Department of Ecology & Evolutionary Biology, University of Connecticut, Storrs, Connecticut, 06269, USA.
Current Address: Evolutionary Ecology Unit, Department of Biology, Lund University, Lund, Sweden.
Evolution. 2021 Oct;75(10):2509-2523. doi: 10.1111/evo.14266. Epub 2021 May 24.
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. Consistent with substantial sexually concordant fitness effects of immune response, we find alignment of multivariate selection across the sexes despite sexual antagonism over morphological shape. 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.
寄生虫可以通过对生存和繁殖的直接影响，或者通过诱导宿主产生具有代价高昂的副作用的免疫防御来间接影响宿主的适应性。免疫防御的进化是由寄生虫感染和免疫反应的成本和收益的复杂相互作用决定的，所有这些成本和收益在性谱系的雄性和雌性宿主中可能不同。在这里，我们研究了在鱼类-绦虫宿主-寄生虫系统中诱导性免疫防御相关的适应性成本。绦虫感染会导致三刺鱼（Gasterosteus aculeatus）腹膜纤维化，限制绦虫的生长，有时会包裹并杀死寄生虫。通过调查两个野生三刺鱼种群，我们证实纤维化疤痕组织的存在与雌雄鱼的寄生虫负荷减少有关。然而，纤维化的鱼觅食成功率和生殖适应性降低（减少雌鱼产卵量和雄鱼筑巢成功率），表明免疫病理的持久存在存在很强的代价。与免疫反应的显著两性一致的适应性效应一致，我们发现尽管在形态上存在两性拮抗，但在两性之间存在多变量选择的一致性。尽管两性都经历了纤维化的代价，但净影响是不平等的，因为在两个研究种群中，雌性的绦虫暴露率更高。为了评估这种风险差异是否会导致两性特定的免疫策略，我们分析了宿主对营养传播寄生虫的免疫反应的定量遗传模型。该模型和实证数据说明了共同的免疫反应成本和收益如何导致雄性和雌性宿主的共同进化利益，尽管两性之间的感染风险不平等。
