Sexual Reproduction and Immunity

Abstract

Sexual reproduction is a highly complicated process shaped in part by the need to optimise reproductive investment, which can differ and evolve antagonistically between the sexes. Sexual reproduction is also intimately linked with immunity through a variety of means. Combining these seemingly disparate biological functions has led to the emergence of the new field of reproductive immunity. One striking parallel between reproduction and immunity is the detection of ‘other’. Failure to detect pathogens results in disease. Failure to ignore self causes autoimmunity. Similarly, individuals, as well as gametes, must choose appropriate partners avoiding interspecific mating on one extreme or reproducing with kin to avoid inbreeding, on the other. The relationship between reproduction and immunity is likely affected by the mating system and the degree of sexual conflict. Reproduction and immunity seem connected in three ways by resource trade‐offs among life‐history traits, by disease reduction due to mate choice of healthy mates and protective genes for the offspring and by mating‐induced immunity to reduce infection risk. Key Concepts Mating and sexual reproduction can be linked to immunity in three ways: Reproduction and immunity can trade‐off. Choosing a healthy partner can result in protection for the actor and its offspring. Mating can directly result in immune responses. This immune activation may be a much older association between the immune system and sexual reproduction. Both immune activation and sexual reproduction involve recognising self from nonself. Immune responses upon mating can serve to protect females from infection and play a role in sperm selection. Mating system likely dictates the intensity and costs of these immune responses on mating.

Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

“…Sexual selection can result in increased male harm to females during mating (22,29,32), either through direct injury or infection with pathogens, and this should in theory favour increased female investment in immunity when female lifetime reproductive success is elevated by increased longevity (5,22–24,27,35,39). Here, we provide a suite of experimental and comparative data collectively showing that sex-differences in immunity can be modulated by sexual conflict in a species where costs of mating are conspicuous.…”

“…While previous studies have quantified female immune responses post mating (5,5,22,23,45,50,53,99,100), it often remains unclear whether male harm via genitalia or ejaculatory compounds (i.e. sexual antagonism) drive such responses, or whether they represent independent female optimization of the trade-off between current and future reproduction (5,22,23,27,49,101). Here, we directly manipulated the level of sexual selection and conflict, which is relatively well understood in C. maculatus (e.g.…”

“…In polygamous species, where sexual selection on males is intense, females are often predicted to gain more than males from investing in survival and longevity at the cost of current reproduction and mating effort (3,9,35) and are therefore also predicted to invest more in immunity than males (but see: (2,10,24,35–37)). Sexual selection may also have pronounced direct effects on optimal investment in immunity, as it may dictate the economics of reproduction (23,27,38,39) and lead to elevated mating rates (40), which in turn may increase disease transmission (16,24,25,28). Indeed, it has been suggested that sexual dimorphism in immunity should increase with sex-differences in optimal mating rates and the strength of sexual selection (5,13,21,23,27,41,42).…”

“…Females, in turn, evolve counter-adaptations to alleviate the harm inflicted by males resulting in a coevolutionary arms race between the sexes (23,43,46,47). Female immune responses may represent one type of such counter-adaptation (23,27,48,49). This suggests that infections or harm on females, induced by sexually selected male mating strategies, may be a significant selection pressure on female immunity in polyandrous taxa (21,24,27,41,50).…”

“…Female immune responses may represent one type of such counter-adaptation (23,27,48,49). This suggests that infections or harm on females, induced by sexually selected male mating strategies, may be a significant selection pressure on female immunity in polyandrous taxa (21,24,27,41,50). Hence, the evolution of sexual dimorphism in immunity may in part be a result of male-imposed costs of mating in females.…”