Ancient cattle genomics, origins, and rapid turnover in the Fertile Crescent

Verdugo, Marta Pereira; Mullin, Victoria E.; Scheu, Amelie; Mattiangeli, Valeria; Daly, Kevin G.; Delser, Pierpaolo Maisano; Hare, Andrew J.; Bürger, Joachim; Collins, Matthew J.; Kehati, Ron; Hesse, Paula Wapnish; Fulton, Deirdre N.; Sauer, Eberhard; Karimlu, Azadeh Fatemeh Mohaseb; Davoudi, Hossein; Khazaeli, Roya; Lhuillier, Johanna; Rapin, Claude; Ebrahimi, Saeed; Khasanov, Mutalib; Vahidi, S.; MacHugh, David E.; Ertuğrul, Okan; Koukouli-Chrysanthaki, Chaido; Σαμψών, Αδαμάντιος; Kazantzis, G.; Kontopoulos, Ioannis; Bulatović, Jelena; Stojanović, Ivana; Mikdad, Abdesalam; Benecke, Norbert; Linstädter, Jörg; Sablin, Mikhail; Bendrey, Robin; Gourichon, Lionel; Arbuckle, Benjamin S.; Mashkour, Marjan; Orton, David; Horwitz, Liora Kolska; Teasdale, Matthew D.; Bradley, Daniel G.

doi:10.1126/science.aav1002

Cited by 138 publications

(60 citation statements)

References 127 publications

(149 reference statements)

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“…A breeding scheme focusing on zebu male has been postulated to be at the root of this discrepancy between the mitochondrial and nuclear ancestries of the present-day African cattle [16][17][18]23]. This hypothesis is based on (i) unbalanced sex ratio in the zebu herds migrated from South Asia, (ii) pastoralists' preferences for male zebu phenotypes such as their large body size, and/or (iii) the male-biased breeding structure of African cattle herds, where typically only a few sires will contribute to the next generation [24][25][26][27]. Nevertheless, the genomic discrepancy in African humped cattle has not been empirically explained yet.…”

Section: Introductionmentioning

confidence: 99%

Mitonuclear incompatibility as a hidden driver behind the genome ancestry of African admixed cattle

et al. 2022

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Background Africa is an important watershed in the genetic history of domestic cattle, as two lineages of modern cattle, Bos taurus and B. indicus, form distinct admixed cattle populations. Despite the predominant B. indicus nuclear ancestry of African admixed cattle, B. indicus mitochondria have not been found on the continent. This discrepancy between the mitochondrial and nuclear genomes has been previously hypothesized to be driven by male-biased introgression of Asian B. indicus into ancestral African B. taurus. Given that this hypothesis mandates extreme demographic assumptions relying on random genetic drift, we propose a novel hypothesis of selection induced by mitonuclear incompatibility and assess these hypotheses with regard to the current genomic status of African admixed cattle. Results By analyzing 494 mitochondrial and 235 nuclear genome sequences, we first confirmed the genotype discrepancy between mitochondrial and nuclear genome in African admixed cattle: the absence of B. indicus mitochondria and the predominant B. indicus autosomal ancestry. We applied approximate Bayesian computation (ABC) to assess the posterior probabilities of two selection hypotheses given this observation. The results of ABC indicated that the model assuming both male-biased B. indicus introgression and selection induced by mitonuclear incompatibility explains the current genomic discrepancy most accurately. Subsequently, we identified selection signatures at autosomal loci interacting with mitochondria that are responsible for integrity of the cellular respiration system. By contrast with B. indicus-enriched genome ancestry of African admixed cattle, local ancestries at these selection signatures were enriched with B. taurus alleles, concurring with the key expectation of selection induced by mitonuclear incompatibility. Conclusions Our findings support the current genome status of African admixed cattle as a potential outcome of male-biased B. indicus introgression, where mitonuclear incompatibility exerted selection pressure against B. indicus mitochondria. This study provides a novel perspective on African cattle demography and supports the role of mitonuclear incompatibility in the hybridization of mammalian species.

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Section: Introductionmentioning

confidence: 99%

Mitonuclear incompatibility as a hidden driver behind the genome ancestry of African admixed cattle

et al. 2022

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“…Chen et al ( 2018 ) showed that indicine cattle can be further subdivided into Indian and Chinese indicines. Recently, genomic analyses of ancient bones have confirmed that interbreeding of local and geographically distinct aurochs with modern cattle has contributed to the genetic diversity of modern cattle (Park et al, 2015 ; Verdugo et al, 2019 ). Thus, all the results obtained show that the domestication of cattle is a very complex process that, although well studied, still leaves a number of questions unanswered (Larson & Burger, 2013 ).…”

Section: Introductionmentioning

confidence: 99%

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

Ćurik

Novosel

Brajkovic

et al. 2021

Evolutionary Applications

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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.

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“…Future applications could include examining ancient Y-chromosome and mitochondrial lineages in ancient cattle ( Verdugo et al 2019 ), wolves, and dogs ( Bergström, Frantz, et al 2020 ; Loog et al 2020 ), for which large turnovers have occurred.…”

Section: Discussionmentioning

confidence: 99%

Placing Ancient DNA Sequences into Reference Phylogenies

Martiniano

Sanctis

Durbin

2022

Molecular Biology and Evolution

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Joint phylogenetic analysis of ancient DNA (aDNA) with modern phylogenies is hampered by low sequence coverage and post-mortem deamination, often resulting in over-conservative or incorrect assignment. We provide a new efficient likelihood-based workflow, pathPhynder, that takes advantage of all the polymorphic sites in the target sequence. This effectively evaluates the number of ancestral and derived alleles present on each branch and reports the most likely placement of an ancient sample in the phylogeny and a haplogroup assignment, together with alternatives and supporting evidence. To illustrate the application of pathPhynder, we show improved Y chromosome assignments for published ancient DNA sequences, using a newly compiled Y variation dataset (120,908 markers from 2,014 samples) that significantly enhances Y haplogroup assignment for low coverage samples. We apply the method to all published male ancient DNA samples from Africa, giving new insights into ancient migrations and the relationships between ancient and modern populations. The same software can be used to place samples with large amounts of missing data into other large non-recombining phylogenies such as the mitochondrial tree.

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Ancient cattle genomics, origins, and rapid turnover in the Fertile Crescent

Cited by 138 publications

References 127 publications

Mitonuclear incompatibility as a hidden driver behind the genome ancestry of African admixed cattle

Mitonuclear incompatibility as a hidden driver behind the genome ancestry of African admixed cattle

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

Placing Ancient DNA Sequences into Reference Phylogenies

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