Human impact on the recent population history of the elusive European wildcat inferred from whole genome data

Abstract

Background The extent and impact of evolutionary change occurring in natural populations in response to rapid anthropogenic impact is still poorly understood on the genome-wide level. Here, we explore the genetic structure, demographic history, population differentiation, and domestic introgression based on whole genome data of the endangered European wildcat in Germany, to assess potential genomic consequences of the species’ recent spread across human-dominated cultural landscapes. Results Reconstruction of demographic history and introgression rates based on 47 wildcat and 37 domestic cat genomes suggested late introgression between wild and domestic cat, coinciding with the introduction of domestic cat during the Roman period, but overall relatively low rates of hybridization and introgression from domestic cats. Main population divergence found between an eastern and central German wildcat clade was found to be of rather recent origin (200 y), and thus the likely consequence of anthropogenic persecution and resulting isolation in population refugia. We found similar effective population sizes and no substantial inbreeding across populations. Interestingly, highly differentiated genes between wild cat populations involved in the tryptophan-kynurenine-serotonin pathway were revealed, which plays a role in behavioral processes such as stress susceptibility and tolerance, suggesting that differential selection acted in the populations. Conclusions We found strong evidence for substantial recent anthropogenic impact on the genetic structure of European wildcats, including recent persecution-driven population divergence, as well as potential adaptation to human-dominate environments. In contrast, the relatively low levels of domestic introgression and inbreeding found in this study indicate a substantial level of “resistance” of this elusive species towards major anthropogenic impacts, such as the omnipresence of domestic cats as well as substantial habitat fragmentation. While those findings have strong implications for ongoing conservation strategies, we demand closer inspection of selective pressures acting on this and other wildlife species in anthropogenic environments.

Impact of feralisation on evolutionary trajectories in the genomes of feral cat island populations

“…Our results point to low levels of inbreeding in domestic cats, which challenges the general assumption that domesticated species show considerable inbreeding [37,38]. Also noticeable is the high inbreeding coe cient of wildcat in comparison to previous studies on European wildcats [39,40]. In addition, we observed a considerable frequency of short ROHs in wildcats indicating ancient inbreeding, which is consistent with the fact that over time long segments in the chromosomes will have a tendency to breakdown due to recombination [41].…”

“…In addition, we included 8 German wildcat individuals (Felis silvestris) in this study. We obtained fastq les for feral and wild cats from the ENA (European Nucleotide Archive) project PRJEB40421 [40]. In addition, we obtained 21 fastq les for 21 non-fancy shorthair breed domestic cat individuals (Additional le 1) from the ENA project PRJNA343389 (data as part of the 99 Lives Cat Genome Sequencing Initiative, 2016).…”

A common statement on anthropogenic hybridization of the European wildcat (Felis silvestris)

“…Domestic cats have been widespread in Europe at least since their introduction by the Romans (Faure and Kitchener, 2009;Krajcarz et al, 2020). There is still substantial genetic differentiation between domestic cats and European wildcats, suggesting the presence of reproductive barriers between the two species (Tiesmeyer et al, 2020;Nieto-Blaźquez et al, 2022). However, this assumption should not be used as proof of the harmlessness of long-term hybridization between both taxa.…”

Haplotype-resolved genome and population genomics of the threatened garden dormouse in Europe

“…While reduced-representation sequencing (RRS) methodologies continue to be the more cost-effective and efficient means of generating genome-wide single nucleotide polymorphism (SNP) datasets for large numbers of samples (Wright et al 2020; Peterson et al 2012), alignment of RRS reads to a high-quality reference genome improves both the precision of SNP calls and the quantity of SNPs recovered when compared to de novo read alignment without a genome assembly (Rochette et al 2019; Brandies et al 2019). Reference genomes are also useful for data of closely-related species, with cross-species alignment shown to be highly effective (Takach et al 2023; DeSaix et al 2019; Burri et al 2015; Nieto-Blázquez et al 2022). Given the value of reference genome assemblies for population and conservation genomic analyses, sequencing of reference genomes for wildlife groups should be a focus of ongoing conservation efforts.…”