The role of infectious disease in the evolution of females: evidence from anther-smut disease on a gynodioecious alpine carnation

In flowering plants, the evolution of females is widely hypothesized to be the first step in the evolutionary pathway to separate male and female sexes, or dioecy. Natural enemies have the potential to drive this evolution if they preferentially attack hermaphrodites over females. We studied sex-based differences in exposure to anther-smut (Microbotryum), a sterilizing pollinator-transmitted disease, in Dianthus pavonius, a gynodioecious perennial herb. We found that within a heavily diseased population, females consistently had lower levels of Microbotryum spore deposition relative to hermaphrodites and that this is difference was driven by rapid floral closing in females following successful pollination. We further show that this protective closing behavior is frequency-dependent; females close faster when they are rare. These results indicate that anther-smut disease is an important source of selection for females, especially since we found in a common garden experiment no evidence t...在显花植物中，学界普遍认为雌性演化是通往雌雄异株（dioecy）演化路径的首要步骤。若自然天敌优先侵袭雌雄同体个体而非雌性个体，则其具备推动这一演化进程的潜力。我们以雌全异株（gynodioecious）多年生草本植物Dianthus pavonius为研究对象，分析了其在暴露于花药黑粉菌（Microbotryum，一种经传粉媒介传播的灭菌性病害）时的性别相关差异。在一个病害发生严重的种群中，我们发现相较于雌雄同体个体，雌性个体的花药黑粉菌孢子沉降量始终更低，且该差异源于雌性个体在成功授粉后会快速闭合花部结构。我们进一步证实，这种具有保护作用的花部闭合行为存在频率依赖性：当雌性个体种群较为稀有时，其花部闭合速度更快。上述结果表明，花药黑粉菌病害是推动雌性演化的重要选择压力来源，尤其值得注意的是，我们在同质园实验（common garden experiment）中未发现……