Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations

Present‐day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified beyond doubt mainly because available methods were unable to quantify the extent of introgression and rule out natural processes. Genetic intro...

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Vydáno v:Molecular ecology Ročník 22; číslo 3; s. 856 - 866
Hlavní autoři: GOEDBLOED, D. J., MEGENS, H.J., Van HOOFT, P., HERRERO-MEDRANO, J. M., LUTZ, W., ALEXANDRI, P., CROOIJMANS, R. P. M. A., GROENEN, M., Van WIEREN, S. E., YDENBERG, R. C., PRINS, H. H. T.
Médium: Journal Article
Jazyk:angličtina
Vydáno: Oxford, UK Blackwell Publishing Ltd 01.02.2013
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ISSN:0962-1083, 1365-294X, 1365-294X
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Abstract Present‐day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified beyond doubt mainly because available methods were unable to quantify the extent of introgression and rule out natural processes. Genetic introgression from domestic pigs may have far‐reaching ecological consequences by altering traits like the reproduction rate or immunology of wild boar. In this study, we demonstrate a novel approach to investigate genetic introgression in a Northwest (NW) European wild boar data set using a genome‐wide single nucleotide polymorphism (SNP) assay developed for domestic pigs. We quantified the extent of introgression using allele frequency spectrum analysis, in silico hybridization simulations and genome distribution patterns of introgressed SNPs. Levels of recent introgression in the study area were expected to be low, as pig farming practices are prevailingly intensive and indoors. However, evidence was found for geographically widespread presence of domestic pig SNPs in 10% of analysed wild boar. This was supported by the identification of two different pig mitochondrial DNA haplotypes in three of the identified hybrid wild boar, suggesting that introgression had occurred from multiple sources (pig breeds). In silico hybridization simulations showed that the level of introgression in the identified hybrid wild boar is equivalent to first‐generation hybrids until fifth‐generation backcrosses with wild boar. The distribution pattern of introgressed SNPs supported these assignments in four of nine hybrids. The other five hybrids are considered advanced‐generation hybrids, resulting from interbreeding among hybrid individuals. Three of nine hybrids were genetically associated with a different wild boar population than the one in which they were sampled. This discrepancy suggests that genetic introgression has occurred through the escape or release of an already hybridized farmed wild boar stock. We conclude that genetic introgression from domestic pigs into NW European wild boar populations is more recent and more common than expected and that genome‐wide SNP analysis is a promising tool to quantify recent hybridization in free‐living populations.
AbstractList Present-day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified beyond doubt mainly because available methods were unable to quantify the extent of introgression and rule out natural processes. Genetic introgression from domestic pigs may have far-reaching ecological consequences by altering traits like the reproduction rate or immunology of wild boar. In this study, we demonstrate a novel approach to investigate genetic introgression in a Northwest (NW) European wild boar data set using a genome-wide single nucleotide polymorphism (SNP) assay developed for domestic pigs. We quantified the extent of introgression using allele frequency spectrum analysis, in silico hybridization simulations and genome distribution patterns of introgressed SNPs. Levels of recent introgression in the study area were expected to be low, as pig farming practices are prevailingly intensive and indoors. However, evidence was found for geographically widespread presence of domestic pig SNPs in 10% of analysed wild boar. This was supported by the identification of two different pig mitochondrial DNA haplotypes in three of the identified hybrid wild boar, suggesting that introgression had occurred from multiple sources (pig breeds). In silico hybridization simulations showed that the level of introgression in the identified hybrid wild boar is equivalent to first-generation hybrids until fifth-generation backcrosses with wild boar. The distribution pattern of introgressed SNPs supported these assignments in four of nine hybrids. The other five hybrids are considered advanced-generation hybrids, resulting from interbreeding among hybrid individuals. Three of nine hybrids were genetically associated with a different wild boar population than the one in which they were sampled. This discrepancy suggests that genetic introgression has occurred through the escape or release of an already hybridized farmed wild boar stock. We conclude that genetic introgression from domestic pigs into NW European wild boar populations is more recent and more common than expected and that genome-wide SNP analysis is a promising tool to quantify recent hybridization in free-living populations.
Present-day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified beyond doubt mainly because available methods were unable to quantify the extent of introgression and rule out natural processes. Genetic introgression from domestic pigs may have far-reaching ecological consequences by altering traits like the reproduction rate or immunology of wild boar. In this study, we demonstrate a novel approach to investigate genetic introgression in a Northwest (NW) European wild boar data set using a genome-wide single nucleotide polymorphism (SNP) assay developed for domestic pigs. We quantified the extent of introgression using allele frequency spectrum analysis, in silico hybridization simulations and genome distribution patterns of introgressed SNPs. Levels of recent introgression in the study area were expected to be low, as pig farming practices are prevailingly intensive and indoors. However, evidence was found for geographically widespread presence of domestic pig SNPs in 10% of analysed wild boar. This was supported by the identification of two different pig mitochondrial DNA haplotypes in three of the identified hybrid wild boar, suggesting that introgression had occurred from multiple sources (pig breeds). In silico hybridization simulations showed that the level of introgression in the identified hybrid wild boar is equivalent to first-generation hybrids until fifth-generation backcrosses with wild boar. The distribution pattern of introgressed SNPs supported these assignments in four of nine hybrids. The other five hybrids are considered advanced-generation hybrids, resulting from interbreeding among hybrid individuals. Three of nine hybrids were genetically associated with a different wild boar population than the one in which they were sampled. This discrepancy suggests that genetic introgression has occurred through the escape or release of an already hybridized farmed wild boar stock. We conclude that genetic introgression from domestic pigs into NW European wild boar populations is more recent and more common than expected and that genome-wide SNP analysis is a promising tool to quantify recent hybridization in free-living populations.Present-day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified beyond doubt mainly because available methods were unable to quantify the extent of introgression and rule out natural processes. Genetic introgression from domestic pigs may have far-reaching ecological consequences by altering traits like the reproduction rate or immunology of wild boar. In this study, we demonstrate a novel approach to investigate genetic introgression in a Northwest (NW) European wild boar data set using a genome-wide single nucleotide polymorphism (SNP) assay developed for domestic pigs. We quantified the extent of introgression using allele frequency spectrum analysis, in silico hybridization simulations and genome distribution patterns of introgressed SNPs. Levels of recent introgression in the study area were expected to be low, as pig farming practices are prevailingly intensive and indoors. However, evidence was found for geographically widespread presence of domestic pig SNPs in 10% of analysed wild boar. This was supported by the identification of two different pig mitochondrial DNA haplotypes in three of the identified hybrid wild boar, suggesting that introgression had occurred from multiple sources (pig breeds). In silico hybridization simulations showed that the level of introgression in the identified hybrid wild boar is equivalent to first-generation hybrids until fifth-generation backcrosses with wild boar. The distribution pattern of introgressed SNPs supported these assignments in four of nine hybrids. The other five hybrids are considered advanced-generation hybrids, resulting from interbreeding among hybrid individuals. Three of nine hybrids were genetically associated with a different wild boar population than the one in which they were sampled. This discrepancy suggests that genetic introgression has occurred through the escape or release of an already hybridized farmed wild boar stock. We conclude that genetic introgression from domestic pigs into NW European wild boar populations is more recent and more common than expected and that genome-wide SNP analysis is a promising tool to quantify recent hybridization in free-living populations.
Present-day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified beyond doubt mainly because available methods were unable to quantify the extent of introgression and rule out natural processes. Genetic introgression from domestic pigs may have far-reaching ecological consequences by altering traits like the reproduction rate or immunology of wild boar. In this study, we demonstrate a novel approach to investigate genetic introgression in a Northwest (NW) European wild boar data set using a genome-wide single nucleotide polymorphism (SNP) assay developed for domestic pigs. We quantified the extent of introgression using allele frequency spectrum analysis, in silico hybridization simulations and genome distribution patterns of introgressed SNPs. Levels of recent introgression in the study area were expected to be low, as pig farming practices are prevailingly intensive and indoors. However, evidence was found for geographically widespread presence of domestic pig SNPs in 10% of analysed wild boar. This was supported by the identification of two different pig mitochondrial DNA haplotypes in three of the identified hybrid wild boar, suggesting that introgression had occurred from multiple sources (pig breeds). In silico hybridization simulations showed that the level of introgression in the identified hybrid wild boar is equivalent to first-generation hybrids until fifth-generation backcrosses with wild boar. The distribution pattern of introgressed SNPs supported these assignments in four of nine hybrids. The other five hybrids are considered advanced-generation hybrids, resulting from interbreeding among hybrid individuals. Three of nine hybrids were genetically associated with a different wild boar population than the one in which they were sampled. This discrepancy suggests that genetic introgression has occurred through the escape or release of an already hybridized farmed wild boar stock. We conclude that genetic introgression from domestic pigs into NW European wild boar populations is more recent and more common than expected and that genome-wide SNP analysis is a promising tool to quantify recent hybridization in free-living populations. [PUBLICATION ABSTRACT]
Author LUTZ, W.
CROOIJMANS, R. P. M. A.
GOEDBLOED, D. J.
MEGENS, H.J.
YDENBERG, R. C.
Van WIEREN, S. E.
GROENEN, M.
PRINS, H. H. T.
Van HOOFT, P.
ALEXANDRI, P.
HERRERO-MEDRANO, J. M.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/22731769$$D View this record in MEDLINE/PubMed
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References Verhoeven KJ, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proceedings of the Royal Society B-Biological Sciences, 278, 2-8.
Giuffra E, Kijas JMH, Amarger V et al. (2000) The origin of the domestic pig: independent domestication and subsequent introgression. Genetics, 154, 1785-1791.
Miller JM, Poissant J, Kijas JW, Coltman DW (2011) A genome-wide set of SNPs detects population substructure and long range linkage disequilibrium in wild sheep. Molecular Ecology Resources, 11, 314-322.
Seeb JE, Carvalho G, Hauser L et al. (2011) Single-nucleotide polymorphism (SNP) discovery and applications of SNP genotyping in nonmodel organisms. Molecular Ecology Resources, 11(Suppl 1), 1-8.
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596-1599.
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
Willing EM, Bentzen P, van Oosterhout C et al. (2010) Genome-wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Molecular Ecology, 19, 968-984.
Alves PC, Pinheiro I, Godinho R et al. (2010) Genetic diversity of wild boar populations and domestic pig breeds (Sus scrofa) in South-western Europe. Biological Journal of the Linnean Society, 101, 797-822.
Gethoffer F, Sodeikat G, Pohlmeyer K (2007) Reproductive parameters of wild boar (Sus scrofa) in three different parts of Germany. European Journal of Wildlife Research, 53, 287-297.
Larkin MA, Blackshields G, Brown NP et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947-2948.
Briedermann L (1990) Schwarzwild. VEB Deutscher Landwirtschaftsverlag, Berlin, Germany.
Goulding MJ (2001) Possible genetic sources of free-living Wild Boar (Sus scrofa) in southern England. Mammal Review, 31, 245-248.
Narum SR, Banks M, Beacham TD et al. (2008) Differentiating salmon populations at broad and fine geographical scales with microsatellites and single nucleotide polymorphisms. Molecular Ecology, 17, 3464-3477.
Purcell S, Neale B, Todd-Brown K et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559-575.
Luetkemeier ES, Sodhi M, Schook LB, Malhi RS (2010) Multiple Asian pig origins revealed through genomic analyses. Molecular Phylogenetics and Evolution, 54, 680-686.
Geisser H, Reyer HU (2005) The influence of food and temperature on population density of wild boar Sus scrofa in the Thurgau (Switzerland). Journal of Zoology, 267, 89-96.
Scandura M, Iacolina L, Crestanello B et al. (2008) Ancient vs. recent processes as factors shaping the genetic variation of the European wild boar: are the effects of the last glaciation still detectable?Molecular Ecology, 17, 1745-1762.
Kraus RHS, Kerstens HHD, Van Hooft P et al. (2011) Genome wide SNP discovery, analysis and evaluation in mallard (Anas platyrhynchos). BMC Genomics, 12, article no. 150.
Fang MY, Andersson L (2006) Mitochondrial diversity in European and Chinese pigs is consistent with population expansions that occurred prior to domestication. Proceedings of the Royal Society B-Biological Sciences, 273, 1803-1810.
Scandura M, Iacolina L, Apollonio M (2011) Genetic diversity in the European wild boar Sus scrofa: phylogeography, population structure and wild × domestic hybridization. Mammal Review, 41, 125-137.
Larson G, Albarella U, Dobney K et al. (2007) Ancient DNA, pig domestication, and the spread of the Neolithic into Europe. Proceedings of the National Academy of Sciences of the United States of America, 104, 15276-15281.
Bieber C, Ruf T (2005) Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. Journal of Applied Ecology, 42, 1203-1213.
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
Morin PA, Luikart G, Wayne RK (2004) SNPs in ecology, evolution and conservation. Trends in Ecology & Evolution, 19, 208-216.
Larson G, Dobney K, Albarella U et al. (2005) Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science, 307, 1618-1621.
Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genetics, 2, e190.
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
Vignal A, Milan D, SanCristobal M, Eggen A (2002) A review on SNP and other types of molecular markers and their use in animal genetics. Genetics Selection Evolution, 34, 275-305.
Price AL, Patterson NJ, Plenge RM et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38, 904-909.
Ramos AM, Crooijmans RPMA, Affara NA, Amaral AJ, Archibald AL (2009) Design of a high-density SNP genotyping assay in the pig using SNPs identified and characterized by next generation sequencing technology. PLoS ONE, 4, e6524.
Glez-Pena D, Gomez-Blanco D, Reboiro-Jato M, Fdez-Riverola F, Posada D (2010) ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Research, 38, W14-W18.
Bonfield JK, Smith KF, Staden R (1995) A new DNA sequence assembly program. Nucleic Acids Research, 23, 4992-4999.
Saezroyuela C, Telleria JL (1986) The increased population of the wild boar (Sus-Scrofa L) in Europe. Mammal Review, 16, 97-101.
Fang M, Berg F, Ducos A, Andersson L (2006) Mitochondrial haplotypes of European wild boars with 2n=36 are closely related to those of European domestic pigs with 2n=38. Animal Genetics, 37, 459-464.
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– reference: Alves PC, Pinheiro I, Godinho R et al. (2010) Genetic diversity of wild boar populations and domestic pig breeds (Sus scrofa) in South-western Europe. Biological Journal of the Linnean Society, 101, 797-822.
– reference: Price AL, Patterson NJ, Plenge RM et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nature Genetics, 38, 904-909.
– reference: Bieber C, Ruf T (2005) Population dynamics in wild boar Sus scrofa: ecology, elasticity of growth rate and implications for the management of pulsed resource consumers. Journal of Applied Ecology, 42, 1203-1213.
– reference: Fang M, Berg F, Ducos A, Andersson L (2006) Mitochondrial haplotypes of European wild boars with 2n=36 are closely related to those of European domestic pigs with 2n=38. Animal Genetics, 37, 459-464.
– reference: Verhoeven KJ, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proceedings of the Royal Society B-Biological Sciences, 278, 2-8.
– reference: Bonfield JK, Smith KF, Staden R (1995) A new DNA sequence assembly program. Nucleic Acids Research, 23, 4992-4999.
– reference: Giuffra E, Kijas JMH, Amarger V et al. (2000) The origin of the domestic pig: independent domestication and subsequent introgression. Genetics, 154, 1785-1791.
– reference: Gethoffer F, Sodeikat G, Pohlmeyer K (2007) Reproductive parameters of wild boar (Sus scrofa) in three different parts of Germany. European Journal of Wildlife Research, 53, 287-297.
– reference: Luetkemeier ES, Sodhi M, Schook LB, Malhi RS (2010) Multiple Asian pig origins revealed through genomic analyses. Molecular Phylogenetics and Evolution, 54, 680-686.
– reference: Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
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– reference: Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
– reference: Purcell S, Neale B, Todd-Brown K et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. American Journal of Human Genetics, 81, 559-575.
– reference: Miller JM, Poissant J, Kijas JW, Coltman DW (2011) A genome-wide set of SNPs detects population substructure and long range linkage disequilibrium in wild sheep. Molecular Ecology Resources, 11, 314-322.
– reference: Kraus RHS, Kerstens HHD, Van Hooft P et al. (2011) Genome wide SNP discovery, analysis and evaluation in mallard (Anas platyrhynchos). BMC Genomics, 12, article no. 150.
– reference: Larkin MA, Blackshields G, Brown NP et al. (2007) Clustal W and clustal X version 2.0. Bioinformatics, 23, 2947-2948.
– reference: Vignal A, Milan D, SanCristobal M, Eggen A (2002) A review on SNP and other types of molecular markers and their use in animal genetics. Genetics Selection Evolution, 34, 275-305.
– reference: Fang MY, Andersson L (2006) Mitochondrial diversity in European and Chinese pigs is consistent with population expansions that occurred prior to domestication. Proceedings of the Royal Society B-Biological Sciences, 273, 1803-1810.
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– reference: Narum SR, Banks M, Beacham TD et al. (2008) Differentiating salmon populations at broad and fine geographical scales with microsatellites and single nucleotide polymorphisms. Molecular Ecology, 17, 3464-3477.
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– reference: Larson G, Dobney K, Albarella U et al. (2005) Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science, 307, 1618-1621.
– reference: Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genetics, 2, e190.
– reference: Saezroyuela C, Telleria JL (1986) The increased population of the wild boar (Sus-Scrofa L) in Europe. Mammal Review, 16, 97-101.
– reference: Goulding MJ (2001) Possible genetic sources of free-living Wild Boar (Sus scrofa) in southern England. Mammal Review, 31, 245-248.
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Snippet Present‐day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified...
Present-day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified...
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pubmed
crossref
wiley
istex
SourceType Aggregation Database
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StartPage 856
SubjectTerms Agricultural practices
Animal populations
Animals
Distribution patterns
DNA, Mitochondrial - genetics
Domestic animals
domestic pig
Ecological effects
Europe
Genetics
Genetics, Population
Genomes
Haplotypes
Heterozygote
Hogs
Hybridization
Hybridization, Genetic
Hybrids
Immunology
introgression
Mitochondrial DNA
Molecular Sequence Data
Polymorphism
Polymorphism, Single Nucleotide
Sequence Analysis, DNA
single nucleotide polymorphism
Sus scrofa
Sus scrofa - genetics
Swine
wild boar
Wildlife
Title Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations
URI https://api.istex.fr/ark:/67375/WNG-59S3PB75-Z/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fj.1365-294X.2012.05670.x
https://www.ncbi.nlm.nih.gov/pubmed/22731769
https://www.proquest.com/docview/1269479966
https://www.proquest.com/docview/1273584262
https://www.proquest.com/docview/1285098202
Volume 22
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