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Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression.

ABSTRACT: 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.

SUBMITTER: Kyriazis CC

PROVIDER: S-EPMC7857301 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression.

Kyriazis Christopher C CC Wayne Robert K RK Lohmueller Kirk E KE

Evolution letters 20201217 1

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 ini ...[more]

PMID: 33552534

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Project description:BACKGROUND:Inbreeding decreases animal performance (inbreeding depression), but not all inbreeding is expected to be equally harmful. Recent inbreeding is expected to be more harmful than ancient inbreeding, because selection decreases the frequency of deleterious alleles over time. Selection efficiency is increased by inbreeding, a process called purging. Our objective was to investigate effects of recent and ancient inbreeding on yield, fertility and udder health traits in Dutch Holstein-Friesian cows. METHODS:In total, 38,792 first-parity cows were included. Pedigree inbreeding ([Formula: see text]) was computed and 75 k genotype data were used to compute genomic inbreeding, among others based on regions of homozygosity (ROH) in the genome ([Formula: see text]). RESULTS:Inbreeding depression was observed, e.g. a 1% increase in [Formula: see text] was associated with a 36.3 kg (SE?=?2.4) decrease in 305-day milk yield, a 0.48 day (SE?=?0.15) increase in calving interval and a 0.86 unit (SE?=?0.28) increase in somatic cell score for day 150 through to 400. These effects equalled -?0.45, 0.12 and 0.05% of the trait means, respectively. When [Formula: see text] was split into generation-based components, inbreeding on recent generations was more harmful than inbreeding on more distant generations for yield traits. When [Formula: see text] was split into new and ancestral components, based on whether alleles were identical-by-descent for the first time or not, new inbreeding was more harmful than ancestral inbreeding, especially for yield traits. For example, a 1% increase in new inbreeding was associated with a 2.42 kg (SE?=?0.41) decrease in 305-day fat yield, compared to a 0.03 kg (SE?=?0.71) increase for ancestral inbreeding. There were no clear differences between effects of long ROH (recent inbreeding) and short ROH (ancient inbreeding). CONCLUSIONS:Inbreeding depression was observed for yield, fertility and udder health traits. For yield traits and based on pedigree, inbreeding on recent generations was more harmful than inbreeding on distant generations and there was evidence of purging. Across all traits, long and short ROH contributed to inbreeding depression. In future work, inbreeding depression and purging should be assessed in more detail at the genomic level, using higher density information and genomic time series.

Dataset Information

Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression.

Publications

Strongly deleterious mutations are a primary determinant of extinction risk due to inbreeding depression.

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