Genome-wide analysis reveals selection for Chinese Rongchang pigs
Lei CHEN1, Shilin TIAN2, Long JIN2, Zongyi GUO1, Dan ZHU1, Lan JING1, Tiandong CHE2, Qianzi TANG2, Siqing CHEN1, Liang ZHANG1, Tinghuan ZHANG1, Zuohua LIU1, Jinyong WANG1(), Mingzhou LI2()
1. Key Laboratory of Pig Industry Sciences, Ministry of Agriculture, Chongqing Academy of Animal Sciences, Chongqing 402460, China 2. Institute of Animal Genetics and Breeding/College of Animal Science and Technology, Sichuan Agricultural University, Chengdu 611130, China
Livestock have undergone domestication and consequently strong selective pressure on genes or genomic regions that control desirable traits. To identify selection signatures in the genome of Chinese Rongchang pigs, we generated a total of about 170 Gb of DNA sequence data with about 6.4-fold coverage for each of six female individuals. By combining these data with the publically available genome data of 10 Asian wild boars, we identified 449 protein-coding genes with selection signatures in Rongchang pigs, which are mainly involved in growth and hormone binding, nervous system development, and drug metabolism. The accelerated evolution of these genes may contribute to the dramatic phenotypic differences between Rongchang pigs and Chinese wild boars. This study illustrated how domestication and subsequent artificial selection have shaped patterns of genetic variation in Rongchang pigs and provides valuable genetic resources that can enhance the use of pigs in agricultural production and biomedical studies.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The sequence alignment/map format and SAMtools. Bioinformatics, 2009, 25(16): 2078–2079 https://doi.org/10.1093/bioinformatics/btp352
pmid: 19505943
19
Huang W, Sherman B T, Lempicki R A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature Protocols, 2009, 4(1): 44–57 https://doi.org/10.1038/nprot.2008.211
pmid: 19131956
Nguyen D T, Lee K, Choi H, Choi M K, Le M T, Song N, Kim J H, Seo H G, Oh J W, Lee K, Kim T H, Park C. The complete swine olfactory subgenome: expansion of the olfactory gene repertoire in the pig genome. BMC Genomics, 2012, 13(1): 584 https://doi.org/10.1186/1471-2164-13-584
pmid: 23153364
22
Marchese S, Pes D, Scaloni A, Carbone V, Pelosi P. Lipocalins of boar salivary glands binding odours and pheromones. European Journal of Biochemistry, 1998, 252(3): 563–568 https://doi.org/10.1046/j.1432-1327.1998.2520563.x
pmid: 9546674
1
Groenen M A M, Archibald A L, Uenishi H, Tuggle C K, Takeuchi Y, Rothschild M F, Rogel-Gaillard C, Park C, Milan D, Megens H J, Li S, Larkin D M, Kim H, Frantz L A F, Caccamo M, Ahn H, Aken B L, Anselmo A, Anthon C, Auvil L, Badaoui B, Beattie C W, Bendixen C, Berman D, Blecha F, Blomberg J, Bolund L, Bosse M, Botti S, Bujie Z, Bystrom M, Capitanu B, Carvalho-Silva D, Chardon P, Chen C, Cheng R, Choi S H, Chow W, Clark R C, Clee C, Crooijmans R P M A, Dawson H D, Dehais P, De Sapio F, Dibbits B, Drou N, Du Z Q, Eversole K, Fadista J, Fairley S, Faraut T, Faulkner G J, Fowler K E, Fredholm M, Fritz E, Gilbert J G R, Giuffra E, Gorodkin J, Griffin D K, Harrow J L, Hayward A, Howe K, Hu Z L, Humphray S J, Hunt T, Hornshøj H, Jeon J T, Jern P, Jones M, Jurka J, Kanamori H, Kapetanovic R, Kim J, Kim J H, Kim K W, Kim T H, Larson G, Lee K, Lee K T, Leggett R, Lewin H A, Li Y, Liu W, Loveland J E, Lu Y, Lunney J K, Ma J, Madsen O, Mann K, Matthews L, McLaren S, Morozumi T, Murtaugh M P, Narayan J, Truong Nguyen D, Ni P, Oh S J, Onteru S, Panitz F, Park E W, Park H S, Pascal G, Paudel Y, Perez-Enciso M, Ramirez-Gonzalez R, Reecy J M, Rodriguez-Zas S, Rohrer G A, Rund L, Sang Y, Schachtschneider K, Schraiber J G, Schwartz J, Scobie L, Scott C, Searle S, Servin B, Southey B R, Sperber G, Stadler P, Sweedler J V, Tafer H, Thomsen B, Wali R, Wang J, Wang J, White S, Xu X, Yerle M, Zhang G, Zhang J, Zhang J, Zhao S, Rogers J, Churcher C, Schook L B. Analyses of pig genomes provide insight into porcine demography and evolution. Nature, 2012, 491(7424): 393–398 https://doi.org/10.1038/nature11622
pmid: 23151582
23
Mak G K, Enwere E K, Gregg C, Pakarainen T, Poutanen M, Huhtaniemi I, Weiss S. Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nature Neuroscience, 2007, 10(8): 1003–1011 https://doi.org/10.1038/nn1928
pmid: 17603480
24
Larson G, Dobney K, Albarella U, Fang M, Matisoo-Smith E, Robins J, Lowden S, Finlayson H, Brand T, Willerslev E, Rowley-Conwy P, Andersson L, Cooper A. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science, 2005, 307(5715): 1618–1621 https://doi.org/10.1126/science.1106927
pmid: 15761152
25
Albert F W, Somel M, Carneiro M, Aximu-Petri A, Halbwax M, Thalmann O, Blanco-Aguiar J A, Plyusnina I Z, Trut L, Villafuerte R, Ferrand N, Kaiser S, Jensen P, Pääbo S. A comparison of brain gene expression levels in domesticated and wild animals. PLoS Genetics, 2012, 8(9): e1002962 https://doi.org/10.1371/journal.pgen.1002962
pmid: 23028369
26
Amaral A J, Ferretti L, Megens H J, Crooijmans R P, Nie H, Ramos-Onsins S E, Perez-Enciso M, Schook L B, Groenen M A. Genome-wide footprints of pig domestication and selection revealed through massive parallel sequencing of pooled DNA. PLoS One, 2011, 6(4): e14782 https://doi.org/10.1371/journal.pone.0014782
pmid: 21483733
27
Li Y, Vonholdt B M, Reynolds A, Boyko A R, Wayne R K, Wu D D, Zhang Y P. Artificial selection on brain-expressed genes during the domestication of dog. Molecular Biology and Evolution, 2013, 30(8): 1867–1876 https://doi.org/10.1093/molbev/mst088
pmid: 23660689
28
Hare B, Plyusnina I, Ignacio N, Schepina O, Stepika A, Wrangham R, Trut L. Social cognitive evolution in captive foxes is a correlated by-product of experimental domestication. Current Biology, 2005, 15(3): 226–230 https://doi.org/10.1016/j.cub.2005.01.040
pmid: 15694305
29
Topál J, Gergely G, Erdohegyi A, Csibra G, Miklósi A. Differential sensitivity to human communication in dogs, wolves, and human infants. Science, 2009, 325(5945): 1269–1272 https://doi.org/10.1126/science.1176960
pmid: 19729660
Chen K, Baxter T, Muir W M, Groenen M A, Schook L B. Genetic resources, genome mapping and evolutionary genomics of the pig (Sus scrofa). International Journal of Biological Sciences, 2007, 3(3): 153–165 https://doi.org/10.7150/ijbs.3.153
pmid: 17384734
3
Rubin C J, Megens H J, Barrio A M, Maqbool K, Sayyab S, Schwochow D, Wang C, Carlborg O, Jern P, Jorgensen C B, Archibald A L, Fredholm M, Groenen M A M, Andersson L. Strong signatures of selection in the domestic pig genome. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(48): 19529–19536 https://doi.org/10.1073/pnas.1217149109
pmid: 23151514
4
Ai H, Fang X, Yang B, Huang Z, Chen H, Mao L, Zhang F, Zhang L, Cui L, He W, Yang J, Yao X, Zhou L, Han L, Li J, Sun S, Xie X, Lai B, Su Y, Lu Y, Yang H, Huang T, Deng W, Nielsen R, Ren J, Huang L. Adaptation and possible ancient interspecies introgression in pigs identified by whole-genome sequencing. Nature Genetics, 2015, 47(3): 217–225 https://doi.org/10.1038/ng.3199
pmid: 25621459
5
Xia Q, Guo Y, Zhang Z, Li D, Xuan Z, Li Z, Dai F, Li Y, Cheng D, Li R, Cheng T, Jiang T, Becquet C, Xu X, Liu C, Zha X, Fan W, Lin Y, Shen Y, Jiang L, Jensen J, Hellmann I, Tang S, Zhao P, Xu H, Yu C, Zhang G, Li J, Cao J, Liu S, He N, Zhou Y, Liu H, Zhao J, Ye C, Du Z, Pan G, Zhao A, Shao H, Zeng W, Wu P, Li C, Pan M, Li J, Yin X, Li D, Wang J, Zheng H, Wang W, Zhang X, Li S, Yang H, Lu C, Nielsen R, Zhou Z, Wang J, Xiang Z, Wang J. Complete resequencing of 40 genomes reveals domestication events and genes in silkworm (Bombyx). Science, 2009, 326(5951): 433–436 https://doi.org/10.1126/science.1176620
pmid: 19713493
6
Rubin C J, Zody M C, Eriksson J, Meadows J R, Sherwood E, Webster M T, Jiang L, Ingman M, Sharpe T, Ka S, Hallböök F, Besnier F, Carlborg O, Bed’hom B, Tixier-Boichard M, Jensen P, Siegel P, Lindblad-Toh K, Andersson L. Whole-genome resequencing reveals loci under selection during chicken domestication. Nature, 2010, 464(7288): 587–591 https://doi.org/10.1038/nature08832
pmid: 20220755
7
Shapiro M D, Kronenberg Z, Li C, Domyan E T, Pan H, Campbell M, Tan H, Huff C D, Hu H, Vickrey A I, Nielsen S C, Stringham S A, Hu H, Willerslev E, Gilbert M T, Yandell M, Zhang G, Wang J. Genomic diversity and evolution of the head crest in the rock pigeon. Science, 2013, 339(6123): 1063–1067 https://doi.org/10.1126/science.1230422
pmid: 23371554
8
Carneiro M, Rubin C J, Di Palma F, Albert F W, Alföldi J, Barrio A M, Pielberg G, Rafati N, Sayyab S, Turner-Maier J, Younis S, Afonso S, Aken B, Alves J M, Barrell D, Bolet G, Boucher S, Burbano H A, Campos R, Chang J L, Duranthon V, Fontanesi L, Garreau H, Heiman D, Johnson J, Mage R G, Peng Z, Queney G, Rogel-Gaillard C, Ruffier M, Searle S, Villafuerte R, Xiong A, Young S, Forsberg-Nilsson K, Good J M, Lander E S, Ferrand N, Lindblad-Toh K, Andersson L. Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication. Science, 2014, 345(6200): 1074–1079 https://doi.org/10.1126/science.1253714
pmid: 25170157
9
Axelsson E, Ratnakumar A, Arendt M L, Maqbool K, Webster M T, Perloski M, Liberg O, Arnemo J M, Hedhammar A, Lindblad-Toh K. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature, 2013, 495(7441): 360–364 https://doi.org/10.1038/nature11837
pmid: 23354050
10
Daetwyler H D, Capitan A, Pausch H, Stothard P, van Binsbergen R, Brøndum R F, Liao X, Djari A, Rodriguez S C, Grohs C, Esquerré D, Bouchez O, Rossignol M N, Klopp C, Rocha D, Fritz S, Eggen A, Bowman P J, Coote D, Chamberlain A J, Anderson C, VanTassell C P, Hulsegge I, Goddard M E, Guldbrandtsen B, Lund M S, Veerkamp R F, Boichard D A, Fries R, Hayes B J. Whole-genome sequencing of 234 bulls facilitates mapping of monogenic and complex traits in cattle. Nature Genetics, 2014, 46(8): 858–865 https://doi.org/10.1038/ng.3034
pmid: 25017103
11
Li M, Tian S, Jin L, Zhou G, Li Y, Zhang Y, Wang T, Yeung C K, Chen L, Ma J, Zhang J, Jiang A, Li J, Zhou C, Zhang J, Liu Y, Sun X, Zhao H, Niu Z, Lou P, Xian L, Shen X, Liu S, Zhang S, Zhang M, Zhu L, Shuai S, Bai L, Tang G, Liu H, Jiang Y, Mai M, Xiao J, Wang X, Zhou Q, Wang Z, Stothard P, Xue M, Gao X, Luo Z, Gu Y, Zhu H, Hu X, Zhao Y, Plastow G S, Wang J, Jiang Z, Li K, Li N, Li X, Li R. Genomic analyses identify distinct patterns of selection in domesticated pigs and Tibetan wild boars. Nature Genetics, 2013, 45(12): 1431–1438 https://doi.org/10.1038/ng.2811
pmid: 24162736
12
Li M, Chen L, Tian S, Lin Y, Tang Q, Zhou X, Li D, Yeung C K L, Che T, Jin L, Fu Y, Ma J, Wang X, Jiang A, Lan J, Pan Q, Liu Y, Luo Z, Guo Z, Liu H, Zhu L, Shuai S, Tang G, Zhao J, Jiang Y, Bai L, Zhang S, Mai M, Li C, Wang D, Gu Y, Wang G, Lu H, Li Y, Zhu H, Li Z, Li M, Gladyshev V N, Jiang Z, Zhao S, Wang J, Li R, Li X. Comprehensive variation discovery and recovery of missing sequence in the pig genome using multiple de novo assemblies. Genome Research, 2017, 27(5): 865–874 https://doi.org/10.1101/gr.207456.116
pmid: 27646534
13
Fu Y, Li C, Tang Q, Tian S, Jin L, Chen J, Li M, Li C. Genomic analysis reveals selection in Chinese native black pig. Scientific Reports, 2016, 6(1): 36354 https://doi.org/10.1038/srep36354
pmid: 27808243
14
Li M, Tian S, Yeung C K, Meng X, Tang Q, Niu L, Wang X, Jin L, Ma J, Long K, Zhou C, Cao Y, Zhu L, Bai L, Tang G, Gu Y, Jiang A, Li X, Li R. Whole-genome sequencing of Berkshire (European native pig) provides insights into its origin and domestication. Scientific Reports, 2014, 4(4): 4678
pmid: 24728479
15
Bosse M, Megens H J, Frantz L A, Madsen O, Larson G, Paudel Y, Duijvesteijn N, Harlizius B, Hagemeijer Y, Crooijmans R P, Groenen M A. Genomic analysis reveals selection for Asian genes in European pigs following human-mediated introgression. Nature Communications, 2014, 5: 4392 https://doi.org/10.1038/ncomms5392
pmid: 25025832
16
Frantz L A, Schraiber J G, Madsen O, Megens H J, Bosse M, Paudel Y, Semiadi G, Meijaard E, Li N, Crooijmans R P, Archibald A L, Slatkin M, Schook L B, Larson G, Groenen M A. Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus. Genome Biology, 2013, 14(9): R107 https://doi.org/10.1186/gb-2013-14-9-r107
pmid: 24070215
