Genomic approaches to identify hybrids and estimate admixture times in European wildcat populations

Abstract

The survival of indigenous European wildcat ( Felis silvestris silvestris ) populations can be locally threatened by introgressive hybridization with free-ranging domestic cats. Identifying pure wildcats and investigating the ancestry of admixed individuals becomes thus a conservation priority. We analyzed 63k cat Single Nucleotide Polymorphisms (SNPs) with multivariate, Bayesian and gene-search tools to better evaluate admixture levels between domestic and wild cats collected in Europe, timing and ancestry proportions of their hybrids and backcrosses, and track the origin (wild or domestic) of the genomic blocks carried by admixed cats, also looking for possible deviations from neutrality in their inheritance patterns. Small domestic ancestry blocks were detected in the genomes of most admixed cats, which likely originated from hybridization events occurring from 6 to 22 generations in the past. We identified about 1,900 outlier coding genes with excess of wild or domestic ancestry compared to random expectations in the admixed individuals. More than 600 outlier genes were significantly enriched for Gene Ontology (GO) categories mainly related to social behavior, functional and metabolic adaptive processes (wild-like genes), involved in cognition and neural crest development (domestic-like genes), or associated with immune system functions and lipid metabolism (parental-like genes). These kinds of genomic ancestry analyses could be reliably applied to unravel the admixture dynamics in European wildcats, as well as in other hybridizing populations, in order to design more efficient conservation plans.

Hybridization between Felis silvestris silvestris and Felis silvestris catus in two contrasted environments in France

“…Despite it has been often reported a nonsignificant difference in body weight between domestic and wildcats (Beugin et al, ), domestic male cats might not be able to gain and maintain territories in a wild environment where wildcats are present as competitors (Sunquist & Sunquist, ). This is probably due to the fact that domestication has influenced some characteristics of the domestic cat (Cameron‐Beaumont, Lowe, & Bradshaw, ; Driscoll, Macdonald, & O'Brien, ; Mattucci et al, ; Wilkins, Wrangham, & Fitch, ), first of all the dependence on food distributed by humans, that has made it less competitive than the ancestor and other wild related subspecies. A low abundance of rodents and/or competition with other carnivore species (Gil‐Sànchez et al, ) such as the red fox ( Vulpes vulpes )—of which populations are increasing in several European countries (Chautan, Pontier, & Artois, ; Goszczyński, Misiorowska, & Juszko, )—may make domestic cats even more heavily dependent on food distributed by humans.…”

“…They provided further information about the relationship between environmental conditions and hybridization risks in French wildcat populations. Further genetic analyses—combining microsatellite and SNP markers, which are more powerful in detecting patterns and histories of admixtures (Mattucci et al, ; Nussberger, Greminger, Grossen, Keller, & Wandeler, ), as well as mitochondrial and Y chromosome markers for evaluating possible asymmetry in hybridization (hybridization between female wildcats and male domestic cats or vice versa; Hertwig et al, ; Rhymer & Simberloff, )—should lead to a deeper insight into the hybridization and long‐term patterns of French wildcat populations.…”

“…Despite it has been often reported a nonsignificant difference in body weight between domestic and wildcats (Beugin et al, 2016), domestic male cats might not be able to gain and maintain territories in a wild environment where wildcats are present as competitors (Sunquist & Sunquist, 2002). This is probably due to the fact that domestication has influenced some characteristics of the domestic cat (Cameron- Beaumont, Lowe, & Bradshaw, 2002;Driscoll, Macdonald, & O'Brien, 2009;Mattucci et al, 2019;Wilkins, Wrangham, & Fitch, 2014 In the Pyrenees, we did not detect a similar sex-biased spatial organization in the wildcat population. However, the opportunistic collection of feces may not provide enough information compared to trapping, to assess the spatial organization pattern of this wildcat population.…”

“…Direction of the gene flow also varied, some studies reporting a gene flow from domestic cats to wildcats (Nussberger, Wandeler, Weber, & Keller, 2014;Oliveira, Godinho, Randi, Ferrand, & Alves, 2007) while others showed the opposite with a detected flow from wildcats to domestic cats (Hertwig et al, 2009). The causes of such a high degree of heterogeneity in hybridization modalities and subsequent introgression are not known, but different environmental conditions (e.g., habitat fragmentation and urban pressure), ecological barriers (Gil-Sànchez, Jaramillo, & Barea-Azcòn, 2015), relative numbers of wild and domestic cats, or population histories (Crispo, Moore, Lee-Yaw, Gray, & Haller, 2011;Mattucci et al, 2019;Pierpaoli et al, 2003) could all play a role. Local investigations of threats are thus required to identify conservation problems and design the best options for wildcat conservation (Lozano & Malo, 2012;Mattucci et al, 2019).…”

Range-wide patterns of human-mediated hybridisation in European wildcats

“…High-throughput analyses of single nucleotide polymorphism (SNP) arrays substantially improved the in-depth assessment of hybridisation (e.g., vonHoldt et al 2013;Goedbloed et al 2013;Nussberger et al 2013). SNPs have been shown to be highly accurate and sensitive in identifying hybrid individuals between wildcats and domestic cats, irrespective of origin and available reference database (Oliveira et al 2015;Steyer et al 2018;Mattucci et al 2019).…”