BACKGROUND: In the Neolithic, domestic sheep migrated into Europe and subsequently spread in westerly and northwesterly directions. Reconstruction of these migrations and subsequent genetic events requires a more detailed characterization of the current phylogeographic differentiation. RESULTS: We collected 50 K single nucleotide polymorphism (SNP) profiles of Balkan sheep that are currently found near the major Neolithic point of entry into Europe, and combined these data with published genotypes from southwest-Asian, Mediterranean, central-European and north-European sheep and from Asian and European mouflons. We detected clines, ancestral components and admixture by using variants of common analysis tools: geography-informative supervised principal component analysis (PCA), breed-specific admixture analysis, across-breed [Formula: see text] profiles and phylogenetic analysis of regional pools of breeds. The regional Balkan sheep populations exhibit considerable genetic overlap, but are clearly distinct from the breeds in surrounding regions. The Asian mouflon did not influence the differentiation of the European domestic sheep and is only distantly related to present-day sheep, including those from Iran where the mouflons were sampled. We demonstrate the occurrence, from southeast to northwest Europe, of a continuously increasing ancestral component of up to 20% contributed by the European mouflon, which is assumed to descend from the original Neolithic domesticates. The overall patterns indicate that the Balkan region and Italy served as post-domestication migration hubs, from which wool sheep reached Spain and north Italy with subsequent migrations northwards. The documented dispersal of Tarentine wool sheep during the Roman period may have been part of this process. Our results also reproduce the documented 18th century admixture of Spanish Merino sheep into several central-European breeds. CONCLUSIONS: Our results contribute to a better understanding of the events that have created the present diversity pattern, which is relevant for the management of the genetic resources represented by the European sheep population.

AgResearch Invermay Agricultural Centre Mosgiel New Zealand

Biotechical Faculty Podgorica Montenegro

College of Animal Science and Technology China Agricultural University Beijing China

Department of Animal Production Faculty of Agriculture and Environment Agricultural University ofTirana Tirana Albania

Department of Animal Science Biotechnical Faculty University of Ljubljana Ljubljana Slovenia

Department of Animal Science University of Zagreb Zagreb Croatia

Department of Genetics Physical Anthropology and Animal Physiology University of Basque Country Leioa Spain

Department of Reproduction and Biomedicine Faculty of Veterinary Medicine Ss Cyril and Methodius University Skopje North Macedonia

Dipartamento Bioscienze Biotecnologie Biofarmaceutica Universita degli Studi di Bari Aldo Moro Bari Italy

Dipartamento Scienze Agroalimentari Ambientali e Animali Universita Udine Udine Italy

Dipartimento di Scienze Animali della Nutrizione e degli Alimenti Universita Cattolica del S Cuore di Piacenza Piacenza Italy

Dipartimento Scienze Agrarie Alimentari e Forestali Universita Studi di Palermo Palermo Italy

Estonian University of Life Sciences Tartu Estonia

Faculty of Agriculture and Natural Resources Arak University Arak Iran

Faculty of Veterinary Medicine Utrecht University Utrecht The Netherlands

Institute of Animal Husbandry Belgrade Zemun Belgrade Serbia

Roslin Institute and Royal School of Veterinary Studies University of Edinburgh Midlothian Scotland UK

State Veterinary Institute Jihlava Jihlava Czech Republic

Université de Limoges INRAE Pereine EA7500 USC1061 Gamaa 87000 Limoges France

See more in PubMed

Larson G, Burger J. A population genetics view of animal domestication. Trends Genet. 2013;29:197–205. PubMed

Vila E, Helmer D. The expansion of sheep herding and the development of wool production in the ancient Near East: an archaeozoological and iconographical approach. In: Breniquet C, Cecile M, editors. Wool economy in the ancient near East and the Aegean. Oxford: Oxbow Books; 2014. pp. 22–40.

Frayn JM. Sheep-rearing and the wool trade in Italy during the Roman period. Liverpool: Francis Cairns; 1984.

Flohr M. The wool economy in Roman Italy. In: Droß-Krüpe K, Nosch ML, editors. Text trade and theories: from the ancient near east to the Mediterranean. Munich: Ugarit Verlag; 2016. p 49–62. https://www.academia.edu/29718525/The_Wool_Economy_of_Roman_Italy.

Munro JH. Medieval woollens: the Western European woollen industries and their struggles for international markets, c. 1000–1500. In: Jenkins DT, editor. The Cambridge history of western textiles. Cambridge: Cambridge University Press; 2003. pp. 229–324.

FAO. The second report on the state of World’s Animal Genetic Resources for Food and Agriculture. Scherf BD, Pilling D, editors. Rome: FAO Commission on Genetic Resources for Food and Agriculture; 2015. http://www.fao.org/3/a-i4787e/index.html.

Peters J, Helmer D, Von Den Driesch A, Saña Segui M. Early animal husbandry in the Northern Levant. Paléorient. 1999;25:1–223.

Rowley-Conwy P, Gourichin L, Helmer D, Vigne JD. Early domestic animals in Italy, Istria, the Tyrrhenian islands and southern France. In: Colledge S, Conolly J, Dobney K, Manning K, Shennan S, editors. The origins and spread of domestic animals in Southwest Asia and Europe. New York: Routledge; 2013. pp. 161–194.

Cymbron T, Freeman AR, Malheiro MI, Vigne JD, Bradley DG. Microsatellite diversity suggests different histories for Mediterranean and Northern European cattle populations. Proc Biol Sci. 2005;272:1837–1843. PubMed PMC

Tresset A, Vigne J-D. Substitution of species, techniques and symbols at the Mesolithic-Neolithic transition in Western Europe. Proc Br Acad. 2007;144:189–210.

Rivollat M, Mendisco F, Pemonge MH, Safi A, Saint-Marc D, Brémond A, et al. When the waves of European neolithization met: first paleogenetic evidence from early farmers in the Southern Paris Basin. PLoS One. 2015;10:e0125521. PubMed PMC

de Vareilles A, Bouby L, Jesus A, Martin L, Rottoli M, Vander Linden M, et al. One sea but many routes to Sail. The early maritime dispersal of Neolithic crops from the Aegean to the western Mediterranean. J Archaeol Sci Rep. 2020;29:102140.

Davison K, Dolukhanov PM, Sarson GR, Shukurov A. Environmental effects on the spread of the Neolithic. 2005; arXiv:q-bio/0505013.

Ryder ML. Sheep. In: Mason IL, editor. Evolution of domesticated animals. London: Longman; 1984. pp. 63–85.

Chessa B, Pereira F, Arnaud F, Amorim A, Goyache F, Mainland I, et al. Revealing the history of sheep domestication usingretrovirus integrations. Science. 2009;324:532–536. PubMed PMC

Ryder ML. Medieval sheep and wool types (Britain) Agric Hist Rev. 1964;12:65–82.

Columella LIM. De re rustica. 1472; Book VII.

Plinius G. Historia Naturalis. Book VIII. p. 190–3.

Rochus CM, Tortereau F, Plisson-Petit F, Restoux G, Moreno-Romieux C, Tosser-Klopp G, et al. Revealing the selection history of adaptive loci using genome-wide scans for selection: an example from domestic sheep. BMC Genomics. 2018;19:71. PubMed PMC

Ciani E, Lasagna E, D’Andrea M, Alloggio I, Marroni F, Ceccobelli S, et al. Merino and Merino-derived sheep breeds: a genome-wide intercontinental study. Genet Sel Evol. 2015;47:64. PubMed PMC

Wood RJ, Orel V. Genetic prehistory in selective breeding: a prelude to Mendel. Oxford: Oxford University Press; 2001.

Kijas JW, Lenstra JA, Hayes B, Boitard S, Neto LR, SanCristobal 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:e1001258. PubMed PMC

Costello E, Svensson E. Historical archaeologies of transhumance across Europe. New York: Routledge; 2018.

Burren A, Signer-Hasler H, Neuditschko M, Tetens J, Kijas J, Drögemüller C, et al. Fine-scale population structure analysis of seven local Swiss sheep breeds using genome-wide SNP data. Anim Genet Resour Genet. 2014;55:67–76.

Ciani E, Crepaldi P, Nicoloso L, Lasagna E, Sarti FM, Moioli B, et al. Genome-wide analysis of Italian sheep diversity reveals a strong geographic pattern and cryptic relationships between breeds. Anim Genet. 2014;45:256–266. PubMed

Mastrangelo S, Portolano B, Di Gerlando R, Ciampolini R, Tolone M, Sardina MT. Genome-wide analysis in endangered populations: a case study in Barbaresca sheep. Animal. 2017;11:1107–1116. PubMed

Mastrangelo S, Di Gerlando R, Tolone M, Tortorici L, Sardina MT, Portolano B. Genome wide linkage disequilibrium and genetic structure in Sicilian dairy sheep breeds. BMC Genet. 2014;15:108. PubMed PMC

Meyermans R, Gorssen W, Janssens S, Wijnrocx K, Lenstra JA, Buys N. Unraveling the genetic diversity of Belgian milk Sheep using medium-density SNP genotypes. Anim Genet. 2019;51:258–265. PubMed PMC

Legarra A, Baloche G, Barillet F, Astruc JM, Soulas C, Aguerre X, et al. Within- and across-breed genomic predictions and genomic relationships for Western Pyrenees dairy sheep breeds Latxa, Manech, and Basco-Béarnaise. J Dairy Sci. 2014;97:3200–3212. PubMed

Manunza A, Cardoso TF, Noce A, Martínez A, Pons A, Bermejo LA, et al. Population structure of eleven Spanish ovine breeds and detection of selective sweeps with BayeScan and hapFLK. Sci Rep. 2016;6:27296. PubMed PMC

Michailidou S, Tsangaris G, Fthenakis GC, Tzora A, Skoufos I, Karkabounas SC, et al. Genomic diversity and population structure of three autochthonous Greek sheep breeds assessed with genome-wide DNA arrays. Mol Genet Genomics. 2018;293:753–768. PubMed

Beynon SE, Slavov GT, Farré M, Sunduimijid B, Waddams K, Davies B, et al. Population structure and history of the Welsh sheep breeds determined by whole genome genotyping. BMC Genet. 2015;16:65. PubMed PMC

Deniskova TE, Dotsev AV, Selionova MI, Kunz E, Medugorac I, Reyer H, et al. Population structure and genetic diversity of 25 Russian sheep breeds based on whole-genome genotyping. Genet Sel Evol. 2018;50:29. PubMed PMC

Gorkhali NA, Dong K, Yang M, Song S, Kader A, Shrestha BS, et al. Genomic analysis identified a potential novel molecular mechanism for high-altitude adaptation in sheep at the Himalayas. Sci Rep. 2016;6:29963. PubMed PMC

Zhao YX, Yang J, Lv FH, Hu XJ, Xie XL, Zhang M, et al. Genomic reconstruction of the history of native sheep reveals the peopling patterns of nomads and the expansion of early Pastoralism in East Asia. Mol Biol Evol. 2017;34:2380–2395. PubMed PMC

Liu Z, Ji Z, Wang G, Chao T, Hou L, Wang J. Genome-wide analysis reveals signatures of selection for important traits in domestic sheep from different ecoregions. BMC Genomics. 2016;17:863. PubMed PMC

Moradi MH, Nejati-Javaremi A, Moradi-Shahrbabak M, Dodds KG, McEwan JC. Genomic scan of selective sweeps in thin and fat tail sheep breeds for identifying of candidate regions associated with fat deposition. BMC Genet. 2012;13:10. PubMed PMC

Belabdi I, Ouhrouch A, Lafri M, Gaouar SBS, Ciani E, Benali AR, et al. Genetic homogenization of indigenous sheep breeds in Northwest Africa. Sci Rep. 2019;9:7920. PubMed PMC

Ben Jemaa S, Kdidi S, Gdura AM, Dayhum AS, Eldaghayes IM, Boussaha M, et al. Inferring the population structure of the Maghreb sheep breeds using a medium-density SNP chip. Anim Genet. 2019;50:526–533. PubMed

Molotsi AH, Taylor JF, Cloete SWP, Muchadeyi F, Decker JE, Whitacre LK, et al. Genetic diversity and population structure of South African smallholder farmer sheep breeds determined using the OvineSNP50 beadchip. Trop Anim Health Prod. 2017;49:1771–1777. PubMed

Edea Z, Dessie T, Dadi H, Do KT, Kim KS. Genetic diversity and population structure of Ethiopian sheep populations revealed by high-density SNP markers. Front Genet. 2017;8:218. PubMed PMC

Ahbara A, Bahbahani H, Almathen F, Al Abri M, Agoub MO, Abeba A, et al. Genome-wide variation, candidate regions and genes associated with fat deposition and tail morphology in Ethiopian indigenous sheep. Front Genet. 2019;10:699. PubMed PMC

Brito LF, McEwan JC, Miller SP, Pickering NK, Bain WE, Dodds KG, et al. Genetic diversity of a New Zealand multi-breed sheep population and composite breeds’ histry revealed by a high-density SNP chip. BMC Genet. 2017;18:25. PubMed PMC

Spangler GL, Rosen BD, Ilori MB, Hanotte O, Kim ES, Sonstegard TS, et al. Whole genome structural analysis of Caribbean hair sheep reveals quantitative link to West African ancestry. PLoS One. 2017;12:e0179021. PubMed PMC

Lv FH, Agha S, Kantanen J, Colli L, Stucki S, Kijas JW, et al. Adaptations to climate-mediated selective pressures in sheep. Mol Biol Evol. 2014;31:3324–3343. PubMed PMC

Barbato M, Hailer F, Orozco-Terwengel P, Kijas J, Mereu P, Cabras P, et al. Genomic signatures of adaptive introgression from European mouflon into domestic sheep. Sci Rep. 2017;7:7623. PubMed PMC

Porter V, Alderson L, Hall SJG, Sponenberg DP. Mason’s world encyclopedia of livestock breeds and breeding. Wallingford: CABI Publishing; 2016.

Huson DH, Bryant D. Application of phylogenetic networks in evolutionary studies. Mol Biol Evol. 2006;23:254–267. PubMed

Malomane DK, Reimer C, Weigend S, Weigend A, Sharifi AR, Simianer H. Efficiency of different strategies to mitigate ascertainment bias when using SNP panels in diversity studies. BMC Genomics. 2018;19:22. PubMed PMC

Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19:1655–1664. PubMed PMC

Mastrangelo S, Ciani E, Sardina MT, Sottile G, Pilla F, Portolano B. Runs of homozygosity reveal genome-wide autozygosity in Italian sheep breeds. Anim Genet. 2018;49:71–81. PubMed

O’Connell J, Gurdasani D, Delaneau O, Pirastu N, Ulivi S, Cocca M, et al. A general approach for haplotype phasing across the full spectrum of relatedness. PLoS Genet. 2014;10:e1004234. PubMed PMC

Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet. 2012;8:e1002453. PubMed PMC

Jombart T, Devillard S, Dufour AB, Pontier D. Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity (Edinb). 2008;101:92–103. PubMed

Kuo YH, Vanderzwan SL, Kasprowicz AE, Sacks BN. Using ancestry-informative SNPs to quantify introgression of European alleles into North American red foxes. J Hered. 2019;110:782–792. PubMed

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155:945–959. PubMed PMC

Patterson N, Moorjani P, Luo Y, Mallick S, Rohland N, Zhan Y, et al. Ancient admixture in human history. Genetics. 2012;192:1065–1093. PubMed PMC

Pickrell JK, Pritchard JK. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 2012;8:e1002967. PubMed PMC

Alberto FJ, Boyer F, Orozco-Terwengel P, Streeter I, Servin B, De Villemereuil P, et al. Convergent genomic signatures of domestication in sheep and goats. Nat Commun. 2018;9:813. PubMed PMC

Naval-Sanchez M, Nguyen Q, McWilliam S, Porto-Neto LR, Tellam R, Vuocolo T, et al. Sheep genome functional annotation reveals proximal regulatory elements contributed to the evolution of modern breeds. Nat Commun. 2018;9:859. PubMed PMC

Benjelloun B, Boyer F, Streeter I, Zamani W, Engelen S, Alberti A, et al. An evaluation of sequencing coverage and genotyping strategies to assess neutral and adaptive diversity. Mol Ecol Resour. 2019;19:1497–1515. PubMed PMC

Upadhyay MR, Chen W, Lenstra JA, Goderie CRJ, Machugh DE, Park SDE, et al. Genetic origin, admixture and population history of aurochs (Bos primigenius) and primitive European cattle. Heredity (Edinb). 2017;118:169–176. PubMed PMC

Kijas JW, Serrano M, McCulloch R, Li Y, Salces Ortiz J, Calvo JH, et al. Genomewide association for a dominant pigmentation gene in sheep. J Anim Breed Genet. 2013;130:468–475. PubMed

Colli L, Milanesi M, Talenti A, Bertolini F, Chen M, Crisà 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;50:58. PubMed PMC

Decker JE, McKay SD, Rolf MM, Kim JW, Molina Alcalá A, Sonstegard TS, et al. Worldwide patterns of ancestry, divergence, and admixture in domesticated cattle. PLoS Genet. 2014;10:e1004254. PubMed PMC

Yang J, Li WR, Lv FH, He SG, Tian SL, Peng WF, et al. Whole-genome sequencing of native sheep provides insights into rapid adaptations to extreme environments. Mol Biol Evol. 2016;33:2576–2592. PubMed PMC

Porto Neto LR, Barendse W. Effect of SNP origin on analyses of genetic diversity in cattle. Anim Prod Sci. 2010;50:792–800.

Moioli B, Pilla F, Ciani E. Signatures of selection identify loci associated with fat tail in sheep. J Anim Sci. 2015;93:4660–4669. PubMed

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;48:55–66. PubMed

Xu SS, Ren X, Yang GL, Xie XL, Zhao YX, Zhang M, et al. Genome-wide association analysis identifies the genetic basis of fat deposition in the tails of sheep (Ovis aries) Anim Genet. 2017;48:560–569. PubMed

Mastrangelo S, Bahbahani H, Moioli B, Ahbara A, Abri A, Almathen F, et al. Novel and known signals of selection for fat deposition in domestic sheep breeds from Africa and Eurasia. PLoS One. 2019;14:e0209632. PubMed PMC

Zhi D, Da L, Liu M, Cheng C, Zhang Y, Wang X, et al. Whole genome sequencing of Hulunbuir short-tailed sheep for identifying candidate genes related to the short-tail phenotype. G3 (Bethesda) 2018;8:377–383. PubMed PMC

Gutiérrez-Gil B, Esteban-Blanco C, Wiener P, Chitneedi PK, Suarez-Vega A, Arranz JJ. High-resolution analysis of selection sweeps identified between fine-wool Merino and coarse-wool Churra sheep breeds. Genet Sel Evol. 2017;49:81. PubMed PMC

Demars J, Cano M, Drouilhet L, Plisson-Petit F, Bardou P, Fabre S, et al. Genome-wide identification of the mutation underlying fleece variation and discriminating ancestral hairy species from modern woolly sheep. Mol Biol Evol. 2017;34:1722–1729. PubMed PMC

Meadows JRS, Kijas JW. Re-sequencing regions of the ovine Y chromosome in domestic and wild sheep reveals novel paternal haplotypes. Anim Genet. 2009;40:119–123. PubMed

Våge DI, Husdal M, Kent MP, Klemetsdal G, Boman IA. A missense mutation in growth differentiation factor 9 (GDF9) is strongly associated with litter size in sheep. BMC Genet. 2013;14:1. PubMed PMC

Jombart T, Devillard S, Balloux F. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 2010;11:95. PubMed PMC

Genomic signatures of selection, local adaptation and production type characterisation of East Adriatic sheep breeds

Identification of Selection Signals on the X-Chromosome in East Adriatic Sheep: A New Complementary Approach

Whole-Genome Resequencing of Worldwide Wild and Domestic Sheep Elucidates Genetic Diversity, Introgression, and Agronomically Important Loci