Population genomic, olfactory, dietary, and gut microbiota analyses demonstrate the unique evolutionary trajectory of feral pigs

Domestication is an intriguing evolutionary process. Many domestic populations are subjected to strong human-mediated selection, and when some individuals return to the wild, they are again subjected to selective forces associated with new environments. Generally, these feral populations evolve into something different from their wild predecessors and their members typically possess a combination of both wild and human selected traits. Feralisation can manifest in different forms on a spectrum from a wild to a domestic phenotype. This depends on how the rewilded domesticated populations can readapt to natural environments based on how much potential and flexibility the ancestral genome retains after its domestication signature. Whether feralisation leads to the evolution of new traits that do not exist in the wild or to convergence with wild forms, however, remains unclear. To address this question, we performed population genomic, olfactory, dietary, and gut microbiota analyses on different populations of Sus scrofa (wild boar, hybrid, feral and several domestic pig breeds). Porcine single nucleotide polymorphisms (SNPs) analysis shows that the feral population represents a cluster distinctly separate from all others. Its members display signatures of past artificial selection, as demonstrated by values of F-ST in specific regions of the genome and bottleneck signature, such as the number and length of runs of homozygosity. Generalised F-ST values, reacquired olfactory abilities, diet, and gut microbiota variation show current responses to natural selection. Our results suggest that feral pigs are an independent evolutionary unit which can persist so long as levels of human intervention remain unchanged.Funding Agencies|Natural Environment Research CouncilUK Research & Innovation (UKRI)Natural Environment Research Council (NERC) [NE/S00078X/1]; European Research CouncilEuropean Research Council (ERC)European Commission [ERC-2013-StG-337574-UNDEAD, ERC-2019-StG-853272-PALAEOFARM]; Natural Environmental Research CouncilUK Research & Innovation (UKRI)Natural Environment Research Council (NERC) [NE/K005243/1, NE/K003259/1, NE/S007067/1]