Purging of deleterious burden in the endangered Iberian lynx.

SignificanceThe dynamics of deleterious variation under contrasting demographic scenarios remain poorly understood in spite of their relevance in evolutionary and conservation terms. Here we apply a genomic approach to study differences in the burden of deleterious alleles between the endangered Iberian lynx (Lynx pardinus) and the widespread Eurasian lynx (Lynx lynx). Our analysis unveils a significantly lower deleterious burden in the former species that should be ascribed to genetic purging, that is, to the increased opportunities of selection against recessive homozygotes due to the inbreeding caused by its smaller population size, as illustrated by our analytical predictions. This research provides theoretical and empirical evidence on the evolutionary relevance of genetic purging under certain demographic conditions.

Genomic patterns in the widespread Eurasian lynx shaped by Late Quaternary climatic fluctuations and anthropogenic impacts.

Disentangling the contribution of long-term evolutionary processes and recent anthropogenic impacts to current genetic patterns of wildlife species is key to assessing genetic risks and designing conservation strategies. Here, we used 80 whole nuclear genomes and 96 mitogenomes from populations of the Eurasian lynx covering a range of conservation statuses, climatic zones and subspecies across Eurasia to infer the demographic history, reconstruct genetic patterns, and discuss the influence of long-term isolation and/or more recent human-driven changes. Our results show that Eurasian lynx populations shared a common history until 100,000 years ago, when Asian and European populations started to diverge and both entered a period of continuous and widespread decline, with western populations, except Kirov, maintaining lower effective sizes than eastern populations. Population declines and increased isolation in more recent times probably drove the genetic differentiation between geographically and ecologically close westernmost European populations. By contrast, and despite the wide range of habitats covered, populations are quite homogeneous genetically across the Asian range, showing a pattern of isolation by distance and providing little genetic support for the several proposed subspecies. Mitogenomic and nuclear divergences and population declines starting during the Late Pleistocene can be mostly attributed to climatic fluctuations and early human influence, but the widespread and sustained decline since the Holocene is more probably the consequence of anthropogenic impacts which intensified in recent centuries, especially in western Europe. Genetic erosion in isolated European populations and lack of evidence for long-term isolation argue for the restoration of lost population connectivity.

Genetic evaluation of the Iberian lynx ex situ conservation programme.

Ex situ programmes have become critical for improving the conservation of many threatened species, as they establish backup populations and provide individuals for reintroduction and reinforcement of wild populations. The Iberian lynx was considered the most threatened felid species in the world in the wake of a dramatic decline during the second half of the 20th century that reduced its numbers to around only 100 individuals. An ex situ conservation programme was established in 2003 with individuals from the two well-differentiated, remnant populations, with great success from a demographic point of view. Here, we evaluate the genetic status of the Iberian lynx captive population based on molecular data from 36 microsatellites, including patterns of relatedness and representativeness of the two remnant genetic backgrounds among founders, the evolution of diversity and inbreeding over the years, and genetic differentiation among breeding facilities. In general terms, the ex situ population harbours most of the genetic variability found in the two wild populations and has been able to maintain reasonably low levels of inbreeding and high diversity, thus validating the applied management measures and potentially representing a model for other species in need of conservation.

Novel efficient genome-wide SNP panels for the conservation of the highly endangered Iberian lynx.

BACKGROUND: The Iberian lynx (Lynx pardinus) has been acknowledged as the most endangered felid species in the world. An intense contraction and fragmentation during the twentieth century left less than 100 individuals split in two isolated and genetically eroded populations by 2002. Genetic monitoring and management so far have been based on 36 STRs, but their limited variability and the more complex situation of current populations demand more efficient molecular markers. The recent characterization of the Iberian lynx genome identified more than 1.6 million SNPs, of which 1536 were selected and genotyped in an extended Iberian lynx sample. METHODS: We validated 1492 SNPs and analysed their heterozygosity, Hardy-Weinberg equilibrium, and linkage disequilibrium. We then selected a panel of 343 minimally linked autosomal SNPs from which we extracted subsets optimized for four different typical tasks in conservation applications: individual identification, parentage assignment, relatedness estimation, and admixture classification, and compared their power to currently used STR panels. RESULTS: We ascribed 21 SNPs to chromosome X based on their segregation patterns, and identified one additional marker that showed significant differentiation between sexes. For all applications considered, panels of autosomal SNPs showed higher power than the currently used STR set with only a very modest increase in the number of markers. CONCLUSIONS: These novel panels of highly informative genome-wide SNPs provide more powerful, efficient, and flexible tools for the genetic management and non-invasive monitoring of Iberian lynx populations. This example highlights an important outcome of whole-genome studies in genetically threatened species.

Bottleneck-associated changes in the genomic landscape of genetic diversity in wild lynx populations.

Demographic bottlenecks generally reduce genetic diversity through more intense genetic drift, but their net effect may vary along the genome due to the random nature of genetic drift and to local effects of recombination, mutation, and selection. Here, we analyzed the changes in genetic diversity following a bottleneck by comparing whole-genome diversity patterns in populations with and without severe recent documented declines of Iberian (Lynx pardinus, n = 31) and Eurasian lynx (Lynx lynx, n = 29). As expected, overall genomic diversity correlated negatively with bottleneck intensity and/or duration. Correlations of genetic diversity with divergence, chromosome size, gene or functional site content, GC content, or recombination were observed in nonbottlenecked populations, but were weaker in bottlenecked populations. Also, functional features under intense purifying selection and the X chromosome showed an increase in the observed density of variants, even resulting in higher θ W diversity than in nonbottlenecked populations. Increased diversity seems to be related to both a higher mutational input in those regions creating a large collection of low-frequency variants, a few of which increase in frequency during the bottleneck to the point they become detectable with our limited sample, and the reduced efficacy of purifying selection, which affects not only protein structure and function but also the regulation of gene expression. The results of this study alert to the possible reduction of fitness and adaptive potential associated with the genomic erosion in regulatory elements. Further, the detection of a gain of diversity in ultra-conserved elements can be used as a sensitive and easy-to-apply signature of genetic erosion in wild populations.