Noninvasive sampling reveals short-term genetic rescue in an insular red fox population

Genetic factors in the decline of small populations are extremely difficult to study in nature. We leveraged a natural experiment to investigate evidence of inbreeding depression and genetic rescue in a remnant population of subalpine-specialized Sierra Nevada red foxes (Vulpes vulpes necator) using noninvasive genetic monitoring during 2010–2017. Only 7 individuals were detected in the first 2 years. These individuals assigned genetically to the historical population and exhibited genetic hallmarks of inbreeding and no evidence of reproduction. Two years into the study, we detected 2 first-generation immigrant males from a recently expanding population of red foxes in the Great Basin Desert. Through annual resampling of individuals (634 red fox DNA samples, 41 individuals) and molecular reconstruction of pedigrees, we documented 1–3 litters/yr for 5 years, all descended directly or indirectly from matings involving immigrant foxes. The observed heterozygosity and allelic richness of the population nearly doubled in 2 years. Abundance increased, indicative of a rapidly expanding population. Throughout the study, adult survival was high. Restoration of gene flow apparently improved the demographic trajectory of this population in the short term. Whether these benefits continue in the longer-term could depend on numerous factors, such as maintenance of any locally adapted alleles. This study highlights the value of noninvasive genetic monitoring to assess rapidly shifting conditions in small populations. Uncertainties about the longer-term trajectory of this population underscore the need to continue monitoring and to research potential for both negative and positive aspects of continued genetic infusion.

小型种群衰退过程中的遗传效应，在自然环境中极难开展研究。本研究依托一项自然实验，于2010至2017年间采用非侵入式遗传监测（noninvasive genetic monitoring），针对特化于亚高山生境的内华达山脉红狐（Vulpes vulpes necator）残存种群，探究近交衰退（inbreeding depression）与遗传拯救（genetic rescue）的相关证据。研究最初两年仅检测到7只个体。这些个体经遗传分型归属历史种群，展现出近交的遗传特征，且未发现繁殖迹象。研究开展两年后，我们检测到2只初代迁入雄性红狐，其来源为大盆地沙漠地区近期扩张的红狐种群。通过对个体的年度重采样（累计获取634份红狐DNA样本，对应41只个体）并开展分子谱系重建（pedigree reconstruction），我们在5年间记录到每年1至3窝幼崽，所有幼崽均直接或间接源自与迁入红狐的交配事件。该种群的观测杂合度（heterozygosity）与等位基因丰富度（allelic richness）在两年内近乎翻倍。种群数量显著增长，表明种群正处于快速扩张阶段。整个研究周期内，成体存活率维持在较高水平。基因流（gene flow）的恢复显然在短期内改善了该种群的种群动态轨迹（demographic trajectory）。此类益处能否在长期得以维持，取决于诸多因素，例如当地适应性等位基因的保留情况。本研究凸显了非侵入式遗传监测在评估小型种群快速变化状况时的应用价值。该种群长期动态轨迹尚存诸多不确定性，这凸显了持续开展监测的必要性，同时也需要进一步研究持续基因注入（genetic infusion）可能带来的正反两方面效应。