Maternal and Paternal Genealogy of Eurasian Taurine Cattle (Bos Taurus)
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Heredity (2009) 103, 404–415 & 2009 Macmillan Publishers Limited All rights reserved 0018-067X/09 $32.00 www.nature.com/hdy ORIGINAL ARTICLE Maternal and paternal genealogy of Eurasian taurine cattle (Bos taurus) J Kantanen1, CJ Edwards2, DG Bradley2, H Viinalass3, S Thessler4, Z Ivanova5, T Kiselyova6, MC´ inkulov7, R Popov8, S Stojanovic´9, I Ammosov10 and J Vilkki1 1Biotechnology and Food Research, MTT Agrifood Research Finland, Jokioinen, Finland; 2Smurfit Institute of Genetics, Trinity College, Dublin, Ireland; 3Institute of Veterinary Medicine and Animal Sciences, Estonian University of Life Sciences, Tartu, Estonia; 4Information Management Unit, MTT Agrifood Research Finland, Helsinki, Finland; 5Yakut State Agricultural Academy, Yakutsk, Sakha, Russia; 6Department of Genetics and Biotechnology, All-Russian Research Institute for Farm Animal Genetics and Breeding, St Petersburgh-Pushkin, Russia; 7Animal Science Department, University of Novi Sad, Novi Sad, Serbia; 8Yakutian Research Institute of Agriculture, Yakutsk, Sakha, Russia; 9Division of Agro-Resources, Ministry of Agriculture and Water Management, Beograd, Serbia and 10Batagay-Alyta, Sakha, Russia Maternally inherited mitochondrial DNA (mtDNA) has been frequency in the Eurasian sample set compared with that used extensively to determine origin and diversity of taurine detected in Near Eastern and Anatolian breeds. The taurine Y- cattle (Bos taurus) but global surveys of paternally inherited Y- chromosomal microsatellite haplotypes were found to be chromosome diversity are lacking. Here, we provide mtDNA structured in a network according to the Y-haplogroups Y1 information on previously uncharacterised Eurasian breeds and Y2. These data do not support the recent hypothesis on and present the most comprehensive Y-chromosomal micro- the origin of Y1 from the local European hybridization of cattle satellite data on domestic cattle to date. The mitochondrial with male aurochsen. Compared with mtDNA, the intensive haplogroup T3 was the most frequent, whereas T4 was culling of breeding males and male-mediated crossbreeding of detected only in the Yakutian cattle from Siberia. The mtDNA locally raised native breeds has accelerated loss of Y- data indicates that the Ukrainian and Central Asian regions are chromosomal variation in domestic cattle, and affected the zones where hybrids between taurine and zebu (B. indicus) contribution of genetic drift to diversity. In conclusion, to cattle have existed. This zebu influence appears to have maintain diversity, breeds showing rare Y-haplotypes should subsequently spread into southern and southeastern Eur- be prioritised in the conservation of cattle genetic resources. opean breeds. The most common Y-chromosomal microsa- Heredity (2009) 103, 404–415; doi:10.1038/hdy.2009.68; tellite haplotype, termed here as H11, showed an elevated published online 15 July 2009 Keywords: cattle; bos taurus; mitochondrial DNA; displacement loop; Y-chromosome; microsatellite Introduction 2001; Edwards et al., 2007a). However, in some areas of the Eurasian continent, phenotypically humpless cattle are Analyses of mitochondrial DNA (mtDNA) D-loop se- known to have been influenced by historical admixture quences and Y-chromosome-specific polymorphisms from zebu cattle. One of such cattle breeds is the (such as single nucleotide polymorphisms, insertion– Mongolian cattle, which belong to the so-called Turano- deletion mutations and microsatellites) have indicated Mongolian type of taurine cattle (Mannen et al., 2004; Lai that humpless taurine (Bos taurus) and humped zebu et al., 2006). Turano-Mongolian cattle are typically found cattle (B. indicus) have clearly distinguishable mtDNA and in Eastern Asia and can be distinguished from the Y-chromosomal haplotypic profiles (Loftus et al., 1994; European taurine cattle by their characteristic cranial Bradley et al., 1996; Hanotte et al., 1997; Mannen et al., formation and the shape of the horns (Felius, 1995). 2004; Go¨therstro¨m et al., 2005; Li et al., 2007b). This MtDNA D-loop sequences of the existing taurine cattle observation points towards two independent domestica- breeds are typically converged into five mtDNA hap- tion events from genetically differentiated aurochs logroups: T, T1, T2, T3 and T4 (Troy et al., 2001; Mannen (B. primigenius) populations for the two basic taxa of et al., 2004 but see also; Achilli et al., 2008). In the domestic cattle. The modern European and northern Eurasian continent, the groups T, T1, T2 and T3 have Asian domestic cattle are of humpless taurine type and been found in modern Near Eastern cattle breeds, descend from the aurochs populations domesticated whereas T, T2 and T3 appear in European breeds (Troy 10 000 years ago in the Near Eastern region (Troy et al., et al., 2001). Compared with the modern Near Eastern taurine cattle, European cattle show a higher frequency of T3 and much lower frequencies of T and T2 (Troy et al., Correspondence: Dr J Kantanen, Biotechnology and Food Research, MTT 2001). In East Asia, T and T1 have not been detected in Agrifood Research Finland, 31600 Jokioinen, Finland. E-mail: juha.kantanen@mtt.fi the Turano-Mongolian cattle, whereas T4 has so far only Received 28 July 2008; revised 24 April 2009; accepted 21 May 2009; been found in Asia (Mannen et al., 2004; Lai et al., 2006). published online 15 July 2009 In their recent whole mitochondrial genomic study, MtDNA and Y-chromosome diversity in cattle J Kantanen et al 405 Achilli et al. (2008) suggested that T4-carrying mt A total of 268 male and female individuals from 34 cattle genomes are derived from T3-carrying genomes, which breeds were examined for mtDNA D-loop sequence were captured during domestication in the Near East. polymorphisms: 235 animals from Europe and 33 from Frequency differences in alleles at Y-chromosomal Central and East Asia. A total of 405 bulls, representing microsatellites and in Y-chromosomal microsatellite 54 cattle breeds, were assessed for five Y-chromosomal haplotypes have been found in cattle (Edwards et al., markers: 343 bulls from Europe, 27 from Central and East 2000; Li et al., 2007b), suggesting their applicability for Asia, and 35 from the Near East and Anatolia. The breeds genetic diversity studies of domestic cattle. In addition to examined were from Byelorussia, Denmark, Estonia, the more recent evolutionary events, Y-chromosomal Faroe Islands, Finland, Germany, Iraq, Iceland, Kazaksh- microsatellites may have a potential to identify deeper tan, Latvia, Lithuania, Norway, Poland, the Russian lineages of Y-chromosomes (Bosch et al., 1999). In taurine Federation, Serbia, Sweden, Syria, Turkey, Ukraine and cattle, to date two Y-chromosomal haplogroups Y1 and Uzbekistan (Supplementary Table S1). Y2 have been defined by sequence polymorphisms. The For the analysis of geographical patterns of mtDNA haplogroup Y1 dominates in modern northern and diversity, published taurine mtDNA D-loop sequences of western European breeds, but has not yet been detected breeds originating from northern Europe (Icelandic in Near Eastern samples (Go¨therstro¨m et al., 2005). This cattle, Norwegian Red, Telemark and Western Fjord observation led Go¨therstro¨m et al. to conclude that the Y1 cattle, n ¼ 37), UK (Jersey, n ¼ 7) and the Near East and haplogroup was introduced to northern and western Anatolia (Anatolian Black, East Anatolian Red, South European taurine cattle by prehistoric backcrossing with Anatolian Red, Turkish Grey, Damascus, Iraqi and Kurdi local aurochs bulls, rather than descending from the breeds, n ¼ 35) were included (Troy et al., 2001). With the domesticated Near Eastern aurochs population. addition of this GenBank data, it was possible to achieve Our current knowledge of mtDNA variation of taurine a more global mtDNA dataset, which corresponded cattle in Eurasia is based on studies of European and geographically with the sampling regions of the Near Eastern breeds (Loftus et al., 1994; Bradley et al., Y-chromosome data. 1996; Troy et al., 2001). In recent years, a few East Asian breeds have also been examined (Mannen et al., 2004; Lai et al., 2006). Global surveys on Y-chromosomal poly- Laboratory analysis morphisms in domestic cattle have not been published. The DNA samples of Byelorussian, Ukrainian, Russian, In addition, no previous study has covered the vast area Central Asian and Serbian breeds were extracted from of the Russian Federation, and the distribution of taurine either 6–10 ml blood samples or semen samples by mtDNA haplogroups in the Baltic Sea region is also standard protocols, involving either organic extraction poorly known. The South of the Russian Federation or salt precipitation (Miller et al., 1988; Zadworny and borders archaeological domestication sites from where Kuhnlein, 1990). For the other breeds, DNA was available animals spread across the Russian territory (Epstein and from previous cattle genetic diversity studies (Bradley Mason, 1984; Tapio et al., 2006b). The Eurasian continent et al., 1996; Edwards et al., 2000; Tapio et al., 2006a). is inhabited by a large number of unique cattle breeds, The mtDNA D-loop region was amplified using the like Busha cattle in the Balkan region, Eastern Finncattle primers published in Cymbron et al. (1999). A 25-ml PCR in Northern Europe and Yakutian cattle in the Sahka reaction mixture included 20 pmol of each primer, 200 mM Republic of the Russian Federation. On the basis of of each dNTP, DynaZyme buffer (Finnzymes, Helsinki, autosomal microsatellite data, these breeds have shown Finland), 100 ng of DNA template and 1 U DynaZyme II genetic divergence from modern commercial West DNA polymerase (Finnzymes). A thermo cycling proto- European breeds, such as Black-and-White Holstein- col of 5 min at 94 1C, followed by 30 cycles of 1 min at Friesian and Red-and-White Ayrshire cattle (Li et al., 94 1C, 1 min at 55 1C, 2 min at 72 1C and a final extension 2007a). Yakutian cattle belong to the Turano-Mongolian step (72 1C for 5 min) was applied. Amplified DNA breeds and have adapted to extreme cold climatic products of 375 bp were purified with ExoSAP-IT conditions (Li et al., 2007a; Granberg et al., 2009). method (Amersham Biosciences, UK).