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Pervasive introgression facilitated domestication and adaptation in the Bos species complex

Nature Ecology & Evolution volume 2, pages 1139–1145 (2018)Cite this article

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Abstract

Species of the Bos genus, including taurine cattle, zebu, gayal, gaur, banteng, yak, wisent and bison, have been domesticated at least four times and have been an important source of meat, milk and power for many human cultures. We sequence the genomes of gayal, gaur, banteng, wisent and bison, and provide population genomic sequencing of an additional 98 individuals. We use these data to determine the phylogeny and evolutionary history of these species and show that the threatened gayal is an independent species or subspecies. We show that there has been pronounced introgression among different members of this genus, and that it in many cases has involved genes of considerable adaptive importance. For example, genes under domestication selection in cattle (for example, MITF) were introgressed from domestic cattle to yak. Also, genes in the response-to-hypoxia pathway (for example, EGLN1, EGLN2 and HIF3a) have been introgressed from yak to Tibetan cattle, probably facilitating their adaptation to high altitude. We also validate that there is an association between the introgressed EGLN1 allele and haemoglobin and red blood cell concentration. Our results illustrate the importance of introgression as a source of adaptive variation and during domestication, and suggest that the Bos genus evolves as a complex of genetically interconnected species with shared evolutionary trajectories.

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Fig. 1: Phylogenetic tree and genetic introgression of species in the Bos genus.
Fig. 2: Distribution of regions in the genome where introgression occurred between Tibetan cattle and yak.
Fig. 3: Genetic introgression of EGLN1 from yak to Tibetan cattle.

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Acknowledgements

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No XDB13020600), National Natural Science Foundation of China (91731304, 31321002, 31272418, 31561143010), the Chinese 973 program (2013CB835204), Animal Branch of the Germplasm Bank of Wild Species (GBOWS) and the Program for Changjiang Scholar and Innovation Research Team in University (IRT_15R621). D.-D.W. was supported by the Youth Innovation Promotion Association, Chinese Academy of Sciences.

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Author notes

  1. These authors contributed equally: Dong-Dong Wu, Xiang-Dong Ding, Sheng Wang, Jan M. Wójcik, Yi Zhang.

Authors and Affiliations

  1. State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China

    Dong-Dong Wu, Ming-Shan Wang & Ya-Ping Zhang

  2. Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, China

    Dong-Dong Wu, Ming-Shan Wang & Ya-Ping Zhang

  3. Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China

    Dong-Dong Wu & Ya-Ping Zhang

  4. Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture, National Engineering Laboratory for Animal Breeding, College of Animal Science and Technology, China Agricultural University, Beijing, China

    Xiang-Dong Ding, Sheng Wang, Yi Zhang & Qin Zhang

  5. Mammal Research Institute Polish Academy of Sciences, Białowieża, Poland

    Jan M. Wójcik & Małgorzata Tokarska

  6. State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan University, Kunming, China

    Yan Li

  7. Department of Animal Breeding and Genetics, Bangladesh Agricultural University, Mymensingh, Bangladesh

    Omar Faruque

  8. Department of Integrative Biology, University of California Berkeley, Berkeley, CA, USA

    Rasmus Nielsen

  9. College of Animal Science and Technology, Shandong Agricultural University, Taian, China

    Qin Zhang

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Contributions

Y.-P.Z., D.-D.W., R.N. and Q.Z. lead the project, and designed and conceived the study. D.-D.W., S.W., X.-D.D. and R.N. prepared the manuscript. D.-D.W., S.W., X.-D.D., Y. Z., Y.L. and M.-S.W. performed the data analysis. J.M.W., M.T. and O.F. performed some sampling and experiments. All authors read the manuscript.

Corresponding authors

Correspondence to Dong-Dong Wu, Rasmus Nielsen, Qin Zhang or Ya-Ping Zhang.

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Supplementary information

Supplementary Information

Supplementary Figures and tables 1–4

Reporting Summary

Supplementary table 5

Genetic introgression between gayal and zebu

Supplementary table 6

Genetic introgression between bali cattle and zebu

Supplementary table 7

Gene enrichment analysis genes within regions showing genetic introgression between zebu and gayal

Supplementary table 8

Gene enrichment analysis genes within regions showing genetic introgression between zebu and bali cattle

Supplementary table 9

Genetic introgression between yak and Tibetan cattle

Supplementary table 10

Gene enrichment analysis genes within regions showing genetic introgression between yak and Tibetan cattle

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Wu, DD., Ding, XD., Wang, S. et al. Pervasive introgression facilitated domestication and adaptation in the Bos species complex. Nat Ecol Evol 2, 1139–1145 (2018). https://doi.org/10.1038/s41559-018-0562-y

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