Consequences for conservation: population density and genetic effects on reproduction of an endangered lagomorph

Understanding reproduction and mating systems is important for managers tasked with conserving vulnerable species. Genetic tools allow biologists to investigate reproduction and mating systems with high resolution and are particularly useful for species that are otherwise difficult to study in their natural environments. We conducted parentage analyses using 19 nuclear DNA microsatellite loci to assess the influence of population density, genetic diversity, and ancestry on reproduction, and to examine the mating system of pygmy rabbits (Brachylagus idahoensis) bred in large naturalized enclosures for the reintroduction and recovery of the endangered distinct population in central Washington, USA. Reproductive output for females and males decreased as population density and individual homozygosity increased. We identified an interaction indicating that male reproductive output decreased as genetic diversity declined at high population densities, but there was no effect at low densities. Males with high amounts (>50%) of Washington ancestry had higher reproductive output than the other ancestry groups, while reproductive output was decreased for males with high northern Utah/Wyoming ancestry and females with high Oregon/Nevada ancestry. Females and males bred with an average of 3.8 and 3.6 mates per year, respectively, and we found no evidence of positive or negative assortative mating with regards to ancestry. Multiple paternity was confirmed in 81% of litters, and we report the first documented cases of juvenile breeding by pygmy rabbits. This study demonstrates how variation in population density, genetic diversity, and ancestry impact fitness for an endangered species being bred for conservation. Our results advance understanding of basic life history characteristics for a cryptic species that is difficult to study in the wild, and provide lessons for managing populations of vulnerable species in captive and free-ranging populations.

解析繁殖与交配系统，对于负责保护脆弱物种的管理者而言至关重要。遗传工具可帮助生物学家以高分辨率开展繁殖与交配系统研究，尤其适用于难以在自然环境中直接观测的物种。本研究采用19个核DNA微卫星位点（microsatellite loci）开展亲权分析，以评估种群密度、遗传多样性及祖先血统对繁殖的影响，并探究为美国华盛顿州中部濒危独特种群的再引入与恢复而繁育、饲养于大型半自然围栏内的侏兔（Brachylagus idahoensis）的交配系统。随着种群密度升高与个体纯合度提升，雌雄个体的繁殖产出均出现下降。本研究发现存在交互效应：在高种群密度条件下，雄性繁殖产出随遗传多样性降低而下降，但在低密度种群中未观察到该效应。拥有超过50%华盛顿地区祖先血统的雄性个体，其繁殖产出高于其他血统组；而携带高比例犹他州北部/怀俄明州血统的雄性，以及携带高比例俄勒冈州/内华达州血统的雌性，其繁殖产出均出现下降。雌雄个体年均配偶数量分别为3.8只与3.6只，未发现基于祖先血统的正选型或负选型交配证据。81%的幼崽窝次被证实存在多父本现象，本研究还首次记录了侏兔幼体繁殖的案例。本研究阐明了种群密度、遗传多样性与祖先血统的变异，如何影响用于保护繁育的濒危物种的适合度。本研究结果加深了人们对这类难以在野外开展研究的隐秘物种基础生活史特征的认知，并为圈养及野生脆弱物种种群的管理提供了参考依据。