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Mixed ancestry from wild and domestic lineages contributes to the rapid expansion of invasive feral swine

Citation

Smyser, Timothy et al. (2020), Mixed ancestry from wild and domestic lineages contributes to the rapid expansion of invasive feral swine, Dryad, Dataset, https://doi.org/10.5061/dryad.jsxksn05z

Abstract

Invasive alien species are a significant threat to both economic and ecological systems.  Identifying processes that give rise to invasive populations is essential for implementing effective control strategies.  We conducted an ancestry analysis of invasive feral swine (Sus scrofa, Linnaeus, 1758), a highly destructive ungulate that is widely distributed throughout the contiguous United States, to describe introduction pathways, sources of newly-emergent populations, and processes contributing to an ongoing invasion.  Comparisons of high-density single nucleotide polymorphism genotypes for 6,566 invasive feral swine to a comprehensive reference set of S. scrofa revealed that the vast majority of feral swine were of mixed ancestry, with dominant genetic associations to Western heritage breeds of domestic pig and European populations of wild boar.  Further, the rapid expansion of invasive feral swine over the past 30 years was attributable to secondary introductions from established populations of admixed ancestry as opposed to direct introductions of domestic breeds or wild boar.  Spatially-widespread genetic associations of invasive feral swine to European wild boar deviated strongly from historical S. scrofa introduction pressure, which was largely restricted to domestic pigs with infrequent, localized wild boar releases.  The deviation between historical introduction pressure and contemporary genetic ancestry suggests wild boar-hybridization may contribute to differential fitness in the environment and heightened invasive potential for individuals of admixed domestic pig-wild boar ancestry.

Methods

Feral swine samples were collected throughout the entirety of the invaded range within the contiguous US as an extension of damage mitigation efforts led by the United States Department of Agriculture (USDA) between 2001 and 2017.  Invasive feral swine were genotyped using Illumina BeadChip microarrays (San Diego, California) developed for porcine (PorcineSNP60 v2, n = 168; Genomic Profiler for Porcine HD, n = 6,398, exclusively licensed to GeneSeek, a Neogen Corporation, Lincoln, Nebraska; Ramos et al., 2009).  Combining genotypes produced across multiple Illumina BeadChips microarrays yielded 29,375 common autosomal loci, with all available loci retained for subsequent analyses.  Based upon the available loci, we removed samples with call rates <95%, thus retaining 6,566 invasive feral swine for analysis.

We assembled our reference set by compiling domestic pig and native wild boar HD SNP genotypes from previously published datasets (n = 2,450; Alexandri et al., 2017; Burgos-Paz et al., 2013; Goedbloed et al., 2013a; Iacolina et al., 2016; Roberts & Lamberson, 2015; Yang et al., 2017), which we augmented with novel genotypes produced by our research group (n = 566; produced with extraction methods described above and genotyped with the Genomic Profiler for Porcine HD (GeneSeek)).  In order to align with feral swine genotypes, we restricted our reference set to datasets similarly produced with either the PorcineSNP60 (v1 and v2; Illumina) or Genomic Profiler for Porcine HD (GeneSeek) BeadChip microarrays (Ramos et al., 2009). 

Usage Notes

We present genotype files for 6,566 invasive feral swine and 2,516 corresponding Sus scrofa reference samples in the *.bed/*.bim/*.fam (binary PED file) file format.  All genotypes were produced with Illumina BeadChip microarrays (San Diego, California) developed for porcine (PorcineSNP60 v1 and 2 or Genomic Profiler for Porcine HD, exclusively licensed to GeneSeek, a Neogen Corporation, Lincoln, Nebraska).  Many of the reference genotypes have been published previously (full citations below with abbreviated citations listed in metadata).  Metadata for both invasive feral swine and reference samples are presented and correspond to more thorough appendices published online that accompany the manuscript “Mixed ancestry from wild and domestic lineages contributes to the rapid expansion of invasive feral swine.”  R-code is presented that will allow users to recreate ancestry analyses with minimal edits required by the user (identify local paths) to execute the code.

Citations:

Alexandri, P., Megens, H.-J., Crooijmans, R. P. M. A., Groenen, M. A. M., Goedbloed, D. J., Herrero-Medrano, J. M., . . . Triantafyllidis, A. (2017). Distinguishing migration events of different timing for wild boar in the Balkans. Journal of Biogeography, 44, 259-270. doi:10.1111/jbi.12861

Burgos-Paz, W., Souza, C. A., Megens, H. J., Ramayo-Caldas, Y., Melo, M., Lemus-Flores, C., . . . Perez-Enciso, M. (2013). Porcine colonization of the Americas: a 60k SNP story. Heredity, 110, 321-330. doi:10.1038/hdy.2012.109

Goedbloed, D. J., Megens, H. J., van Hooft, P., Herrero-Medrano, J. M., Lutz, W., Alexandri, P., . . . Prins, H. H. T. (2013). Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations. Molecular Ecology, 22, 856-866. doi:10.1111/j.1365-294X.2012.05670.x

Iacolina, L., Scandura, M., Goedbloed, D. J., Alexandri, P., Crooijmans, R. P. M. A., Larson, G., . . . Megens, H. J. (2016). Genomic diversity and differentiation of a managed island wild boar population. Heredity, 116, 60-67. doi:10.1038/hdy.2015.70

Roberts, K. S., & Lamberson, W. R. (2015). Relationships among and variation within rare breeds of swine. Journal of Animal Science, 93, 3810-3813. doi:10.2527/jas.2015-9001

Yang, B., Cui, L., Perez-Enciso, M., Traspov, A., Crooijmans, R. P. M. A., Zinovieva, N., . . . Megens, H.-J. (2017). Genome-wide SNP data unveils the globalization of domesticated pigs. Genetics Selection Evolution, 49, 71. doi:10.1186/s12711-017-0345-y

 

Funding

Research was supported by the National Feral Swine Damage Management Program, the National Wildlife Disease Program, and the National Wildlife Research Center.