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The effects of recent changes in breeding preferences on maintaining traditional Dutch chicken genomic diversity

Heredity 121, 564–578 (2018) | Download Citation

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Abstract

Traditional Dutch chicken breeds are marginalised breeds of ornamental and cultural-historical importance. In the last decades, miniaturising of existing breeds (so called neo-bantam) has become popular and resulted in alternatives to original large breeds. However, while backcrossing is increasing the neo-bantams homozygosity, genetic exchange between breeders may increase their genetic diversity. We use the 60 K SNP array to characterise the genetic diversity, demographic history, and level of inbreeding of Dutch heritage breeds, and particularly of neo-bantams. Commercial white layers are used to contrast the impact of management strategy on genetic diversity and demography. A high proportion of alleles was found to be shared between large fowls and neo-bantams, suggesting gene flow during neo-bantams development. Population admixture analysis supports these findings, in addition to revealing introgression from neo-bantams of the same breed and of phenotypically similar breeds. The prevalence of long runs of homozygosity (ROH) confirms the importance of recent inbreeding. A high diversity in management, carried out in small breeding units explains the high heterogeneity in diversity and ROH profile displayed by traditional breeds compared to commercial lines. Population bottlenecks may explain the long ROHs in large fowls, while repetitive backcrossing for phenotype selection may account for them in neo-bantams. Our results highlight the importance of using markers to inform breeding programmes on potentially harmful homozygosity to prevent loss of genetic diversity. We conclude that bantamisation has generated unique and identifiable genetic diversity. However, this diversity can only be preserved in the near future through structured breeding programmes.

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References

  1. Alexander DH, Novembre J (2009) Fast model-based rstimation of ancestry in unrelated individuals. Genome Res 19:1655–1664

  2. Behr AA, Liu KZ, Liu-Fang G, Nakka P, Ramachandran S (2016) Pong: fast analysis and visualization of latent clusters in population genetic data. Bioinformatics 32:2817–2823

  3. Berthouly C, Maillard JC, Doan LP, Van TN, Bed’Hom B, Leroy G et al (2010) Revealing fine scale subpopulation structure in the Vietnamese H’mong cattle breed for conservation purposes. BMC Genet 11:45

  4. Bosse M, Megens HJ, Madsen O, Paudel Y, Frantz LAF, Schook LB et al (2012) Regions of homozygosity in the porcine genome: consequence of demography and the recombination landscape. PLoS Genet 8:e1003100

  5. Burt DW (2005) Chicken genome: current status and future opportunities. Genome Res 15:1692–1698

  6. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4:7

  7. Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205

  8. Dana N, Megens HJ, Crooijmans RPMA, Hanotte O, Mwacharo J, Groenen MAM et al (2011) East asian contribution to dutch traditional and western commerical chickens inferred from mtDNA analysis. Anim Genet 42:125–133

  9. Druml T, Salajpal K, Dikie M, Urosevic M, Grilz-Seger G, Baumung R (2012) Genetic diversity, population structure and subdivision of local Balkan pig breeds in Austria, Croatia, Serbia and Bosnia-Herzegovina and its practical value in conservation programs. Genet Sel Evol 44:5

  10. Eding H, Meuwissen T (2001) Marker-based estimates of between and within population kinships for the conservation of genetic diversity. J Anim Breed Genet 118:141–159

  11. Elferink MG, Megens HJ, Vereijken A, Hu X, Crooijmans RPMA, Groenen MAM (2012) Signatures of selection in the genomes of commercial and non-commercial chicken breeds. PLoS ONE 7:e32720

  12. Felsenstein J (2004). PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle

    • Gheyas AA, Boschiero C, Eory L, Ralph H, Kuo R, Woolliams JA et al (2014) Functional classification of 15 million SNPs detected from diverse chicken populations. DNA Res 22:205–217

    • Granevitze Z, Hillel J, Chen GH, Cuc NTK, Feldman M, Eding H et al (2007) Genetic diversity within chicken populations from different continents and management histories. Anim Genet 38:576–583

    • Granevitze Z, Hillel J, Feldman M, Six A, Eding H, Weigend S (2009) Genetic structure of a wide-spectrum chicken gene pool. Anim Genet 40:686–693

    • Groenen MAM, Megens HJ, Zare Y, Warren WC, Hillier LW, Crooijmans RPMA et al (2011) The development and characterization of a 60K SNP chip for chicken. BMC Genom 12:274

    • Groeneveld LF, Lenstra JA, Eding H, Toro MA, Scherf B, Pilling D et al (2010) Genetic diversity in farm animals—a review. Anim Genet 41:6–31

    • Herrero-Medrano JM, Megens HJ, Groenen MAM, Ramis G, Bosse M, Pérez-Enciso M et al (2013) Conservation genomic analysis of domestic and wild pig populations from the Iberian Peninsula. BMC Genet 14:106

    • Hillel J, Groenen MAM, Tixier-Boichard M, Korol AB, David L, Kirzhner V et al (2003) Biodiversity of 52 chicken populations assessed by microsatellite typing of DNA pools. Genet Sel Evol 35:533–557

    • Howrigan DP, Simonson MA, Keller MC (2011) Detecting autozygosity through runs of homozygosity: a comparison of three autozygosity detection algorithms. BMC Genom 12:460

    • Kanginakudru S, Metta M, Jakati RD, Nagaraju J (2008) Genetic evidence from Indian red jungle fowl corroborates multiple domestication of modern day chicken. BMC Evol Biol 8:174

    • Kim ES, Cole JB, Huson H, Wiggans GR, Van Tassel CP, Crooker BA et al (2013) Effect of artificial selection on runs of homozygosity in U.S. Holstein cattle. PLoS ONE 8:1–14

    • Liu YP, Wu GS, Yao YG, Miao YW, Luikart G, Baig M et al (2006) Multiple maternal origins of chickens: out of the Asian jungles. Mol Phylogenet Evol 38:12–19

    • Van Marle-Köster E, Hefer CA, Nel LH, Groenen MAM (2008) Genetic diversity and population structure of locally adapted South African chicken lines: Implications for conservation. South Afr J Anim Sci 38:271–281

    • Van Marle-Koster E, Nel LH (2000) Genetic characterization of native southern African chicken populations: evaluation and selection of polymorphic microsatellite markers. S Afr J Anim Sci 30:1–6

    • McQuillan R, Leutenegger AL, Abdel-Rahman R, Franklin CS, Pericic M, Barac-Lauc L et al (2008) Runs of Homozygosity in European Populations. Am J Hum Genet 83:359–372

    • Miao YW, Peng MS, Wu GS, Ouyang YN, Yang ZY, Yu N et al (2013) Chicken domestication: an updated perspective based on mitochondrial genomes. Heredity 110:277–282

    • Miyamoto N, Fernández-Manjarrés JF, Morand-prieur M-E, Bertolino P, Frascaria-Lacoste N (2008) What sampling is needed for reliable estimations of genetic diversity in Fraxinus excelsior L. (Oleaceae)? Ann Sci 65:403–403

    • Mtileni BJ, Muchadeyi FC, Maiwashe A, Groeneveld E, Groeneveld LF, Dzama K et al (2011) Genetic diversity and conservation of South African indigenous chicken populations. J Anim Breed Genet 128:209–218

    • Muir WM, Wong GKS, Zhang Y, Wang J, Groenen MAM, Crooijmans RPMA et al (2008) Genome-wide assessment of worldwide chicken SNP genetic diversity indicates significant absence of rare alleles in commercial breeds. Proc Natl Acad Sci USA 105:17312–17317

    • Pham MH, Berthouly-Salazar C, Tran XH, Chang WH, Crooijmans RPMA, Lin DY et al (2013) Genetic diversity of Vietnamese domestic chicken populations as decision-making support for conservation strategies. Anim Genet 44:509–521

    • Pickrell JK, Pritchard JK (2012) Inference of population splits and mixtures from genome-wide allele frequency data PLoS Genet 8:e1002967

    • Pruett CL, Winker K, Pruett CL, Winker K (2008) The effects of sample size on population genetic diversity estimates in song sparrows Melospiza melodia. J Avian Biol J Compil 39:252–256

    • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575

    • Purfield DC, Berry DP, McParland S, Bradley DG (2012) Runs of homozygosity and population history in cattle. BMC Genet 13:70

    • Reich D, Thangaraj KKK, Patterson N, Price AL, Singh L (2009) Reconstructing Indian Population History. Nature 461:489–494

    • Rubin C-J, Zody MC, Eriksson J, Meadows JRS, Sherwood E, Webster MT et al (2010) Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464:587–591

    • Szpiech ZA, Xu J, Pemberton TJ, Peng W, Zöllner S, Rosenberg NA et al (2013) Long runs of homozygosity are enriched for deleterious variation. Am J Hum Genet 93:90–102

    • Tadano R, Nishibori M, Imamura Y, Matsuzaki M, Kinoshita K, Mizutani M et al (2008) High genetic divergence in miniature breeds of Japanese native chickens compared to Red Junglefowl, as revealed by microsatellite analysis. Anim Genet 39:71–78

    • Team RC (2008) R: A Language and Environment for Statistical Computing.

      • Tixier-Boichard M, Bed’Hom B, Rognon X (2011) Chicken domestication: from archeology to genomics. Comptes Rendus - Biol 334:197–204

      • Toro MA, Fernández J, Caballero A (2009) Molecular characterization of breeds and its use in conservation. Livest Sci 120:174–195

      • Wilkinson S, Wiener P, Teverson D, Haley CS, Hocking PM (2012) Characterization of the genetic diversity, structure and admixture of British chicken breeds. Anim Genet 43:552–563

      • Woelders H, Zuidberg CA, Hiemstra SJ (2006) Animal genetic resources conservation in the Netherlands and Europe: poultry perspective. Poult Sci 85:216–222

      • Zanetti E, De Marchi M, Dalvit C, Cassandro M (2010) Genetic characterization of local Italian breeds of chickens undergoing in situ conservation. Poult Sci 89:420–7

      • Zheng X, Levine D, Shen J, Gogarten SM, Laurie C, Weir BS (2012) A high-performance computing toolset for relatedness and principal component analysis of SNP data. Bioinformatics 28:3326–3328

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      Acknowledgements

      We would like to acknowledge the owners and breed associations of the chicken populations used in this study for their help and cooperation during sampling. We would also like to thank the Centre for Genetic Resources for providing some of the samples used in this study. The research leading to some of these results has been conducted as part of the IMAGE project, which received funding from the European Union’s Horizon 2020 Research and Innovation Programme under the Grant Agreement No. 677353.

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      Affiliations

      1. Animal Breeding and Genetics Group, Wageningen University & Research, Wageningen, The Netherlands

        • Chiara Bortoluzzi
        • , Richard P. M. A. Crooijmans
        • , Mirte Bosse
        • , Martien A. M. Groenen
        •  & Hendrik-Jan Megens

      2. Centre for Genetic Resources (CGN), Wageningen University & Research, Wageningen, The Netherlands

        • Sipke Joost Hiemstra

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      The authors declare that they have no conflict of interest.

      Corresponding author

      Correspondence to Chiara Bortoluzzi.

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      https://doi.org/10.1038/s41437-018-0072-3