Mating strategies explain sex-biased infections in an emerging fungal disease

Macy J Kailing, Joseph R Hoyt, J Paul White, Jennifer A Redell, Heather M Kaarakka, Kate E Langwig
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Abstract

Mating dynamics can govern species impacts from novel pressures by influencing demographic processes that affect mortality risk. Understanding how mating systems shape interactions among individuals can improve predictions of the effects of environmental change on populations. Here, we examined sex differences in mating phenology in populations where mating activity coincides with exposure to P. destructans, a lethal fungal pathogen, to understand how reproductive strategies contribute to disease impacts. As P. destructans can replicate only at the cool temperatures at which bats hibernate, we expected differences in activity among sexes to modify disease dynamics. We used passive antenna systems installed at the entrances of hibernacula to characterize activity patterns of bats impacted by white-nose syndrome. We also measured pathogen loads on bats during autumn mating and early hibernation to assess how infection severity 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 period and later in autumn than females. Importantly, these differences in mating phenology likely led to more severe infections in females during early hibernation as male activity and thus warm body temperatures inhibited pathogen growth. Differences in activity between sexes and in the transition from swarm to hibernation likely reflects males maximizing their mating opportunities while females conserve energy to meet the cost of spring migration and reproduction. More broadly, our results show how mating 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.
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交配策略解释了一种新出现的真菌疾病中的性别差异感染
交配动态可通过影响死亡风险的人口统计过程来控制物种在新压力下的影响。了解交配系统如何形成个体间的相互作用,可以改善环境变化对种群影响的预测。在这里,我们研究了交配活动与暴露于致命真菌病原体毁坏性咽炎(P. destructans)同时发生的种群中交配表型的性别差异,以了解繁殖策略是如何对疾病影响产生作用的。由于毁伤性蝙蝠疫霉只能在蝙蝠冬眠时的低温环境中复制,我们预计性别间的活动差异会改变疾病的动态变化。我们使用安装在冬眠室入口处的被动天线系统来描述受白鼻综合症影响的蝙蝠的活动模式。我们还测量了秋季交配和冬眠早期蝙蝠身上的病原体负荷,以评估感染严重程度如何随宿主物候变化而变化。我们发现,雌性蝙蝠在秋季活动的天数较少,在雄性蝙蝠之后到达,并且主要在最温暖的夜晚活动。与雌性相比,雄性在整个交配期和更晚的秋季都非常活跃。重要的是,由于雄性的活动以及温暖的体温抑制了病原体的生长,这些交配物候学上的差异很可能导致雌性在冬眠早期受到更严重的感染。两性之间的活动差异以及从蜂群到冬眠的过渡可能反映了雄性最大限度地利用交配机会,而雌性则节约能量以满足春季迁徙和繁殖的需要。从更广泛的意义上讲,我们的研究结果表明了交配物候如何导致一种新型疾病对不同性别的影响,并强调了了解物种交配系统对预测环境变化影响的价值。
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