Natural selection on feralization genes contributed to the invasive spread of wild pigs throughout the United States

Author:

Barmentlo Niek W. G.12ORCID,Meirmans Patrick G.2ORCID,Stiver William H.3,Yarkovich Joseph G.3,McCann Blake E.4,Piaggio Antoinette J.5,Wright Dominic6ORCID,Smyser Timothy J.5ORCID,Bosse Mirte17ORCID

Affiliation:

1. Section Ecology & Evolution, Amsterdam Institute for Life and Environment (A‐LIFE) Vrije Universiteit Amsterdam Amsterdam The Netherlands

2. Institute for Biodiversity and Ecosystem Dynamics University of Amsterdam Amsterdam The Netherlands

3. Great Smoky Mountains National Park Gatlinburg Tennessee USA

4. Theodore Roosevelt National Park Medora North Dakota USA

5. USDA APHIS WS National Wildlife Research Center Fort Collins Colorado USA

6. Department of Physics, Chemistry and Biology Linköping University Linköping Sweden

7. Wageningen University & Research – Animal Breeding and Genomics Wageningen The Netherlands

Abstract

AbstractDespite a long presence in the contiguous United States (US), the distribution of invasive wild pigs (Sus scrofa × domesticus) has expanded rapidly since the 1980s, suggesting a more recent evolutionary shift towards greater invasiveness. Contemporary populations of wild pigs represent exoferal hybrid descendants of domestic pigs and European wild boar, with such hybridization expected to enrich genetic diversity and increase the adaptive potential of populations. Our objective was to characterize how genetic enrichment through hybridization increases the invasiveness of populations by identifying signals of selection and the ancestral origins of selected loci. Our study focused on invasive wild pigs within Great Smoky Mountains National Park, which represents a hybrid population descendent from the admixture of established populations of feral pigs and an introduction of European wild boar to North America. Accordingly, we genotyped 881 wild pigs with multiple high‐density single‐nucleotide polymorphism (SNP) arrays. We found 233 markers under putative selection spread over 79 regions across 16 out of 18 autosomes, which contained genes involved in traits affecting feralization. Among these, genes were found to be related to skull formation and neurogenesis, with two genes, TYRP1 and TYR, also encoding for crucial melanogenesis enzymes. The most common haplotypes associated with regions under selection for the Great Smoky Mountains population were also common among other populations throughout the region, indicating a key role of putatively selective variants in the fitness of invasive populations. Interestingly, many of these haplotypes were absent among European wild boar reference genotypes, indicating feralization through genetic adaptation.

Publisher

Wiley

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