and male-biased immune suppression when sexual activity was high and food was abundant. The immunological cost to males of increased sexual activity was found to be due in part to reduced time spent feeding. We suggest that for species similarly limited in their reproduction, phenotypic plasticity will be an important determinant of sex differences in immune function and other life-history traits.     

Evaluating human autosomal loci for sexually antagonistic viability selection in two large biobanks

Sex and sexual differentiation are pervasive across the tree of life. Because females and males often have substantially different functional requirements, we expect selection to differ between the sexes. Recent studies in diverse species, including humans, suggest that sexually antagonistic viability selection creates allele frequency differences between the sexes at many different loci. However, theory and population-level simulations indicate that sex-specific differences in viability would need to be very large to produce and maintain reported levels of between-sex allelic differentiation. We address this contradiction between theoretical predictions and empirical observations by evaluating evidence for sexually antagonistic viability selection on autosomal loci in humans using the largest cohort to date (UK Biobank, n = 487,999) along with a second large, independent cohort (BioVU, n = 93,864). We performed association tests between genetically ascertained sex and autosomal loci. Although we found dozens of genome-wide significant associations, none replicated across cohorts. Moreover, closer inspection revealed that all associations are likely due to cross-hybridization with sex chromosome regions during genotyping. We report loci with potential for mis-hybridization found on commonly used genotyping platforms that should be carefully considered in future genetic studies of sex-specific differences. Despite being well powered to detect allele frequency differences of up to 0.8% between the sexes, we do not detect clear evidence for this signature of sexually antagonistic viability selection on autosomal variation. These findings suggest a lack of strong ongoing sexually antagonistic viability selection acting on single locus autosomal variation in humans.     

Sex differences in nutrient-dependent reproductive ageing

Evolutionary theories of aging predict that fitness-related traits, including reproductive performance, will senesce because the strength of selection declines with age. Sexual selection theory predicts, however, that male reproductive performance (especially sexual advertisement) will increase with age. In both bodies of theory, diet should mediate age-dependent changes in reproductive performance. In this study, we show that the sexes exhibit dramatic, qualitative differences in age-dependent reproductive performance trajectories and patterns of reproductive ageing in the cricket Teleogryllus commodus. In females, fecundity peaked early in adulthood and then declined. In contrast, male sexual advertisement increased across the natural lifespan and only declined well beyond the maximum field lifespan. These sex differences were robust to deviations from sex-specific dietary requirements. Our results demonstrate that sexual selection can be at least as important as sex-dependent mortality in shaping the signal of reproductive ageing.     

Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

Males and females have different routes to successful reproduction, resulting in sex differences in lifespan and age-specific allocation of reproductive effort. The trade-off between current and future reproduction is often resolved differently by males and females, and both sexes can be constrained in their ability to reach their sex-specific optima owing to intralocus sexual conflict. Such genetic antagonism may have profound implications for evolution, but its role in ageing and lifespan remains unresolved. We provide direct experimental evidence that males live longer and females live shorter than necessary to maximize their relative fitness in Callosobruchus maculatus seed beetles. Using artificial selection in a genetically heterogeneous population, we created replicate long-life lines where males lived on average 27 per cent longer than in short-life lines. As predicted by theory, subsequent assays revealed that upward selection on male lifespan decreased relative male fitness but increased relative female fitness compared with downward selection. Thus, we demonstrate that lifespan-extending genes can help one sex while harming the other. Our results show that sexual antagonism constrains adaptive life-history evolution, support a novel way of maintaining genetic variation for lifespan and argue for better integration of sex effects into applied research programmes aimed at lifespan extension.     

Sex-specific fitness effects of nutrient intake on reproduction and lifespan

Diet affects both lifespan and reproduction [1-9], leading to the prediction that the contrasting reproductive strategies of the sexes should result in sex-specific effects of nutrition on fitness and longevity [6, 10] and favor different patterns of nutrient intake in males and females. However, males and females share most of their genome and intralocus sexual conflict may prevent sex-specific diet optimization. We show that both male and female longevity were maximized on a high-carbohydrate low-protein diet in field crickets Teleogryllus commodus, but male and female lifetime reproductive performances were maximized in markedly different parts of the nutrient intake landscape. Given a choice, crickets exhibited sex-specific dietary preference in the direction that increases reproductive performance, but this sexual dimorphism in preference was incomplete, with both sexes displaced from the optimum diet for lifetime reproduction. Sexes are, therefore, constrained in their ability to reach their sex-specific dietary optima by the shared biology of diet choice. Our data suggest that sex-specific selection has thus far failed fully to resolve intralocus sexual conflict over diet optimization. Such conflict may be an important factor linking nutrition and reproduction to lifespan and aging.     

Field estimates of parentage reveal sexually antagonistic selection on body size in a population of Anolis lizards

Sexual dimorphism evolves when selection favors different phenotypic optima between the sexes. Such sexually antagonistic selection creates intralocus sexual conflict when traits are genetically correlated between the sexes and have sex‐specific optima. Brown anoles are highly sexually dimorphic: Males are on average 30% longer than females and 150% heavier in our study population. Viability selection on body size is known to be sexually antagonistic, and directional selection favors large male size whereas stabilizing selection constrains females to remain small. We build on previous studies of viability selection by measuring sexually antagonistic selection using reproductive components of fitness over three generations in a natural population of brown anoles. We estimated the number of offspring produced by an individual that survived to sexual maturity (termed RS^V), a measure of individual fitness that includes aspects of both individual reproductive success and offspring survival. We found directional selection on male body size, consistent with previous studies of viability selection. However, selection on female body size varied among years, and included periods of positive directional selection, quadratic stabilizing selection, and no selection. Selection acts differently in the sexes based on both survival and reproduction and sexual conflict appears to be a persistent force in this species.     

SEXUAL SELECTION AFFECTS THE EVOLUTION OF LIFESPAN AND AGEING IN THE DECORATED CRICKET GRYLLODES SIGILLATUS

Recent work suggests that sexual selection can influence the evolution of ageing and lifespan by shaping the optimal timing and relative costliness of reproductive effort in the sexes. We used inbred lines of the decorated cricket, Gryllodes sigillatus, to estimate the genetic (co)variance between age‐dependent reproductive effort, lifespan, and ageing within and between the sexes. Sexual selection theory predicts that males should die sooner and age more rapidly than females. However, a reversal of this pattern may be favored if reproductive effort increases with age in males but not in females. We found that male calling effort increased with age, whereas female fecundity decreased, and that males lived longer and aged more slowly than females. These divergent life‐history strategies were underpinned by a positive genetic correlation between early‐life reproductive effort and ageing rate in both sexes, although this relationship was stronger in females. Despite these sex differences in life‐history schedules, age‐dependent reproductive effort, lifespan, and ageing exhibited strong positive intersexual genetic correlations. This should, in theory, constrain the independent evolution of these traits in the sexes and may promote intralocus sexual conflict. Our study highlights the importance of sexual selection to the evolution of sex differences in ageing and lifespan in G. sigillatus.     

Sex-Specific Aggression and Antipredator Behaviour in Young Brown Trout

Sex differences in adult behaviour are often interpreted as consequences of sexual selection and/or different reproductive roles in males and females. Sex-specific juvenile behaviour, however, has received less attention. Adult brown trout males are more aggressive than females during spawning and juvenile aggression may be genetically correlated with adult aggression in fish. We therefore tested the prediction that immature brown trout males are more aggressive and bolder than immature females. Because previous work has suggested that precocious maturation increases dominance in salmonids, we included precocious males in the study to test the prediction that early sexual maturation increase male aggression and boldness. Aggression and dominance relations were estimated in dyadic contests, whereas boldness was measured as a response to simulated predation risk using a model heron. Independent of maturity state, males initiated more than twice as many agonistic interactions as females in intersexual contests. However, males were not significantly more likely to win these contests than females. The response to a first predator attack did not differ between sex categories, but males reacted less to a second predator attack than females. Sexual maturity did not affect the antipredator response in males. Since there is no evidence from field studies that stream-living immature male and female salmonids differ in growth rate, it appears unlikely that the sex differences demonstrated are behavioural consequences of sex-specific investment in growth. It seems more likely that sex-specific behaviour arises as a correlated response to sexually selected gene actions promoting differential behaviour in adult males and females during reproduction. Alternatively, sex differences may develop gradually during juvenile life, because a gradual developmental program should be less costly than a sudden behavioural change at the onset of sexual maturity.     

Female-biased sexual size dimorphism in the yellow-pine chipmunk (Tamias amoenus): sex-specific patterns of annual reproductive success and survival

Sexual size dimorphism is ultimately the result of independent, sex-specific selection on body size. In mammals, male-biased sexual size dimorphism is the predominant pattern, and it is usually attributed to the polygynous mating system prevalent in most mammals. This sole explanation is unsatisfying because selection acts on both sexes simultaneously, therefore any explanation of sexual size dimorphism should explain why one sex is relatively large and the other is small. Using mark-recapture techniques and DNA microsatellite loci to assign parentage, we examined sex-specific patterns of annual reproductive success and survival in the yellow-pine chipmunk (Tamias amoenus), a small mammal with female-biased sexual size dimorphism, to test the hypothesis that the dimorphism was related to sex differences in the relationship between body size and fitness. Chipmunks were monitored and body size components measured over three years in the Kananaskis Valley, Alberta, Canada. Male reproductive success was independent of body size perhaps due to trade-offs in body size associated with behavioral components of male mating success: dominance and running speed. Male survival was consistent with stabilizing selection for overall body size and body size components. The relationship between reproductive success and female body size fluctuated. In two of three years the relationship was positive, whereas in one year the relationship was negative. This may have been the result of differences in environmental conditions among years. Large females require more energy to maintain their soma than small females and may be unable to maintain lactation in the face of challenging environmental conditions. Female survival was positively related to body size, with little evidence for stabilizing selection. Sex differences in the relationship between body size and fitness (reproductive success and survival) were the result of different processes, but were ultimately consistent with female-biased sexual size dimorphism evident in this species.     

Response to Midgley: the costs of reproduction cannot differ between the sexes

Many studies have compared the reproductive cost and vegetative growth at a particular time point. In our review (Liu et al. 2021b), we summarized those results but did not compare absolute reproductive costs between the sexes (Hultine et al. 2016; Juvany and Munné-Bosch 2016). Moreover, we did not propose that the observed vegetative and environmental differences between the sexes were the only reasons for differences in sexual functioning, especially in the spreading and receiving of pollen (Midgley 2022). Yet, we need further evidence to support the argument. Previous studies have shown that differences in primary and physiological traits between the sexes strongly depend on the plant species and their environmental conditions, and that they may arise from a number of reasons, such as differences in trait optima of each sex along a series of resource gradients, sexual selection and sex-specific responses to sexual selection (Barrett and Josh 2013; Geber et al. 1999; Juvany and Munné-Bosch 2016; Kohorn et al. 1994; Rabska et al. 2021; Retuerto et al. 2018; Scopece et al. 2021; Wang et al. 2021). In the comment, Midgley (2022) stated that our general argument is that ‘the net reproductive costs are higher for females because they not only flower but must also produce fruits/cones/seeds (Figure 3). Midgley (2022) suggests (Figure 2) that females can ameliorate their higher costs of reproduction by maximizing resource acquisition and resource gain’. However, in our review, we summarized the general opinion and pointed out that this pattern was not universal (see more detail in Liu et al. 2021b). In consistent with previous reviews, our review argues that there is no widespread rule in sex-related differences in the cost of reproduction despite the general opinion that females have higher reproductive costs than males (Darwin 1877; Liu et al. 2021b; Lloyd and Webb 1977). We summarized possible factors causing biased sex ratios in plants, rather than only underpinning the higher net reproductive costs in females than in males (Liu et al. 2021b). Similarly, we proposed possible mechanisms causing sexual differences in responses to biotic stress, rather than underpinning the higher net reproductive costs in females than in males (Liu et al. 2021b), which is also adapted from Núñez-Farfán and Valverde (2020).     

A phylogenetic analysis of sex-specific evolution of ecological morphology in <Emphasis Type="Italic">Liolaemus</Emphasis> lizards

Adaptive radiation theory predicts that phenotypic traits involved in ecological performance evolve in different directions in populations subjected to divergent natural selection, resulting in the evolution of ecological diversity. This idea has largely been supported through comparative studies exploring relationships between ecological preferences and quantitative traits among different species. However, intersexual perspectives are often ignored. Indeed, although it is well established that intersexual competition and sex-specific parental and reproductive roles may often subject sex-linked phenotypes to antagonistic selection effects, most ecomorphological research has explored adaptive evolution on a single sex, or on means obtained from both sexes together. The few studies taking sexual differences into account reveal the occurrence of sex-specific ecomorphs in some clades of lizards, and conclude that the independent contribution of the sexes to the morphological diversity produced by adaptive radiation can be substantial. Here, we investigate whether microhabitat use results in the evolution of sex-specific ecomorphs across 44 Liolaemus lizard species. We found that microhabitat structure does not predict variation in body size and shape in either of the sexes. Yet, we found that males and females tend to occupy significantly different positions in multivariate morphological spaces, indicating that treating males and females as ecologically and phenotypically equivalent units may lead to incomplete or mistaken estimations of the diversity produced by adaptive evolution.     

Sex roles and sex ratios in animals

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.     

Quantitative genetics and sex-specific selection on sexually dimorphic traits in bighorn sheep

Sexual conflict at loci influencing traits shared between the sexes occurs when sex-specific selection pressures are antagonistic relative to the genetic correlation between the sexes. To assess whether there is sexual conflict over shared traits, we estimated heritability and intersexual genetic correlations for highly sexually dimorphic traits (horn volume and body mass) in a wild population of bighorn sheep (Ovis canadensis) and quantified sex-specific selection using estimates of longevity and lifetime reproductive success. Body mass and horn volume showed significant additive genetic variance in both sexes, and intersexual genetic correlations were 0.24+/-0.28 for horn volume and 0.63+/-0.30 for body mass. For horn volume, selection coefficients did not significantly differ from zero in either sex. For body weight, selection coefficients were positive in females but did not differ from zero in males. The absence of detectable sexually antagonistic selection suggests that currently there are no sexual conflicts at loci influencing horn volume and body mass.     

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.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

Sex differences in impaling behaviour of Great Grey Shrike Lanius excubitor: Do males have better impaling skills than females?

Prey impaling in shrikes Laniidae is considered to be a feeding adaptation to dismember and consume large prey and is unique among food-storing animals. However, other exaptations of this behaviour were recorded, including signals in mate choice, where cache size is a sign of male quality. Thus, due to a strong sexual selection, male and female birds might differ in their behavioural patterns of impaling behaviour. We examined sex differences in impaling behaviour of the Great Grey Shrike Lanius excubitor - one of the species where caches are known to be sexual signals. Data were collected in western Poland during breeding seasons in the years 2006-2010. In the studied population, we recorded several sex-specific differences in impaling behaviour. Males impaled prey, invertebrates as well as vertebrates, faster and with fewer attempts per impaling event than females. Sexes differed in the location of impaled prey; males selected more visible places, especially during the mating and courtship phase, whereas females impaled prey in concealed locations. Males also had slightly better impaling success compared to females. We suggest that sex differences in impaling behaviour may be due to different uses of impaled prey, and the better impaling skills of males may be the result of better experience in impaling which is forced by sexual selection in this species. We also discuss other factors which might trigger sex-specific differences in food caching by shrikes.     

Sex-specific chick provisioning and diving behaviour in the wedge-tailed shearwater Puffinus pacificus

Mechanisms that drive sex-specific foraging behaviour in seabirds are not fully understood. In some cases, sexual-size dimorphism has been implicated. However, recent empirical work indicates that foraging behaviour may also differ between sexes of monomorphic seabird taxa. We simultaneously examined sex-specific differences in adult foraging behaviour, chick provisioning rates and maximum dive-depths in a monomorphic seabird, the wedge-tailed shearwater Puffinus pacificus . We found significant divergence between sexes. Mean foraging trip length was longer, provisioning rate lower and mean maximum dive-depth shallower in females. We found no evidence of divergence in foraging behaviour due to condition-dependant increases in self-provisioning by females, or differences in the nest attendance patterns of each sex. In addition, chick body condition did not influence meal mass or trip length differently in one or other sex. Consistent with results obtained for dimorphic species we suggest that inter-sexual competition at the foraging grounds provides the most parsimonious explanation for the sex-specific differences observed in this monomorphic species. Based on our findings we believe this possibility warrants further critical investigation.     

Sex‐specific foraging behaviour in tropical boobies: does size matter?

Sex differences in the foraging behaviour of adults have been observed in a number of sexually size-dimorphic birds, and the usual inference has been that these sex-specific differences are driven primarily by differences in body size. An alternative explanation is that foraging differences result from sex differences unrelated to size, such as sex-specific nutritional requirements. To examine these alternative hypotheses, the foraging behaviour of parents was compared between two sympatric and congeneric species of seabird, the Brown Booby Sula leucogaster , which is highly sexually size-dimorphic (females 38% larger) and the Red-footed Booby S. sula , in which sex differences in body size are less marked (females 15% larger). Using temperature and depth loggers, we found that there were highly significant differences in the foraging trip durations and diving behaviour of male and female Brown Boobies. These sex differences were less marked in Red-footed Boobies. Thus, our interspecies comparison revealed that the magnitude of the difference between the sexes matched the sexual size dimorphism of the species, providing support for the size hypothesis.     

Genetic constraints and the evolution of display trait sexual dimorphism by natural and sexual selection

The evolution of sexual dimorphism involves an interaction between sex-specific selection and a breakdown of genetic constraints that arise because the two sexes share a genome. We examined genetic constraints and the effect of sex-specific selection on a suite of sexually dimorphic display traits in Drosophila serrata. Sexual dimorphism varied among nine natural populations covering a substantial portion of the species range. Quantitative genetic analyses showed that intersexual genetic correlations were high because of autosomal genetic variance but that the inclusion of X-linked effects reduced genetic correlations substantially, indicating that sex linkage may be an important mechanism by which intersexual genetic constraints are reduced in this species. We then explored the potential for both natural and sexual selection to influence these traits, using a 12-generation laboratory experiment in which we altered the opportunities for each process as flies adapted to a novel environment. Sexual dimorphism evolved, with natural selection reducing sexual dimorphism, whereas sexual selection tended to increase it overall. To this extent, our results are consistent with the hypothesis that sexual selection favors evolutionary divergence of the sexes. However, sex-specific responses to natural and sexual selection contrasted with the classic model because sexual selection affected females rather than males.     

Sex expression, sex-specific traits, and the effects of salinity on growth and reproduction of Amaranthus cannabinus (Amaranthaceae), a dioecious annual

Amaranthus cannabinus was studied to investigate some of the ecological factors thought to be involved in the evolution of dioecy and to investigate the effects of salinity on sex expression and sex-specific selection. In the field portion of this study, sex ratios, stability of sex expression, spatial distribution, allocation strategies, and phenologies of the sexes were investigated in New Jersey freshwater and salt marsh populations of water hemp. To examine the effects of salinity on vegetative and reproductive development of males and females, plants were grown in the greenhouse at three salinity levels. Adult sex ratios were found to be 1:1. Temporal deviations from a 1:1 sex ratio varied by population and were due to differences in flowering phenology and mortality between the sexes. No plants were observed to change sex expression, and there was no evidence of spatial segregation of the sexes in the field. In both the field and the greenhouse, females allocated more resources to vegetative tissues and had a longer growing period than males. The results of this study suggest that increased reproductive efficiency through sex-specific growth patterns may have been an important selective factor involved in the evolution of dioecy in A. cannabinus.