Large‐scale mitogenome sequencing reveals consecutive expansions of domestic taurine cattle and supports sporadic aurochs introgression

Abstract

The contribution of domestic cattle in human societies is enormous, making cattle, along with other essential benefits, the economically most important domestic animal in the world today. To expand existing knowledge on cattle domestication and mitogenome diversity, we performed a comprehensive complete mitogenome analysis of the species (802 sequences, 114 breeds). A large sample was collected in South‐east Europe, an important agricultural gateway to Europe during Neolithization and a region rich in cattle biodiversity. We found 1725 polymorphic sites (810 singletons, 853 parsimony‐informative sites and 57 indels), 701 unique haplotypes, a haplotype diversity of 0.9995 and a nucleotide diversity of 0.0015. In addition to the dominant T 3 and several rare haplogroups (Q, T 5 , T 4 , T 2 and T 1 ), we have identified maternal line in Austrian Murbodner cattle that possess surviving aurochs’ mitochondria haplotype P 1 that diverged prior to the Neolithization process. This is convincing evidence for rare female‐mediated adaptive introgression of wild aurochs into domesticated cattle in Europe. We revalidated the existing haplogroup classification and provided Bayesian phylogenetic inference with a more precise estimated divergence time than previously available. Occasionally, classification based on partial mitogenomes was not reliable; for example, some individuals with haplogroups P and T 5 were not recognized based on D‐loop information. Bayesian skyline plot estimates (median) show that the earliest population growth began before domestication in cattle with haplogroup T 2 , followed by Q (~10.0–9.5 kyBP), whereas cattle with T 3 (~7.5 kyBP) and T 1 (~3.0–2.5 kyBP) expanded later. Overall, our results support the existence of interactions between aurochs and cattle during domestication and dispersal of cattle in the past, contribute to the conservation of maternal cattle diversity and enable functional analyses of the surviving aurochs P 1 mitogenome.

Recovery of mitogenomes from whole genome sequences to infer maternal diversity in 1883 modern taurine and indicine cattle

“…Like us, Cubric-Curik and colleagues found that MitoToolpy assigned T6 to some Angus animals, but they reported no statistical evidence for T6 using BEAST software 56 which assigned the same animals to the T3 group (agreement was good for most other haplogroups). In agreement with Cubric-Curik et al 30 , we recommend using whole mitogenomes with MitoToolpy because some haplogroups failed to separate using only the D-loop region. In addition to the conventional diversity indices, we have investigated alternate ways of analysing population structure and haplotypes of the entire mitogenome, that do not rely on predefined haplogroups and therefore capture a broader spectrum of the diversity.…”

“…The R haplogroup is relatively rare and previously has been identified occasionally in Italian breeds 30 , 55 . The low representation of P, Q, T4, T5 and T6 was also in line with a recent study by Cubric-Curik et al 30 . Like us, Cubric-Curik and colleagues found that MitoToolpy assigned T6 to some Angus animals, but they reported no statistical evidence for T6 using BEAST software 56 which assigned the same animals to the T3 group (agreement was good for most other haplogroups).…”

“…Our large sample size enabled identification of all major haplogroups (I1, I2, P, Q, T1 to T6) except for R, subgrouping within haplogroups and breeds as well as annotation of the private variants. The R haplogroup is relatively rare and previously has been identified occasionally in Italian breeds 30 , 55 . The low representation of P, Q, T4, T5 and T6 was also in line with a recent study by Cubric-Curik et al 30 .…”

“…To date, most mitochondrial molecular diversity studies in cattle are primarily evaluated based on the non-coding hypervariable control region (D-loop) or involved limited breeds either within a country or within a region 15 , 20 , 28 , 29 . While the partial or whole D-loop region is informative for population genetics because it is hyper-variable, whole mitochondrial genome sequences are more likely to reflect the full range of mitochondrial genomic diversity 30 . Now that large sequence databases for cattle are available, it is timely to undertake a comprehensive study involving worldwide breeds, countries and continents for a holistic understanding of the mitochondrial genomic landscape in modern cattle.…”

A Fast Method for the Selection of Samples in Populations with Available Genealogical Data

“…As a result, it would take hours and days to process pedigrees with the number of individuals in the orders of magnitude of 10 5 and 10 6 , respectively. Magellan software was successfully used in population genetics analysis [5], but the sample selection is possible only on the comparatively small pedigrees.…”