Origin and spread of Bos taurus: new clues from mitochondrial genomes belonging to haplogroup T1

Abstract

Background: Most genetic studies on modern cattle have established a common origin for all taurine breeds in the Near East, during the Neolithic transition about 10 thousand years (ka) ago. Yet, the possibility of independent and/or secondary domestication events is still debated and is fostered by the finding of rare mitochondrial DNA (mtDNA) haplogroups like P, Q and R. Haplogroup T1, because of its geographic distribution, has been the subject of several investigations pointing to a possible independent domestication event in Africa and suggesting a genetic contribution of African cattle to the formation of Iberian and Creole cattle. Whole mitochondrial genome sequence analysis, with its proven effectiveness in improving the resolution of phylogeographic studies, is the most appropriate tool to investigate the origin and structure of haplogroup T1.

Methodology: A survey of >2200 bovine mtDNA control regions representing 28 breeds (15 European, 10 African, 3 American) identified 281 subjects belonging to haplogroup T1. Fifty-four were selected for whole mtDNA genome sequencing, and combined with ten T1 complete sequences from previous studies into the most detailed T1 phylogenetic tree available to date.

Conclusions: Phylogenetic analysis of the 64 T1 mitochondrial complete genomes revealed six distinct sub-haplogroups (T1a-T1f). Our data support the overall scenario of a Near Eastern origin of the T1 sub-haplogroups from as much as eight founding T1 haplotypes. However, the possibility that one sub-haplogroup (T1d) arose in North Africa, in domesticated stocks, shortly after their arrival from the Near East, can not be ruled out. Finally, the previously identified "African-derived American" (AA) haplotype turned out to be a sub-clade of T1c (T1c1a1). This haplotype was found here for the first time in Africa (Egypt), indicating that it probably originated in North Africa, reached the Iberian Peninsula and sailed to America, with the first European settlers.

Figure 1. Tree of Complete Bovine mtDNA Sequences Belonging to Haplogroup T1.

This tree was built as previously described , . The position of the Bovine Reference Sequence (BRS) is indicated for reading off-sequence motifs. Divergence time estimates are those obtained using ML as reported in Table 3. Branches display mutations with numbers according to the BRS; they are transitions unless a base is explicitly indicated for transversions (to A, G, C, or T) or a suffix for indels (+, d) and should be read as if the BRS was an artificial root. Recurrent mutations are underlined; back mutations at positions that separate the T1 tree from the BRS are prefixed with the superscript @. Note that the reconstruction of recurrent mutations in the control region is ambiguous in a number of cases. Heteroplasmy is marked with a suffix (h). The numbering of sequences is the same as in Table 2. The orange line connecting T1e and T1f to nps 16050 and 16113 reflects the uncertainty of their classification as quasi-sister taxa of sub-haplogroups T1a to T1d and implies the possibility that either one or the other or both might well descend from a T1′2′3′ – T1 intermediate (see Discussion for more details). Note that a potential affiliation of sequence #44 within sub-haplogroup T1e should be also considered (see Results). The pie charts summarize the typing results of the survey performed on our entire dataset of 281 T1 mtDNAs (Table 1) with diagnostic T1 sub-haplogroups markers. The numbers of mtDNAs for each sub-haplogroup are shown and include the 54 mtDNAs completely sequenced in this study, but not those previously published (#3, 4, 10, 22, 23, 29, 37, 46, 49 and 62) (see also Table 2). Colors in the pie charts indicate geographical origins.