Human‐driven habitat fragmentation and loss have led to a proliferation of small and isolated plant and animal populations with high risk of extinction. One of the main threats to extinction in these populations is inbreeding depression, which is primarily caused by recessive deleterious mutations becoming homozygous due to inbreeding. The typical approach for managing these populations is to maintain high genetic diversity, increasingly by translocating individuals from large populations to initiate a “genetic rescue.” However, the limitations of this approach have recently been highlighted by the demise of the gray wolf population on Isle Royale, which declined to the brink of extinction soon after the arrival of a migrant from the large mainland wolf population. Here, we use a novel population genetic simulation framework to investigate the role of genetic diversity, deleterious variation, and demographic history in mediating extinction risk due to inbreeding depression in small populations. We show that, under realistic models of dominance, large populations harbor high levels of recessive strongly deleterious variation due to these mutations being hidden from selection in the heterozygous state. As a result, when large populations contract, they experience a substantially elevated risk of extinction after these strongly deleterious mutations are exposed by inbreeding. Moreover, we demonstrate that, although genetic rescue is broadly effective as a means to reduce extinction risk, its effectiveness can be greatly increased by drawing migrants from small or moderate‐sized source populations rather than large source populations due to smaller populations harboring lower levels of recessive strongly deleterious variation. Our findings challenge the traditional conservation paradigm that focuses on maximizing genetic diversity in small populations in favor of a view that emphasizes minimizing strongly deleterious variation. These insights have important implications for managing small and isolated populations in the increasingly fragmented landscape of the Anthropocene.

中文翻译：

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强烈有害的突变是近交衰退导致灭绝风险的主要决定因素


人类造成的栖息地破碎和丧失导致小型且孤立的动植物种群激增，面临很高的灭绝风险。这些种群灭绝的主要威胁之一是近交衰退，这主要是由近交导致的隐性有害突变变成纯合引起的。管理这些种群的典型方法是保持高度的遗传多样性，越来越多地通过从大量种群中转移个体来发起“基因拯救”。然而，最近皇家岛上灰狼种群的消亡凸显了这种方法的局限性，在大量大陆狼种群的迁徙到来后不久，灰狼种群就跌至灭绝的边缘。在这里，我们使用一种新颖的群体遗传模拟框架来研究遗传多样性、有害变异和人口历史在调节小群体近交衰退导致的灭绝风险中的作用。我们表明，在现实的优势模型下，大量群体存在高水平的隐性强烈有害变异，因为这些突变在杂合状态下被隐藏而无法被选择。因此，当大量种群收缩时，在近亲繁殖暴露出这些强烈有害的突变后，它们面临灭绝的风险大大增加。此外，我们证明，虽然基因拯救作为降低灭绝风险的一种手段广泛有效，但通过从小型或中等规模的来源种群而不是大型来源种群中吸引移民，可以大大提高其有效性，因为较小的种群具有较低的遗传水平。隐性强烈有害变异。 我们的研究结果挑战了传统的保护范式，传统的保护范式侧重于最大限度地提高小种群的遗传多样性，转而支持强调最大限度地减少有害变异的观点。这些见解对于在人类世日益分散的景观中管理小而孤立的人口具有重要意义。