McIntire Kristina M, Dziuba Marcin K, Haywood Elizabeth B, Robertson Miles L, Vaandrager Megan, Baird Emma, Corcoran Fiona E, Nelson Taleah, Cortez Michael H, Duffy Meghan A
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA.
Department of Mathematics, Florida State University, Tallahassee, Florida, USA.
Ecology. 2025 Sep;106(9):e70165. doi: 10.1002/ecy.70165.
Pathogens can alter the phenotype not only of exposed hosts, but also of future generations. Transgenerational immune priming, where parental infection drives reduced susceptibility of offspring, has been particularly well explored, but pathogens can also alter life history traits of offspring. Here, we examined the potential for transgenerational impacts of a microsporidian pathogen, Ordospora pajunii, by experimentally measuring the impact of maternal exposure on offspring fitness in the presence and absence of parasites, and then developing mathematical models that explored the population-level impacts of these transgenerational effects. We did not find evidence of transgenerational immune priming: offspring of exposed mothers became infected at high rates, similar to offspring of unexposed mothers, and the infection burden did not differ between these two groups. We also did not find any evidence of transgenerational tolerance, where daughters of exposed mothers have higher fitness after infection. Instead, we found evidence for negative transgenerational impacts of infection: uninfected offspring of exposed mothers had substantially greater early life mortality than uninfected offspring of unexposed mothers. Offspring of exposed mothers also had reduced growth rates, fewer clutches, and fewer offspring. We propose that these observations should be considered transgenerational virulence, where a pathogen reduces the fitness of the offspring of infected hosts. Our parameterized mathematical model allowed us to explore the impacts of transgenerational virulence at the population level. If transgenerational virulence manifests as decreased reproduction or increased mortality in offspring, as we saw in the empirical portion of our study, this reduces total host density, infection prevalence, and infected host density, which could have implications for both host conservation and spillover risk. We propose that transgenerational virulence might be common and is a concept worthy of further empirical and theoretical exploration.
病原体不仅可以改变受感染宿主的表型，还能影响其后代的表型。亲代感染使后代易感性降低的代际免疫激发现象已得到充分研究，但病原体也能够改变后代的生活史特征。在此，我们通过实验测量母体暴露在有无寄生虫情况下对后代适合度的影响，进而构建数学模型来探究这些代际效应在种群水平上的影响，以此研究微孢子虫病原体——帕氏鄂尔多斯孢虫（Ordospora pajunii）产生代际影响的可能性。我们没有发现代际免疫激发的证据：暴露母体的后代感染率很高，与未暴露母体的后代相似，且两组之间的感染负担并无差异。我们也没有找到任何代际耐受性的证据，即暴露母体的女儿在感染后具有更高的适合度。相反，我们发现了感染产生负面代际影响的证据：暴露母体的未感染后代在生命早期的死亡率显著高于未暴露母体的未感染后代。暴露母体的后代生长率也较低，产卵次数更少，后代数量也更少。我们认为这些观察结果应被视为代际毒力，即病原体降低受感染宿主后代的适合度。我们的参数化数学模型使我们能够在种群水平上探究代际毒力的影响。如果代际毒力表现为后代繁殖率下降或死亡率增加，正如我们在研究的实证部分所看到的那样，这会降低宿主总密度、感染率和受感染宿主密度，这可能对宿主保护和溢出风险都有影响。我们认为代际毒力可能很常见，是一个值得进一步进行实证和理论探索的概念。
