Natural Selection on Feralization Genes Contributed to the Invasive Spread of Wild Pigs Throughout the United States

Authors

Niek W. G. Barmentlo, Vrije Universiteit AmsterdamFollow
Patrick G. Meirmans, University of Amsterdam
William H. Stiver, United States National Park Service, Great Smoky Mountains National Park
Joseph G. Yarkovich, United States National Park Service, Great Smoky Mountains National Park
Blake E. McCann, Theodore Roosevelt National ParkFollow
Antoinette J. Piaggio, United States Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, Wildlife Genetics Lab, Fort Collins, ColoradoFollow
Dominic Wright, Linköping University
Timothy J. Smyser, United States Department of Agriculture, Animal and Plant Health Inspection Service, Wildlife Services, National Wildlife Research Center, Fort Collins, ColoradoFollow
Mirte Bosse, Vrije Universiteit AmsterdamFollow

ORCID IDs

Barmentlo https://orcid.org/0000-0001-5256-3591

Meirmans https://orcid.org/0000-0002-6395-8107

Wright https://orcid.org/0000-0003-2329-2635

Smyser https://orcid.org/0000-0003-4542-3077

Bosse https://orcid.org/0000-0003-2433-2483

Document Type

Article

Date of this Version

2024

Citation

Molecular Ecology (2024) 33: e17383

doi:10.1111/mec.17383

Handling editor: David Coltman

Code: https://github.com/Niekbarmentlo/-Feral-swine-selective-sweep-pipeline

Genotyping data: https://doi.org/10.48338/VU01-Q7LFEL

Comments

United States government work

Abstract

Despite 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.