A genome scan of recent positive selection signatures in three sheep populations
ZHAO Fu-ping, WEI Cai-hong, ZHANG Li, LIU Jia-sen, WANG Guang-kai, ZENG Tao, DU Li-xin
1、National Center for Molecular Genetics and Breeding of Animal, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100193, P.R.China
2、Institute of Animal Science, Inner Mongolia Academy of Agricultural & Animal Husbandry Sciences, Hohhot 010031, P.R.China
3、College of Animal Science and Technology, Sichuan Agricultural University, Ya’an 625014, P.R.China
摘要 Domesticated sheep have been exposed to artificial selection for the production of fiber, meat, and milk as well as to natural selection. Such selections are likely to have imposed distinctive selection signatures on the sheep genome. Therefore, detecting selection signatures across the genome may help elucidate mechanisms of selection and pinpoint candidate genes of interest for further investigation. Here, detection of selection signatures was conducted in three sheep breeds, Sunite (n=66), German Mutton (n=159), and Dorper (n=93), using the Illumina OvineSNP50 Genotyping BeadChip array. Each animal provided genotype information for 43 273 autosomal single nucleotide polymorphisms (SNPs). We adopted two complementary haplotype-based statistics of relative extended haplotype homozygosity (REHH) and the cross-population extended haplotype homozygosity (XP-EHH) tests. In total, 707, 755, and 438 genomic regions subjected to positive selection were identified in Sunite, German Mutton, and Dorper sheep, respectively, and 42 of these regions were detected using both REHH and XP-EHH analyses. These genomic regions harbored many important genes, which were enriched in gene ontology terms involved in muscle development, growth, and fat metabolism. Fourteen of these genomic regions overlapped with those identified in our previous genome-wide association studies, further indicating that these genes under positive selection may underlie growth developmental traits. These findings contribute to the identification of candidate genes of interest and aid in understanding the evolutionary and biological mechanisms for controlling complex traits in Chinese and western sheep.
Abstract Domesticated sheep have been exposed to artificial selection for the production of fiber, meat, and milk as well as to natural selection. Such selections are likely to have imposed distinctive selection signatures on the sheep genome. Therefore, detecting selection signatures across the genome may help elucidate mechanisms of selection and pinpoint candidate genes of interest for further investigation. Here, detection of selection signatures was conducted in three sheep breeds, Sunite (n=66), German Mutton (n=159), and Dorper (n=93), using the Illumina OvineSNP50 Genotyping BeadChip array. Each animal provided genotype information for 43 273 autosomal single nucleotide polymorphisms (SNPs). We adopted two complementary haplotype-based statistics of relative extended haplotype homozygosity (REHH) and the cross-population extended haplotype homozygosity (XP-EHH) tests. In total, 707, 755, and 438 genomic regions subjected to positive selection were identified in Sunite, German Mutton, and Dorper sheep, respectively, and 42 of these regions were detected using both REHH and XP-EHH analyses. These genomic regions harbored many important genes, which were enriched in gene ontology terms involved in muscle development, growth, and fat metabolism. Fourteen of these genomic regions overlapped with those identified in our previous genome-wide association studies, further indicating that these genes under positive selection may underlie growth developmental traits. These findings contribute to the identification of candidate genes of interest and aid in understanding the evolutionary and biological mechanisms for controlling complex traits in Chinese and western sheep.
This work was supported by the National Natural Science Foundation of China (31200927), the National Modern Agricultural Industry Technology Fund for Scientists in the Sheep Industry System of China (CARS-39-04B), and the Agricultural Science and Technology Innovation Program, China (ASTIP-IAS-TS-6).
Corresponding Authors:
DU Li-xin,Tel: +86-10-62819997, E-mail: lxdu@263.net
E-mail: lxdu@263.net
About author: ZHAO Fu-ping, E-mail: zhaofuping@caas.cn; WEI Cai-hong,E-mail: weicaihong@caas.cn;* These authors contributed equally to this study
ZHAO Fu-ping, WEI Cai-hong, ZHANG Li, LIU Jia-sen, WANG Guang-kai, ZENG Tao, DU Li-xin.
2016.
A genome scan of recent positive selection signatures in three sheep populations. Journal of Integrative Agriculture, 15(1): 162-174.
Akey J M. 2009. Constructing genomic maps of positiveselection in humans: Where do we go from here? GenomeResearch, 19, 711-722
Akey J M, Zhang G, Zhang K, Jin L, Shriver M D. 2002.Interrogating a high-density SNP map for signatures ofnatural selection. Genome Research, 12, 1805-1814
Biswas S, Akey J M. 2006. Genomic insights into positiveselection. Trends in Genetics, 22, 437-446
Browning S R, Browning B L. 2007. Rapid and accuratehaplotype phasing and missing-data inference for wholegenomeassociation studies by use of localized haplotypeclustering. American Journal of Human Genetics, 81,1084-1097
Browning S R, Weir B S. 2010. Population structure withlocalized haplotype clusters. Genetics, 185, 1337-1344
Chen H, Patterson N, Reich D. 2010. Population differentiationas a test for selective sweeps. Genome Research, 20,393-402
Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F,Mainland I, Kao R R, Pemberton J M, Beraldi D, Stear M J.2009. Revealing the history of sheep domestication usingretrovirus integrations. Science, 324, 532-536
CNCAGR (China National Commission of Animal GeneticResources). 2012. Animal Genetic Resources in China- Sheep and Goats. China Agriculture Press, China. (inChinese)
Conrad D F, Jakobsson M, Coop G, Wen X, Wall J D,Rosenberg N A, Pritchard J K. 2006. A worldwide survey ofhaplotype variation and linkage disequilibrium in the humangenome. Nature Genetics, 38, 1251-1260
Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. 2009. GOrilla:A tool for discovery and visualization of enriched GO termsin ranked gene lists. BMC Bioinformatics, 10, 48.
Fan H, Wu Y, Qi X, Zhang J, Li J, Gao X, Zhang L, Li J, GaoH. 2014. Genome-wide detection of selective signaturesin Simmental cattle. Journal of Applied Genetics, 55, 1-9
Fay J C, Wu C I. 2000. Hitchhiking under positive Darwinianselection. Genetics, 155, 1405-1413
Gu J, Orr N, Park S D, Katz L M, Sulimova G, MacHugh D E,Hill E W. 2009. A genome scan for positive selection inthoroughbred horses. PLoS ONE, 4, e5767.
Kijas J W, Lenstra J A, Hayes B, Boitard S, Neto L R P, SanCristobal M, Servin B, McCulloch R, Whan V, Gietzen K.2012. Genome-wide analysis of the world’s sheep breedsreveals high levels of historic mixture and strong recentselection. PLoS Biology, 10, e1001258.
Lewontin R, Krakauer J. 1973. Distribution of gene frequencyas a test of the theory of the selective neutrality ofpolymorphisms. Genetics, 74, 175-195
Lynch M, Walsh B. 1998. Genetics and Analysis of QuantitativeTraits. Sinauer Associates, Sunderland, MA.
Pan D, Zhang S, Jiang J, Jiang L, Zhang Q, Liu J. 2013.Genome-wide detection of selective signature in Chineseholstein. PLOS ONE, 8, e60440.
Qanbari S, Gianola D, Hayes B, Schenkel F, Miller S, MooreS, Thaller G, Simianer H. 2011. Application of site andhaplotype-frequency based approaches for detectingselection signatures in cattle. BMC Genomics, 12, 318.
Qanbari S, Pimentel E, Tetens J, Thaller G, Lichtner P, SharifiA, Simianer H. 2010. A genome-wide scan for signaturesof recent selection in Holstein cattle. Animal Genetics, 41,377-389
Rubin C J, Zody M C, Eriksson J, Meadows J R, Sherwood E,Webster M T, Jiang L, Ingman M, Sharpe T, Ka S. 2010.Whole-genome resequencing reveals loci under selectionduring chicken domestication. Nature, 464, 587-591
Sabeti P C, Reich D E, Higgins J M, Levine H Z P, Richter DJ, Schaffner S F, Gabriel S B, Platko J V, Patterson N J,McDonald G J. 2002. Detecting recent positive selectionin the human genome from haplotype structure. Nature,419, 832-837
Sabeti P C, Varilly P, Fry B, Lohmueller J, Hostetter E, CotsapasC, Xie X, Byrne E H, McCarroll S A, Gaudet R. 2007.Genome-wide detection and characterization of positiveselection in human populations. Nature, 449, 913-918
Tajima F. 1989. Statistical method for testing the neutralmutation hypothesis by DNA polymorphism. Genetics,123, 585-595
Tang K, Thornton K R, Stoneking M. 2007. A new approach forusing genome scans to detect recent positive selection inthe human genome. PLoS Biology, 5, e171.
Voight B F, Kudaravalli S, Wen X, Pritchard J K. 2006. A mapof recent positive selection in the human genome. PLoSBiology, 4, e72.
Weir B S, Cardon L R, Anderson A D, Nielsen D M, Hill WG. 2005. Measures of human population structure showheterogeneity among genomic regions. Genome Research,15, 1468-1476
Wright S. 1949. The genetical structure of populations. Annalsof Eugenics, 15, 323-354
Zhang H, Wang S Z, Wang Z P, Da Y, Wang N, Hu X X, Zhang YD, Wang Y X, Leng L, Tang Z Q. 2012. A genome-wide scanof selective sweeps in two broiler chicken lines divergentlyselected for abdominal fat content. BMC Genomics, 13, 704.
Zhang L, Liu J, Zhao F, Ren H, Xu L, Lu J, Zhang S, Zhang X,Wei C, Lu G. 2013. Genome-wide association studies forgrowth and meat production traits in sheep. PLOS ONE,8, e66569.
Zhao F, Wang G, Zeng T, Wei C, Zhang L, Wang H, Zhang S,Liu R, Liu Z, Du L. 2014. Estimations of genomic linkagedisequilibrium and effective population sizes in three sheeppopulations. Livestock Science, 170, 22-29
