Population structure and history of the Welsh sheep breeds determined by whole genome genotyping

BMC Genetics

Denis M. Larkin⁶  Lynfa Davies⁴  C. Jamie Newbold⁵  Iona M. MacLeod¹  James Kijas³  William Haresign⁵  Brian Davies⁵  Kate Waddams⁵  Bolormaa Sunduimijid²  Marta Farré⁵  Gancho T. Slavov⁵  Sarah E. Beynon⁵ 

[1] Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Melbourne 3010, VIC, Australia;Victorian Department of Environment and Primary Industries, Bundoora 3083, VIC, Australia;Commonwealth Scientific and Industrial Research Organisation (CSIRO), 306 Carmody Road, St Lucia 4067, QLD, Australia;Hybu Cig Cymru, Meat Promotion Wales, Tŷ Rheidol, Parc Merlin, Aberystwyth SY23 3FF, UK;Institute of Biological, Environmental and Rural Sciences, Aberystwyth University, Penglais, Aberystwyth SY23 3DA, Ceredigion, UK;Royal Veterinary College, University of London, Royal College Street, London NW1 0TU, UK

关键词: Linkage disequilibrium;    Sequencing;    SNP;    Selective breeding;    Demography;    Genotyping;    Population structure;    Selection;    Welsh native breeds;    Ovis aries;   

Others  :  1216013
DOI  :  10.1186/s12863-015-0216-x

 received in 2014-11-28, accepted in 2015-05-13,  发布年份 2015

【 摘 要 】

Background

One of the most economically important areas within the Welsh agricultural sector is sheep farming, contributing around £230 million to the UK economy annually. Phenotypic selection over several centuries has generated a number of native sheep breeds, which are presumably adapted to the diverse and challenging landscape of Wales. Little is known about the history, genetic diversity and relationships of these breeds with other European breeds. We genotyped 353 individuals from 18 native Welsh sheep breeds using the Illumina OvineSNP50 array and characterised the genetic structure of these breeds. Our genotyping data were then combined with, and compared to, those from a set of 74 worldwide breeds, previously collected during the International Sheep Genome Consortium HapMap project.

Results

Model based clustering of the Welsh and European breeds indicated shared ancestry. This finding was supported by multidimensional scaling analysis (MDS), which revealed separation of the European, African and Asian breeds. As expected, the commercial Texel and Merino breeds appeared to have extensive co-ancestry with most European breeds. Consistently high levels of haplotype sharing were observed between native Welsh and other European breeds. The Welsh breeds did not, however, form a genetically homogeneous group, with pairwise F_STbetween breeds averaging 0.107 and ranging between 0.020 and 0.201. Four subpopulations were identified within the 18 native breeds, with high homogeneity observed amongst the majority of mountain breeds. Recent effective population sizes estimated from linkage disequilibrium ranged from 88 to 825.

Conclusions

Welsh breeds are highly diverse with low to moderate effective population sizes and form at least four distinct genetic groups. Our data suggest common ancestry between the native Welsh and European breeds. These findings provide the basis for future genome-wide association studies and a first step towards developing genomics assisted breeding strategies in the UK.

【 授权许可】

   
2015 Beynon et al.

【 图 表 】

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【 参考文献 】

• [1]Giuffra E, Kijas JMH, Amarger V, Carlborg Ö, Jeon J-T, Andersson L. The origin of the domestic pig: independent domestication and subsequent introgression. Genetics. 2000; 154(4):1785-91.
• [2]Petersen JL, Mickelson JR, Cothran EG, Andersson LS, Axelsson J, Bailey E et al.. Genetic diversity in the modern horse illustrated from genome-wide SNP data. PLoS One. 2013; 8(1):e54997.
• [3]Larkin DM, Daetwyler HD, Hernandez AG, Wright CL, Hetrick LA, Boucek L et al.. Whole-genome resequencing of two elite sires for the detection of haplotypes under selection in dairy cattle. Proc Natl Acad Sci U S A. 2012; 109(20):7693-8.
• [4]Ernst CW, Steibel JP. Molecular advances in QTL discovery and application in pig breeding. Trends Genet. 2013; 29(4):215-24.
• [5]Stinchcombe JR, Hoekstra HE. Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity. 2007; 100(2):158-70.
• [6]Goddard ME, Hayes BJ. Genomic selection. J Anim Breed Genet. 2007; 124(6):323-30.
• [7]Dekkers JC. Commercial application of marker- and gene-assisted selection in livestock: strategies and lessons. J Anim Sci. 2004; 82(E-Suppl):E313-28.
• [8]Notter DR. The importance of genetic diversity in livestock populations of the future. J Anim Sci. 1999; 77(1):61-9.
• [9]Ajmone‐Marsan P. A global view of livestock biodiversity and conservation–GLOBALDIV. Anim Genet. 2010; 41(s1):1-5.
• [10]Rare Breeds Survival Trust. [https://www.rbst.org.uk/]. accessed 2014.
• [11]Kijas JW, Lenstra JA, Hayes B, Boitard S, Porto Neto LR, San Cristobal M et al.. Genome-wide analysis of the world’s sheep breeds reveals high levels of historic mixture and strong recent selection. PLoS Biol. 2012; 10(2):e1001258.
• [12]Genome-wide survey of SNP variation uncovers the genetic structure of cattle breeds. Science. 2009; 324(5926):528-32.
• [13]Elsik CG, Tellam RL, Worley KC. The genome sequence of taurine cattle: a window to ruminant biology and evolution. Science. 2009; 324(5926):522-8.
• [14]Groenen MAM, Archibald AL, Uenishi H, Tuggle CK, Takeuchi Y, Rothschild MF et al.. Analyses of pig genomes provide insight into porcine demography and evolution. Nature. 2012; 491(7424):393-8.
• [15]Trow-Smith R. A History of British Livestock Husbandry to 1700. Routledge and Paul, Oxford; 1957.
• [16]Trow-Smith R. A history of british livestock husbandry, 1700–1900. Routledge & K. Paul Ltd., London; 1959.
• [17]Illumina. OvineSNP50 Genotyping Beadchip. http://www.illumina.com/documents//products/datasheets/datasheet_ovinesnp50.pdf 2010.
• [18]QIAGEN Genomic DNA Handbook. http://www. qiagen.com/knowledge-and-support/resource-center/resource-download.aspx?id=402bb209-4104-4956-a005-6226ff0b67d5&lang=en webcite
• [19]Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D et al.. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007; 81(3):559-75.
• [20]Price AL, Patterson NJ, Plenge RM, Weinblatt ME, Shadick NA, Reich D. Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet. 2006; 38(8):904-9.
• [21]Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genet. 2006; 2(12):e190.
• [22]Tenesa A, Navarro P, Hayes BJ, Duffy DL, Clarke GM, Goddard ME et al.. Recent human effective population size estimated from linkage disequilibrium. Genome Res. 2007; 17(4):520-6.
• [23]Lischer HEL, Excoffier L. PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs. Bioinformatics. 2012; 28(2):298-9.
• [24]Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000; 155(2):945-59.
• [25]Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics. 2003; 164(4):1567-87.
• [26]Falush D, Stephens M, Pritchard JK. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes. 2007; 7(4):574-8.
• [27]Hubisz MJ, Falush D, Stephens M, Pritchard JK. Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour. 2009; 9(5):1322-32.
• [28]Jakobsson M, Rosenberg NA. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics. 2007; 23(14):1801-6.
• [29]Rosenberg NA. Distruct: a program for the graphical display of population structure. Mol Ecol Notes. 2004; 4(1):137-8.
• [30]Team RDC. R: a language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria; 2005. http://cran. r-project.org/doc/FAQ/R-FAQ.html webcite
• [31]Felsenstein J. PHYLIP-phylogeny interference package (version 3.2). Cladistics. 1989; 5:164-6.
• [32]Rambaut A. FigTree v1. 4.0. A graphical viewer of phylogenetic trees. http://tree.bio.ed.ac.uk/software/figtree/, accessed 2012.
• [33]Li H, Durbin R. Inference of human population history from individual whole-genome sequences. Nature. 2011; 475(7357):493-6.
• [34]MacLeod IM, Larkin DM, Lewin HA, Hayes BJ, Goddard ME. Inferring demography from runs of homozygosity in whole-genome sequence, with correction for sequence errors. Mol Biol Evol. 2013; 30(9):2209-23.
• [35]MacLeod IM, Meuwissen THE, Hayes BJ, Goddard ME. A novel predictor of multilocus haplotype homozygosity: comparison with existing predictors. Genet Res. 2009; 91(06):413-26.
• [36]Heaton MP, Leymaster KA, Kalbfleisch TS, Kijas JW, Clarke SM, McEwan J et al.. SNPs for parentage testing and traceability in globally diverse breeds of sheep. PLoS One. 2014; 9(4):e94851.
• [37]Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009; 25(14):1754-60.
• [38]Marth GT, Korf I, Yandell MD, Yeh RT, Gu Z, Zakeri H et al.. A general approach to single-nucleotide polymorphism discovery. Nat Genet. 1999; 23(4):452-6.
• [39]Roach JC, Glusman G, Smit AF, Huff CD, Hubley R, Shannon PT et al.. Analysis of genetic inheritance in a family quartet by whole-genome sequencing. Science. 2010; 328(5978):636-9.
• [40]Scally A, Durbin R. Revising the human mutation rate: implications for understanding human evolution. Nat Rev Genet. 2012; 13(10):745-53.
• [41]Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, Gibbs RA et al.. A map of human genome variation from population-scale sequencing. Nature. 2010; 467(7319):1061-73.
• [42]Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci. 1973; 70(12):3321-3.
• [43]Pollott G. The breeding structure of the British sheep industry 2012. Kenilworth, Warwickshire: EBLEX; 2012.
• [44]Kim Y, Ryu J, Woo J, Kim JB, Kim CY, Lee C. Genome-wide association study reveals five nucleotide sequence variants for carcass traits in beef cattle. Anim Genet. 2011; 42(4):361-5.
• [45]Snelling WM, Allan MF, Keele JW, Kuehn LA, McDaneld T, Smith TPL et al.. Genome-wide association study of growth in crossbred beef cattle. J Anim Sci. 2010; 88(3):837-48.
• [46]Kim KS, Larsen N, Short T, Plastow G, Rothschild MF. A missense variant of the porcine melanocortin-4 receptor (MC4R) gene is associated with fatness, growth, and feed intake traits. Mamm Genome. 2000; 11(2):131-5.
• [47]Diamond J. Evolution, consequences and future of plant and animal domestication. Nature. 2002; 418(6898):700-7.
• [48]Zeder MA. Domestication and early agriculture in the Mediterranean Basin: origins, diffusion, and impact. Proc Natl Acad Sci. 2008; 105(33):11597-604.
• [49]Bruford MW, Bradley DG, Luikart G. DNA markers reveal the complexity of livestock domestication. Nat Rev Genet. 2003; 4(11):900-10.
• [50]Feulner PGD, Gratten J, Kijas JW, Visscher PM, Pemberton JM, Slate J. Introgression and the fate of domesticated genes in a wild mammal population. Mol Ecol. 2013; 22(16):4210-21.
• [51]Johnston SE, Gratten J, Berenos C, Pilkington JG, Clutton-Brock TH, Pemberton JM et al.. Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature. 2013; 502(7469):93-5.
• [52]Kijas JW, Townley D, Dalrymple BP, Heaton MP, Maddox JF, McGrath A et al.. A genome wide survey of SNP variation reveals the genetic structure of sheep breeds. PLoS One. 2009; 4(3):e4668.
• [53]Wolf B, Smith C, Sales D. Growth and carcass composition in the crossbred progeny of six terminal sire breeds of sheep. Anim Prod. 1980; 31(03):307-13.
• [54]Leymaster KA, Jenkins TG. Comparison of Texel- and Suffolk-sired crossbred lambs for survival, growth, and compositional traits. J Anim Sci. 1993; 71(4):859-69.
• [55]National Sheep Association (NSA). British Sheep, vol. 9. Malvern; 1998.
• [56]Oltenacu EA, Boylan WJ. Productivity of purebred and crossbred finnsheep. I. Reproductive traits of ewes and lamb survival. J Anim Sci. 1981; 52(5):989-97.
• [57]Leslie S, Winney B, Hellenthal G, Davison D, Boumertit A, Day T, et al. The fine-scale genetic structure of the British population. Nature. 2015;519(7543):309–314.
• [58]Ryder M. A survey of European primitive breeds of sheep. Genet Sel Evol. 1981; 13:381-418. BioMed Central Full Text
• [59]Dýrmundsson ÓR, Niżnikowski R. North European short-tailed breeds of sheep: a review. Anim. 2010; 4(08):1275-82.
• [60]History of the Lleyn. http://www. lleynsheep.com/society/history/ webcite
• [61]Álvarez I, Royo L, Fernandez I, Gutiérrez J, Gómez E, Goyache F. Genetic relationships and admixture among sheep breeds from Northern Spain assessed using microsatellites. J Anim Sci. 2004; 82(8):2246-52.
• [62]Gautier M, Laloë D, Moazami-Goudarzi K. Insights into the genetic history of french cattle from dense SNP data on 47 worldwide breeds. PLoS One. 2010; 5(9):e13038.
• [63]Williams-Davies J. Welsh sheep and their wool. Gomer Press, Dyfed; 1981.
• [64]Jones C, Davies S, Macdonald N. Examining the social consequences of extreme weather: the outcomes of the 1946/1947 winter in upland Wales, UK. Clim Change. 2012; 113:1-19.
• [65]Alderson L. Rare Breeds. In: A shire book. Tarxien Malta: Gutenberg Press; 2001.
• [66]Watchlist. 2014. [https://www.rbst.org.uk/watchlist-2014.pdf] accessed 2014
• [67]Ma L, Wiggans GR, Wang S, Sonstegard TS, Yang J, Crooker BA et al.. Effect of sample stratification on dairy GWAS results. BMC Genomics. 2012; 13:536. BioMed Central Full Text
• [68]Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, Wohlfarth B et al.. The last glacial maximum. Science. 2009; 325(5941):710-4.
• [69]Tian C, Gregersen PK, Seldin MF. Accounting for ancestry: population substructure and genome-wide association studies. Hum Mol Genet. 2008; 17(R2):R143-50.
• [70]Goddard ME, Hayes BJ. Mapping genes for complex traits in domestic animals and their use in breeding programmes. Nat Rev Genet. 2009; 10(6):381-91.