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

Abstract

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 FST in specific regions of the genome and bottleneck signature, such as the number and length of runs of homozygosity. Generalised FST 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.

Resilience to Historical Human Manipulations in the Genomic Variation of Italian Wild Boar Populations

“…This was attributed to a likely shared ancestry, but also at least in part to a recent genetic introgression from mainland populations, due to translocations for hunting purposes. Our results are also coherent with recent findings described by Petrelli et al (2022) who investigated population genomic and selection patterns in WB living on the island.…”

“…Populations of north-eastern Italy, not included in the present study, showed a different composition from those living in central Italy, revealing higher similarities with eastern European populations (Scandura et al, 2008). Similarly, in southern Italy, a highly detectable rate of introgression from DPs was found in WB living north to WCal population (Cilento area), where a high morphological variation was also described (Fulgione et al, 2016;Petrelli et al, 2022). Unfortunately, no genetic nor phenotypical information is instead available for reintroduced WB that are spreading across Sicily, as well as for other areas of more recent recolonization.…”

“…Using the same set of markers, no hybrid was indeed detected by Iacolina et al (2018) in a subsample of 19 Italian WB (from Tuscany) among those considered in the present study, whereas 3 hybrids out of 25 individuals (12%) were detected in a random sample of Sardinian WB. Conversely, using a multiple-marker approach (coat color, MC1R, SNPs), (Petrelli et al, 2022) found a complete overlap among the genomes of Southern Italian known hybrids with those of the sympatric WB, likely as a result of deep introgression into the latter.…”

The Boar War: Five Hot Factors Unleashing Boar Expansion and Related Emergency

“…This selective breeding and crossbreeding for specific traits resulted in a huge diversity of wild, domestic and feral forms, manifesting a variety of combinations of both naturally and artificially selected phenotypic patterns [24][25][26][27][28]. The relationship between these different Sus scrofa forms living sympatrically in several regions around the world is a tangled one, and many studies have explored the related evolutionary and management implications [29][30][31][32][33][34][35].…”

“…Highly plastic ecological behaviour allows wild boar to inhabit a wide range of habitat types (e.g., Mediterranean scrubland, semi-desert and tropical rain forests, grasslands, and anthropogenic habitats) [50][51][52][53]. Furthermore, the species is a generalist omnivore, shaping its diet on the local availability of plants and animals, which it feeds on opportunistically [34,38,54,55]. Its invasiveness depends on the niche permissiveness in terms of limiting factors, such as the presence of road networks (linked to car collision events) or natural predators [56,57].…”