The multifaceted origin of taurine cattle reflected by the mitochondrial genome

Abstract

A Neolithic domestication of taurine cattle in the Fertile Crescent from local aurochsen (Bos primigenius) is generally accepted, but a genetic contribution from European aurochsen has been proposed. Here we performed a survey of a large number of taurine cattle mitochondrial DNA (mtDNA) control regions from numerous European breeds confirming the overall clustering within haplogroups (T1, T2 and T3) of Near Eastern ancestry, but also identifying eight mtDNAs (1.3%) that did not fit in haplogroup T. Sequencing of the entire mitochondrial genome showed that four mtDNAs formed a novel branch (haplogroup R) which, after the deep bifurcation that gave rise to the taurine and zebuine lineages, constitutes the earliest known split in the mtDNA phylogeny of B. primigenius. The remaining four mtDNAs were members of the recently discovered haplogroup Q. Phylogeographic data indicate that R mtDNAs were derived from female European aurochsen, possibly in the Italian Peninsula, and sporadically included in domestic herds. In contrast, the available data suggest that Q mtDNAs and T subclades were involved in the same Neolithic event of domestication in the Near East. Thus, the existence of novel (and rare) taurine haplogroups highlights a multifaceted genetic legacy from distinct B. primigenius populations. Taking into account that the maternally transmitted mtDNA tends to underestimate the extent of gene flow from European aurochsen, the detection of the R mtDNAs in autochthonous breeds, some of which are endangered, identifies an unexpected reservoir of genetic variation that should be carefully preserved.

Figure 1. Tree of Complete MtDNA Sequences from Cattle.

This tree illustrates the relationships between the common macro-haplogroups T and I and the rare mtDNAs belonging to haplogroups P, Q and R. Haplogroup E (dashed line) refers to the partial previously reported mtDNA data from a German aurochs , . Divergence times are an average of the ML and ρ estimates reported in Table 2. BRS indicates the Bos taurus reference sequence (GenBank acc. no. V00654) . Mutations are shown on the branches and are numbered according to the BRS; they are transitions unless a base is explicitly indicated; suffixes indicate transversions (to A, G, C, or T) or indels (+, d) and have to be read as if BRS was an artificial root. Recurrent mutations are underlined, and true back mutations with respect to evolutionary direction are prefixed with the superscript β (beta) in addition (which is thus in alternation with prefix @ on the path between the overall root and BRS). Heteroplasmy is marked with a suffix (h). Mutations explicitly listed above the REPQTI node are those reverted at least once in the branches below that node, while the additional 659 mutations are those shared between Bison bison and Bos grunniens as reported in Achilli et al. , except for 249@, 5743@, 7356@, 12377@, 15627@, 15994@, and 16264. Note that the reconstruction of recurrent mutations in the control region is ambiguous in a number of cases. Breeds for the samples harbouring mtDNAs belonging to haplogroups Q, P and R are as follows: Chianina (1); Romagnola (2); Italian Red Pied (3); Romagnola (4); Cabannina (5, 6); “Beef cattle”, Korea (7); Agerolese (8); Cinisara (9, 10); Romagnola (11).

Figure 2. Most Parsimonious Phylogeny of Cattle MtDNA.

This unrooted tree is drawn to scale using ML distances (Table 2) and includes all available P, Q and R complete mtDNA sequences, including those reported in Achilli et al. . The placement of the E branch (dashed line) is based on a partial control-region and coding-region data from a German aurochs , . The Paleolithic painting of aurochsen (B. primigenius) is from the Lascaux cave (southern France).