Activity patterns during the mating season predict sex-biased infections in an emerging fungal disease

Mating dynamics can govern species impacts from rapid global change by influencing population rates of growth and adaptation, as well as individual traits that affect mortality risks from novel pressures. Here, we examined sex differences in the activity of Myotis lucifugus during their mating season, which coincides with exposure to the lethal fungal pathogen (Pseudogymnoascus destructans) that causes white-nose syndrome. We expected differences in activity between sexes to modify seasonal P. destructans dynamics as the pathogen can replicate only at the cool temperatures at which bats hibernate. We used passive antenna systems installed at the entrances of hibernacula and PIT tags to characterize activity patterns of bats. We also measured pathogen loads on bats during the autumn mating and early hibernation periods to assess how infection changed according to host phenology. We found that females spent fewer days active during autumn, arrived after males, and were primarily active on the warmest nights. Males remained highly active throughout the mating season and later in autumn than females. Importantly, differences in phenology corresponded to higher pathogen loads on females during early hibernation as male activity, and thus warm body temperatures, inhibit pathogen growth. Differences in activity between sexes and in the transition from swarm to hibernation likely reflect males maximizing their mating opportunities while females conserve energy to meet the cost of spring migration and reproduction. More broadly, our results show how activity during the mating season and phenology can contribute to sex-biased impacts of a novel disease and highlight the value of understanding species’ mating systems to anticipate the impacts of environmental change.

交配动态可通过调控种群增长与适应速率，以及影响个体应对新型胁迫的存活相关性状，决定物种在快速全球变化中的受影响效应。本研究以小棕蝠（Myotis lucifugus）为研究对象，探究其交配季的性别间活动差异——该时段恰好也是其接触引发白鼻综合征的致死真菌性病原体伪裸囊菌（Pseudogymnoascus destructans）的时期。我们推测，性别间的活动差异会改变伪裸囊菌的季节动态，因为该病原体仅能在蝙蝠冬眠的低温环境中完成繁殖。本研究借助安装在冬眠洞穴入口处的无源天线系统与PIT标签（Passive Integrated Transponder），对蝙蝠的活动模式进行系统表征。我们还在秋季交配与冬眠初期阶段，测定了蝙蝠携带的病原体载荷量，以评估感染程度如何随宿主物候发生变化。研究结果显示，雌性小棕蝠在秋季的活跃天数更少，抵达交配场的时间晚于雄性，且主要在气温最高的夜间开展活动。雄性则在整个交配季均保持较高活跃度，且秋季活跃时段显著长于雌性。值得注意的是，物候差异使得雌性在冬眠早期携带的病原体载荷量更高——这是由于雄性的活动及其伴随的较高体温可有效抑制病原体的繁殖。性别间的活动差异，以及蝙蝠从集群交配到进入冬眠的过渡模式差异，大概率反映了雄性最大化交配机会、雌性则储存能量以应对春季迁徙与繁殖成本的生存策略。从更广泛的研究视角来看，本研究结果阐明了交配季活动与物候如何推动新型疾病产生性别偏向性的影响效应，并凸显了理解物种交配系统对于预判环境变化影响的重要学术价值。