Slowinski Samuel P, Kido Allyson K, Alexander Laura W, Shirdon Andrea H, Bruns Emily L
Department of Biology, University of Maryland, College Park, MD 20784.
School of Biological Sciences, University of New England, Biddeford, ME 04005.
Proc Natl Acad Sci U S A. 2025 Apr 8;122(14):e2419192122. doi: 10.1073/pnas.2419192122. Epub 2025 Apr 4.
High juvenile susceptibility drives infectious disease epidemics across kingdoms, yet the evolutionary mechanisms that maintain this susceptibility are unclear. We tested the hypothesis that juvenile susceptibility is maintained by high costs of resistance by quantifying the genetic correlation between host fitness and age-specific innate resistance to a fungal pathogen in a wild plant. We separately measured the resistance of 45 genetic families of the wild plant, to its endemic fungal pathogen, at four ages in a controlled inoculation experiment. We then grew these same families in a field common garden and tracked survival and fecundity over a 2-y period and quantified the correlation between age-specific resistance and fitness in the field. We found significant fitness costs associated with disease resistance at juvenile but not at adult host stages. We then used an age-structured compartmental model to show that the magnitude of these costs is sufficient to prevent the evolution of higher juvenile resistance in models, allowing the disease to persist. Taken together, our results show that costs of resistance vary across host lifespan, providing an evolutionary explanation for the maintenance of juvenile susceptibility.
高幼年易感性驱动跨物种的传染病流行，然而维持这种易感性的进化机制尚不清楚。我们通过量化野生植物中宿主适合度与针对真菌病原体的年龄特异性先天抗性之间的遗传相关性，来检验幼年易感性由高抗性成本维持这一假说。在一项受控接种实验中，我们分别在四个年龄段测量了该野生植物45个遗传家系对其地方性真菌病原体的抗性。然后，我们将这些相同的家系种植在田间普通园圃中，在两年时间内跟踪其存活率和繁殖力，并量化田间年龄特异性抗性与适合度之间的相关性。我们发现，在幼年宿主阶段而非成年宿主阶段，抗病性与适合度成本显著相关。然后，我们使用一个年龄结构的隔间模型来表明，这些成本的大小足以阻止模型中幼年抗性的进化，从而使疾病持续存在。综合来看，我们的结果表明，抗性成本在宿主寿命期间有所不同，这为幼年易感性的维持提供了一种进化解释。
