Genome-Wide Footprints of Pig Domestication and Selection Revealed through Massive Parallel Sequencing of Pooled DNA

A.J. Amaral, L. Ferretti, H.J.W.C. Megens, R.P.M.A. Crooijmans, H. Nie, S.E. Ramos-Onsins, M. Perez-Enciso, L.B. Schook, M.A.M. Groenen

Research output: Contribution to journalArticleAcademicpeer-review

88 Citations (Scopus)

Abstract

Background Artificial selection has caused rapid evolution in domesticated species. The identification of selection footprints across domesticated genomes can contribute to uncover the genetic basis of phenotypic diversity. Methodology/Main Findings Genome wide footprints of pig domestication and selection were identified using massive parallel sequencing of pooled reduced representation libraries (RRL) representing ~2% of the genome from wild boar and four domestic pig breeds (Large White, Landrace, Duroc and Pietrain) which have been under strong selection for muscle development, growth, behavior and coat color. Using specifically developed statistical methods that account for DNA pooling, low mean sequencing depth, and sequencing errors, we provide genome-wide estimates of nucleotide diversity and genetic differentiation in pig. Widespread signals suggestive of positive and balancing selection were found and the strongest signals were observed in Pietrain, one of the breeds most intensively selected for muscle development. Most signals were population-specific but affected genomic regions which harbored genes for common biological categories including coat color, brain development, muscle development, growth, metabolism, olfaction and immunity. Genetic differentiation in regions harboring genes related to muscle development and growth was higher between breeds than between a given breed and the wild boar. Conclusions/Significance These results, suggest that although domesticated breeds have experienced similar selective pressures, selection has acted upon different genes. This might reflect the multiple domestication events of European breeds or could be the result of subsequent introgression of Asian alleles. Overall, it was estimated that approximately 7% of the porcine genome has been affected by selection events. This study illustrates that the massive parallel sequencing of genomic pools is a cost-effective approach to identify footprints of selection.
Original languageEnglish
Article numbere14782
Number of pages12
JournalPLoS ONE
Volume6
Issue number4
DOIs
Publication statusPublished - 2011

Fingerprint

Muscle Development
domestication
DNA Sequence Analysis
Sus scrofa
muscle development
Swine
sequence analysis
Genes
Genome
breeds
swine
genome
DNA
Pietrain
Muscle
wild boars
Growth
Color
Smell
genomics

Keywords

  • major histocompatibility complex
  • recent positive selection
  • class-i region
  • linkage disequilibrium
  • genetic diversity
  • breeds
  • generation
  • signatures
  • chimpanzee
  • mutation

Cite this

Amaral, A.J. ; Ferretti, L. ; Megens, H.J.W.C. ; Crooijmans, R.P.M.A. ; Nie, H. ; Ramos-Onsins, S.E. ; Perez-Enciso, M. ; Schook, L.B. ; Groenen, M.A.M. / Genome-Wide Footprints of Pig Domestication and Selection Revealed through Massive Parallel Sequencing of Pooled DNA. In: PLoS ONE. 2011 ; Vol. 6, No. 4.
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abstract = "Background Artificial selection has caused rapid evolution in domesticated species. The identification of selection footprints across domesticated genomes can contribute to uncover the genetic basis of phenotypic diversity. Methodology/Main Findings Genome wide footprints of pig domestication and selection were identified using massive parallel sequencing of pooled reduced representation libraries (RRL) representing ~2{\%} of the genome from wild boar and four domestic pig breeds (Large White, Landrace, Duroc and Pietrain) which have been under strong selection for muscle development, growth, behavior and coat color. Using specifically developed statistical methods that account for DNA pooling, low mean sequencing depth, and sequencing errors, we provide genome-wide estimates of nucleotide diversity and genetic differentiation in pig. Widespread signals suggestive of positive and balancing selection were found and the strongest signals were observed in Pietrain, one of the breeds most intensively selected for muscle development. Most signals were population-specific but affected genomic regions which harbored genes for common biological categories including coat color, brain development, muscle development, growth, metabolism, olfaction and immunity. Genetic differentiation in regions harboring genes related to muscle development and growth was higher between breeds than between a given breed and the wild boar. Conclusions/Significance These results, suggest that although domesticated breeds have experienced similar selective pressures, selection has acted upon different genes. This might reflect the multiple domestication events of European breeds or could be the result of subsequent introgression of Asian alleles. Overall, it was estimated that approximately 7{\%} of the porcine genome has been affected by selection events. This study illustrates that the massive parallel sequencing of genomic pools is a cost-effective approach to identify footprints of selection.",
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Genome-Wide Footprints of Pig Domestication and Selection Revealed through Massive Parallel Sequencing of Pooled DNA. / Amaral, A.J.; Ferretti, L.; Megens, H.J.W.C.; Crooijmans, R.P.M.A.; Nie, H.; Ramos-Onsins, S.E.; Perez-Enciso, M.; Schook, L.B.; Groenen, M.A.M.

In: PLoS ONE, Vol. 6, No. 4, e14782, 2011.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Genome-Wide Footprints of Pig Domestication and Selection Revealed through Massive Parallel Sequencing of Pooled DNA

AU - Amaral, A.J.

AU - Ferretti, L.

AU - Megens, H.J.W.C.

AU - Crooijmans, R.P.M.A.

AU - Nie, H.

AU - Ramos-Onsins, S.E.

AU - Perez-Enciso, M.

AU - Schook, L.B.

AU - Groenen, M.A.M.

PY - 2011

Y1 - 2011

N2 - Background Artificial selection has caused rapid evolution in domesticated species. The identification of selection footprints across domesticated genomes can contribute to uncover the genetic basis of phenotypic diversity. Methodology/Main Findings Genome wide footprints of pig domestication and selection were identified using massive parallel sequencing of pooled reduced representation libraries (RRL) representing ~2% of the genome from wild boar and four domestic pig breeds (Large White, Landrace, Duroc and Pietrain) which have been under strong selection for muscle development, growth, behavior and coat color. Using specifically developed statistical methods that account for DNA pooling, low mean sequencing depth, and sequencing errors, we provide genome-wide estimates of nucleotide diversity and genetic differentiation in pig. Widespread signals suggestive of positive and balancing selection were found and the strongest signals were observed in Pietrain, one of the breeds most intensively selected for muscle development. Most signals were population-specific but affected genomic regions which harbored genes for common biological categories including coat color, brain development, muscle development, growth, metabolism, olfaction and immunity. Genetic differentiation in regions harboring genes related to muscle development and growth was higher between breeds than between a given breed and the wild boar. Conclusions/Significance These results, suggest that although domesticated breeds have experienced similar selective pressures, selection has acted upon different genes. This might reflect the multiple domestication events of European breeds or could be the result of subsequent introgression of Asian alleles. Overall, it was estimated that approximately 7% of the porcine genome has been affected by selection events. This study illustrates that the massive parallel sequencing of genomic pools is a cost-effective approach to identify footprints of selection.

AB - Background Artificial selection has caused rapid evolution in domesticated species. The identification of selection footprints across domesticated genomes can contribute to uncover the genetic basis of phenotypic diversity. Methodology/Main Findings Genome wide footprints of pig domestication and selection were identified using massive parallel sequencing of pooled reduced representation libraries (RRL) representing ~2% of the genome from wild boar and four domestic pig breeds (Large White, Landrace, Duroc and Pietrain) which have been under strong selection for muscle development, growth, behavior and coat color. Using specifically developed statistical methods that account for DNA pooling, low mean sequencing depth, and sequencing errors, we provide genome-wide estimates of nucleotide diversity and genetic differentiation in pig. Widespread signals suggestive of positive and balancing selection were found and the strongest signals were observed in Pietrain, one of the breeds most intensively selected for muscle development. Most signals were population-specific but affected genomic regions which harbored genes for common biological categories including coat color, brain development, muscle development, growth, metabolism, olfaction and immunity. Genetic differentiation in regions harboring genes related to muscle development and growth was higher between breeds than between a given breed and the wild boar. Conclusions/Significance These results, suggest that although domesticated breeds have experienced similar selective pressures, selection has acted upon different genes. This might reflect the multiple domestication events of European breeds or could be the result of subsequent introgression of Asian alleles. Overall, it was estimated that approximately 7% of the porcine genome has been affected by selection events. This study illustrates that the massive parallel sequencing of genomic pools is a cost-effective approach to identify footprints of selection.

KW - major histocompatibility complex

KW - recent positive selection

KW - class-i region

KW - linkage disequilibrium

KW - genetic diversity

KW - breeds

KW - generation

KW - signatures

KW - chimpanzee

KW - mutation

U2 - 10.1371/journal.pone.0014782

DO - 10.1371/journal.pone.0014782

M3 - Article

VL - 6

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 4

M1 - e14782

ER -