Analysis of genome-wide DNA arrays reveals the genomic population structure and diversity in autochthonous Greek goat breeds


Autoři: S. Michailidou aff001;  G. Th. Tsangaris aff003;  A. Tzora aff004;  I. Skoufos aff004;  G. Banos aff001;  A. Argiriou aff002;  G. Arsenos aff001
Působiště autorů: Laboratory of Animal Husbandry, School of Veterinary Medicine, School of Health Sciences, Aristotle University of Thessaloniki, Thessaloniki, Greece aff001;  Institute of Applied Biosciences, Center for Research and Technology Hellas, Thermi, Greece aff002;  Proteomics Research Unit, Biomedical Research Foundation of the Academy of Athens, Athens, Greece aff003;  School of Agriculture, Department of Agriculture, Division of Animal Production, University of Ioannina, Kostakioi Artas, Greece aff004;  Scotland's Rural College and The Roslin Institute University of Edinburgh, Edinburgh, Scotland, United Kingdom aff005
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226179

Souhrn

Goats play an important role in the livestock sector in Greece. The national herd consists mainly of two indigenous breeds, the Eghoria and Skopelos. Here, we report the population structure and genomic profiles of these two native goat breeds using Illumina’s Goat SNP50 BeadChip. Moreover, we present a panel of candidate markers acquired using different genetic models for breed discrimination. Quality control on the initial dataset resulted in 48,841 SNPs kept for downstream analysis. Principal component and admixture analyses were applied to assess population structure. The rate of inbreeding within breed was evaluated based on the distribution of runs of homozygosity in the genome and respective coefficients, the genomic relationship matrix, the patterns of linkage disequilibrium, and the historic effective population size. Results showed that both breeds exhibit high levels of genetic diversity. Level of inbreeding between the two breeds estimated by the Wright’s fixation index FST was low (Fst = 0.04362), indicating the existence of a weak genetic differentiation between them. In addition, grouping of farms according to their geographical locations was observed. This study presents for the first time a genome-based analysis on the genetic structure of the two indigenous Greek goat breeds and identifies markers that can be potentially exploited in future selective breeding programs for traceability purposes, targeted genetic improvement schemes and conservation strategies.

Klíčová slova:

Farms – Goats – Homozygosity – Inbreeding – Molecular genetics – Population genetics – Species diversity – Greek people


Zdroje

1. Food and Agriculture Organization of the United Nations. Accessed 10 Jan 2018 [Internet]. 2014. Available from: http://www.fao.org/faostat/en/

2. Gelasakis AI, Rose G, Giannakou R, Valergakis GE, Theodoridis A, Fortomaris P, et al. Typology and characteristics of dairy goat production systems in Greece. Livest Sci. 2017;197:22–9. WOS:000395843100005.

3. Hatziminaoglou Y, Boyazoglu J. The goat in ancient civilisations: from the Fertile Crescent to the Aegean Sea. Small Ruminant Res. 2004;51(2):123–9. WOS:000188873900002.

4. Cappuccio I, Pariset L, Ajmone-Marsan P, Dunner S, Cortes O, Erhardt G, et al. Allele frequencies and diversity parameters of 27 single nucleotide polymorphisms within and across goat breeds. Molecular Ecology Notes. 2006;6(4):992–7. doi: 10.1111/j.1471-8286.2006.01425.x

5. Pariset L, Cuteri A, Ligda C, Ajmone-Marsan P, Valentini A, Consortium E. Geographical patterning of sixteen goat breeds from Italy, Albania and Greece assessed by Single Nucleotide Polymorphisms. BMC ecology. 2009;9:20. doi: 10.1186/1472-6785-9-20 19725964; PubMed Central PMCID: PMC2754418.

6. Colli L, Joost S, Negrini R, Nicoloso L, Crepaldi P, Ajmone-Marsan P, et al. Assessing The Spatial Dependence of Adaptive Loci in 43 European and Western Asian Goat Breeds Using AFLP Markers. Plos One. 2014;9(1). ARTN e86668 10.1371/journal.pone.0086668. WOS:000330617100024.

7. Naderi S, Rezaei HR, Taberlet P, Zundel S, Rafat SA, Naghash HR, et al. Large-Scale Mitochondrial DNA Analysis of the Domestic Goat Reveals Six Haplogroups with High Diversity. Plos One. 2007;2(10). ARTN e1012 10.1371/journal.pone.0001012. WOS:000207456000011.

8. Tosser-Klopp G, Bardou P, Bouchez O, Cabau C, Crooijmans R, Dong Y, et al. Design and characterization of a 52K SNP chip for goats. PloS one. 2014;9(1):e86227. doi: 10.1371/journal.pone.0086227 24465974; PubMed Central PMCID: PMC3899236.

9. Bickhart DM, Rosen BD, Koren S, Sayre BL, Hastie AR, Chan S, et al. Single-molecule sequencing and chromatin conformation capture enable de novo reference assembly of the domestic goat genome. Nature genetics. 2017;49(4):643–50. doi: 10.1038/ng.3802 28263316; PubMed Central PMCID: PMC5909822.

10. Dong Y, Xie M, Jiang Y, Xiao N, Du X, Zhang W, et al. Sequencing and automated whole-genome optical mapping of the genome of a domestic goat (Capra hircus). Nature biotechnology. 2013;31(2):135–41. doi: 10.1038/nbt.2478 23263233.

11. Bertolini F, Cardoso TF, Marras G, Nicolazzi EL, Rothschild MF, Amills M, et al. Genome-wide patterns of homozygosity provide clues about the population history and adaptation of goats. Genet Sel Evol. 2018;50:59. WOS:000450519100005. doi: 10.1186/s12711-018-0424-8 30449279

12. Bertolini F, Servin B, Talenti A, Rochat E, Kim ES, Oget C, et al. Signatures of selection and environmental adaptation across the goat genome post-domestication. Genet Sel Evol. 2018;50(1):57. WOS:000450519100003. doi: 10.1186/s12711-018-0421-y 30449276

13. Cardoso TF, Amills M, Bertolini F, Rothschild M, Marras G, Boink G, et al. Patterns of homozygosity in insular and continental goat breeds. Genet Sel Evol. 2018;50:56. WOS:000450519100002. doi: 10.1186/s12711-018-0425-7 30449277

14. Colli L, Milanesi M, Talenti A, Bertolini F, Chen MH, Crisa A, et al. Genome-wide SNP profiling of worldwide goat populations reveals strong partitioning of diversity and highlights post-domestication migration routes. Genet Sel Evol. 2018;50(1):58. WOS:000450519100004. doi: 10.1186/s12711-018-0422-x 30449284

15. Stella A, Nicolazzi EL, Van Tassell CP, Rothschild MF, Colli L, Rosen BD, et al. AdaptMap: exploring goat diversity and adaptation. Genet Sel Evol. 2018;50:61. WOS:000451145000001. doi: 10.1186/s12711-018-0427-5 30453882

16. Talenti A, Palhiere I, Tortereau F, Pagnacco G, Stella A, Nicolazzi EL, et al. Functional SNP panel for parentage assessment and assignment in worldwide goat breeds. Genet Sel Evol. 2018;50:55. WOS:000450519100001. doi: 10.1186/s12711-018-0423-9 30449282

17. Rahmatalla SA, Arends D, Reissmann M, Ahmed AS, Wimmers K, Reyer H, et al. Whole genome population genetics analysis of Sudanese goats identifies regions harboring genes associated with major traits. Bmc Genet. 2017;18:1–10. WOS:000413487800001. doi: 10.1186/s12863-016-0468-0

18. Boettcher PJ, Tixier-Boichard M, Toro MA, Simianer H, Eding H, Gandini G, et al. Objectives, criteria and methods for using molecular genetic data in priority setting for conservation of animal genetic resources. Anim Genet. 2010;41:64–77. WOS:000276775100005.

19. Bruford MW, Ginja C, Hoffmann I, Joost S, Orozco-terWengel P, Alberto FJ, et al. Prospects and challenges for the conservation of farm animal genomic resources, 2015–2025. Frontiers in genetics. 2015;6:314. doi: 10.3389/fgene.2015.00314 26539210; PubMed Central PMCID: PMC4612686.

20. Dalvit C, De Marchi M, Cassandro M. Genetic traceability of livestock products: A review. Meat Sci. 2007;77(4):437–49. doi: 10.1016/j.meatsci.2007.05.027 22061927.

21. Brito LF, Kijas JW, Ventura RV, Sargolzaei M, Porto-Neto LR, Canovas A, et al. Genetic diversity and signatures of selection in various goat breeds revealed by genome-wide SNP markers. Bmc Genomics. 2017;18:229. WOS:000396758600001. doi: 10.1186/s12864-017-3610-0 28288562

22. Felius M, Theunissen B, Lenstra JA. Conservation of cattle genetic resources: the role of breeds. J Agr Sci-Cambridge. 2015;153(1):152–62. WOS:000347711200014.

23. R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2010.

24. Becker RA, Wilks. AR. R version by Ray Brownrigg. Enhancements by Thomas P Minka and Alex Deckmyn. maps: Draw Geographical Maps. R package version 3.3.0. https://CRAN.R-project.org/package=maps.2018.

25. South A. rworldmap: A New R package for Mapping Global Data. The R Journal Vol. 3/1: 35–43. 2011.

26. South A. rworldxtra: Country boundaries at high resolution. R package version 1.01. https://CRAN.R-project.org/package=rworldxtra. 2012.

27. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, 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. WOS:000249128200012. doi: 10.1086/519795 17701901

28. Schaffner SF. The X chromosome in population genetics. Nat Rev Genet. 2004;5(1):43–51. WOS:000187641100015. doi: 10.1038/nrg1247 14708015

29. Hodgkinson A, Eyre-Walker A. Variation in the mutation rate across mammalian genomes. Nature Reviews Genetics. 2011;12:756. doi: 10.1038/nrg3098 21969038

30. Alexander DH, Lange K. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC bioinformatics. 2011;12:246. doi: 10.1186/1471-2105-12-246 21682921; PubMed Central PMCID: PMC3146885.

31. Buchmann R, Hazelhurst S. The ‘Genesis’ Manual. University of the Witwatersrand, Johannesburg. 2015.

32. Milanesi M, Capomaccio S, Vajana E, Bomba L, Garcia JF, Ajmone-Marsan P, et al. BITE: an R package for biodiversity analyses. bioRxiv. 2017:181610. doi: 10.1101/181610

33. Pickrell JK, Pritchard JK. Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data. Plos Genet. 2012;8(11). ARTN e100296710.1371/journal.pgen.1002967. WOS:000311891600002.

34. Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10(3):564–7. WOS:000276407300020. doi: 10.1111/j.1755-0998.2010.02847.x 21565059

35. VanRaden PM. Efficient Methods to Compute Genomic Predictions. J Dairy Sci. 2008;91(11):4414–23. WOS:000260277200035. doi: 10.3168/jds.2007-0980 18946147

36. Yang JA, Lee SH, Goddard ME, Visscher PM. GCTA: A Tool for Genome-wide Complex Trait Analysis. Am J Hum Genet. 2011;88(1):76–82. WOS:000286501500007. doi: 10.1016/j.ajhg.2010.11.011 21167468

37. Al-Mamun HA, Clark SA, Kwan P, Gondro C. Genome-wide linkage disequilibrium and genetic diversity in five populations of Australian domestic sheep. Genetics, selection, evolution: GSE. 2015;47:90. doi: 10.1186/s12711-015-0169-6 26602211; PubMed Central PMCID: PMC4659207.

38. McQuillan R, Leutenegger AL, Abdel-Rahman R, Franklin CS, Pericic M, Barac-Lauc L, et al. Runs of homozygosity in European populations. Am J Hum Genet. 2008;83(3):359–72. WOS:000259307200007. doi: 10.1016/j.ajhg.2008.08.007 18760389

39. Biscarini F, Cozzi P, Gaspa G, G. M. detectRUNS: Detect Runs of Homozygosity and Runs of Heterozygosity in Diploid Genomes. R package version 0.9.5. 2018. https://CRAN.R-project.org/package=detectRUNS.

40. Khatkar MS, Nicholas FW, Collins AR, Zenger KR, Al Cavanagh J, Barris W, et al. Extent of genome-wide linkage disequilibrium in Australian Holstein-Friesian cattle based on a high-density SNP panel. Bmc Genomics. 2008;9:187. WOS:000256398400001. doi: 10.1186/1471-2164-9-187 18435834

41. Barbato M, Orozco-TerWengel P, Tapio M, Bruford MW. SNeP: a tool to estimate trends in recent effective population size trajectories using genome-wide SNP data. Front Genet. 2015;6:109. WOS:000352769500001. doi: 10.3389/fgene.2015.00109 25852748

42. Corbin LJ, Liu AYH, Bishop SC, Woolliams JA. Estimation of historical effective population size using linkage disequilibria with marker data. J Anim Breed Genet. 2012;129(4):257–70. WOS:000306277300002. doi: 10.1111/j.1439-0388.2012.01003.x 22775258

43. Weir BS, Cockerham CC. Estimating F-Statistics for the Analysis of Population Structure. Evolution. 1984;38(6):1358–70. doi: 10.1111/j.1558-5646.1984.tb05657.x 28563791.

44. Turner SD. qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. bioRxiv. 2014:005165. doi: 10.1101/005165

45. Kavakiotis I, Triantafyllidis A, Ntelidou D, Alexandri P, Megens HJ, Crooijmans RP, et al. TRES: Identification of Discriminatory and Informative SNPs from Population Genomic Data. J Hered. 2015;106(5):672–6. doi: 10.1093/jhered/esv044 26137847.

46. Shriver MD, Smith MW, Jin L, Marcini A, Akey JM, Deka R, et al. Ethnic-affiliation estimation by use of population-specific DNA markers. Am J Hum Genet. 1997;60(4):957–64. WOS:A1997WT61400026. 9106543

47. Wright S. The Genetical Structure of Populations. Ann Eugenic. 1951;15(4):323–54. WOS:A1951XY09200006.

48. Rosenberg NA, Li LM, Ward R, Pritchard JK. Informativeness of genetic markers for inference of ancestry. Am J Hum Genet. 2003;73(6):1402–22. WOS:000187491100015. doi: 10.1086/380416 14631557

49. Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A. GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered. 2004;95(6):536–9. doi: 10.1093/jhered/esh074 15475402.

50. Oliveros JC. Venny. An interactive tool for comparing lists with Venn's diagrams. https://bioinfogp.cnb.csic.es/tools/venny/index.html 2007–2015.

51. Paetkau D, Slade R, Burden M, Estoup A. Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol. 2004;13(1):55–65. WOS:000187005700006. doi: 10.1046/j.1365-294x.2004.02008.x 14653788

52. Paetkau D, Calvert W, Stirling I, Strobeck C. Microsatellite Analysis of Population-Structure in Canadian Polar Bears. Mol Ecol. 1995;4(3):347–54. WOS:A1995RF43700007. doi: 10.1111/j.1365-294x.1995.tb00227.x 7663752

53. Rannala B, Mountain JL. Detecting immigration by using multilocus genotypes. Proceedings of the National Academy of Sciences of the United States of America. 1997;94(17):9197–201. WOS:A1997XR76500053. doi: 10.1073/pnas.94.17.9197 9256459

54. Mastrangelo S, Portolano B, Di Gerlando R, Ciampolini R, Tolone M, Sardina MT, et al. Genome-wide analysis in endangered populations: a case study in Barbaresca sheep. Animal: an international journal of animal bioscience. 2017;11(7):1107–16. doi: 10.1017/S1751731116002780 28077191.

55. Manunza A, Noce A, Serradilla JM, Goyache F, Martinez A, Capote J, et al. A genome-wide perspective about the diversity and demographic history of seven Spanish goat breeds. Genet Sel Evol. 2016;48:52. WOS:000381071000001. doi: 10.1186/s12711-016-0229-6 27455838

56. Nicoloso L, Bomba L, Colli L, Negrini R, Milanesi M, Mazza R, et al. Genetic diversity of Italian goat breeds assessed with a medium-density SNP chip. Genet Sel Evol. 2015;47:62. WOS:000358985500001. doi: 10.1186/s12711-015-0140-6 26239391

57. Lashmar SF, Visser C, van Marle-Koster E. SNP-based genetic diversity of South African commercial dairy and fiber goat breeds. Small Ruminant Res. 2016;136:65–71. WOS:000374606400010.

58. Visser C, Lashmar SF, Van Marle-Koster E, Poli MA, Allain D. Genetic Diversity and Population Structure in South African, French and Argentinian Angora Goats from Genome-Wide SNP Data. PloS one. 2016;11(5). WOS:000376588600059.

59. Canon J, Garcia D, Garcia-Atance MA, Obexer-Ruff G, Lenstra JA, Ajmone-Marsan P, et al. Geographical partitioning of goat diversity in Europe and the Middle East. Anim Genet. 2006;37(4):327–34. WOS:000239112100004. doi: 10.1111/j.1365-2052.2006.01461.x 16879341

60. Lenstra JA, Tigchelaar J, Biebach I, Hallsson JH, Kantanen J, Nielsen VH, et al. Microsatellite diversity of the Nordic type of goats in relation to breed conservation: how relevant is pure ancestry? J Anim Breed Genet. 2017;134(1):78–84. WOS:000393777200010. doi: 10.1111/jbg.12226 27339108

61. Pemberton TJ, Absher D, Feldman MW, Myers RM, Rosenberg NA, Li JZ. Genomic patterns of homozygosity in worldwide human populations. Am J Hum Genet. 2012;91(2):275–92. doi: 10.1016/j.ajhg.2012.06.014 22883143; PubMed Central PMCID: PMC3415543.

62. Szmatola T, Gurgul A, Ropka-Molik K, Jasielczuk I, Zabek T, Bugno-Poniewierska M. Characteristics of runs of homozygosity in selected cattle breeds maintained in Poland. Livest Sci. 2016;188:72–80. WOS:000377729500011.

63. Peripolli E, Munari DP, Silva M, Lima ALF, Irgang R, Baldi F. Runs of homozygosity: current knowledge and applications in livestock. Anim Genet. 2017;48(3):255–71. doi: 10.1111/age.12526 27910110.

64. Bosse M, Megens HJ, Madsen O, Paudel Y, Frantz LA, Schook LB, et al. Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genet. 2012;8(11):e1003100. doi: 10.1371/journal.pgen.1003100 23209444; PubMed Central PMCID: PMC3510040.

65. Mdladla K, Dzomba EF, Huson HJ, Muchadeyi FC. Population genomic structure and linkage disequilibrium analysis of South African goat breeds using genome-wide SNP data. Anim Genet. 2016;47(4):471–82. WOS:000379936600007. doi: 10.1111/age.12442 27306145

66. Keller MC, Visscher PM, Goddard ME. Quantification of Inbreeding Due to Distant Ancestors and Its Detection Using Dense Single Nucleotide Polymorphism Data. Genetics. 2011;189(1):237–U920. WOS:000294721600019. doi: 10.1534/genetics.111.130922 21705750

67. Purfield DC, Berry DP, McParland S, Bradley DG. Runs of homozygosity and population history in cattle. Bmc Genet. 2012;13:70. WOS:000312139400001. doi: 10.1186/1471-2156-13-70 22888858

68. Zhang QQ, Calus MPL, Guldbrandtsen B, Lund MS, Sahana G. Estimation of inbreeding using pedigree, 50k SNP chip genotypes and full sequence data in three cattle breeds. Bmc Genet. 2015;16. WOS:000358122200001.

69. Burren A, Neuditschko M, Signer-Hasler H, Frischknecht M, Reber I, Menzi F, et al. Genetic diversity analyses reveal first insights into breed-specific selection signatures within Swiss goat breeds. Anim Genet. 2016;47(6):727–39. WOS:000387359100010. doi: 10.1111/age.12476 27436146

70. Howrigan DP, Simonson MA, Keller MC. Detecting autozygosity through runs of homozygosity: A comparison of three autozygosity detection algorithms. Bmc Genomics. 2011;12:460. WOS:000295741300001. doi: 10.1186/1471-2164-12-460 21943305

71. Ku CS, Naidoo N, Teo SM, Pawitan Y. Regions of homozygosity and their impact on complex diseases and traits. Human genetics. 2011;129(1):1–15. doi: 10.1007/s00439-010-0920-6 WOS:000286396200001. 21104274

72. Alvarenga AB, Rovadoscki GA, Petrini J, Coutinho LL, Morota G, Spangler ML, et al. Linkage disequilibrium in Brazilian Santa Ines breed, Ovis aries. Sci Rep. 2018;8(1):8851. doi: 10.1038/s41598-018-27259-7 29892085; PubMed Central PMCID: PMC5995818.

73. Selvaggi M, Laudadio V, Dario C, Tufarelli V. Major proteins in goat milk: an updated overview on genetic variability. Mol Biol Rep. 2014;41(2):1035–48. doi: 10.1007/s11033-013-2949-9 WOS:000330860900052. 24381104

74. Wu HJ, Luo J, Wu N, Matand K, Zhang LJ, Han XF, et al. Cloning, sequence and functional analysis of goat ATP-binding cassette transporter G2 (ABCG2). Mol Biotechnol. 2008;39(1):21–7. doi: 10.1007/s12033-007-9024-5 WOS:000254964700003. 18256940

75. Souza CJ, MacDougall C, MacDougall C, Campbell BK, McNeilly AS, Baird DT. The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. The Journal of endocrinology. 2001;169(2):R1–6. doi: 10.1677/joe.0.169r001 11312159.

76. Ahlawat S, Sharma R, Roy M, Mandakmale S, Prakash V, Tantia MS. Genotyping of Novel SNPs in BMPR1B, BMP15, and GDF9 Genes for Association with Prolificacy in Seven Indian Goat Breeds. Anim Biotechnol. 2016;27(3):199–207. doi: 10.1080/10495398.2016.1167706 WOS:000377448200008. 27135147

77. Pan ZY, Di R, Tang QQ, Jin HH, Chu MX, Huang DW, et al. Tissue-specific mRNA expression profiles of GDF9, BMP15, and BMPR1B genes in prolific and non-prolific goat breeds. Czech J Anim Sci. 2015;60(10):452–8. doi: 10.17221/8525-Cjas WOS:000365982300004.

78. Polley S, De S, Batabyal S, Kaushik R, Yadav P, Arora JS, et al. Polymorphism of fecundity genes (BMPR1B, BMP15 and GDF9) in the Indian prolific Black Bengal goat. Small Ruminant Res. 2009;85(2–3):122–9. doi: 10.1016/j.smallrumres.2009.08.004 WOS:000271917600008.

79. Dutta R, Laskar S, Borah P, Kalita D, Das B, Zaman G, et al. Polymorphism and nucleotide sequencing of BMPR1B gene in prolific Assam hill goat. Mol Biol Rep. 2014;41(6):3677–81. doi: 10.1007/s11033-014-3232-4 WOS:000336404500016. 24535267

80. Martin P, Palhière I, Maroteau C, Bardou P, Canale-Tabet K, Sarry J, et al. Author Correction: A genome scan for milk production traits in dairy goats reveals two new mutations in Dgat1 reducing milk fat content. Sci Rep-Uk. 2018;8(1):4060. doi: 10.1038/s41598-018-22118-x 29497092

81. Brito LF, Jafarikia M, Grossi DA, Kijas JW, Porto-Neto LR, Ventura RV, et al. Characterization of linkage disequilibrium, consistency of gametic phase and admixture in Australian and Canadian goats. Bmc Genet. 2015;16:67. WOS:000356769300001. doi: 10.1186/s12863-015-0220-1 26108536

82. Mucha S, Mrode R, MacLaren-Lee I, Coffey M, Conington J. Estimation of genomic breeding values for milk yield in UK dairy goats. J Dairy Sci. 2015;98(11):8201–8. doi: 10.3168/jds.2015-9682 26342984.

83. Badke YM, Bates RO, Ernst CW, Schwab C, Steibel JP. Estimation of linkage disequilibrium in four US pig breeds. Bmc Genomics. 2012;13:24. doi: 10.1186/1471-2164-13-24 22252454; PubMed Central PMCID: PMC3269977.

84. Kijas JW, Porto-Neto L, Dominik S, Reverter A, Bunch R, McCulloch R, et al. Linkage disequilibrium over short physical distances measured in sheep using a high-density SNP chip. Anim Genet. 2014;45(5):754–7. doi: 10.1111/age.12197 25040320.

85. Qanbari S, Pimentel EC, Tetens J, Thaller G, Lichtner P, Sharifi AR, et al. The pattern of linkage disequilibrium in German Holstein cattle. Anim Genet. 2010;41(4):346–56. doi: 10.1111/j.1365-2052.2009.02011.x 20055813.

86. Du FX, Clutter AC, Lohuis MM. Characterizing linkage disequilibrium in pig populations. International journal of biological sciences. 2007;3(3):166–78. doi: 10.7150/ijbs.3.166 17384735; PubMed Central PMCID: PMC1802018.

87. Meadows JRS, Chan EKF, Kijas JW. Linkage disequilibrium compared between five populations of domestic sheep. Bmc Genet. 2008;9:61. Artn 6110.1186/1471-2156-9-61. WOS:000260658300001. doi: 10.1186/1471-2156-9-61 18826649

88. Meuwissen T. Genetic management of small populations: A review. Acta Agr Scand a-An. 2009;59(2):71–9. Pii 91353833410.1080/09064700903118148. WOS:000268709600001.

89. Sardina MT, Tortorici L, Mastrangelo S, Di Gerlando R, Tolone M, Portolano B. Application of microsatellite markers as potential tools for traceability of Girgentana goat breed dairy products. Food Res Int. 2015;74:115–22. doi: 10.1016/j.foodres.2015.04.038 WOS:000358971200012. 28411975

90. Dimauro C, Cellesi M, Steri R, Gaspa G, Sorbolini S, Stella A, et al. Use of the canonical discriminant analysis to select SNP markers for bovine breed assignment and traceability purposes. Anim Genet. 2013;44(4):377–82. WOS:000329200100003. doi: 10.1111/age.12021 23347105

91. Ramos AM, Megens HJ, Crooijmans RPMA, Schook LB, Groenen MAM. Identification of high utility SNPs for population assignment and traceability purposes in the pig using high-throughput sequencing. Anim Genet. 2011;42(6):613–20. WOS:000296325900006. doi: 10.1111/j.1365-2052.2011.02198.x 22035002

92. Kim ES, Elbeltagy AR, Aboul-Naga AM, Rischkowsky B, Sayre B, Mwacharo JM, et al. Multiple genomic signatures of selection in goats and sheep indigenous to a hot arid environment. Heredity. 2016;116(3):255–64. WOS:000371736700002. doi: 10.1038/hdy.2015.94 26555032

93. Armstrong C, Richardson DS, Hipperson H, Horsburgh GJ, Küpper C, Percival-Alwyn L, et al. Genomic associations with bill length and disease reveal drift and selection across island bird populations. Evolution Letters. 2018;2(1):22–36. doi: 10.1002/evl3.38 30283662

94. Bosse M, Spurgin LG, Laine VN, Cole EF, Firth JA, Gienapp P, et al. Recent natural selection causes adaptive evolution of an avian polygenic trait. Science. 2017;358(6361):365–8. WOS:000413251000042. doi: 10.1126/science.aal3298 29051380

95. Frankham R. Genetics and extinction. Biol Conserv. 2005;126(2):131–40. doi: 10.1016/j.biocon.2005.05.002 WOS:000231663000001.

96. Yuan Z, Liu E, Liu Z, Kijas JW, Zhu C, Hu S, et al. Selection signature analysis reveals genes associated with tail type in Chinese indigenous sheep. Anim Genet. 2017;48(1):55–66. WOS:000391943100006. doi: 10.1111/age.12477 27807880

97. Su R, Zhang WG, Sharma R, Chang ZL, Yin J, Li JQ. Characterization of BMP2 gene expression in embryonic and adult Inner Mongolia Cashmere goat (Capra hircus) hair follicles. Can J Anim Sci. 2009;89(4):457–62. WOS:000274002400004.

98. Dunner S, Sevane N, Garcia D, Leveziel H, Williams JL, Mangin B, et al. Genes involved in muscle lipid composition in 15 European Bos taurus breeds. Anim Genet. 2013;44(5):493–501. doi: 10.1111/age.12044 23611291.

99. Xu L, Zhao F, Ren H, Li L, Lu J, Liu J, et al. Co-expression analysis of fetal weight-related genes in ovine skeletal muscle during mid and late fetal development stages. Int J Biol Sci. 2014;10(9):1039–50. doi: 10.7150/ijbs.9737 25285036; PubMed Central PMCID: PMC4183924.

100. Wan L, Ma J, Wang N, Wang D, Xu G. Molecular cloning and characterization of different expression of MYOZ2 and MYOZ3 in Tianfu goat. PloS one. 2013;8(12):e82550. doi: 10.1371/journal.pone.0082550 24367523; PubMed Central PMCID: PMC3867352.

101. Wu XM, Viveiros MM, Eppig JJ, Bai YC, Fitzpatrick SL, Matzuk MM. Zygote arrest 1 (Zar1) is a novel maternal-effect gene critical for the oocyte-to-embryo transition. Nature genetics. 2003;33(2):187–91. WOS:000180773700018. doi: 10.1038/ng1079 12539046

102. Fernandes GA, Costa RB, de Camargo GMF, Carvalheiro R, Rosa GJM, Baldi F, et al. Genome scan for postmortem carcass traits in Nellore cattle. J Anim Sci. 2016;94(10):4087–95. WOS:000388955400004. doi: 10.2527/jas.2016-0632 27898882

103. Tizioto PC, Taylor JF, Decker JE, Gromboni CF, Mudadu MA, Schnabel RD, et al. Detection of quantitative trait loci for mineral content of Nelore longissimus dorsi muscle. Genet Sel Evol. 2015;47:15. WOS:000350951400001. doi: 10.1186/s12711-014-0083-3 25880074

104. Seabury CM, Oldeschulte DL, Saatchi M, Beever JE, Decker JE, Halley YA, et al. Genome-wide association study for feed efficiency and growth traits in US beef cattle. Bmc Genomics. 2017;18(1):386. WOS:000401578600003. doi: 10.1186/s12864-017-3754-y 28521758

105. Kaminski S, Hering DM, Olenski K, Lecewicz M, Kordan W. Genome-wide association study for sperm membrane integrity in frozen-thawed semen of Holstein-Friesian bulls. Anim Reprod Sci. 2016;170:135–40. WOS:000378672900017. doi: 10.1016/j.anireprosci.2016.05.002 27236378


Článek vyšel v časopise

PLOS One


2019 Číslo 12