Introgressive hybridisation between domestic pigs (Sus scrofa domesticus) and endemic Corsican wild boars (S. s. meridionalis): effects of human-mediated interventions

François Casabianca,Lorraine Richart,Oscar Maestrini,Frank Drygala,Michel Mittelbronn,Alain C. Frantz,Hannah Weigand,Chantal Schwartz,Anna Schleimer

doi:10.1038/s41437-022-00517-1

Abstract

Owing to the intensified domestication process with artificial trait selection, introgressive hybridisation between domestic and wild species poses a management problem. Traditional free-range livestock husbandry, as practiced in Corsica and Sardinia, is known to facilitate hybridisation between wild boars and domestic pigs (Sus scrofa). Here, we assessed the genetic distinctness and genome-wide domestic pig ancestry levels of the Corsican wild boar subspecies S. s. meridionalis, with reference to its Sardinian conspecifics, employing a genome-wide single nucleotide polymorphism (SNP) assay and mitochondrial control region (mtCR) haplotypes. We also assessed the reliance of morphological criteria and the melanocortin-1 receptor (MC1R) coat colour gene to identify individuals with domestic introgression. While Corsican wild boars showed closest affinity to Sardinian and Italian wild boars compared to other European populations based on principal component analysis, the observation of previously undescribed mtCR haplotypes and high levels of nuclear divergence (Weir’s θ > 0.14) highlighted the genetic distinctness of Corsican S. s. meridionalis. Across three complementary analyses of mixed ancestry (i.e., STRUCTURE, PCADMIX, and ELAI), proportions of domestic pig ancestry were estimated at 9.5% in Corsican wild boars, which was significantly higher than in wild boars in Sardinia, where free-range pig keeping was banned in 2012. Comparison of morphologically pure- and hybrid-looking Corsican wild boars suggested a weak correlation between morphological criteria and genome-wide domestic pig ancestry. The study highlights the usefulness of molecular markers to assess the direct impacts of management practices on gene flow between domestic and wild species.

Highlights

We focus on introgressive hybridisation between domestic pigs and wild boars in Corsica and Sardinia, which have recently seen the introduction of differing management approaches
Mitochondrial control region haplotypes Sequence analysis of a 472-bp-long-fragment of the mitochondrial control region (mtCR) from 81 Corsican suids (38 wild boars, 18 hybrid boars, 25 domestic pigs) revealed a total of 11 different haplotypes, with a total of 25 variable sites consisting of 20 transitions, one transversion and four insertions/deletions (Table 1)
One domestic pig carried a haplotype that had only been recorded in domestic pigs and a further three pigs carried a haplotype previously observed in a Croatian wild boar (Table 1)

Summary

Introduction

Domestication exerts a strong selective pressure on species through genetic processes, such as inbreeding, genetic drift, natural selection to captivity, and artificial selection of desirable traits (Mignon-Grasteau et al 2005; Price 1984). Over the past 10,000 years, human interventions have led to domesticated species that are morphologically, behaviourally, and genetically distinct from their wild/ancestral conspecifics (Mignon-Grasteau et al 2005; Zeder 2012). The evolutionary histories of many domesticated species show clear signatures of past introgressive hybridisation, i.e. the exchange of genetic material when fertile hybrids backcross with parental species. The effects of introgressive hybridisation on the morphology, behaviour, and adaptive potential of the introgressed species are largely context-dependent. Lies one of the main concerns about hybridisation between domestic and wild species; introgression dynamics are largely unpredictable and alterations to the local gene pool could induce a loss of adaptation (Bourret et al 2011), increased invasiveness and population sizes

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