Mitochondrial genomes of extinct aurochs survive in domestic cattle
Archaeological and genetic evidence suggest that modern cattle might result from two domestication events of aurochs (Bos primigenius) in southwest Asia, which gave rise to taurine (Bos taurus) and zebuine (Bos indicus) cattle, respectively [1, 2, 3]. However, independent domestication in Africa [4, 5] and East Asia  has also been postulated and ancient DNA data raise the possibility of local introgression from wild aurochs [7, 8, 9]. Here, we show by sequencing entire mitochondrial genomes from modern cattle that extinct wild aurochsen from Europe occasionally transmitted their mitochondrial DNA (mtDNA) to domesticated taurine breeds. However, the vast majority of mtDNAs belong either to haplogroup I (B. indicus) or T (B. taurus). The sequence divergence within haplogroup T is extremely low (eight-fold less than in the human mtDNA phylogeny ), indicating a narrow bottleneck in the recent evolutionary history of B. taurus. MtDNAs of haplotype T fall into subclades whose ages support a single Neolithic domestication event for B. taurusin the Near East, 9–11 thousand years ago (kya).
An Unusual Pattern of Ancient Mitochondrial DNA Haplogroups in Northern African Cattle,
Which is too fiddly to reproduce here.
Microsatellite DNA Variation and the Evolution, Domestication and Phylogeography of Taurine and Zebu Cattle (Bos taurus and Bos indicus)
D. E. MacHugh, M. D. Shriver, R. T. Loftus, P. Cunningham and D. G. Bradley
Department of Genetics, Trinity College, Dublin 2, Ireland
Genetic variation at 20 microsatellite loci was surveyed to determine the evolutionary relationships and molecular biogeography of 20 different cattle populations from Africa, Europe and Asia. Phylogenetic reconstruction and multivariate analysis highlighted a marked distinction between humpless (taurine) and humped (zebu) cattle, providing strong support for a separate origin for domesticated zebu cattle. A molecular clock calculation using bison (Bison sp.) as an outgroup gave an estimated divergence time between the two subspecies of 610,000-850,000 years. Substantial differences in the distribution of alleles at 10 of these loci were observed between zebu and taurine cattle. These markers subsequently proved very useful for investigations of gene flow and admixture in African populations. When these data were considered in conjunction with previous mitochondrial and Y chromosomal studies, a distinctive male-mediated pattern of zebu genetic introgression was revealed. The introgression of zebu-specific alleles in African cattle afforded a high resolution perspective on the hybrid nature of African cattle populations and also suggested that certain West African populations of valuable disease-tolerant taurine cattle are under threat of genetic absorption by migrating zebu herds.
Evidence for two independent domestications of cattle.
R T Loftus, D E MacHugh, D G Bradley, P M Sharp, and P Cunningham
Department of Genetics, Trinity College, Dublin, Ireland.
AbstractThe origin and taxonomic status of domesticated cattle are controversial. Zebu and taurine breeds are differentiated primarily by the presence or absence of a hump and have been recognized as separate species (Bos indicus and Bos taurus). However, the most widely held view is that both types of cattle derive from a single domestication event 8000-10,000 years ago. We have examined mtDNA sequences from representatives of six European (taurine) breeds, three Indian (zebu) breeds, and four African (three zebu, one taurine) breeds. Similar levels of average sequence divergence were observed among animals within each of the major continental groups: 0.41% (European), 0.38% (African), and 0.42% (Indian). However, the sequences fell into two very distinct geographic lineages that do not correspond with the taurine-zebu dichotomy: all European and African breeds are in one lineage, and all Indian breeds are in the other. There was little indication of breed clustering within either lineage. Application of a molecular clock suggests that the two major mtDNA clades diverged at least 200,000, and possibly as much as 1 million, years ago. This relatively large divergence is interpreted most simply as evidence for two separate domestication events, presumably of different subspecies of the aurochs, Bos primigenius. The clustering of all African zebu mtDNA sequences within the taurine lineage is attributed to ancestral crossbreeding with the earlier B. taurus inhabitants of the continent.
Mitochondrial diversity and the origins of African and European cattle
Daniel G. Bradley, David E. MacHugh, Patrick Cunningham, and Ronan T. Loftus
The nature of domestic cattle origins in Africa are unclear as archaeological data are relatively sparse. The earliest domesticates were humpless, or Bos taurus, in morphology and may have shared a common origin with the ancestors of European cattle in the Near East. Alternatively, local strains of the wild ox, the aurochs, may have been adopted by peoples in either continent either before or after cultural influence from the Levant. This study examines mitochondrial DNA displacement loop sequence variation in 90 extant bovines drawn from Africa, Europe, and India. Phylogeny estimation and analysis of molecular variance verify that sequences cluster significantly into continental groups. The Indian Bos indicus samples are most markedly distinct from the others, which is indicative of a B. taurus nature for both European and African ancestors. When a calibration of sequence divergence is performed using comparisons with bison sequences and an estimate of 1 Myr since the Bison/Bos Leptobos common ancestor, estimates of 117-275,000 B.P. and 22-26,000 B.P. are obtained for the separation between Indians and others and between African and European ancestors, respectively. As cattle domestication is thought to have occurred approximately 10,000 B.P., these estimates suggest the domestication of genetically discrete aurochsen strains as the origins of each continental population. Additionally, patterns of variation that are indicative of population expansions (probably associated with the domestication process) are discernible in Africa and Europe. Notably, the genetic signatures of these expansions are clearly younger than the corresponding signature of African/European divergence.
Extensive MHC class II DRB3 diversity in African and European cattle
Sofia Mikko1 and Leif Anderson1
Genetic deversity at the highly polymorphic BoLA-DRB3 locus was investigated by DNA sequence analyses of 18 African cattle from two breeds representing the two subspecies of cattle, Bos primigenius indicus and Bos primigenius taurus. Yhe polymorphism was compared with that found in a sample ofd 32 European cattle from four breeds, all classified as B. p. taurus. Particularly extensive genetic diversity was found among African cattle, in which as many as 18 alleles were recognized in this small random sample of animals from two breeds. The observed similarity in allele frequency distribution between the two African populations, N’Dama and Zebu cattle, is consistent with the recent recognition of gene flow between B. p. indicus and B. P taurus cattle in Africa. A total of 30 DRB3 alleles were documented and as many as 26 of these were classified as major allelic types showing at least five amino acid substitutions compared with other major types. The observation of extensive genetic diversity at MHC loci in cattle, as well as in other farm animals, provides a compelling argument against matin-type preferences as a primary cause in maintaining major histocompatibility complex diversity, since the reproduction of these animals has been controlled by humans for many generations.
The nucleotide sequence data reported in this paper have been submitted to the EMBL nucleotide sequence database and have been given the accession numbers X87641-X87670
An Unusual Pattern of Ancient Mitochondrial DNA Haplogroups in Northern African Cattle
Comparative DNA studies of the control region for mitochondrial DNA (mtDNA) have revealed surprising complexity in the evolutionary history of Old and New World livestock species (Bruford et al. 2003). For the greater Mediterranean area, these analyses have shown that the mitochondrial control region haplotypes for modern cattle (i.e., Bos taurus) belong to one of 4 sequence clusters or haplogroups (Fig. 1). Most (94%) modern cattle populations from Northern Africa carry haplogroup T1, which is rarely found outside of Africa (6% in the Near East and absent elsewhere). In contrast, modern populations from mainland Europe carry 2 very similar haplogroups, T and T3 (94%), which decrease in the Middle East (65%-74%) and almost completely disappear in Africa (6%). Haplogroup T2 makes up the remainder of this mtDNA diversity and is present at 6% in Europe and 21%-27% in the Near East, but is absent from Africa. These haplogroup distributions have been interpreted as indicating a Near East origin for European B. taurus and the independent domestication of cattle in Africa (Bradley et al. 1996, Troy et al. 2001, Hanotte et al. 2002).
In this note, we report on the analysis of an ancient mtDNA (control region) sequence as
obtained from a bovine skeletal sample from an early, first millennium, archaeological site near the community of Adi Nefas, Eritrea in Northeastern Africa (900 yr before the present; YBP; Schmidt and Curtis 2001) (Fig. 1). This newly acquired ancient DNA sequence is combined with data for the same mitochondrial control region as determined for 4 specimens from Mali, Northwestern Africa (ca. 900-2200 YBR; Edwards et al. 2004). In concert with the modern mtDNA data, these 5 ancient DNA sequences raise the possibility that the mtDNA gene pool for Northern African cattle was more diverse ca. 900-2000 yr ago.
MATERIALS AND METHODS
The original source of the ancient DNA from Eritrea consisted of a bone section (2 g) that was obtained from a larger piece of fragmented bone. Multiple DNA extractions, amplifications, cloning, and sequencing were performed according to established procedures for ancient DNA (Mulligan 2005). The DNA amplifications and sequencing
relied on the primer pair, AN1 (5′-ACGCGGCAT GGTAATTAAGC-3′) and AN2 (5′-GCCCCAT
GCATATAAGCAAG-3′), for an internal segment of the mitochondrial control region (see below).
Throughout this study, rigorous safeguards were routinely employed to ensure the authenticity of the final sequence, e.g., the DNA extractions and amplifications were conducted in a separate laboratory and building with positive air pressure and HEPA air filtration where no previous bovid material, either contemporary or ancient, had ever been
analyzed. In general, hot arid climates result in poorer organic preservation than colder climates (Edwards et al. 2004). Thus, the fact that this specimen was associated with a cool highland environment may have facilitated the successful DNA extraction.
RESULTS AND DISCUSSION
The new ancient DNA sequence from Adi Nefas, Eritrea was 116 base pairs in length
(GenBank accession no.: AY524815), corresponding to positions 16,042-16,157 of the bovine mtDNA genome (Anderson et al. 1982). This mtDNA sequence is identical to a known control region haplotype for B. taurus (L27727; Loftus et al. 1994). Thus, as a representative of L27727, this ancient DNA sequence belongs to the combined haplogroup T/T3, which is common in modern cattle populations from Europe and the Near East, but rare in those from Northern Africa (Fig. 1). Furthermore, as characteristic of B. taurus, it corroborates the initial morphological identification Fig.
The previously reported ancient mtDNA sequences for the 4 Mali individuals consist of 1
T/T3 and 3 T1 haplotypes (Edwards et al. 2004). Combining the new Eritrean sequence with these 4 Mali orthologues resulted in an ancient mtDNA sample for Northern Africa of 2 T/T3 and 3 T1 haplotypes (Fig. 1). Assuming that these 5 represent a valid random sample (which admittedly is unlikely), a standard binomial test reveals that the probability of drawing by chance 2 or more T/T3 sequences out of five, given the contemporary haplogroup frequencies for Northern African cattle (Fig. 1), is only 3.5%. Minimally, this result highlights the fact that this set of 5 ancient DNA sequences appearsunusual, because of the greater frequency of the rare T/T3 haplogroups compared to modern populations of Northern African cattle.
In conclusion, our results raise the possibility that the mtDNA gene pool for Northern African cattle ca. 900-2000 yr ago was more polymorphic in terms of the frequencies of the T1 and T/T3 haplogroups that currently predominate in African and European populations, respectively. This older polymorphism in Northern African cattle may reflect a transition from an even more-diverse ancestral gene pool (as characteristic of its Near East progenitor) and/or the later secondary introduction of T/T3 haplotypes into this region by the immigration of European cattle (Hanotte et al. 2002, Bruford et al. 2003). Concomitantly, selective pressures from domestication and breeding efforts and/or genetic drift may have then led to the final homogenization of this older polymorphism into the current situation of essentially only the T1 haplogroup occurring in Northern Africa. These possibilities reemphasize the fact that both ancient and modern DNA data are of value in the ultimate resolution of the complex history of African cattle
(Edwards et al. 2004).
Early history of European domestic cattle as revealed by ancient DNA
We present an extensive ancient DNA analysis of mainly Neolithic cattle bones sampled from archaeological sites along the route of Neolithic expansion, from Turkey to North-Central Europe and Britain. We place this first reasonable population sample of Neolithic cattle mitochondrial DNA sequence diversity in context to illustrate the continuity of haplotype variation patterns from the first European domestic cattle to the present. Interestingly, the dominant Central European pattern, a starburst phylogeny around the modal sequence, T3, has a Neolithic origin, and the reduced diversity within this cluster in the ancient samples accords with their shorter history of post-domestic accumulation of mutation.
Genetics and Domestic Cattle Origins
Genetics has the potential to provide a novel layer of information pertaining to the origins and relationships of domestic cattle. While it is important not to overstate the power of archeological inference from genetic data, some previously widespread conjectures are inevitably contradicted with the addition of new information. Conjectures regarding domesticated cattle that fall into this category include a single domestication event with the development of Bos indicus breeds from earlier Bos taurus domesticates; the domestication of a third type of cattle in Africa having an intermediate morphology between the two taxa; and the special status of the Jersey breed as a European type with some exotic influences. In reality, a wideranging survey of the genetic variation of modern cattle reveals that they all derive from either zebu or taurine progenitors or are hybrids of the two. The quantitative divergence between Bos indicus and Bos taurus strongly supports a predomestic separation; that between African and European taurines also suggests genetic input from native aurochsen populations on each continent. Patterns of genetic variants assayed from paternally, maternally, and biparentally inherited genetic systems reveal that extensive hybridization of the two subspecies is part of the ancestry of Northern Indian, peripheral European, and almost all African cattle breeds. In Africa, which is the most extensive hybrid zone, the sexual asymmetry of the process of zebu introgression into native taurine breeds is strikingly evident.
Figure 1. This map shows approximate distributions for the various types of domesticated cattle found in Asia, Africa, and Europe. Also shown are distributions for the closely related Bibos species, banteng and gaur. This diagram is modified from Payne6 and Epstein and Mason.5