Sex-biased immunity is driven by relative differences in reproductive investment.
ABSTRACT: Sex differences in immunity are often observed, with males generally having a weaker immune system than females. However, recent data in a sex-role-reversed species in which females compete to mate with males suggest that sexually competitive females have a weaker immune response. These findings support the hypothesis that sexual dimorphism in immunity has evolved in response to sex-specific fitness returns of investment in traits such as parental investment and longevity, but the scarcity of data in sex-reversed species prevents us from drawing general conclusions. Using an insect species in which males make a large but variable parental investment in their offspring, we use two indicators of immunocompetence to test the hypothesis that sex-biased immunity is determined by differences in parental investment. We found that when the value of paternal investment was experimentally increased, male immune investment became relatively greater than that of females. Thus, in this system, in which the direction of sexual competition is plastic, the direction of sex-biased immunity is also plastic and appears to track relative parental investment.
Project description:Sex differences in immunity are found in many species. Known immune mechanisms in birds and mammals suggest that pathogen detection may be amplified in females, whereas in males, pathogen killing is amplified. We show that these immunological profiles emerge as distinct peaks on a fitness landscape defined by sensitivity-specificity and infection-immunopathology immune tradeoffs. What selection pressures might drive males and females towards separate peaks? Surprisingly, modeling immune trade-offs alone results in a pattern of sex differences that is the reverse of what is observed. By integrating these trade-offs into a life-history framework, where the schedule and magnitude of reproductive investment differs between the sexes, we find that increased age-specific infection and mortality risks during parental investment can push females towards the peak that aligns with empirical observations. Overall, our model suggests enhanced pathogen detection (in females) versus enhanced pathogen killing (in males) is best explained if shared immune tradeoffs interact with sex-specific reproductive schedules and risks. We suggest ways to test this framework empirically.
Project description:Males and females are defined by the relative size of their gametes (anisogamy), but secondary sexual dimorphism in fertilization, parental investment and mating competition is widespread and often remarkably stable over evolutionary timescales. Recent theory has clarified the causal connections between anisogamy and the most prevalent differences between the sexes, but deviations from these patterns remain poorly understood. Here, we study how sex differences in parental investment and mating competition coevolve with parental care specialization. Parental investment often consists of two or more distinct activities (e.g. provisioning and defence) and parents may care more efficiently by specializing in a subset of these activities. Our model predicts that efficient care specialization broadens the conditions under which biparental investment can evolve in lineages that historically had uniparental care. Major transitions in sex roles (e.g. from female-biased care with strong male mating competition to male-biased care with strong female competition) can arise following ecologically induced changes in the costs or benefits of different care types, or in the sex ratio at maturation. Our model provides a clear evolutionary mechanism for sex-role transitions, but also predicts that such transitions should be rare. It consequently contributes towards explaining widespread phylogenetic inertia in parenting and mating systems.
Project description:Parental care elevates reproductive success by allocating resources into the upbringing of the offspring. However, it also imposes strong costs for the care-giving parent and can foster sexual dimorphism. Trade-offs between the reproductive system and the immune system may result in differential immunological capacities between the care-providing and the non-care-providing parent. Usually, providing care is restricted to the female sex making it impossible to study a sex-independent influence of parental investment on sexual immune dimorphism. The decoupling of sex-dependent parental investment and their influences on the parental immunological capacity, however, is possible in syngnathids, which evolved the unique male pregnancy on a gradient ranging from a simple carrying of eggs on the trunk (Nerophinae, low paternal investment) to full internal pregnancy (Syngnathus, high paternal investment). In this study, we compared candidate gene expression between females and males of different gravity stages in three species of syngnathids (Syngnathus typhle, Syngnathus rostellatus and Nerophis ophidion) with different male pregnancy intensities to determine how parental investment influences sexual immune dimorphism. While our data failed to detect sexual immune dimorphism in the subset of candidate genes assessed, we show a parental care specific resource-allocation trade-off between investment into pregnancy and immune defense when parental care is provided.
Project description:Immune system maintenance and upregulation is costly. Sexual selection intensity, which increases male investment into reproductive traits, is expected to create trade-offs with immune function. We assayed phenoloxidase (PO) and lytic activity of individuals from populations of the Indian meal moth, Plodia interpunctella, which had been evolving under different intensities of sexual selection. We found significant divergence among populations, with males from female-biased populations having lower PO activity than males from balanced sex ratio or male-biased populations. There was no divergence in anti-bacterial lytic activity. Our data suggest that it is the increased male mating demands in female-biased populations that trades-off against immunity, and not the increased investment in sperm transfer per mating that characterizes male-biased populations.
Project description:Models suggest that dispersal patterns will influence age- and sex-dependent helping behavior in social species. Duolocal social systems (where neither sex disperses and mating is outside the group) are predicted to be associated with mothers favoring sons over daughters (because the latter are in reproductive competition with each other). Other models predict daughter-biased investment when benefits of wealth to sons are less than daughters. Here, we test whether sex-biased investment is occurring in the duolocal Mosuo of southwestern China. Using demographic and observational data from Mosuo, we show support for both hypotheses, in that 1) males are more likely to disperse from their natal household if their mother dies, but females are not; 2) a large number of brothers increases the likelihood that both females and males disperse, whereas a large number of sisters only increases female dispersal; 3) mothers help daughters reproduce earlier and reduce death risk of daughter's children, but not sons or sons' children; 4) data on multiple paternity show that female reproductive success does not suffer from multiple partners, and in males multiple mates are associated with higher reproductive success, indicating that mothers can benefit from investing in their sons' mating effort; and 5) gift decisions reveal similar kin effects to those shown in the demographic data, with mothers helping adult daughters and adult sons equally, but helping only her daughter's children, not her son's children. Mosuo mothers may invest resources for parental investment in their daughters and their offspring, while investing in their sons mating effort.
Project description:It is often hypothesized that intra-sexual competition accelerates actuarial senescence, or the increase in mortality rates with age. However, an alternative hypothesis is that parental investment is more important to determining senescence rates. We used a unique model system, the white-throated sparrow (Zonotrichia albicollis), to study variation in actuarial senescence. In this species, genetically determined morphs display discrete mating strategies and disassortative pairing, providing an excellent opportunity to test the predictions of the above hypotheses. Compared to tan-striped males, white-striped males are more polygynous and aggressive, and less parental. Tan-striped females receive less parental support, and invest more into parental care than white-striped females, which are also more aggressive. Thus, higher senescence rates in males and white-striped birds would support the intra-sexual competition hypothesis, whereas higher senescence rates in females and tan-striped birds would support the parental investment hypothesis. White-striped males showed the lowest rate of actuarial senescence. Tan-striped females had the highest senescence rate, and tan-striped males and white-striped females showed intermediate, relatively equal rates. Thus, results were inconsistent with sexual selection and competitive strategies increasing senescence rates, and instead indicate that senescence may be accelerated by female-biased parental care, and lessened by sharing of parental duties.
Project description:BACKGROUND:The disposable soma theory of ageing assumes that organisms optimally trade-off limited resources between reproduction and longevity to maximize fitness. Early reproduction should especially trade-off against late reproduction and longevity because of reduced investment into somatic protection, including immunity. Moreover, as optimal reproductive strategies of males and females differ, sexually dimorphic patterns of senescence may evolve. In particular, as males gain fitness through mating success, sexual competition should be a major factor accelerating male senescence. In a single experiment, we examined these possibilities by establishing artificial populations of the mealworm beetle, Tenebrio molitor, in which we manipulated the sex-ratio to generate variable levels of investment into reproductive effort and sexual competition in males and females. RESULTS:As predicted, variation in sex-ratio affected male and female reproductive efforts, with contrasted sex-specific trade-offs between lifetime reproduction, survival and immunity. High effort of reproduction accelerated mortality in females, without affecting immunity, but high early reproductive success was observed only in balanced sex-ratio condition. Male reproduction was costly on longevity and immunity, mainly because of their investment into copulations rather than in sexual competition. CONCLUSIONS:Our results suggest that T. molitor males, like females, maximize fitness through enhanced longevity, partly explaining their comparable longevity.
Project description:A major component of sex-allocation theory, the Trivers-Willard model (TWM), posits that sons and daughters are differentially affected by variation in the rearing environment. In many species, the amount of parental care received is expected to have differing effects on the fitness of males and females. When this occurs, the TWM predicts that selection should favour adjustment of the offspring sex ratio in relation to the expected fitness return from offspring. However, evidence for sex-by-environment effects is mixed, and little is known about the adaptive significance of producing either sex. Here, we test whether offspring sex ratios vary according to predictions of the TWM in the house wren (Troglodytes aedon, Vieillot). We also test the assumption of a sex-by-environment effect on offspring using two experiments, one in which we manipulated age differences among nestlings within broods, and another in which we held nestling age constant but manipulated brood size. As predicted, females with high investment ability overproduced sons relative to those with lower ability. Males were also overproduced early within breeding seasons. In our experiments, the body mass of sons was more strongly affected by the sibling-competitive environment and resource availability than that of daughters: males grew heavier than females when reared in good conditions but were lighter than females when in poor conditions. Parents rearing broods with 1:1 sex ratios were more productive than parents rearing broods biased more strongly towards sons or daughters, suggesting that selection favours the production of mixed-sex broods. However, differences in the condition of offspring as neonates persisted to adulthood, and their reproductive success as adults varied with the body mass of sons, but not daughters, prior to independence from parental care. Thus, selection should favour slight but predictable variations in the sex ratio in relation to the quality of offspring that parents are able to produce. Offspring sex interacts with the neonatal environment to influence offspring fitness, thus favouring sex-ratio adjustment by parents. However, increased sensitivity of males to environmental conditions, such as sibling rivalry and resource availability, reduces the fitness returns from highly male-biased broods.
Project description:Sex-biased genes are considered to account for most of phenotypic differences between males and females. In order to explore the sex-biased gene expression in crab, we performed the whole-body transcriptome analysis in male and female juveniles of the Chinese mitten crab Eriocheir sinensis using next-generation sequencing technology. Of the 23,349 annotated unigenes, 148 were identified as sex-related genes. A total of 29 candidate genes involved in primary sex determination pathways were detected, indicating the sex determination cascade of the mitten crab might be more complex than previously supposed. Differential expression analysis showed 448 differentially expressed genes (DEGs) between the two transcriptomes. Most of DEGs were involved in processes such as metabolism and immunity, and not associated with obvious sexual function. The pathway predominantly enriched for DEGs were related to lysosome, which might reflect the differences in metabolism between males and females. Of the immune DGEs, 18 up-regulated genes in females were humoral immune factors, and eight up-regulated genes in males were pattern recognition receptors, suggesting sex differences of immune defense might exist in the mitten crab. In addition, two reproduction-related genes, vitellogenin and insulin-like androgenic gland factor, were identified to express in both sexes but with significantly higher level in males. Our research provides the first whole-body RNA sequencing of sex-specific transcriptomes for juvenile E. sinensis and will facilitate further studies on molecular mechanisms of crab sexual dimorphism.
Project description:Coronavirus disease 2019 (COVID-19) has shown high infection and mortality rates all over the world, and despite the global efforts, there is so far no specific therapy available for COVID-19. Interestingly, while the severity and mortality of COVID-19 are higher in males than in females, the underlying molecular mechanisms are unclear. In this review, we explore sex-related differences that may be contributing factors to the observed male-biased mortality from COVID-19. Males are considered the weaker sex in aspects related to endurance and infection control. Studies show that viral RNA clearance is delayed in males with COVID-19. A recent study has indicated that the testis can harbor coronavirus, and consequently, males show delayed viral clearance. However, the role of testis involvement in COVID-19 severity and mortality needs further research. Males and females show a distinct difference in immune system responses with females eliciting stronger immune responses to pathogens. This difference in immune system responses may be a major contributing factor to viral load, disease severity, and mortality. In addition, differences in sex hormone milieus could also be a determinant of viral infections as estrogen has immunoenhancing effects while testosterone has immunosuppressive effects. The sex-specific severity of COVID-19 infections indicates that further research on understanding the sex differences is needed. Inclusion of both males and females in basic research and clinical trials is required to provide critical information on sex-related differences that may help to better understand disease outcome and therapy.