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Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction.

ABSTRACT: The observation that small isolated populations often suffer reduced fitness from inbreeding depression has guided conservation theory and practice for decades. However, investigating the genome-wide dynamics associated with inbreeding depression in natural populations is only now feasible with relatively inexpensive sequencing technology and annotated reference genomes. To characterize the genome-wide effects of intense inbreeding and isolation, we performed whole-genome sequencing and morphological analysis of an iconic inbred population, the gray wolves (Canis lupus) of Isle Royale. Through population genetic simulations and comparison with wolf genomes from a variety of demographic histories, we find evidence that severe inbreeding depression in this population is due to increased homozygosity of strongly deleterious recessive mutations. Our results have particular relevance in light of the recent translocation of wolves from the mainland to Isle Royale, as well as broader implications for management of genetic variation in the fragmented landscape of the modern world.

SUBMITTER: Robinson JA

PROVIDER: S-EPMC6541468 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction.

Robinson Jacqueline A JA Räikkönen Jannikke J Vucetich Leah M LM Vucetich John A JA Peterson Rolf O RO Lohmueller Kirk E KE Wayne Robert K RK

Science advances 20190529 5

The observation that small isolated populations often suffer reduced fitness from inbreeding depression has guided conservation theory and practice for decades. However, investigating the genome-wide dynamics associated with inbreeding depression in natural populations is only now feasible with relatively inexpensive sequencing technology and annotated reference genomes. To characterize the genome-wide effects of intense inbreeding and isolation, we performed whole-genome sequencing and morpholo ...[more]

PMID: 31149628

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Project description:Caribou (Rangifer tarandus) have experienced dramatic declines in both range and population size across Canada over the past century. Boreal caribou (R. t. caribou), 1 of the 12 Designatable Units, has lost approximately half of its historic range in the last 150 years, particularly along the southern edge of its distribution. Despite this overall northward contraction, some populations have persisted at the trailing range edge, over 150 km south of the continuous boreal caribou range in Ontario, along the coast and nearshore islands of Lake Superior. The population history of caribou along Lake Superior remains unclear. It appears that these caribou likely represent a remnant distribution at the trailing edge of the receding population of boreal caribou, but they may also exhibit local adaptation to the coastal environment. A better understanding of the population structure and history of caribou along Lake Superior is important for their conservation and management. Here, we use high-coverage whole genomes (N = 20) from boreal, eastern migratory, and barren-ground caribou sampled in Manitoba, Ontario, and Quebec to investigate population structure and inbreeding histories. We discovered that caribou from the Lake Superior range form a distinct group but also found some evidence of gene flow with the continuous boreal caribou range. Notably, caribou along Lake Superior demonstrated relatively high levels of inbreeding (measured as runs of homozygosity; ROH) and genetic drift, which may contribute to the differentiation observed between ranges. Despite inbreeding, caribou along Lake Superior retained high heterozygosity, particularly in genomic regions without ROH. These results suggest that they present distinct genomic characteristics but also some level of gene flow with the continuous range. Our study provides key insights into the genomics of the southernmost range of caribou in Ontario, beginning to unravel the evolutionary history of these small, isolated caribou populations.

Project description:Background and aimsHabitat degradation and landscape fragmentation dramatically lower population sizes of rare plant species. Decreasing population sizes may, in turn, negatively affect genetic diversity and reproductive fitness, which can ultimately lead to local extinction of populations. Although such extinction vortex dynamics have been postulated in theory and modelling for decades, empirical evidence from local extinctions of plant populations is scarce. In particular, comparisons between current vs. historical genetic diversity and differentiation are lacking despite their potential to guide conservation management.MethodsWe studied the population genetic signatures of the local extinction of Biscutella laevigata subsp. gracilis populations in Central Germany. We used microsatellites to genotype individuals from 15 current populations, one ex situ population, and 81 herbarium samples from five extant and 22 extinct populations. In the current populations, we recorded population size and fitness proxies, collected seeds for a germination trial and conducted a vegetation survey. The latter served as a surrogate for habitat conditions to study how habitat dissimilarity affects functional connectivity among the current populations.Key resultsBayesian clustering revealed similar gene pool distribution in current and historical samples but also indicated that a distinct genetic cluster was significantly associated with extinction probability. Gene flow was affected by both the spatial distance and floristic composition of population sites, highlighting the potential of floristic composition as a powerful predictor of functional connectivity which may promote decision-making for reintroduction measures. For an extinct population, we found a negative relationship between sampling year and heterozygosity. Inbreeding negatively affected germination.ConclusionsOur study illustrates the usefulness of historical DNA to study extinction vortices in threatened species. Our novel combination of classical population genetics together with data from herbarium specimens, an ex situ population and a germination trial underlines the need for genetic rescue measures to prevent extinction of B. laevigata in Central Germany.

Dataset Information

Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction.

Publications

Genomic signatures of extensive inbreeding in Isle Royale wolves, a population on the threshold of extinction.

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