Extreme genomic erosion after recurrent demographic bottlenecks in the highly endangered Iberian lynx

Abstract

Background: Genomic studies of endangered species provide insights into their evolution and demographic history, reveal patterns of genomic erosion that might limit their viability, and offer tools for their effective conservation. The Iberian lynx (Lynx pardinus) is the most endangered felid and a unique example of a species on the brink of extinction.

Results: We generate the first annotated draft of the Iberian lynx genome and carry out genome-based analyses of lynx demography, evolution, and population genetics. We identify a series of severe population bottlenecks in the history of the Iberian lynx that predate its known demographic decline during the 20th century and have greatly impacted its genome evolution. We observe drastically reduced rates of weak-to-strong substitutions associated with GC-biased gene conversion and increased rates of fixation of transposable elements. We also find multiple signatures of genetic erosion in the two remnant Iberian lynx populations, including a high frequency of potentially deleterious variants and substitutions, as well as the lowest genome-wide genetic diversity reported so far in any species.

Conclusions: The genomic features observed in the Iberian lynx genome may hamper short- and long-term viability through reduced fitness and adaptive potential. The knowledge and resources developed in this study will boost the research on felid evolution and conservation genomics and will benefit the ongoing conservation and management of this emblematic species.

Keywords: Conservation genomics; Genetic diversity; Genetic drift; Inbreeding; Lynx.

Fig. 1

Evolutionary and demographic history of Iberian and Eurasian lynx. a Eurasian and Iberian lynx divergence adjusted to a model of divergence with gene flow. Results suggest a relatively recent divergence of the two lynx species followed by a period of gene flow that lasted until recently (circa 2473 years ago). b Effective population size through time estimated for each of the 11 Iberian lynx and a single Eurasian individual using PSMC. Demographic histories are similar for the ten Iberian lynx and slightly different for the Eurasian lynx, although both species follow largely parallel fluctuations of population size probably related to glacial cycles; glacial periods are shaded in blue with glacial maxima in darker tone. c Based on the allele frequency spectrum, ∂a∂i infers a model with two successive abrupt bottlenecks, one around 47 kya, coincident with the last important decline observed in PSMC output, and a second one at 315 years ago, both reducing to approximately one-tenth the previous population size. The most recent documented bottleneck occurring during the 20th century is not recovered by these methods

Fig. 2

Comparison of transposable element dynamics. a Absolute number of species-specific SINE, LINE, and ERV insertions estimated for lynx, cat, and tiger. For SINEs and LINEs, the number of TE insertions was calculated based on pairwise comparisons between domestic cat and lynx and between domestic cat and tiger. The numbers shown represent the accumulation of insertions in each species since the last common ancestor of lynx, cat, and tiger (Additional file 1: Section 15). The number of TE insertions within genes and the percentage of insertions in sense with respect to the gene are shown on top of each bar. LTR long terminal repeat. b Phylogenetic tree depicts the number of LINE insertions mapped onto each branch (in blue above branch) and the number of insertions that are in sense (+) or antisense (-) orientation with respect to the genes (in green below branch). Relative proportions are shown as pie charts, with those significantly departing from the average genome-background frequency of 37% (Lynx) indicated by an asterisk. Branch lengths were set manually to reflect the number of LINE insertions on each branch

Fig. 3

Patterns of genome evolution. a Magnitude of W → S bias within faster evolving regions (FRs) identified in pairwise comparisons between cat and the lynx ancestor and between Iberian and Eurasian lynx. b Heterozygosity in regions defined as FRs in Eurasian or Iberian lynx. Iberian lynx values are reported for the whole species and for the reference individual. Whereas FRs in cat and the lynx ancestor are associated with higher W → S biases, FRs in both lynx species are associated with reduced heterozygosity and fixation of ancestral polymorphisms. c dN/dS ratios estimated for different mammalian lineages. Increased ratios in lynx indicate the relaxation of purifying selection following the divergence of Iberian and Eurasian lynx

Fig. 4

Patterns of genomic variation in 11 Iberian and one Eurasian lynx. a Average heterozygosity in non-overlapping syntenic 100-kb windows in one Iberian lynx from Doñana, one from Andújar (Sierra Morena) and one Eurasian lynx; chromosome A1 is shown as an illustrative example. Long runs of homozygosity are evident in the Iberian individuals. b Length of the genome covered by runs of homozygosity of different sizes in each Iberian lynx individual. Both large and medium size ROH are more abundant in Doñana, indicating higher inbreeding and a longer recent history of low effective size. c Linkage disequilibrium (LD) decay in Iberian lynx populations. Doñana has remained small (50–80 lynxes) and isolated at least since the 1950s, whereas Andújar was part of a large and well connected population until the 1960s; then it became progressively contracted and isolated and reached its lowest size at around 60 animals by 2002. d Heterozygous SNP rates in genome-sequenced mammals. Modified from Cho et al. [43] and updated with the addition of data for Altai Neanderthal [114], cheetah and feral domestic cat [115], Yangtze river dolphin [116], gibbon [117], minke whale [118], Eastern mountain gorilla [46], dromedary and Bactrian camel [119], Wrangle Is. mammoth [120], and blind mole rat [121]. The Iberian lynx genome- and species-wide SNP rate and heterozygosity are the lowest reported to date