History, demography and genetic status of Balkan and Caucasian Lynx lynx (Linnaeus, 1758) populations revealed by genome‐wide variation

Abstract

Aim Genome‐wide genetic data can provide key input for both taxonomy and conservation, but its use in this context remains limited. In this study, we performed the first genome‐wide assessment of genetic variation in two populations of the Eurasian lynx, the Balkan population, the most threatened, and the Caucasian population, a possible glacial refugium, with the aim to place them in the context of the species, investigate their demographic history and evaluate their genetic status. Location The Balkans and the Caucasus. Methods We obtained whole genome resequencing data from seven Balkan and 12 Caucasian lynx, and analysed them along with novel and existing data from other populations. Based on a total 105 whole genome and 114 mitogenome sequences, we reconstructed phylogenetic and historical relationships, ancient and recent demography, and patterns of genetic diversity and inbreeding. Results Both the Balkan and the Caucasian lynx appear as distinct mitochondrial lineages that diverged from the rest of the Eurasian lynx lineages ca. 92.6 kya, and from each other ca. 46.4 kya. Autosomal data suggest, however, that the Balkan lynx is closely related with the Carpathian population, and revealing alarmingly low genetic diversity and high inbreeding. In contrast, the Caucasian lynx shows a longer history of relative isolation from the rest of lynx populations and high genetic diversity, consistent with its large long‐term effective population size. Main conclusions The taxonomic status of the Balkan lynx remains unresolved due to the evidence of long‐term isolation in the mitogenome, contrasting with extensive autosomal admixture and intense recent genetic drift in the nuclear genome. Our results alert on genetic risks and call for the consideration of genetic rescue from closely related Carpathian lynxes. In contrast, substantial mitogenomic and autosomal divergence with no signs of genetic drift supports the identification of the Caucasian lynx as a separate subspecies with good genetic health.

Diverging ecological traits between the Balkan lynx and neighbouring populations as a basis for planning its genetic rescue

“…Based on available knowledge provided by this study and previous results of genetic analyses, we suggest reinforcement with the use of only (or predominantly) male Carpathian lynx, which would mimic the natural male-biased gene flow, as was apparently repeated through sex-biased dispersal from the Carpathian population in the past (Bazzicalupo et al 2022). This would provide ecologically similar individuals to the existing Balkan population and at the same time enable it to retain the unique mitogenome of this population.…”

“…In this study, we assessed which of the two genetically and geographically closest lynx subspecies to the critically endangered Balkan lynx (Mengüllüoglu et al 2021a;Bazzicalupo et al 2022) is more suitable for population rescue from the ecological standpoint. We analysed prey preference, prey availability and habitat preference to infer whether the Carpathian or the Caucasian subspecies better suits the environment in south-western Balkans.…”

“…Mitochondrial DNA has been widely used to assess the genetic relatedness among the populations from a phylogenetic perspective (Moritz 1994). Recent studies have suggested that Balkan lynx is mitogenomically closest to the lynx populations in Anatolia (see Clade B, Lineage B2 in Mengüllüoglu et al 2021a), but closest to Carpathian lynx populations regarding autosomal genomes, likely due to male-biased dispersal and introgression (Bazzicalupo et al 2022). Given the distinct haplotypes found in the Balkan population (Gugolz et al 2008;Lucena-Perez et al 2020), it is important to consider the genetic uniqueness of the mitogenomes in this population and the implications of potential translocations from other populations, given that the Balkan lynx is recognized as both an evolutionary significant unit (Melovski et al 2013) and its own subspecies (Kitchener et al 2017).…”

“…The evolutionary history of the Balkan lynx lineage stretches for more than 50 kya years (Mengüllüoğlu et al 2021a;Bazzicalupo et al 2022) and, during this time, its population has always been relatively small compared to other populations in Asia, or Europe (Bazzicalupo et al 2022). Given the long-term process of inbreeding, it is likely that reproductive success is already affected by inbreeding depression.…”

“…Similar issues affected the reintroduced Dinaric lynx population, but negative trends were reversed with the start of the translocation of Eurasian lynx from the Carpathians to Slovenia and Croatia (Krofel et al 2021). The intense genetic drift in the bottlenecked Balkan lynx contributes to further genetic erosion, whereas observed low genetic diversity and extremely small effective population size call for immediate genetic rescue actions (Bazzicalupo et al 2022). Provided that the closest neighbours of the Balkan lynx population are Carpathian L. l. carpathicus (which were also reintroduced to the Dinaric Mountains) and Caucasian lynx L. l. dinniki, it is logical to seek potential alternatives for genetic rescue from these two subspecies (Mengüllüoğlu et al 2021a).…”