Human‐modified canids in human‐modified landscapes: The evolutionary consequences of hybridization for grey wolves and free‐ranging domestic dogs

Abstract

Introgressive hybridization between domestic animals and their wild relatives is an indirect form of human-induced evolution, altering gene pools and phenotypic traits of wild and domestic populations. Although this process is well documented in many taxa, its evolutionary consequences are poorly understood. In this study, we assess introgression patterns in admixed populations of Eurasian wolves and free-ranging domestic dogs (FRDs), identifying chromosomal regions with significantly overrepresented hybrid ancestry and assessing whether genes located within these regions show signatures of selection. Although the dog admixture proportion in West Eurasian wolves (2.7%) was greater than the wolf admixture proportion in FRDs (0.75%), the number and average length of chromosomal blocks showing significant overrepresentation of hybrid ancestry were smaller in wolves than FRDs. In wolves, 6% of genes located within these blocks showed signatures of positive selection compared to 23% in FRDs. We found that introgression from wolves may provide a considerable adaptive advantage to FRDs, counterbalancing some of the negative effects of domestication, which can include reduced genetic diversity and excessive tameness. In wolves, introgression from FRDs is mostly driven by drift, with a small number of positively selected genes associated with brain function and behaviour. The predominance of drift may be the consequence of small effective size of wolf populations, which reduces efficiency of selection for weakly advantageous or against weakly disadvantageous introgressed variants. Small wolf population sizes result largely from human-induced habitat loss and hunting, thus linking introgression rates to anthropogenic processes.Our results imply that maintenance of large population sizes should be an important element of wolf management strategies aimed at reducing introgression rates of dogderived variants.

Consequences of Hybridization in Mammals: A Systematic Review

“…Accordingly, reproductive isolation between domesticated mammals and their wild ancestors is frequently incomplete due to their recent divergence. For example, hybridization between wolves and domestic dogs results in introgression of hybridization-derived variants into gene pools of both canids [ 139 ]. In wolves, introgression of dog variants is mostly driven by drift, with only a small number of genes experiencing negative or positive selection due to this process [ 139 ].…”

“…For example, hybridization between wolves and domestic dogs results in introgression of hybridization-derived variants into gene pools of both canids [ 139 ]. In wolves, introgression of dog variants is mostly driven by drift, with only a small number of genes experiencing negative or positive selection due to this process [ 139 ]. In free-ranging domestic dogs, the observed proportion of candidate genes under positive selection was larger than those under negative selection, suggesting that introgression from wolves may provide dogs with an adaptive advantage [ 139 ].…”

Human‐induced evolution: Signatures, processes and mechanisms underneath anthropogenic footprints on natural systems

“…Capturing signatures of hybridization events is critical to maintain the integrity of wild specimens in the ever‐expanding era of the Anthropocene (Ottenburghs, 2021 ). In this context, genome scans are useful to reveal signatures of human‐driven hybridization as those can identify introgression patterns among admixed populations of domesticated and wild species (Pilot et al, 2021 ). Introgression from free‐ranging domestic dogs into populations of Eurasian wolves for example has shown that the transfer of genetic material might reduce Eurasian's wolf viability by genetic swamping.…”

“…Introgression from free‐ranging domestic dogs into populations of Eurasian wolves for example has shown that the transfer of genetic material might reduce Eurasian's wolf viability by genetic swamping. This effect further impact genetic diversity that is already negatively affected by genetic drift associated with small population sizes resulting from hunting and habitat loss (Pilot et al, 2021 ). The study provides new perspective to address conservation efforts of wolf's genetic integrity; namely, it advocates the maintenance of large population sizes as an important measure of management strategies in order to avoid swamping by dog‐derived variants in wolf's genome (Pilot et al, 2021 ).…”

“…This effect further impact genetic diversity that is already negatively affected by genetic drift associated with small population sizes resulting from hunting and habitat loss (Pilot et al, 2021 ). The study provides new perspective to address conservation efforts of wolf's genetic integrity; namely, it advocates the maintenance of large population sizes as an important measure of management strategies in order to avoid swamping by dog‐derived variants in wolf's genome (Pilot et al, 2021 ). Because of the longstanding contact and dependence on human activities, farmed animals might pose a similar risk to natural populations upon reproduction with wild animals (Le Luyer et al, 2017 ; Leitwein et al, 2021 ).…”