Male and female reproductive fitness costs of an immune response in natural populations

Abstract

<jats:p>Parasites can mediate host fitness both directly, via effects on survival and reproduction, or indirectly by inducing host immune defense with costly side-effects. The evolution of immune defense is determined by a complex interplay of costs and benefits of parasite infection and immune response, all of which may differ for male and female hosts in sexual lineages. Here, we examine fitness costs associated with an inducible immune defense in a fish-cestode host-parasite system. Cestode infection induces peritoneal fibrosis in threespine stickleback (Gasterosteus aculeatus), constraining cestode growth and sometimes encasing and killing the parasite. Surveying two wild populations of stickleback, we confirm that the presence of fibrosis scar tissue is associated with reduced parasite burden in both male and female fish. However, fibrotic fish had lower foraging success and reproductive fitness (reduced female egg production and male nesting success), indicating strong costs of the lingering immunopathology. We show that these substantial sexually-concordant fitness effects of immune response act to align multivariate selection across the sexes, masking the signature of sexual antagonism that acted on morphology alone. Although both sexes experienced costs of fibrosis, the net impacts are unequal because in the two study populations females had higher cestode exposure. To evaluate whether this difference in risk should drive sex-specific immune strategies, we analyze a quantitative genetic model of host immune response to a trophically transmitted parasite. The model and empirical data illustrate how shared costs and benefits of immune response lead to shared evolutionary interests of male and female hosts, despite unequal infection risks across the sexes.</jats:p>

Evolution of a costly immunity to cestode parasites is a pyrrhic victory

“…If fibrosis reduces the ability or motivation to build a nest and defend it against rivals and egg predators, we expect fibrosis rates of successfully nesting males to be lower than non-nesting males caught nearby outside of the aggregation of nests. In each of two lakes (Roselle and Boot) we confirmed that nesting males had lower fibrosis than males who had failed to nest (odds ratios of 0.41 and 0.56 respectively, both P < 0.01), controlling for infection status and body size (De Lisle and Bolnick 2020). The mechanisms of these fitness costs of fibrosis are still under investigation, but may include increased metabolic demands, locomotor constraints from more rigid tissues, or constrained female ovary expansion due to adhesion to surrounding tissue.…”

Phylogenetically conserved peritoneal fibrosis response to an immunologic adjuvant in ray-finned fishes

“…Our study was motivated by inter-population variation in threespine sticklebacks’ ability to encapsulate parasitic tapeworm S. solidus (Weber et al 2017b). The inter-population variation probably stems from an evolutionary trade-off between the benefit of resistance (early encapsulation of the worm) and the risk of organ adhesion, excessive fibroblast proliferation, and ultimately partial sterility in the stickleback (Weber et al, in preparation; De Lisle and Bolnick 2020). Previous records on peritoneal fibrosis in threespine stickleback are mostly lacking (but see Hoffman 1975, p.175), although the phenomenon is found in numerous populations across the species’ circumpolar range.…”

“…This fibrosis has been found to effectively suppress growth of certain parasites, or even lead to parasite death (Weber et al, in preparation). However, the benefits of tissue repair and parasite containment can come with a cost from chronic type 2 immune response during persistent or recurrent infections, which may develop into serious health issues or even death (Gause et al 2013; De Lisle and Bolnick 2020). Here, we measure the extent of evolutionary conservation of a key immune phenotype, fibrosis.…”

“…This presumably beneficial form of resistance has costs in greatly suppressing female gonad development and male reproduction (De Lisle and Bolnick 2020; Weber et al, in preparation). These costs may explain why the intensive peritoneal response to S. solidus has evolved in only some lake populations, and in some geographic regions of the sticklebacks’ range (Weber et al 2017a).…”

Sexually Transmitted Infections Select for Different Levels of Immunocompetence And Reproductive Efforts in The Two Sexes

“…In non-human species, surveying two wild populations of stickleback confirmed that the presence of fibrosis scar tissue is associated with reduced parasite burden in both male and female fish. However, fibrotic fish had lower reproductive success (reduced male nesting and female egg), indicating big costs of the lingering immunopathology (De Lisle and Bolnick 2020).…”