Graduate Group in Applied Mathematics, University of California, Davis, Davis, California 95616.
Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, Connecticut 06269.
Evolution. 2021 Nov;75(11):2842-2856. doi: 10.1111/evo.14353. Epub 2021 Oct 12.
When predators consume prey, they risk becoming infected with their prey's parasites, which can then establish the predator as a secondary host. A predator population's diet therefore influences what parasites it is exposed to, as has been repeatedly shown in many species such as threespine stickleback (Gasterosteus aculeatus) (more benthic-feeding individuals obtain nematodes from oligocheate prey, whereas limnetic-feeding individuals catch cestodes from copepod prey). These differing parasite encounters, in turn, determine how natural selection acts on the predator's immune system. We might therefore expect that ecoevolutionary dynamics of a predator's diet (as determined by its ecomorphology) should drive correlated evolution of its immune traits. Conversely, the predator's immunity to certain parasites might alter the relative costs and benefits of different prey, driving evolution of its ecomorphology. To evaluate the potential for ecological morphology to drive evolution of immunity, and vice versa, we use a quantitative genetics framework coupled with an ecological model of a predator and two prey species (the diet options). Our analysis reveals fundamental asymmetries in the evolution of ecomorphology and immunity. When ecomorphology rapidly evolves, it determines how immunity evolves, but not vice versa. Weak trade-offs in ecological morphology select for diet generalists despite strong immunological trade-offs, but not vice versa. Only weak immunological trade-offs can explain negative diet-infection correlations across populations. The analysis also reveals that eco-evo-immuno feedbacks destabilize population dynamics when trade-offs are sufficiently weak and heritability is sufficiently high. Collectively, these results highlight the delicate interplay between multivariate trait evolution and the dynamics of ecological communities.
当捕食者捕食猎物时，它们有感染猎物寄生虫的风险，这些寄生虫随后可以使捕食者成为次要宿主。捕食者种群的饮食因此会影响它所接触到的寄生虫，这在许多物种中已经反复得到证实，如三刺鱼（Gasterosteus aculeatus）（更多底栖觅食的个体从寡毛类猎物中获得线虫，而浮游觅食的个体则从桡足类猎物中获得绦虫）。这些不同的寄生虫接触，反过来又决定了自然选择如何作用于捕食者的免疫系统。因此，我们可能会期望捕食者饮食的生态进化动态（由其生态形态决定）会推动其免疫特征的相关进化。相反，捕食者对某些寄生虫的免疫力可能会改变不同猎物的相对成本和收益，从而推动其生态形态的进化。为了评估生态形态驱动免疫进化的潜力，以及反之亦然，我们使用定量遗传学框架，并结合捕食者和两种猎物物种（饮食选择）的生态模型。我们的分析揭示了生态形态和免疫进化的基本不对称性。当生态形态快速进化时，它决定了免疫的进化方式，但反之则不然。尽管存在强烈的免疫权衡，但生态形态的弱权衡仍会选择饮食的泛化者，而不是反之亦然。只有微弱的免疫权衡才能解释种群间的负饮食-感染相关性。该分析还表明，当权衡足够弱且遗传力足够高时，生态-进化-免疫反馈会使种群动态不稳定。总的来说，这些结果强调了多变量特征进化与生态群落动态之间的微妙相互作用。
