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Genomic Diversity and Population Structure of the Indigenous Greek and Cypriot Cattle Populations Dimitris Papachristou, Panagiota Koutsouli, George P

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Genomic Diversity and Population Structure of the Indigenous Greek and Cypriot Cattle Populations Dimitris Papachristou, Panagiota Koutsouli, George P Genomic diversity and population structure of the indigenous Greek and Cypriot cattle populations Dimitris Papachristou, Panagiota Koutsouli, George P. Laliotis, Elisabeth Kunz, Maulik Upadhyay, Doris Seichter, Ingolf Russ, Bunevski Gjoko, Nikolaos Kostaras, Iosif Bizelis, et al. To cite this version: Dimitris Papachristou, Panagiota Koutsouli, George P. Laliotis, Elisabeth Kunz, Maulik Upadhyay, et al.. Genomic diversity and population structure of the indigenous Greek and Cypriot cattle pop- ulations. Genetics Selection Evolution, BioMed Central, 2020, 52 (1), pp.43. 10.1186/s12711-020- 00560-8. hal-02910744 HAL Id: hal-02910744 https://hal.archives-ouvertes.fr/hal-02910744 Submitted on 3 Aug 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Papachristou et al. Genet Sel Evol (2020) 52:43 https://doi.org/10.1186/s12711-020-00560-8 Genetics Selection Evolution RESEARCH ARTICLE Open Access Genomic diversity and population structure of the indigenous Greek and Cypriot cattle populations Dimitris Papachristou1, Panagiota Koutsouli1, George P. Laliotis1, Elisabeth Kunz2, Maulik Upadhyay2, Doris Seichter3, Ingolf Russ3, Bunevski Gjoko4, Nikolaos Kostaras5, Iosif Bizelis1 and Ivica Medugorac2* Abstract Background: The indigenous cattle populations from Greece and Cyprus have decreased to small numbers and are currently at risk of extinction due to socio-economic reasons, geographic isolation and crossbreeding with commer- cial breeds. This study represents the frst comprehensive genome-wide analysis of 10 indigenous cattle populations from continental Greece and the Greek islands, and one from Cyprus, and compares them with 104 international breeds using more than 46,000 single nucleotide polymorphisms (SNPs). Results: We estimated several parameters of genetic diversity (e.g. heterozygosity and allelic diversity) that indicated a severe loss of genetic diversity for the island populations compared to the mainland populations, which is mainly due to the declining size of their population in recent years and subsequent inbreeding. This high inbreeding status also resulted in higher genetic diferentiation within the Greek and Cyprus cattle group compared to the remaining geographical breed groups. Supervised and unsupervised cluster analyses revealed that the phylogenetic patterns in the indigenous Greek breeds were consistent with their geographical origin and historical information regarding crosses with breeds of Anatolian or Balkan origin. Cyprus cattle showed a relatively high indicine ancestry. Greek island populations are placed close to the root of the tree as defned by Gir and the outgroup Yak, whereas the mainland breeds share a common historical origin with Buša. Unsupervised clustering and D-statistics analyses provided strong support for Bos indicus introgression in almost all the investigated local cattle breeds along the route from Anatolia up to the southern foothills of the Alps, as well as in most cattle breeds along the Apennine peninsula to the southern foothills of the Alps. Conclusions: All investigated Cyprus and Greek breeds present complex mosaic genomes as a result of historical and recent admixture events between neighbor and well-separated breeds. While the contribution of some mainland breeds to the genetic diversity pool seems important, some island and fragmented mainland breeds sufer from a severe decline of population size and loss of alleles due to genetic drift. Conservation programs that are a compro- mise between what is feasible and what is desirable should focus not only on the still highly diverse mainland breeds but also promote and explore the conservation possibilities for island breeds. Background Cattle is a species that is present worldwide and well adapted to diverse environments, and has evolved into *Correspondence: [email protected] 2 Population Genomics Group, Department of Veterinary Sciences, LMU the most important species for production purposes Munich, Lena-Christ-Str. 48, 82152 Martinsried, Germany since its domestication. Te presence of cattle was inval- Full list of author information is available at the end of the article uable in the evolution of human societies with a great © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Papachristou et al. Genet Sel Evol (2020) 52:43 Page 2 of 23 impact on agricultural development, diet alterations, cattle populations since 1950. After the 1960s, with the cultural heritage and social structure [1, 2]. Molecular implementation of artifcial insemination, many indig- evidence [3] has indicated two domestication events in enous populations were crossbred with highly selected cattle from which the taurine (Bos taurus) and indicine commercial breeds [18, 19]. For example, Brachyceros, (Bos indicus) species arose, sharing the aurochs (Bos which is a Greek autochthonous breed with short horns primigenius) as common ancestor ~ 250,000 years ago resembling the Albanian and Buša cattle, was crossed [4]. During the introduction of domesticated cattle into with Swiss Brown in some regions [20]. In the mid- Europe, the Mediterranean coast played a crucial role dle of the 20th century, eight indigenous cattle breeds [2, 5]. Terefore, Greece and Cyprus, which are closely were reported in Greece. Nowadays, four of these are located to the core region of the domestication of cattle, considered as ofcially extinct (Tinos, Andros, Chios, i.e. in the near East, represented an important crossroad Kerkyra), three as threatened (Brachyceros, Katerini for the dispersion of human groups and their herds from and Sykia) and one (Kea) as a rare breed [21, 22]. Te Anatolia towards Europe [6–8]. aforementioned breeds were mainly bred in mountain- Historically, the Southern Balkan peninsula has been ous regions and/or on islands with poor infrastructure. characterized by the free movement of humans and ani- Te latter combined with geographical and natural bar- mals, especially in the areas near the current borders, riers as well as the absence of artifcial insemination led from almost the Neolithic throughout Antiquity, the to reproductive isolation, fragmentation, and gradual Roman, Byzantine and Ottoman empire times to nearly depletion of the genetic diversity in these breeds [23]. 40 years before the present [6, 9]. Pastoralism, the sea- Genetic diversity studies during the past years have sonal movement of herds and people to exploit the graz- been conducted in a large number of domestic cat- ing lands across the Balkan region, is a common practice tle breeds [13, 24–30]. Improving our knowledge on since centuries [10, 11]. Migration events that enhanced the genetic diversity within and among local breeds is the gene fow among the domesticated cattle populations, considered an issue of crucial importance for enhanc- genetic drift, physical isolation due to geographic barriers ing their efcient use with regard to sustainable animal [12] during the above historic periods, and human weak farming in a harsh and less intensifed environment, selection pressures led to the formation of well-adapted and for implementing further conservation programs local cattle breeds in rather marginal and harsh environ- [31]. Since the indigenous breeds exhibit adaptive abil- ments [6, 13]. ity to their local environment and remarkable longevity, Te farming and breeding practices associated with the genetic pool of unselected local breeds can repre- these local breeds difer substantially from those in high- sent a valuable source of genes [32]. However, with a performing breeds [14]: (i) they are fairly undiferentiated few exceptions [33, 34], little research has been carried and unselected; (ii) pedigree records are incomplete or do out on the genetic diversity and genetic relationships of not exist; (iii) breeding associations either do not exist or indigenous cattle from South East Europe with regard are recently established for conservation purposes only; to Greece and Cyprus. (iv) accordingly, there are no classical breed standards Tus, using
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