Scholarly article on topic 'Uniparental genetic systems: a male and a female perspective in the domestic cattle origin and evolution'

Uniparental genetic systems: a male and a female perspective in the domestic cattle origin and evolution Academic research paper on "Biological sciences"

Share paper
Academic journal
Electronic Journal of Biotechnology
OECD Field of science
{"Animal breeding" / "Bovine domestication" / "Cattle genetic diversity" / "Genetic resources" / "Genome-assisted selection" / "Inherited marker systems"}

Abstract of research paper on Biological sciences, author of scientific article — Piera Di Lorenzo, Hovirag Lancioni, Simone Ceccobelli, Ludovica Curcio, Francesco Panella, et al.

Abstract Over the last 20years, the two uniparentally inherited marker systems, namely mitochondrial DNA and Y chromosome have been widely employed to solve questions about origin and prehistorical range expansions, demographic processes, both in humans and domestic animals. The mtDNA and the Y chromosome, with their unique patterns of inheritance, continue to be extremely important source of information. These markers played significant roles in farm animals in the evaluation of the genetic variation within- and among-breed strains and lines and have widely applied in the fields of linkage mapping, paternity tests, prediction of breeding values in genome-assisted selection, analysis of genetic diversity within breeds detection of population admixture, assessment of inbreeding and relationships between breeds, and assignment of individuals to their breed of origin. This approach offers a unique opportunity to save genetic resources and achieving improved productivity. In the past years, significant progress was achieved in reconstructing detailed cattle phylogenies; many studies indicated multiple parental sources and several levels of phylogeographic structuring. More detailed researches are still in progress in order to provide a more comprehensive picture of such extant variability. This paper is focused on reviewing the use of the two uniparental markers as valuable tool for the characterization of cattle genetic diversity. Furthermore, their implications in animal breeding, management and genetic resources conservation are also reported.

Academic research paper on topic "Uniparental genetic systems: a male and a female perspective in the domestic cattle origin and evolution"

Contents lists available at ScienceDirect

Electronic Journal of Biotechnology


Uniparental genetic systems: a male and a female perspective in the domestic cattle origin and evolution

Piera Di Lorenzo a1, Hovirag Lancionib1, Simone Ceccobellia1, Ludovica Curcioc, Francesco Panella a, Emiliano Lasagna

a Dipartimento di Scienze Agrarie, Alimentari e Ambientali, Universitä degli Studi di Perugia, Borgo XX Giugno 74,06121 Perugia, Italy b Dipartimento di Chimica, Biologia e Biotecnologie, Universitä degli Studi di Perugia, Perugia, 06123, Italy c Area Ricerca e Sviluppo, Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche, Via G. Salvemini 1,06126 Perugia, Italy


Over the last 20 years, the two uniparentally inherited marker systems, namely mitochondrial DNA and Y chromosome have been widely employed to solve questions about origin and prehistorical range expansions, demographic processes, both in humans and domestic animals. The mtDNA and the Y chromosome, with their unique patterns of inheritance, continue to be extremely important source of information. These markers played significant roles in farm animals in the evaluation of the genetic variation within- and among-breed strains and lines and have widely applied in the fields of linkage mapping, paternity tests, prediction of breeding values in genome-assisted selection, analysis of genetic diversity within breeds detection of population admixture, assessment of inbreeding and relationships between breeds, and assignment of individuals to their breed of origin. This approach offers a unique opportunity to save genetic resources and achieving improved productivity. In the past years, significant progress was achieved in reconstructing detailed cattle phylogenies; many studies indicated multiple parental sources and several levels of phylogeographic structuring. More detailed researches are still in progress in order to provide a more comprehensive picture of such extant variability. This paper is focused on reviewing the use of the two uniparental markers as valuable tool for the characterization of cattle genetic diversity. Furthermore, their implications in animal breeding, management and genetic resources conservation are also reported.

©2016 Pontificia Universidad Católica de Valparaíso. Production and hosting by Elsevier B.V. All rights reserved. This is an open access article under the CC BY-NC-ND license (



Article history: Received 2 March 2016 Accepted 29 June 2016 Available online 4 August 2016

Keywords: Animal breeding Bovine domestication Cattle genetic diversity Genetic resources Genome-assisted selection Inherited marker systems


1. Uniparental molecular markers......................................................70

2. Mitochondrial DNA............................................................70

3. Y chromosome..............................................................70

4. Genetic resources in domestic cattle....................................................71

5. The cattle domestication.........................................................71

6. Use of uniparental markers in domestic cattle................................................72

6.1. The female perspective of the mitochondrial DNA...........................................72

6.2. The male perspective of the Y chromosome variation.........................................74

7. Conclusions...............................................................75

Conflict of interest statement..........................................................75



* Corresponding author.

E-mail address: (E. Lasagna). 1 These authors contributed equally to this work. Peer review under responsibility of Pontificia Universidad Católica de Valparaíso.

0717-3458/© 2016 Pontificia Universidad Católica de Valparaíso. Production and hosting by Elsevier B.V. All rights reserved. This is an open access article under the CC BY-NC-ND license (

1. Uniparental molecular markers

Ove the last 20 years, the two uniparentally inherited marker systems, namely mitochondrial DNA (mtDNA) and the Y chromosome have been widely employed to solve questions about origin and prehistorical range expansions, demographic processes, both in humans [1] and domestic animals [2,3,4,5,6]. Even if whole genomic approaches are now opening up new clues on the livestock complexity and admixture, mtDNA and the Y chromosome, continue to be an extremely important source of information because of their unique pattern of inheritance [7,8,9,10]. As they are uniparentally inherited, they evolve exclusively through the sequential accumulation of mutations along the maternal and paternal lineages, respectively; these markers played significant roles in farm animals, namely in the evaluation of the genetic variation within- and among-breed lineages, moreover have been widely applied in the fields of linkage mapping, paternity tests, prediction of breeding values, genome-assisted selection, analysis of genetic diversity within breeds, detection of population admixture, assessment of inbreeding, relationships between breeds, and assignment of individuals to their breed of origin [11]. This approach often provides not only new insights into the timing and location of domestication events that produced the extant farm animals [12,13], but also even offers a unique opportunity to conserve genetic resources, promote and defend local products [14,15]. In this last case the genetic traceability of livestock products is an essential tool to safeguard public and animal health, and to valorize typical foods [16]. The past few years have seen significant progress in reconstructing detailed livestock phylogenies especially in cattle (here reviewed), dog [17,18], pig [19,20], horse [21,22,23], sheep [24, 25], goat [26,27,28,29] and chicken [30,31] deepening genealogical branching of the tree topologies for both mtDNA and Y chromosome. These studies indicated multiple parental sources and several levels of phylogeographic structuring.

This paper is focused on reviewing the use of the two uniparental markers as valuable tool for the characterization of cattle genetic diversity. Implications in animal breeding, management and conservation of genetic resources are also reported.

2. Mitochondrial DNA

Mitochondrial DNA is the best studied among all available genetic markers systems. There are several reasons for this peculiarity:

1) its exclusively maternal inheritance makes possible to retrace the genetic history of the female lines.

2) its elevated variability in natural populations due to the high mutation rate, estimated to be at least five times higher than that observed in nuclear DNA, can generate signals about population history over short time frames.

3) mtDNA may be analyzed in both male and female donors, this facilitates the collection of representative samples.

4) the small size of the molecule allows easy amplification and sequencing because of the multiple copies in the cells, moreover the mitochondrial genes are strongly conserved across animals, very few are the duplications, no introns, and very short are the intergenic regions.

Rapidly, the analysis of mtDNA has revealed to be the most convenient and cheapest molecular tool to explore the genetic variability of a species, and became the backbone of molecular genetic investigations in livestock: genetic structure and segregation pattern are still now used to tracing back the origins of breeds as well as to identifying individuals.

The mtDNA has been extensively used as a tool for inferring the evolutionary and demographic past of livestock populations defining their ancestral species and contributing to evidence for the localization of domestication sites [13,22,32,33,34,35,36,37]. Moreover

it has been proven to be highly informative to determine the level of their genetic variability, which is essential in defining conservation priorities for regional breed's specific programs [25,38].

In livestock mtDNA has been used to describe variation in putative wild ancestor populations and modern domestic populations. By now, complete mitogenome sequences are routinely used to produce phylogenetic trees, more and more informative. Although human detailed phylogeny is still too far to be reached, livestock mtDNA surveys led to unravel new genetic flow patterns and phylogeographic structures such as in cattle [39,40,41,42,43], dogs [35], horses [22], pigs [44] and chicken [45].

3. Y chromosome

As a consequence of its uniparental transmission and lack of recombination, the DNA sequence of every Y chromosome preserves a unique record of mutational events that occurred in the genome of previous (male) generations. Studies of polymorphisms in the non-recombining portion of the Y chromosome represent an easy and rapid way to detect and quantify male-mediated admixture, and have been proposed for detecting male-mediated migration events, reconstructing paternal history and trace individual founder lines or families [46,47,48,49]. The absence of interchromosomal recombination out of the pseudoautosomal region (PAR) preserves original arrangements of mutational events, and thus male lineages can be traced both within and among populations. Effective population size is often reduced further by the relatively high variability of male reproductive success. As a result, the Y chromosome is a sensitive indicator of recent demographic events, such as population bottlenecks, founder effects and population expansions [50]. In several species, males are more mobile than females and compete for reproduction or, in livestock case, are selected on the basis of breeding objectives. Therefore, while mtDNA variants stay mostly within the herd, Y-chromosomal variants may reflect the origin of sires as influenced by introgression and upgrading. It has been shown that domestic cattle can display marked sex-biased admixture and migration patterns, for example, the zebu genome spread across Africa through male-mediated gene flow [51,52,53,54,55]. This produced different distributions of the maternal mtDNA and paternal Y chromosome, with the autosomal genome representing an independent picture from two uniparental extremes.

Interestingly, while recent developments in cytogenetic technologies should facilitate the isolation ofY-chromosomal specific markers [56], for most livestock species there are still few Y polymorphic sites. This is probably a consequence of the demographic history of domestication and breed formation. In polygynous species, like most livestock, we expect indeed that a small number of male lineages would have contributed to the genetic pool of the species. Beside dog and cats, polymorphic Y microsatellite markers are currently available only for cattle [53,57,58,59,60], yak [61,62], buffalo [63,64,65] and partially for horse [66]. At the present time these markers have not been yet isolated in some major livestock species, e.g. small ruminants, camelids or the domestic pig.

In the study of human male lineages, the use of Y-specific microsatellites has allowed for refined analyses of the genetic diversity of paternal lineages that can be found within major haplogroups [67, 68,69,70,71]. Similarly, in cattle, microsatellite analysis has identified several Y-haplotypes in Portuguese [72], northern and eastern European [73], western-continental, British and Sub-Saharan African [74] breeds, as well as in American Creole [75] breeds. Even though different set of markers were used in these studies, and each only partially covered the diversity pattern of the paternal lineages, they confirmed that Y-markers exhibit a strong phylogeographic structure in cattle. Although Y-chromosome diversity is lower than autosomal, it has been shown that the studies of male lineages added much to what can be inferred only from mtDNA and autosomal variation [6,72,76,77,

78,79,80,81]. Moreover, compared with mtDNA, the small number of males used for breeding and male-mediated crossbreeding has accelerated the loss of Y-chromosomal variation in domestic cattle. For example, several cattle (such as Russian, Ukrainian and Scandinavian) have been influenced by gene flow from commercial cattle breeds leading to the genetic dilution of many worldwide local breeds [73].

4. Genetic resources in domestic cattle

Cattle breeds are recognized as an important part of biodiversity and genetic heritage. According to FAO [82], out of the 1350 cattle breeds worldwide, 14.8% are extinct [83]. Therefore, it is very important to preserve the genetic diversity of the remaining breeds, mostly captured in non-selected autochthonous breeds [84]. This decrease in the number of cattle breeds has several reasons, such as modernization and reorientation of the agricultural production, socio-economic changes and cultural developments. Between the 1950's and 1980's, the willingness to increase productivity, intensification and specialization of animal production has dramatically affected the local cattle breeds and resulted in loss of sequence variation in DNA and breeds diversity [85,86]. However, in the last two decades the interest for preserving the locally adapted breeds has considerably increased and several conservation strategies were implemented in Europe and worldwide.

The development of the cattle genetic resources has been always more a multifaceted and continuously dynamic process, both on the global and local level, strictly tied to human history. It has resulted in a worldwide population of cattle with a considerable phenotypic and molecular diversity. Felius et al. [87] surveyed the complex history of cattle genetic resources throughout the time on different continents, and argued that the current genetic diversity of cattle emerged during three main and overlapping phases: i) domestication and subsequent wild introgression; ii) natural adaptation to a diverse agricultural habitat; and iii) breed development.

5. The cattle domestication

Domestic cattle are classified into two major species, the taurine or humpless cattle (Bos taurus) and the zebu or humped cattle (Bos indicus). Both descend from the wild aurochs (Bos primigenius). More precisely, the subspecies B. p. primigenius in Southwest Asia and B. p. namadicus in India were the ancestors of taurine and zebu cattle, respectively.

In his record ofthe Gallic Wars, Julius Caesar wrote about aurochsen: "They are a little below the elephant in size, and of the appearance, color, and shape of a bull. Their strength and speed are extraordinary, they spare neither man nor wild beast which they have espied". At the end of the last glacial period (12,000 years ago) B. primigenius was endemic over almost the whole Eurasian continent and Northern Africa. By the 13th century A.D., aurochsen were extremely rare and restricted to Eastern Europe, with the last recorded aurochs dying in Poland in 1627 [40]. Only few contemporary pictures of aurochs exist, but skeletal remains allow reconstructing its morphology. The size, shape or gender ratios allow a differentiation of fossil remains from wild and domestic cattle [34].

Cattle domestication represents a major development in the Neolithic transition and was an important step in human history, leading to extensive modifications of the diet, the behavior, and the socioeconomic structure of many populations [88] of the Old World that at different times adopted cattle breeding [89,90]. Archaeological evidences suggest that taurine cattle have been domesticated between 10,300-10,800 years ago in the Fertile Crescent, most probably on the western Turkish-Syrian border [91,92]. In addition, isotope analysis of organic material revealed traces of milk in excavated pottery, indicating the storage of dairy products already 9 kiloyears (ky) ago [93].

A comparison of the mtDNA of taurine and indicine cattle represented one of the first contributions of DNA research to a reconstruction of the

cattle domestication [94]. The divergence of their control regions implied separate domestications, which most likely started 10 ky ago in South-western Asia and the Indus valley respectively [34,95]. The most recent molecular estimates of the divergence time of these aurochs subspecies and thus of taurine and zebu cattle are 147 ky ago [96] or 335 ky ago [40], and 350 ky ago [97]. Although these estimates have large confidence intervals, all indicate that taurine and zebu cattle have been domesticated separately. This was followed by the spread of domesticated herds throughout the Old World accompanying human trade and migration. After domestication, survival and diffusion of B. taurus was completely dependent on humans; thus the phylogeographic patterns of cattle genetic diversity should mirror human activities or movements and may provide information complementary to archaeological and anthropological data [98]. When domesticated herds diffused from the Fertile Crescent into Europe, Africa and the rest of Asia, local B. primigenius populations were numerous and widespread. Moreover, the coexistence of autochthonous wild aurochs and the newly introduced cattle lasted for thousands of years in many geographical areas, thus providing potential conditions not only for spontaneous interbreeding between wild animals and domestic herds, but also for pastoralists to create secondary centers of domestication involving local aurochs populations. In contrast to the wide distribution of the aurochs domestication events took place in certain areas, reflecting the difficulty of sustained managing and breeding of these large wild animals [99]. The most plausible scenario is a single and regionally restricted domestication process of cattle in the Near East with subsequent migration into Europe during the Neolithic transition without significant maternal interbreeding with the endogenous wild stock [100].

A recent coalescent-based analysis using ancient Iranian taurine samples suggested a severe Near Eastern domestication bottleneck, with an estimated effective size of just 80 female founders [99]. Scheu and colleagues' model suggests that a high proportion (73%) of domesticated cattle in Anatolia and the Near East may have migrated into Europe. This indicates that the expansion into Europe was a far less severe bottleneck than assumed before, and that much of the variation present in the original Anatolian/Near Eastern population survived in initial European cattle populations [100]. While genetic studies support a Near Eastern origin for European B. taurus cattle, there is considerable debate regarding the extent of genetic exchange between early domestic cattle and indigenous aurochs during the development of animal herding in Europe. Comprehensive data sets of ancient and modern cattle DNA from other areas reveal a more complex scenario: fossil remains [101], together with the predominance of one taurine mitochondrial haplogroup T1 in Africa [42,102] and a new haplogroup in Eastern Asia, T4, [73,103] suggested at least two other domestication centers.

The identification of sequences of putative aurochs haplogroups Q and R in modern Italian cattle does support the limited local adoption of wild aurochs matrilines in Southern Europe [39,40,104].

In contrast to mtDNA studies, analyses of paternally inherited Y chromosome haplotypes remain equivocal as to whether local wild male aurochs contributed to European B. taurus populations [79,105,106].

The interface between early European domestic populations and wild aurochs was significantly more complex than previously thought and important questions remain unanswered, including the phylogenetic status of aurochs, whether gene flow from aurochs into early domestic populations occurred [107].

However, independent domestication in Africa [52,54] and East Asia [103] has also been postulated and ancient DNA data raise the possibility of local introgression from wild aurochs. Zebus were probably imported into Africa after the Arabian invasions in the 7th century [52]. Interestingly, the discovery that African zebus carry taurine mtDNA implies that African zebus were the result of crossing zebu bulls with taurine cows [52]. The first auroch mtDNA sequences, collected in Great Britain, typed far from those of modern cattle

breeds, suggesting little auroch introgression [102]. Later, however, more ancient auroch sequences from Italy and from the Bronze Age of the Iberian Peninsula revealed haplotype distributions similar to those of modern European cattle breeds [78,88]. Only one Iberian sample appeared more closely related to the British auroch sequences [78]. Thus, the introgression of auroch mtDNA into modern cattle breeds has taken place, but it is not clear to what degree or whether this varied depending upon geographical location. Thus, detailed and continent-wide evaluation of the early spatiotemporal demography of B. taurus has so far been hindered by the lack of data from the key bridging areas of the Neolithic, namely Anatolia, the Balkans, and the Western Mediterranean.

6. Use of uniparental markers in domestic cattle

6.1. The female perspective of the mitochondrial DNA

From a genetic point of view, animal domestication can be reconstructed through phylogeographic analyses of both nuclear and mitochondrial genomic data [13]. Early molecular and evolutionary studies on cattle have focused on mtDNA, in particular on short segments of its control region [94,102,103]. However, mtDNA control-region variation is often characterized by high levels of recurrent mutations and reversions, thus blurring the structure of the phylogenetic tree and making the distinction between some important branches within the tree virtually impossible. In fact, following the most detailed approach used for the human phylogeny [108,109,110,111], researches tend to use complete mitogenomes to reconstruct the history of animal domestication such as in cattle [40, 41,42,104], chicken [45], horse [21,22] and sheep [25].

The analysis of mtDNA sequence diversity has provided useful information on the origin and diversification of current cattle populations [102,105,112]. The mitochondrial signals of wild aurochs' domestication can be seen in modern cattle breeds [102,112,113]. In particular cattle domestication in the Near East is thought to have taken place around 10,500 years ago, giving rise to taurine cattle (mainly mitochondrial haplogroup T), whereas domestication in southern Asia has been dated later to about 8500 years ago resulting in modern zebu (indicine) cattle (mitochondrial haplogroup I). Molecular diversity approach revealed that modern taurine mitochondrial genomes cluster within a number of closely related branches, termed T, T1, T2, T3, and T4, geographically well structured: T1 predominantly found in Africa; T2 originates in the Near East and Western Asia; and T3 found in Europe and originates from the expansion of a small cattle population domesticated in the Middle East.

Frequency and geographic distributions of the T lineages were very compatible with the scenario of a single ancestral Near Eastern population source and a later spread out following the domestication event. However alternative models were proposed to explain some peculiar features in the geographic distributions of T1 [114], T3 [88] and T4 [103].

Lenstra and colleagues [8] combined the results of several regional studies of the cattle mtDNA control region resulting in a global meta-analysis suggesting strong founder effects during colonization of Europe, East Asia, Africa and America, but little temporal variation.

The most recent whole mitogenome sequencing approach has revealed the fine phylogenetic structure of what is now termed "macro-haplogroup T" (Table 1). This is dissected in two clades, T1'2'3 and T5 [40,41]. The latter was a previously unknown haplogroup, reported only in Italy [104] and Croatia [83], while T1'2'3 is formed by the previously defined T1, T2 and T3. Haplogroup T4 turned out to be a derived sub-clade within T3 [41,42], probably spread over East Asia by a founder effect during the eastward migration of cattle.

The age estimates of super-haplogroup T (~16 ky), and those ofT1, T2, T3 and T5 haplogroups were all compatible with the scenario that their founding haplotypes were present and directly involved in the

domestication event that occurred 10-11 ky ago in the Near East. The exception was T4 whose younger age is suggestive of an origin within domestic cattle, probably while diffusing from the Near East towards Eastern Asia [39,40,42]. Haplogroup T4 was not observed in the west, but has been found in East-Chinese ancient DNA dating to 4500 years ago [115], in modern Korean beef cattle [39] and in more than half of the Japanese cattle [103]. The high T4 frequency (21%) in the Yakutian cattle and control-region haplotypes shared with European samples, suggested that the Yakutian cattle have prehistoric maternal ancestries in domesticated Near Eastern cattle indicating a link between the Yakut and cattle from East-China [73].

Complete mtDNA sequences have allowed not only an accurate phylogeny, but even strengthened a Southwest-Asian origin for all major T haplogroups, including the African T1 and East-Asian T4 [41, 116].

A recent comprehensive phylogenetic analysis of 64 T1 mitochondrial complete genomes identified eight haplotypes as founders of the African T1 population [41].

Estimates of coalescence times for the T1 sub-haplogroups (6200 to 12,900 years ago) and their current geographic distributions are compatible with a Southwest-Asian origin for most T1 sub-haplogroups, which for sub-haplogroup T1c1 has been confirmed by it discovery in Iraq. Sporadic in the Old World it reaches 31% of frequencies of in the Caribbean Lesser Antilles islands and even 50% in Brazilian Criollo cattle. Data also suggest that one sub-haplogroup, T1d, might represent a mitochondrial line that has developed in the African continent shortly after the domestication event in the Near East, while T1c1a1, found for the first time in an African breed, it probably originated in North Africa, reached the Iberian Peninsula and sailed to America, with the first European settlers [41]. Ancient gene flow across the Gibraltar Strait has been recently confirmed also by SNP genotyping [117]. Recent data from ancient Neolithic/Chalcolithic Iberian cattle population have pointed out that T1 haplogroup already exists simultaneously in South-Western Europe [118]. Up to date there are no data for the presence of T1 haplogroup in ancient South-Eastern Europe.

The frequency of the T3 haplogroup increases from ~ 40% in South-West Asia to almost 100% in North-West Europe, with a concomitant decrease of T2. The latter has appreciable frequencies in Italian, Balkan and Asian taurine cattle, but is found only sporadically in the remaining European regions, Northern Africa and in bones from France dating to 5000 years ago [113] and in Switzerland derived from the Roman period [119].

Data available from ancient DNA confirmed that most Neolithic European cattle already carried T3 haplotypes [120,121]. This is in accordance with Bayesian analysis of taurine mtDNA variants coalescence, showing population expansion during the last 10 ky [122]. Even if T3 haplogroup is dominant in Europe and North-Central Asia [40,41,73,75,88,102,123,124], two interesting exceptions in Europe are remarkable:

i) four ancient breeds from Tuscany have almost the same mtDNA diversity as found in Southwestern Asia, suggesting an ancient maternal origin and a direct link between Tuscan and Western-Asian cattle [125]. For the Chianina breed this was confirmed by microsatellite data [126]. Microsatellites also indicated that the Maremmana and the Cabannina, the two other Tuscan breeds, have been subject to Podolian and Brown Mountain breed introgression respectively.

ii) the appreciable frequencies ofT1 haplogroup in several Spanish and Portuguese breeds, indicated migration from Africa to the north. This may have occurred either during the Neolithic spread of cattle or later, for instance during the Islamic occupation. Importation of Iberian cattle into the newly discovered American continent explains the relatively high frequency of the T1 haplogroup in Caribbean and South American cattle [75,127,128,129,130,131].

Table 1

Sources and haplogroup affiliation for the Bos taurus complete mtDNA sequences.

Macroarea and breeds T1'2'3 T1 T2 T3* T3a T3b T3c T3d T4 T5 I P Q R Total References and GenBank accessions

America 5 5

Creole 5 5 [41]

Eastern Asia 2 13 2 4 6 3 30

Hanwoo 1 1 2 [147]; HQ025805

Japanese Black 4 3 7 AB074962-AB074968

Korean 1 12 2 3 18 AY526085; DQ124371-DQ124386; NC006853

Mongolian 1 1 [40]

Nandan 1 1 KT033901

Unknown 1 1 KP143771

Iran and Iraq 1 5 5 23 16

Iranian 4 2 1 7 [39]

Iraqi 1 1 3 22 9 [39]

Greece 2 2

Greek 2 2 [39]

Northern Europe 2 1 24 2 20 2 21 1 55

Angus 1 7 7 1 16 [148]; AY676857; AY676859; AY676862-AY676873

Charolaise 1 1 2 AY676858; AY676861

Fleckvieh 1 1 [149]

Galbvieh 1 1 AY676860

Heck cattle 1 1 HM045018

Holstein-Friesian 7 2 5 1 1 16 DQ124403-DQ124418

Hungarian Grey 1 1 GQ129207

Limousine 1 1 2 [41]; AY676856

Longhorn 1 1 [148]

Red Mountain 2 3 1 6 [150]

Simmental 1 1 AY676855

Ukrainian grey 1 1 GQ129208

White Park 3 12 6 [151]

Iberian Peninsula 2 2 4

Alentejana 2 2 [41]

Betizuak 2 2 [39]

Italy 1 35 6 12 1 6 2 16 10 89

Agerolese 3 1 4 [40,41]

Bruna 1 1 [41]

Cabannina 1 2 3 6 [39,104]

Calvana 1 1 [41]

Chianina 8 3 3 4 5 23 [39,40,104,41]

Cinisara 5 1 2 8 [39,40,41]

Frisona italiana 1 3 4 [39]

Grigia Alpina 2 2 [104]

Marchigiana 7 1 8 [104,41]

Maremmana 3 2 5 [39,41]

Modicana 1 1 [39]

Pettiazza 1 1 [39]

Pezzata rossa italiana 1 1 2 [40]; JQ967333

Piemontese 1 1 2 [39]

Podolica 3 1 4 [39,41]

Rendena 1 1 [39]

Romagnola 3 5 6 14 [40,104,41]

Valdostana 1 1 2 [39]

Malta 1 1 2

Maltese 1 1 2 [43]

Northern Africa 18 6 5 2 31

Domiaty 8 3 1 2 14 [41,42]

Menofi 10 3 4 17 [41,42]

Africa 36 36

Nguni 34 34 [152]

Sheko 2 2 [41]

Unknown 1 2 20 2 3 1 29

Hybrid bison/cattle 12 12 [148]

Unknown 1 2 8 2 3 1 17 [153]; DQ124387-DQ124402

Total 1 100 24 81 5 32 3 3 10 47 1 18 10 299

In bold: total number of mtDNAs in the specific macroarea. T3*: all T3 mtDNAs that did not cluster within any of the defined subclades.

The most recent finding based on both prehistoric aurochs and cattle populations defined a new Balkan-specific T6 haplogroup and argued the possibility for an independent event of Neolithic cattle domestication on the South-eastern Balkans followed by a second wave of parallel dissemination of cattle herds via the Mediterranean route [132].

Although the vast majority of modern cattle harbor mitogenomes belonging to haplogroups T and I, other haplogroups have been

identified (named Q P and R), all radiating prior to the T node, thus phylogenetically closer to T than to I (Table 1). Haplogroup P was the most common haplogroup in European aurochs and has so far been identified in only two modern cattle [39,133]. Its occurrence in the modern cattle gene pool is generally explained by rare introgression events between female European aurochs and domesticated cattle introduced from the Near East [40]. Haplogroup Qis relatively close to

haplogroup T sequences and has been suggested to have entered the cattle mtDNA gene pool during the initial domestication process in the Near East. In contrast, haplogroup R is phylogenetically very distinct from P, Q and T and has so far only been found in modern Italian cattle [104]. As haplogroup P, it most probably represents a remnant of introgression from wild aurochs into the early domestic cattle gene pool.

While there is very little doubt that the uncommon haplogroups P and R are derived from European wild aurochs cows either because of sporadic interbreeding events (naturally occurring and/or human-mediated) or possibly, in the case of haplogroup R, as consequence of a minor event of B. primigenius domestication in Italy [104], the origin of haplogroup Qis less clear.

With an estimated age of about 48 ky for the QT node, haplogroup Q is the closest to super-haplogroup T; it was first discovered in a local Italian breed (Cabannina, two mtDNAs with the same haplotype), following other fourteen additional Q mitogenomes, but all derived from Italian breeds (Cabannina, Chianina, Grey Alpine, Italian Red Pied, and Romagnola) [39,40,104]. Haplogroup Q is found both in ancient Neolithic and modern cattle [80,104].

A recent phylogenetic analyses conducted on 31 Egyptian mitogenomes from Nile Delta taurine breeds confirmed the prevalence of haplogroup T1 in North African cattle, but also showed rather high frequencies for haplogroups T2 (19.4%), T3 (16.1%) and Q1 (6.5%), with an unexpected extreme haplotype diversity [42]. Researchers argued that the Egyptian Q1 mitogenomes are direct local derivatives from Q1 founder mtDNAs brought to Egypt by the first domestic herds. In other words, similar to T1, T2 and T3, Q1 was among the haplogroups involved in domestication in the Near East, from where it spread along with the others. Recent data on the ancient cattle population (from Neolithic to Bronze ages) have shown predominate presence of Q haplogroup up to 50% in Iran (7000-5000 BC) as well as in South-Eastern Europe (the Balkans, 6200-2200 BC) [100] and in a Northern Finnish Post-Medieval sample [134]. The new Q1 lineage found in the Pirenaica extend the geographic distribution of the Q haplogroup to the south-west of the European continent [135].

Regarding zebu cattle, mtDNA sequences allowed the identification of two major haplogroups: I1 and I2. These indicine maternal lineages diffused from South Asia to Southwest and Central Asia [136,137]. Haplogroups I1 predominated in the cattle that moved eastwards to Southeast Asia and China. I2 haplogroup is a rare and more ancient than I1 haplogroup; it was only detected in Yunnan-Guizhou Plateau, Tibet region and Mongolia [123,138,139].

Chen and colleagues [136] suggested that zebu domestication involved at least two different wild female populations [140] or, more likely, a single domestication event in the Indus Valley with a subsequent introgression process of wild (I2) females into proto-domesticated herds. Populations with a mixed taurine and indicine maternal origin are found in Southwest Asia, Central Asia, China, Mongolian and Brazil [8].

Finally, two haplogroups, termed E and C, have been reported only in ancient specimens and are probably extinct. Haplogroup, E, was identified in a 6 ky old aurochs from Germany [80,133], while haplogroup C was found in a specimen that might represent an early Holocene attempt to manage cattle in northern China [141].

6.2. The male perspective of the Y chromosome variation

In contrast to mtDNA, which shows the maternal origin and therefore stays with the herds, Y chromosomal haplotypes are markers of paternal origin and male introgression.

Generally Y chromosome phylogenetic surveys are few and most have been focused on taurine and zebuine crosses [53,80,142,143]. Furthermore, lower levels of genetic diversity have been found in the Y chromosome than in autosomes, probably due to commonly used breeding schemes of a few selected males that produce a large number of offspring [81,144]. The identification of five SNPs has permitted the classification of extant breeds into three Y-chromosome haplogroups, named Y1, Y2 and Y3 [106] (Fig. 1 and Table 2). Y3 haplogroup was identified only in zebu, while Y1 and Y2 are so far the two major and well divergent. Y1 was found to be predominant in

Fig. 1. Geographical distribution of the Y haplogroups among the world's cattle breeds (for further details see Table 2).

Conflict of interest statement

The authors have no conflicts of interest to disclose.

Table 2

Sources and Y haplogroup distribution for the Bos taurus in the world.

Region Section map Number of breeds/populations Y1 Y2 Y3 Reference

South of America A 158 57 20 81 [751

Eastern Europe В 65 53 12 [134] [39]

Northern Europe Southern -central Europe 184 1543 112 236 72 1307

Southeastern Europe 10 10

Western Europe 404 334 70

Anatolia peninsula 32 1 31

Western Russia 9 9 -

Central Russia С 25 24 1

Russian Siberia 23 23

China 584 12 359 213 [1531

Marocco □ 10 10 [74]

Burkina Faso 8 8

Guinea 9 2 7

Ethiopia 40 1 - 39 ran

The colours identify the four section maps reported in Fig. 1.

northern European and in north Spanish breeds, has a low frequency in Southwest Asian bulls and it is carried by male offspring of recent European imports [50]. Y2 is prevalent in Central and South Europe, with a clear dividing zone in central Europe [43,50], and Anatolian and African taurine bulls. Remains of European aurochs bulls for which their wild origin was validated via their mtDNA all carried Y2 haplotypes [105]. Since these cannot yet be differentiated from European or Southwest Asian Y2 haplotypes, this neither proves nor disproved wild male introgression. Wild-domestic crossbreeding was suggested by intermediate sized Neolithic bones found in what is now the Czech Republic [145]. The Y1 distribution pattern is interpreted as reflecting later expansion of dairy breeds [50,105,106]. Specific Y2 haplotypes provides evidence for introgression of African aurochs in domestic herds [6,124]. An African origin of taurine cattle, in spite of a Southwest Asian maternal origin, has been confirmed by autosomal SNPs analysis [117].

Overall a north-south gradient of genetic diversity in modern European cattle has been reported, resulting in an almost complete fixation of the Y1 type in the contemporary northern cattle breeds most likely due to recent demographic events [106,134].

Some authors assessed the paternal gene pools of cattle breeds and the influence of foreign bulls during crossings by microsatellite markers. A set of five cattle Y-specific microsatellite loci was surveyed in several cattle breeds reared in different geographical areas [6,50,73] or local breeds such as Ethiopian cattle [81], Portuguese cattle [72], the [59] and from Poland [146].

These studies have allowed for refined analyses of the genetic diversity of paternal lineages, identifying several Y-haplotypes within major haplogroups. However, with the exception of 1NRA189 marker, an overall low diversity of the Y-chromosome markers was observed, possibly due to either a low mutation rate or selection affecting the allelic diversity [50,59,72,146].

It has been also shown that particular microsatellite alleles were either indicus-specific allele, such as 1NRA189 (88 bp) [76], 1NRA124 (130 bp) [53,76] and BM861 (156 bp) [60,76], or were found only in a few individuals from indigenous breeds of different geographical origin, specifically 1NRA189 (90 bp), 1NRA189 (82 bp) [73] and 1NRA124 (134 bp) [60].

7. Conclusions

The outcome of combined mitogenome analyses and Y chromosomal studies has greatly improved our understanding of the origin of extant cattle, providing the reconstructing of its evolutionary history. However, refined comparative analyses with preserved B. primigenius specimens highlighted the complexity of the cattle domestication process and left some question unsolved.

Uniparental genetic systems contributed essentially both to the male and female heritage reconstructions by providing geographic and historic anchor points for specific breeding and conservation programs.


The authors want to thank the two anonymous referees for their valuable comments and constructive suggestions.


[1] Underhill PA, Kivisild T. Use of Y chromosome and mitochondrial DNA population structure in tracing human migrations. Annu Rev Genet 2007;41:539-64.

http: //

[2] Vila C, Seddon J, Ellegren H. Genes of domestic mammals augmented by backcrossing with wild ancestors. Trends Genet 2005;21:214-8.

[3] Luikart G, Gielly L, Excoffier L, Vigne JD, BouvetJ, Taberlet P. Multiple maternal origins and weak phylogeographic structure in domestic goats. Proc Natl Acad Sci USA 2001 ;98:5927-32.

[4] Jansen T, Forster P, Levine MA, Oelke H, Hurles M, Renfrew C, et al. Mitochondrial DNA and the origins of the domestic horse. Proc Natl Acad Sci U S A 2002;99: 10905-10.

[5] Larson G, Dobney K, Albarella U, Fang M, Matisoo Smith E, Robins J, et al. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 2005;307:1618-21.

[6] Perez Pardal L, Royo LJ, Beja Pereira A, Chen S, Cantet J, Traoré A, et al. Multiple paternal origins of domestic cattle revealed by Y-specific interspersed multilocus microsatellites. Heredity 2010;105:511-9.

[7] Lenstra JA, Groeneveld LF, Eding H, Kantanen J, Williams JL, Taberlet P, et al. Molecular tools and analytical approaches for the characterization of farm animal genetic diversity. Anim Genet 2012;43:483-502.

http: //

[8] Lenstra JA, Ajmone-Marsan P, Beja-Pereira A, Bollongino R, Bradley DG, Colli L, et al. Meta-analysis of mitochondrial DNA reveals several population bottlenecks during worldwide migrations of cattle. Diversity 2014;6:178-87.

http: //

[9] Yang W, Kang X, Yang Q, Lin Y, Fang M. Review on the development of genotyping methods for assessing farm animal diversity. J Anim Sci Biotechnol 2013;4:2. http: //

[10] 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. Front Genet 2015;6:314.

[11] Vignal A, Milan D, Sancristobal M, Eggen A. A review on SNP and other types of molecular markers and their use in animal genetics. Genet Sel Evol 2002;34: 275-305.

[12] Ajmone-Marsan P, Garcia JF, Lenstra JA. On the origin of cattle: How aurochs became domestic and colonized the world. Evol Anthropol 2010;19:148-57.

[13] Groeneveld LF, Lenstra JA, Eding H, Toro MA, Scherf B, Pilling D, et al. Genetic diversity infarm animals—A review. Anim Genet 2010;41:6-31.

http: //

[14] Toro M, Fernández J, Caballero A. Molecular characterization of breeds and its use in conservation. Livest Sci 2009;120:174-95.

[15] Joost S, Bruford MW. The Genomic-Resources Consortium^. Advances in farm animal genomic resources. Front Genet 2016;6:333.

[16] Dalvit C, De Marchi M, Cassandro M. Genetic traceability of livestock products: A review. Meat Sci 2007;77:437-49.

[17] Ding ZL, Oskarsson M, Ardalan A, Angleby H, Dahlgren LG, Tepeli C, etal. Origins of domestic dog in southern East Asia is supported by analysis of Y-chromosome DNA. Heredity 2012;108:507-14.

[18] Brown SK, Pedersen NC, Jafarishorijeh S, Bannasch DL, Ahrens KD, Wu JT, et al. Phylogenetic distinctiveness of Middle Eastern and Southeast Asian village dog Y chromosomes illuminates dog origins. PLoS One 2011;6, e28496. /journal.pone.0028496.

[19] Ramírez O, Gigli E, Bover P, Alcover JA, Bertranpetit J, Castresana J, et al. Paleogenomics in a temperate environment: Shotgun sequencing from an extinct Mediterranean caprine. PLoS One 2009;4, e5670.

[20] Cliffe KM, Day AE, Bagga M, Siggens K, Quilter CR, Lowden S, et al. Analysis of the non-recombining Y chromosome defines polymorphisms in domestic pig breeds: Ancestral bases identified by comparative sequencing. Anim Genet 2010;41: 619-29.

[21] Lippold S, Matzke NJ, Reissmann M, Hofreiter M. Whole mitochondrial genome sequencing ofdomestic horses reveals incorporation ofextensive wild horse diversity during domestication. BMC Evol Biol 2011;11:328.

[22] Achilli A, Olivier A, Soares P, Lancioni H, Kashani BH, Perego UA, et al. Mitochondrial genomes from modern horses reveal the major haplogroups that underwent domestication. Proc Natl Acad Sci U S A 2012;109:2449-54.

http: //

[23 ] Wallner B, Vogl C, Shukla P, Burgstaller JP, Druml T, Brem G. Identification of genetic variation on the horse y chromosome and the tracing of male founder lineages in modern breeds. PLoS One 2013;8, e60015. http: //

[24] Meadows JRS, Hanotte O, Drögemüller C, Calvo J, Godfrey R, Coltman D, et al. Globally dispersed Y chromosomal haplotypes in wild and domestic sheep. Anim Genet 2006;37:444-53.

[25] Lancioni H, Di Lorenzo P, Ceccobelli S, Perego UA Miglio A, Landi V, et al. Phyloge-netic relationships of three Italian Merino-derived sheep breeds evaluated through a complete mitogenome analysis. PLoS One 2013;8, e73712.

http: //

[26] Pereira L, Freitas F, Fernandes V, Pereira JB, Costa MD, Costa S, et al. The diversity present in 5140 human mitochondrial genomes. Am J Hum Genet 2009;84: 628-40.

[27] Nomura K, Yonezawa T, Mano S, Kawakami S, Shedlock AM, Hasegawa M, et al. Domestication process of the goat revealed by an analysis of the nearly complete mi-tochondrial protein-encoding genes. PLoS One 2013;8, e67775. /journal.pone.0067775.

[28] Doro MG, Piras D, Leoni gG, Casu G, Vaccargiu S, Parracciani D, et al. Phylogeny and patterns of diversity of goat mtDNA haplogroup A revealed by resequencing complete mitogenomes. PLoS One 2014;9, e95969.

http: //

[29] Colli L, Lancioni H, Cardinali I, Olivieri A, Capodiferro MR, Pellecchia M, et al. Whole mitochondrial genomes unveil the impact of domestication on goat matrilineal variability. BMC Genomics 2015;16:1115.

[30] Ceccobelli S, Di Lorenzo P, Lancioni H, Castellini C, Monteagudo Ibanez LV, Sabbioni A, et al. Phylogeny, genetic relationships and population structure of five Italian local chicken breeds. Ital J Anim Sci 2013;12:410-7.

[31 ] Ceccobelli S, Di Lorenzo P, Lancioni H, Monteagudo Ibanez LV, Tejedor MT, Castellini C, et al. Genetic diversity and phylogeographic structure of sixteen Mediterranean chicken breeds assessed with microsatellites and mitochondrial DNA. Livest Sci 2015;175:27-36.

[32] Bruford MW, Bradley DG, Luikart G. DNA markers reveal the complexity of livestock domestication. Nat Rev Genet 2003;4:900-10.

[33] Fernández H, Hughes S, Vigne JD, Helmer D, Hodgins G, Miquel C, et al. Divergent mtDNA lineages of goats in an Early Neolithic site, far from the initial domestication areas. Proc Natl Acad Sci U S A 2006;103:15375-9.

[34] Zeder MA, Emshwiller E, Smith BD, Bradley DG. Documenting domestication: The intersection of genetics and archaeology. Trends Genet 2006;22:139-55.

[35] Pang JF, Kluetsch C, Zou XJ, Zang AB, Luo LY, Angleby H, et al. mtDNA data indicate a single origin for dogs south of Yangtze River, less than 16,300 years ago, from numerous wolves. Mol Biol Evol 2009;26:2849-64.

http: //

[36] Jin L, Zhang M, Ma J, Zhang J, Zhou C, Liu Y, et al. Mitochondrial DNA evidence indicates the local origin of domestic pigs in the upstream region of the Yangtze River. PLoS One 2012;7, e51649.

[37] Di Lorenzo P, Ceccobelli S, Panella F, Attard G, Lasagna E. The role of mitochondrial DNA to determine the origin of domestic chicken. Worlds Poult Sci J 2015;71: 311-8.

[38] Taberlet P, Coissac E, Pansu J, Pompanon F. Conservation genetics of cattle, sheep, and goats. C R Biol 2011;334:247-54.

[39] Achilli A, Olivieri A, Pellecchia M, Uboldi C, Colli L, Al Zahery N, et al. Mitochondrial genomes of extinct aurochs survive in domestic cattle. Curr Biol 2008;18:157-8. http: //

[40] Achilli A, Bonfiglio S, Olivieri A, Malusa A, Pala M, Kashani BH, et al. The multiface-ted origin of taurine cattle reflected by the mitochondrial genome. PLoS One 2009; 4, e5753.

[41] Bonfiglio S, Ginja C, De Gaetano A, Achilli A, Olivieri A, Colli L, et al. Origin and spread of Bos taurus: New clues from mitochondrial genomes belonging to haplogroup T1. PLoS One 2012;7, e38601.

[42] Olivieri A, Gandini F, Achilli A, Fichera A, Rizzi E, Bonfiglio S, et al. Mitogenomes from Egyptian Cattle Breeds: New clues on the origin of haplogroup Qand the early spread of Bos taurus from the Near East. PLoS One 2015;10, e0141170. http: //

[43] Lancioni H, Di Lorenzo P, Cardinali I, Ceccobelli S, Capodiferro MR, Fichera A, et al. Survey of uniparental genetic markers in the Maltese cattle breed reveals a significant founder effect but does not indicate local domestication. Anim Genet 2016; 10, e0141170.

[44] Wu GS, Yao YG, Qu KX, Ding ZL, Li H. Palanichamy MG, et al. Population phylogenomic analysis of mitochondrial DNA in wild boars and domestic pigs revealed multiple domestication events in East Asia. Genome Biol 2007;8:245. http ://

[45] Miao YW, Peng MS, Wu GS, Ouyang YN, Yang ZY, Yu N, et al. Chicken domestication: An updated perspective based on mitochondrial genomes. Heredity 2013; 110:277-82.

[46] Casanova M, Leroy P, Boucekkine C, Weissenbach J, Bishop C, Fellous M, et al. A human Y-linked DNA polymorphism and its potential for estimating genetic and evolutionary distance. Science 1985;230:1403-6.

http: //

[47] Ngo KY, Vernaud G, Johnsson C, Lucotte G, Weissenbach J. A DNA probe detecting multiple haplotypes of the human Y chromosome. Am J Hum Genet 1986;38:407-18.

[48] Malaspina P, Persichetti F, Novelletto A, lodice C, Terranato L, Wolfe J, et al. The human Y chromosome shows a low level of DNA polymorphism. Ann Hum Genet 1990;54:297-305. /j.1469-1809.1990.tb00385.x.

[49] King TE, Jobling MA. Founders, drift, and infidelity: The relationship between Y chromosome diversity and patrilineal surnames. Mol Biol Evol 2009;26:1093-102.

[50] Edwards CJ, Ginja C, Kantanen J, Perez Pardal L, Tresset A, Stock F, et al. Dual origins of dairy cattle farming — Evidence from a comprehensive survey of European Y-chromosomal variation. PLoS One 2011;6, e15922.

[51] Machugh D, Shriver M, Loftus R, Cunningham P, Bradley D. Microsatellite DNA variation and the evolution, domestication and phylogeography of Taurine and Zebu cattle (Bos taurus and Bos indicus). Genetics 1997;146:1071-86.

[52] Bradley DG, Loftus RT, Cunningham P, Machugh DE. Genetics and domestic cattle origins. Evol Anthropol 1998;6:79-86.<79::AlD-EVAN2>3.0.œ;2-R

[53] Hanotte O, Tawah CL, Bradley DG, Okomo M, Verjee Y, Ochieng J, et al. Geographic distribution and frequency of a taurine Bos taurus and an indicine Bos indicus Y specific allele amongst sub-Saharan African cattle breeds. Mol Ecol 2000;9:387-96.

[54] Hanotte O, Bradley DG, OchiengJW, Verjee Y, Hill EW, Rege JE. African pastoralism: Genetic imprints of origins and migrations. Science 2002;296:336-9.

http: //

[55] Machugh DE, Bradley DG. Livestock genetic origins: Goats buck the trend. Proc Natl Acad Sci U S A 2001;98:5382-4.

[56] Petit E, Balloux F, Excoffier L. Mammalian population genetics: Why not Y? Trends Ecol Evol 2002;17:28-33.

[57] Budowle B, Adamowicz M, Aranda XG, Barna C, Chakraborty R, Cheswick D, et al. Twelve short tandem repeat loci Y chromosome haplotypes: Genetic analysis on populations residing in North America. Forensic Sci Int 2005;150:1-15.

[58] Cai X, Chen H, Wang S, Xue K, Lei C. Polymorphisms of two Y chromosome microsatellites in Chinese cattle. Genet Sel Evol 2006;38:525-34.

http: //

[59] Cortes O, Tupac-Yupanqui l, DunnerS, Fernández J, Cañón J. Y chromosome genetic diversity in the Lidia bovine breed: A highly fragmented population. J Anim Breed Genet 2011;128:491-6.

[60] Ozsensoy Y, Kurar E, Bulöut Z, Nizamlioglu M. Y chromosome analysis of native Turkish cattle breeds by microsatellite markers. Turk J Biol 2014;38:388-95.

[61] Xuebin Q.Genetic diversity, differentiation and relationship of domestic yak population: a microsatellite an mitochondrial DNA study. Lanzhou, China: Lanzhou University; 2004 262PhD Thesis.

[62] Nguyen TT, Genini S, Ménétrey F, Malek M, Vögell P, Goe MR, et al. Application of bovine microsatellite markers for genetic diversity analysis of Swiss yak (Poephagus grunniens). Anim Genet 2006;36:484-9.

[63] Zhang XM, Yue XP, Zhang CM, Lan XY, Chen H, Lei CZ. Screening and polymorphism of Y chromosome microsatellite markers in swamp buffalo. Hereditas 2010;32: 242-7.

[64] Smitz N, Cornélis D, Chardonnet P, Caron A, De Garine-Wichatitsky M, Jori F, et al. Genetic structure of fragmented southern populations of African Cape buffalo (Syncerus caffer caffer). BMC Evol Biol 2014;14:203.

[65] Ma ZJ, Chen SM, Sun YG, Xi YL, Li RZ, Xu JT, et al. Y-STR1NRA189 polymorphisms in Chinese yak breeds. Genet Mol Res 2015;14:18859-62.

[66] Wallner B, Piumi F, Brem G, Müller M, Achmann R Isolation of Y chromosome-specific microsatellites in the horse and cross-species amplification in the genus Equus. J Hered 2004;95:158-64.

[67] Jobling MA, Tyler-Smith C. The human Y chromosome: An evolutionary marker comes of age. Nat Rev Genet 2003;4:598-612.

[68] Balaresque P, Bowden GR, Adams SM, Leung HY, King TE, Rosser ZH, et al. A predominantly neolithic origin for European paternal lineages. PLoS Biol 2010;8, e1000285.

[69] Underhill PA, Myres NM, Rootsi S, Metspalu M, Zhivotovsky LA, King JR, et al. Separating the post-Glacial coancestry of European and Asian Y chromosomes within haplogroup R1a. Eur J Hum Genet 2010;18:479-84.

http: //

[70] Scozzari R Massaia A, D'atanasio E, Myres NM, Perego UA, Trombetta B, et al. Molecular dissection of the basal clades in the human Y chromosome phylogenetic tree. PLoS One 2012;7, e49170.

[71] Seielstad M, Bekele E, Ibrahim M, Touré A, Mamadou T. A view of modern human origins from Y chromosome microsatellite variation. Genome Res 1999;9:558-67.

[72] Ginja C, Telo Da Gama L, Penedo MC. Y Chromosome haplotype analysis in portuguese cattle breeds using SNPs and STRs. J Hered 2009;100:148-57.

[73] Kantanen J, Edwards CJ, Bradley DG, Vinalass H, Thessler S, Ivanova Z, et al. Maternal and paternal genealogy of Eurasian taurine cattle (Bos taurus). Heredity 2009; 103:404-15.

[74] Pérez-Pardal L, Royo LJ, Álvarez 1, De León FA, Fernández 1, Casais R, et al. Female segregation patterns of the putative Y-chromosome-specific microsatellite markers INRA124 and INRA126 do not support their use for cattle population studies. Anim Genet 2009;40:560-4.

[75] Ginja C, Penedo MC, Melucci L, Quiroz J, Martinez Lopez OR, Revidatti MA, et al. Origins and genetic diversity of New World Creole cattle: lnferences from

[85 [86 [87

[89 [90

mitochondrial and Y chromosome polymorphisms. Anim Genet 2010;41:128-41. http://dx.doi.Org/10.1111/j.1365-2052.2009.01976.x.

Edwards CJ, Gaillard C, Bradley DG, Machugh DE. Y-specific microsatellite polymorphisms in a range of bovid species. Anim Genet 2000;31:127-30.

Lindgren G, Backstrom N, Swinburne J, Hellborg L, Einarsson A, Sandberg K, et al. Limited number of patrilines in horse domestication. Nat Genet 2004;36:335-6. http: //

Änderung C, Bouwman A, Persson P, Carretero JM, Ortega AI, Elburg R, et al. Prehistoric contacts over the Straits of Gibraltar indicated by genetic analysis of Iberian Bronze Age cattle. Proc Natl Acad Sci U S A 2005;102:8431-5.

Götherström A, Anderung C, Hellborg L, Elburg R, Smith C, Bradley DG, et al. Cattle domestication in the Near East was followed by hybridization with aurochs bulls in Europe. Proc RSoc B 2005;272:2345-50.

Edwards CJ, Bollongino R, Scheu A, Chamberlain A, Tresset A, Vigne JD, et al. Mitochondrial DNA analysis shows a Near Eastern Neolithic origin for domestic cattle and no indication of domestication of European aurochs. Proc R Soc B 2007;274: 1377-85. http: //

Li MH, Zerabruk M, Vangen O, Olsaker I, Kantanen J. Reduced genetic structure of north Ethiopian cattle revealed by Y-chromosome analysis. Heredity 2007;98: 214-21.

FAO. Status and trends report on animal genetic resources. Information document. CGRFA/WG-AnGR-5/09/Inf.7, Rome. Rome: FAO; 2009. p. 2008 [Available at: AnGR_5_09_Inf_7.pdf].

Ivankovic A, Paprika S, Ramljak J, Dovc P, Konjacic M. Mitochondrial DNA-based genetic evaluation of autochthonous cattle breeds in Croatia. Czech J Anim Sci 2014; 59:519-28.

Medugorac I, Medugorac A, Russ I, Veit-Kensch CE, Taberlet P, Luntz B, et al. Genetic diversity of European cattle breeds highlights the conservation value of traditional unselected breeds with high effective population size. Mol Ecol 2009;18:3394-410.

Hiemstra SJ, Dehaas Y, Maki-Tanila A, Gandini G. Local cattle breeds in Europe. Development of policies and strategies for self-sustaining breeds. Wageningen Academic Publisher; 2010 1-154. Magee DA, Machugh DE, Edwards CJ. Interrogation of modern and ancient genomes reveals the complex domestic history of cattle. Anim Front 2014;4:7-22.

Felius M, Beerling ML, Buchanan DS, Theunissen B, Koolmees PA, Lenstra JA. On the history of cattle genetic resources. Diversity 2014;6:705-50.

Beja-Pereira A, Caramelli D, Lalueza-Fox C, Vernesi C, Ferrand N, Casoli A, et al. The origin of European cattle: Evidence from modern and ancient DNA. Proc Natl Acad Sci U S A 2006;103:8113-8. Mason IL, Belyaev DK. Evolution of domestic animals. Edited by Mason IL. New York: Longman; 1984.

Clutton-Brock J. The walking larder: Patterns of domestication, pastoralism and

predation. Am Ethnol 1989;17:802-3.

http: //

Helmer D, Gourichon L, Monchot H, Peters J, Saña SM. Identifying early domestic cattle from Pre-Pottery Neolithic sites on the Midddle Euphratesusing sexual dimorphism. In: Vigne Jd, Helmer D, Peters J, editors. The first steps of animal domestication: new archaeozoological approaches. Oxford (UK): Oxbow Books; 2005. p. 86-95.

Vigne JD, Carrére I, Briois F, Guilaine J. The early process of the mammal domestication in the Near East: New evidence from the Pre-Neolithic and Pre-Pottery Neolithic in Cyprus. Curr Anthropol 2011;4:255-71.

Evershed RP, Payne S, Sherratt AG, Copley MS, Coolidge J, Urem Kotsu D, et al. Earliest date for milk use in the Near East and southeastern Europe linked to cattle herding. Nature 2008;455:528-31. Bradley DG, Machugh DE, Cunningham P, Loftus RT. Mitochondrial diversity and the origins of African and European cattle. Proc Natl Acad Sci U S A 1996;93: 5131-5.

Meadow R Patel AK. Prehistoric pastoralism in Northwestern South Asia from the Neolithic through the Harappan period. In: Weber SA, Belcher WR editors. Indus ethnobiology. New perspectives from the field. Lanham: Lexington Books; 2003. p. 65-94.

Ho SY, Larson G, Edwards CJ, Heupink TH, Lakin KE, Holland PW, et al. Correlating Bayesian date estimates with climatic events and domestication using a bovine case study. Biol Lett 2008;4:370-4. Hassanin A, An J, Ropiquet A, Nguyen TT, Couloux A. Combining multiple autosomal introns for studying shallow phylogeny and taxonomy of Laurasiatherian mammals: Application to the tribe Bovini (Cetartiodactyla, Bovidae). Mol Phylogenet Evol 2013;66:766-75. http ://

Kidd KK, Osterhoff D, Erhard L, Stone WH. The use of genetic relationships among cattle breeds in the formulation of rational breeding policies: An example with South Devon (South Africa) and Gelbvieh (Germany). Anim Blood Groups Biochem Genet 1974;5:21-8.

Bollongino R Burger J, Powell A, Mashkour M, Vigne JD, Thomas MG. Modern taurine cattle descended from small number of near-eastern founders. Mol Biol Evol 2012;29:2101-4.

Scheu A, Powell A, Bollongino R Vigne JD, Tresset A, ^akirlar C, et al. The genetic prehistory of domesticated cattle from their origin to the spread across Europe. BMC Genet 2015;16:54. Brass M. Revisiting a hoary chestnut: The nature of early cattle domestication in North-East Africa. Sahara 2013;24:65.

Troy CS, Machugh DE, Bailey JF, Magee DA, Loftus RT, Cunningam P, et al. Genetic evidence for Near-Eastern origins of European cattle. Nature 2001;410:1088-99.

Mannen H, Kohno M, Nagata Y, Tsuji S, Bradley DG, Yeo JS, et al. Independent mitochondrial origin historical genetic differentiation in North Eastern Asian cattle. Mol Phylogenet Evol 2004;32:539-44. http: //

Bonfiglio S, Achilli A, Olivieri A, Negrini R Colli L, Liotta L, et al. The enigmatic origin of bovine mtDNA Haplogroup R: Sporadic interbreeding or an independent event of Bos primigenius domestication in Italy? PLoS One 2010;5, e15760. http: // /journal.pone.0015760.

Bollongino R Elsner J, Vigne JD, Burger J. Y-SNPs do not indicate hybridisation between European aurochs and domestic cattle. PLoS One 2008;3, e3418. http: // /journal.pone.0003418.

Svensson E, Gotherstrom A. Temporal fluctuations of Y-chromosomal variation in Bos taurus. Biol Lett 2008;4:752-4. Park SD, Magee DA, Mcgettigan PA, Teasdale MD, Edwards CJ, Lohan AJ, et al. Genome sequencing of the extinct Eurasian wild aurochs, Bos primigenius, illuminates the phylogeography and evolution of cattle. Genome Biol 2015;16:234.

Behar DM, Van Oven M, Rosset S, Metspalu M, Loogväli EL, Silva NM, et al. A "Co-pernican" reassessment of the human mitochondrial DNA tree from its root. Am J Hum Genet 2012;90:675-84. Achilli A, Perego UA, Lancioni H, Olivieri A, Gandini F, Hooshiar Kashani B, et al. Reconciling migration models to the Americas with the variation of North American native mitogenomes. Proc Natl Acad Sci U S A 2013;110:14308-13. http: //

Cerezo M, Achilli A, Olivieri A, Perego UA, Gómez-Carballa A, Brisighelli F, et al. Reconstructing ancient mitochondrial DNA links between Africa and Europe. Genome Res 2012;22:821-6. Kivisild T. Maternal ancestry and population history from whole mitochondrial genomes. Invest Genet 2015;6:3. Loftus RT, Machugh DE, Ngere LO, Balain DS, Badi AM, Bradley DG, et al. Mitochondrial genetic variation in European, African and Indian cattle populations. Anim Genet 1994;25:265-71. Edwards JE, Machugh DE, Dobney KM, Martin L, Russel N, Horwitz LK, et al. Ancient DNA analysis of 101 cattle remains: Limits and prospects. J Archaeol Sci 2004;31: 695-710.

Bailey JF, Richards MB, Macaulay VA, Colson IB, James IT, Bradley DG, et al. Ancient DNA suggests a recent expansion of European cattle from a diverse wild progenitor species. Proc R Soc B 1996;263:1467-73. http: //

Cai X, Mipam T, Zhao F, Sun L. Isolation and characterization of polymorphic microsatellites in the genome of yak (Bos grunniens). Mol Biol Rep 2014;41: 3829-37.

Horsburgh KA Prost S, Gosling A, Stanton JA, Rand C, Matisoo-Smith EA. The genetic diversity of the Nguni breed of African Cattle (Bos spp.): Complete mitochondrial genomes of haplogroup T1. PloS one 2013;8, e71956. [Se repite con Referencia [152]]. Decker JE, McKay SD, Rolf MM, Kim J, Alcalá AM, Sonstegard TS, et al. Worldwide patterns of ancestry, divergence, and admixture in domesticated cattle. PLoS Genet 2014;10, e1004254. Colominas L, Edwards CJ, Beja-Pereira A, Vigne JD, Silva rM, Castanyer P, et al. Detecting the T1 cattle haplogroup in the Iberian Peninsula from Neolithic to medieval times: New clues to continuous cattle migration through time. J Archaeol Sci 2015;59:110-7. Schlumbaum A, Turgay M, Schibler J. Near East mtDNA haplotype variants in Roman cattle from Augusta Raurica, Switzerland, and in the Swiss Evoléne breed. Anim Genet 2006;37:373-5. http: // /j.1365-2052.2006.01435.x.

Bollongino R Edwards CJ, Alt KW, Burger J, Bradley DG. Early history of European domestic cattle as revealed by ancient DNA. Biol Lett 2006;2:155-9. http: //

Lari M, Rizzi E, Mona S, Corti G, Catalano G, Chen K, et al. The complete mitochondrial genome of an 11,450-year-old aurochsen (Bos primigenius) from Central Italy. BMC Evol Biol 2011;11:32. Finlay EK, Gaillard C, Vahidi sM, Mirhoseini SZ, Jianlin H, Qi XB, et al. Bayesian inference of population expansions in domestic bovines. Biol Lett 2007;3:449-52.

Jia S, Zhou Y, Lei C, Yao R Zhang Z, Fang X, et al. A new insight into cattle's maternal origin in six Asian countries. J Genet Genomics 2010;37:173-80. http: //

Stock F, Gifford-Gonzalez D. Genetics and African cattle domestication. Afr Archaeol Rev 2013;30:51-72. Pellecchia M, Negrini R Colli L, Patrini M, Milanesi E, Achilli A, et al. The mystery of Etruscan origins: Novel clues from Bos taurus mitochondrial DNA. Proc R Soc B 2007;274:1175-9. Gargani M, Pariset L, Lenstra JA, DE Minicis E, European Cattle Genetic Diversity Consortium^, Valentini A. Microsatellite genotyping of medieval cattle from central Italy suggests an old origin of Chianina and Romagnola cattle. Front Genet 2015;6: 1 -6.

[127] Magee DA, Meghen C, Harrison S, Troy CS, Cymbron T, Gaillard C, et al. A partial african ancestry for the creole cattle populations of the Caribbean. J Hered 2002;93: 429-32.

[128] Carvajal Carmona LG, Bermudez N, Olivera Angel M, Estrada L, Ossa J, Bedoya G, et al. Abundant mtDNA diversity and ancestral admixture in Colombian criollo cattle (Bos taurus). Genetics 2003;165:1457-63.

[129] Mirol PM, Giovambattista G, Lirón JP, Dulout FN. African and European mitochon-drial haplotypes in South American Creole cattle. Heredity 2003;91:248-54. http: //

[130] Miretti MM, Dunner S, Naves M, Contel EP, Ferro JA. Predominant African-derived mtDNA in Caribbean and Brazilian creole cattle is also found in Spanish cattle (Bos taurus). J Hered 2004;95:450-3.

[131 ] Lirón JP, Peral-García P, Giovambattista G. Genetic characterization of Argentine and Bolivian Creole cattle breeds assessed through microsatellites. J Hered 2006; 97:331-9.

[132] Hristov P, Spassov N, Iliev N, Radoslavov G. An independent event of Neolithic cattle domestication on the South-eastern Balkans: Evidence from prehistoric aurochs and cattle populations. Mitochondrial DNA 2015;29:1-9.

[133] Stock F, Edwards CJ, Bollongino R, Finlay EK, Burger J, Bradley DG. Cytochrome b sequences of ancient cattle and wild ox support phylogenetic complexity in the ancient and modern bovine populations. Anim Genet 2009;40:694-700.

[134] Niemi M, Bläuer A, Iso Touru T, Harjula J, Nyström Edmark V, Rannamäe E, et al. Temporal fluctuation in North East Baltic Sea region cattle population revealed by mitochondrial and Y-chromosomal DNA analyses. PLoS One 2015;10, e0123821.

[135] Lopez Oceja A, Muro-Verde A, Gamarra D, Cardoso S, De Pancorbo MM. New Qlin-eage found in bovine (Bos taurus) of Iberian Peninsula. Mitochondrial DNA2015; 27:3597-601.

[136] Chen S, Lin BZ, Baig M, Mitra B, Lopes RJ, Santos AM, et al. Zebu cattle are an exclusive legacy of the South Asia neolithic. Mol Biol Evol 2010;27:1-6.

[137] Magee DA, Mannen H, Bradley D. Duality in Bos indicus mtDNA diversity: Support for geographical complexity in zebu domestication. In: Petraglia MD, Allchin B, editors. The evolution and history of human populations in South Asia: Inter-disciplinary studies in archaeology, biological anthropology, linguistics, and genetics. Dordrecht: Springer; 2007. p. 385-91.

[138] Lei CZ, Chen H, Zhang HC, Cai X, Liu RY, Luo LY, et al. Origin and phylogeographical structure of Chinese cattle. Anim Genet 2006;37:579-82. /j.1365-2052.2006.01524.x.

[139] Yue XP, Dechow C, Chang TC, Dejarnette JM, Marshall CE, Lei CZ, et al. Copy number variations of the extensively amplified Y-linked genes, HSFY and ZNF280BY, in cattle and their association with male reproductive traits in Holstein bulls. BMC Ge-nomics 2014;15:113.

[140] Baig M, Beja-Pereira A, Mohammad R, Kulkarni K, Farah S, Luikart G. Phylogeography and origin of Indian domestic cattle. Curr Sci 2005;89:38-40.

[141] Zhang R, Cheng M, Li X, Chen F, Zheng J, Wang X, et al. Y-SNPs haplotype diversity in four Chinese cattle breeds. Anim Biotechnol 2013;24:288-92.

[142] Verkaar EL, Zijlstra C, Van't Veld EM, Boutaga K, Van Boxtel DC, Lenstra JA. Organization and concerted evolution of the ampliconic Y-chromosomal TSPY genes from cattle. Genomics 2004;84:468-74.

[143] Änderung C, Hellborg L, Seddon J, Hanotte O, Götherström A. Investigation of X-and Y-specific single nucleotide polymorphisms in taurine (Bos taurus) and indicine (Bos indicus) cattle. Anim Genet 2007;38:595-600.

[144] Hellborg L, Ellegren H. Low levels of nucleotide diversity in mammalian Y chromosomes. Mol Biol Evol 2004;21:158-63.

[145] Kysely RA, Hajek MB. MtDNA haplotype identification of aurochs remains originating from the Czech Repubic Environ Archaeol 2012;17:118-25.

[146] Prusak B, Sawicka-Zugaj W, Korwin-Kossakowska A, Grzybowski T. Y chromosome genetic diversity and breed relationships in native Polish cattle assessed by microsatellite markers. Turk J Biol 2015;39:611-7.

[147] Wang X, Zhang YQ, He DC, Yang XM, Li B, Wang DC, et al. The complete mito-chondrial genome of Bos taurus coreanae (Korean native cattle). Mitochon-drial DNA 2014;27:120-1.

[148] Douglas KC, Halbert ND, Kolenda C, Childers C, Hunter DL, Derr JN. Complete mitochondrial DNA sequence analysis of Bison bison and bison-cattle hybrids: Function and phylogeny. Mitochondrion 2011;11:166-75.

[149] Hiendleder S, Lewalski H, Janke A. Complete mitochondrial genomes of Bos taurus and Bos indicus provide new insights into intra-species variation, taxonomy and domestication. Cytogenet Genome Res 2008;120:150-6.

http: //

[150] Ludwig A, Lieckfeldt D, Hesse UG, Froelich K. Tracing the maternal roots of the domestic Red Mountain Cattle. Mitochondrial DNA 2014;27:1080-3.

[151] Ludwig A, Alderson L, Fandrey E, Lieckfeldt D, Soederlund TK, Froelich K. Tracing the genetic roots of the indigenous White Park Cattle. Anim Genet 2013;44:383-6. http: //

[152] Anderson S, de Bruijn MH, Coulson AR, Eperon IC, Sanger F, Young IG. Complete sequence of bovine mitochondrial DNA conserved features of the mammalian mi-tochondrial genome. J Mol Biol 1982;156:683-717.

[153] Li R, Xie WM, Chang ZH, Wang SQ, Dang RH, Lan XY, et al. Y chromosome diversity and paternal origin of Chinese cattle. Mol Biol Rep 2013;40:6633-6.