Differentiation of the domestic pig and wild boar using genotyping-by-sequencing

Domestic pigs and wild boars have undergone frequent interspecies crossbreeding; therefore, the presence of hybrids makes it challenging to find genetic markers that distinguish both subspecies. The aim of this research is to identify the DNA regions that underwent strong selection during the domestication of the pig and to give an insight into the genetic diversity of the Polish wild boar and domestic pigs by implementing the genotyping-by-sequencing (GBS) technique. We studied two groups of animals: one consisted of domestic pigs (Landrace, Large White, Duroc, Puławska and Pietrain), while the second group included wild boars from Poland. The filtered single nucleotide polymorphisms (SNP) panel used in this study included 7,298 markers that were spread across 18 porcine autosomes and unmapped contigs. The maximum-likelihood phylogenetic trees and multidimensional scaling (MDS) clearly separated the populations of pigs from the wild boars. We also detected genome regions that demonstrated the most significant genetic differences between the domestic pigs and wild boars. These regions were distributed on eight different autosomes and overlapped with 48 different pig RefSeq genes. The KEGG pathway, Reactome and GO terms were further used to assign a functional significance to the identified genes that were associated with inter alia muscle development (MYOG, MEOX2), pre-weaning mortality stress (MYO7A) and sensory perception (TAS1R3).

[1]  B. Servin,et al.  Genome‐wide analysis of hybridization in wild boar populations reveals adaptive introgression from domestic pig , 2022, Evolutionary applications.

[2]  M. Groenen,et al.  A natural knockout of the MYO7A gene leads to pre‐weaning mortality in pigs , 2021, Animal genetics.

[3]  A. Radko,et al.  Microsatellite DNA Analysis for Diversity Study, Individual Identification and Parentage Control in Pig Breeds in Poland , 2021, Genes.

[4]  M. Cichna‐Markl,et al.  Applicability of a duplex and four singleplex real-time PCR assays for the qualitative and quantitative determination of wild boar and domestic pig meat in processed food products , 2020, Scientific Reports.

[5]  E. Barta,et al.  Development of Wild Boar Species-Specific DNA Markers for a Potential Quality Control and Traceability Method in Meat Products , 2020, Food Analytical Methods.

[6]  F. Tancredi,et al.  Matching STR and SNP genotyping to discriminate between wild boar, domestic pigs and their recent hybrids for forensic purposes , 2020, Scientific Reports.

[7]  R. Brauning,et al.  GBS Data Identify Pigmentation-Specific Genes of Potential Role in Skin-Photosensitization in Two Tunisian Sheep Breeds , 2019, Animals : an open access journal from MDPI.

[8]  M. Cichna‐Markl,et al.  Differentiation between wild boar and domestic pig in food by targeting two gene loci by real-time PCR , 2019, Scientific Reports.

[9]  H. Megens,et al.  Hotspots of recent hybridization between pigs and wild boars in Europe , 2018, Scientific Reports.

[10]  David Haussler,et al.  The UCSC Genome Browser database: 2019 update , 2018, Nucleic Acids Res..

[11]  Sudhir Kumar,et al.  MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. , 2018, Molecular biology and evolution.

[12]  Xuewei Li,et al.  Detection of Selection Signatures in Chinese Landrace and Yorkshire Pigs Based on Genotyping-by-Sequencing Data , 2018, Front. Genet..

[13]  T. Szmatoła,et al.  Genotyping-by-sequencing performance in selected livestock species. , 2018, Genomics.

[14]  P. M. Galetti,et al.  Genetic Pattern and Demographic History of Salminus brasiliensis: Population Expansion in the Pantanal Region during the Pleistocene , 2018, Front. Genet..

[15]  R. Kuehn,et al.  Substantial hybridisation between wild boars (Sus scrofa scrofa) and East Balkan pigs (Sus scrofa f. domestica) in natural environment as a result of semi-wild rearing in Bulgaria , 2017 .

[16]  Deuk Hwan Lee,et al.  Predictive performance of genomic selection methods for carcass traits in Hanwoo beef cattle: impacts of the genetic architecture , 2017, Genetics Selection Evolution.

[17]  K. Rębała,et al.  STR Profiling for Discrimination between Wild and Domestic Swine Specimens and between Main Breeds of Domestic Pigs Reared in Belarus , 2016, PloS one.

[18]  M. Jakobsson,et al.  Clumpak: a program for identifying clustering modes and packaging population structure inferences across K , 2015, Molecular ecology resources.

[19]  Rudiger Brauning,et al.  Construction of relatedness matrices using genotyping-by-sequencing data , 2015, BMC Genomics.

[20]  M. Groenen,et al.  Genomic diversity and differentiation of a managed island wild boar population , 2015, Heredity.

[21]  Yeisoo Yu,et al.  Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing , 2015, BMC Genomics.

[22]  L. Fontanesi,et al.  Differentiation of meat from European wild boars and domestic pigs using polymorphisms in the MC1R and NR6A1 genes. , 2014, Meat science.

[23]  K. Arman,et al.  A highly sensitive and specific tetraplex PCR assay for soybean, poultry, horse and pork species identification in sausages: development and validation. , 2014, Meat science.

[24]  Robert J. Elshire,et al.  TASSEL-GBS: A High Capacity Genotyping by Sequencing Analysis Pipeline , 2014, PloS one.

[25]  A. Piestrzynska-Kajtoch,et al.  The species identification of bovine, porcine, ovine and chicken components in animal meals, feeds and their ingredients, based on COX I analysis and ribosomal DNA sequences , 2013 .

[26]  E. Skrzypczak,et al.  Variability in the melanocortin 1 receptor (MC1R) gene in wild boars and local pig breeds in Poland. , 2013, Animal genetics.

[27]  I. Jackson,et al.  Signatures of Diversifying Selection in European Pig Breeds , 2013, PLoS genetics.

[28]  B. vonHoldt,et al.  STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method , 2012, Conservation Genetics Resources.

[29]  Anushya Muruganujan,et al.  PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees , 2012, Nucleic Acids Res..

[30]  A. M. Barrio,et al.  Strong signatures of selection in the domestic pig genome , 2012, Proceedings of the National Academy of Sciences.

[31]  Bronwen L. Aken,et al.  Analyses of pig genomes provide insight into porcine demography and evolution , 2012, Nature.

[32]  J. Čítek,et al.  The impact of MYOG, MYF6 and MYOD1 genes on meat quality traits in crossbred pigs , 2012 .

[33]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[34]  Chuan-Yun Li,et al.  KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases , 2011, Nucleic Acids Res..

[35]  Robert J. Elshire,et al.  A Robust, Simple Genotyping-by-Sequencing (GBS) Approach for High Diversity Species , 2011, PloS one.

[36]  Andreia J. Amaral,et al.  Genome-Wide Footprints of Pig Domestication and Selection Revealed through Massive Parallel Sequencing of Pooled DNA , 2011, PloS one.

[37]  K. Patel,et al.  A hypoplastic model of skeletal muscle development displaying reduced foetal myoblast cell numbers, increased oxidative myofibres and improved specific tension capacity. , 2010, Developmental biology.

[38]  G. Bertorelle,et al.  Ancient vs. recent processes as factors shaping the genetic variation of the European wild boar: are the effects of the last glaciation still detectable? , 2008, Molecular ecology.

[39]  I. González,et al.  Differentiation of European wild boar (Sus scrofa scrofa) and domestic swine (Sus scrofa domestica) meats by PCR analysis targeting the mitochondrial D-loop and the nuclear melanocortin receptor 1 (MC1R) genes. , 2008, Meat science.

[40]  David S. Williams Usher syndrome: Animal models, retinal function of Usher proteins, and prospects for gene therapy , 2008, Vision Research.

[41]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[42]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[43]  Takeshi Hayashi,et al.  Fine mapping of a swine quantitative trait locus for number of vertebrae and analysis of an orphan nuclear receptor, germ cell nuclear factor (NR6A1). , 2007, Genome research.

[44]  P. Humpolíček,et al.  Impact of MYOD family genes on pork traits in Large White and Landrace pigs. , 2007, Journal of animal breeding and genetics = Zeitschrift fur Tierzuchtung und Zuchtungsbiologie.

[45]  C. Wright,et al.  The concerted action of Meox homeobox genes is required upstream of genetic pathways essential for the formation, patterning and differentiation of somites , 2003, Development.

[46]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[47]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[48]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[49]  S. Jeffery Evolution of Protein Molecules , 1979 .

[50]  M. Twarużek,et al.  High domestic pig contribution to the local gene pool of free-living European wild boar: a case study in Poland , 2017, Mammal Research.

[51]  M. Groenen,et al.  Edinburgh Research Explorer Genome-wide SNP data unveils the globalization of domesticated pigs , 2022 .

[52]  Andrew H. Paterson,et al.  Application of genotyping by sequencing technology to a variety of crop breeding programs. , 2016, Plant science : an international journal of experimental plant biology.

[53]  Theunis Piersma,et al.  The interplay between habitat availability and population differentiation , 2012 .

[54]  C. Stamatis,et al.  Detection of hybrids between wild boars (Sus scrofa scrofa) and domestic pigs (Sus scrofa f. domestica) in Greece, using the PCR-RFLP method on melanocortin-1 receptor (MC1R) mutations , 2010 .

[55]  K. Steel,et al.  Identification of a new mutation of the myosin VII head region in Usher syndrome type 1 , 1997, Human mutation.

[56]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .