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Cited by 416Genetic and phenotypic traits in livestockGenetic diversity and population structureForensic and Genetic Research

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Whole-genome resequencing reveals world-wide ancestry and adaptive introgression events of domesticated cattle in East Asia

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Chen, Ningbo, Cai, Yudong, Chen, Qiuming, Li, Ran, Wang, Kun, Huang, Yongzhen, Hu, Songmei, Huang, Shisheng, Zhang, Hucai, Zheng, Zhuqing, Song, Weining, Ma, Zhijie, Ma, Yun, Dang, Ruihua, Zhang, Zijing, Xu, Lei, Jia, Yutang, Liu, Shanzhai, Yue, Xiangpeng, Deng, Weidong, Zhang, Xiaoming, Sun, Zhouyong, Lan, Xianyong, Han, Jianlin, Chen, Hong, Bradley, Daniel G, Jiang, Yu, Lei, Chuzhao·2018·Nature Communications
DOI 10.1038/s41467-018-04737-0PMC PMC6002414
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Abstract

Cattle domestication and the complex histories of East Asian cattle breeds warrant further investigation. Through analysing the genomes of 49 modern breeds and eight East Asian ancient samples, worldwide cattle are consistently classified into five continental groups based on Y-chromosome haplotypes and autosomal variants. We find that East Asian cattle populations are mainly composed of three distinct ancestries, including an earlier East Asian taurine ancestry that reached China at least ~3.9 kya, a later introduced Eurasian taurine ancestry, and a novel Chinese indicine ancestry that diverged from Indian indicine approximately 36.6-49.6 kya. We also report historic introgression events that helped domestic cattle from southern China and the Tibetan Plateau achieve rapid adaptation by acquiring ~2.93% and ~1.22% of their genomes from banteng and yak, respectively. Our findings provide new insights into the evolutionary history of cattle and the importance of introgression in adaptation of cattle to new environmental challenges in East Asia.

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Fig. 1 Population structuring and relationship of East Asian cattle. a Geographic map indicating the origins of the cattle breeds in this study. Breed name associated with serial number is listed in Fig. 2a. Principal component analysis (PCA) showing PC1 against PC2 (b) and PC1 against PC3 (c). d A neighbour-joining phylogenetic tree constructed using whole-genome SNP data. The scale bar represents pairwise distances between different individuals. Colours reflect the geographic regions of sampling
Fig. 1 Population structuring and relationship of East Asian cattle. a Geographic map indicating the origins of the cattle breeds in this study. Breed name associated with serial number is listed in Fig. 2a. Principal component analysis (PCA) showing PC1 against PC2 (b) and PC1 against PC3 (c). d A neighbour-joining phylogenetic tree constructed using whole-genome SNP data. The scale bar represents pairwise distances between different individuals. Colours reflect the geographic regions of samplingCC BY · PubMed Central
Fig. 2 Autosomal and Y-chromosome evidence for the origin of modern cattle. a Model-based clustering of cattle breeds using ADMIXTURE with K = 5. Breeds are arranged by geographic regions and labelled with serial numbers. b Spatial distribution of five ADMIXTURE coefficients labelled according to geographical maxima. c Y haplogroup distribution of modern cattle. The size of each circle is proportional to the number of samples per breed. Five breeds and their corresponding colour codes are selected to represent the five types of ancestry and haplogroup
Fig. 2 Autosomal and Y-chromosome evidence for the origin of modern cattle. a Model-based clustering of cattle breeds using ADMIXTURE with K = 5. Breeds are arranged by geographic regions and labelled with serial numbers. b Spatial distribution of five ADMIXTURE coefficients labelled according to geographical maxima. c Y haplogroup distribution of modern cattle. The size of each circle is proportional to the number of samples per breed. Five breeds and their corresponding colour codes are selected to represent the five types of ancestry and haplogroupCC BY · PubMed Central
Fig. 3 Y-chromosome haplogroup and phylogeny of complete mitogenomes from modern cattle. a Median-joining (MJ) network of Y-chromosome haplotypes using 745 SNPs. b Rooted maximum-likelihood phylogenetic tree detailing the relationships among all available bovine haplogroups of I, P, Q, R and T mitogenomes, an American bison mitogenome and three yak mitogenomes. c MJ network of mitogenomes from Bos indicus. The black line and circle in b and c represent published reference sequences, respectively
Fig. 3 Y-chromosome haplogroup and phylogeny of complete mitogenomes from modern cattle. a Median-joining (MJ) network of Y-chromosome haplotypes using 745 SNPs. b Rooted maximum-likelihood phylogenetic tree detailing the relationships among all available bovine haplogroups of I, P, Q, R and T mitogenomes, an American bison mitogenome and three yak mitogenomes. c MJ network of mitogenomes from Bos indicus. The black line and circle in b and c represent published reference sequences, respectivelyCC BY · PubMed Central
Fig. 4 Relationship of ancient Chinese cattle to present-day cattle and genetic diversity of the five “core” cattle groups. a Neighbour-joining tree of the relationship between the ancient Chinese cattle and five “core” groups. The scale bar represents the pairwise distances between different individuals. b Shared drift with ancient Shimao cattle in 42 modern-day cattle populations using the outgroup-f3 statistics (Indicine cattle; Ancient, X). The indicine cattle include three individuals of Hariana, Sahiwal and Tharparkar cattle. c Genome-wide distribution of nucleotide diversity of five “core” cattle groups in 50-kb non-overlapping windows. The horizontal line inside the box corresponds to the median of this distribution, the bottom and top of the box are the first and third quartiles. Data points outside the whiskers can be considered as outliers. d Venn diagram showing unique and shared SNPs among the five “core” cattle groups
Fig. 4 Relationship of ancient Chinese cattle to present-day cattle and genetic diversity of the five “core” cattle groups. a Neighbour-joining tree of the relationship between the ancient Chinese cattle and five “core” groups. The scale bar represents the pairwise distances between different individuals. b Shared drift with ancient Shimao cattle in 42 modern-day cattle populations using the outgroup-f3 statistics (Indicine cattle; Ancient, X). The indicine cattle include three individuals of Hariana, Sahiwal and Tharparkar cattle. c Genome-wide distribution of nucleotide diversity of five “core” cattle groups in 50-kb non-overlapping windows. The horizontal line inside the box corresponds to the median of this distribution, the bottom and top of the box are the first and third quartiles. Data points outside the whiskers can be considered as outliers. d Venn diagram showing unique and shared SNPs among the five “core” cattle groupsCC BY · PubMed Central
Fig. 5 Phylogenetic analyses of SNP data confirm the Bos javanicus introgression into Chinese indicine cattle or the yak introgression into Tibetan taurine cattle. a, b Bos javanicus introgression plots constructed based on whole-genome sequencing data from two representative segments on chromosomes 5 and 13. The relative frequencies of Bos indicus-specific alleles are in red dots while Bos javanicus-specific alleles in blue dots. Bos javanicus-specific alternate alleles were identified as those that appeared in Bos javanicus genomes and were absent from taurine and Indian indicine cattle genomes. c Yak introgression plots constructed based on whole-genome sequencing data from a reprehensive segment on chromosome 11. The yak-specific alleles were identified using the same method. The relative frequencies of Bos taurus-specific are in green dots while Bos grunniens-specific are in sky blue. Vertical mouldings in d–f represent the SNP regions on chromosomes 5, 13 and 11 used for neighbour-joining (NJ) phylogeny analysis. The patterns of high-frequency SNPs at the T2R12, TAS2R9 and TAS2R6 regions are shown in d, at the ASIP region in e and at the IL-37 region in f. The star (*) denotes non-synonymous SNPs. Nucleotides with brown box in d and e represent Bos javanicus-specific homozygote genotypes, and with orange box represent heterozygote genotypes. Nucleotides with brown box in f represent Bos grunniens-specific homozygote genotypes. NJ phylogeny of 12 haplotypes supporting the introgression of banteng into Chinese indicine cattle (g, h) and the introgression of yak into Tibetan taurine cattle (i). The reliability of the tree branches (shown at the nodes) is tested with 1000 bootstrap replicates
Fig. 5 Phylogenetic analyses of SNP data confirm the Bos javanicus introgression into Chinese indicine cattle or the yak introgression into Tibetan taurine cattle. a, b Bos javanicus introgression plots constructed based on whole-genome sequencing data from two representative segments on chromosomes 5 and 13. The relative frequencies of Bos indicus-specific alleles are in red dots while Bos javanicus-specific alleles in blue dots. Bos javanicus-specific alternate alleles were identified as those that appeared in Bos javanicus genomes and were absent from taurine and Indian indicine cattle genomes. c Yak introgression plots constructed based on whole-genome sequencing data from a reprehensive segment on chromosome 11. The yak-specific alleles were identified using the same method. The relative frequencies of Bos taurus-specific are in green dots while Bos grunniens-specific are in sky blue. Vertical mouldings in d–f represent the SNP regions on chromosomes 5, 13 and 11 used for neighbour-joining (NJ) phylogeny analysis. The patterns of high-frequency SNPs at the T2R12, TAS2R9 and TAS2R6 regions are shown in d, at the ASIP region in e and at the IL-37 region in f. The star (*) denotes non-synonymous SNPs. Nucleotides with brown box in d and e represent Bos javanicus-specific homozygote genotypes, and with orange box represent heterozygote genotypes. Nucleotides with brown box in f represent Bos grunniens-specific homozygote genotypes. NJ phylogeny of 12 haplotypes supporting the introgression of banteng into Chinese indicine cattle (g, h) and the introgression of yak into Tibetan taurine cattle (i). The reliability of the tree branches (shown at the nodes) is tested with 1000 bootstrap replicatesCC BY · PubMed Central
Fig. 6 Coalescence-based inference of demographic history of cattle using MSMC and ∂a∂i. a Population size history inference of Bos taurus (BTA) and Bos indicus (BIN) lineages based on four haplotypes each from high-coverage European taurine (Hereford), Eurasian taurine (Gelbvieh), East Asian taurine (Tibetan), Chinese indicine (Wannan) and Indian indicine (Hariana and Sahiwal) individuals. The large grey-shaded boxes illustrate the Early Holocene Optimum, the last glacial maximum (LGM), and the second Pleistocene Glacial Period. b Inferred relative cross-coalescence rates between pairs of populations over time based on four haplotypes each from Hereford, Gelbvieh, Tibetan, Wannan and Indian breeds (Hariana and Sahiwal). The x-axis shows time and the y-axis a measure of similarity for each pair of compared populations. c ∂a∂i result showing the divergence time of Chinese indicine and Indian indicine cattle. The ancestral population is in grey, Chinese indicine cattle is in red and Indian indicine cattle is in orange. The width shows the relative effective population size. The figures at the arrows indicate the average number of migrants per generation between Chinese indicine and Indian indicine cattle
Fig. 6 Coalescence-based inference of demographic history of cattle using MSMC and ∂a∂i. a Population size history inference of Bos taurus (BTA) and Bos indicus (BIN) lineages based on four haplotypes each from high-coverage European taurine (Hereford), Eurasian taurine (Gelbvieh), East Asian taurine (Tibetan), Chinese indicine (Wannan) and Indian indicine (Hariana and Sahiwal) individuals. The large grey-shaded boxes illustrate the Early Holocene Optimum, the last glacial maximum (LGM), and the second Pleistocene Glacial Period. b Inferred relative cross-coalescence rates between pairs of populations over time based on four haplotypes each from Hereford, Gelbvieh, Tibetan, Wannan and Indian breeds (Hariana and Sahiwal). The x-axis shows time and the y-axis a measure of similarity for each pair of compared populations. c ∂a∂i result showing the divergence time of Chinese indicine and Indian indicine cattle. The ancestral population is in grey, Chinese indicine cattle is in red and Indian indicine cattle is in orange. The width shows the relative effective population size. The figures at the arrows indicate the average number of migrants per generation between Chinese indicine and Indian indicine cattleCC BY · PubMed Central

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Research works printed but not linked: 3

  1. National Bureau of Statistics. China Statistical Yearbook 2016 (China Statistics Press, Beijing, 2016).
  2. Vigne, J. D., Peters, J. & Helmer, D. The First Steps of Animal Domestication (Oxbow Books, Oxford, 2005).
  3. Flad, R., Yuan, J. & Li, S. C. On the source and features of the Neolithic domestic animals in the Gansu and Qinghai region, China. Archaeology 5, 80–86 (2009).

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Metadata

Authors
Chen, N., Cai, Y., Chen, Q., Li, R., Wang, K., Huang, Y., Hu, S., Huang, S., Zhang, H., Zheng, Z., Song, W., Ma, Z., Ma, Y., Dang, R., Zhang, Z., Xu, L., Jia, Y., Liu, S., Yue, X., Deng, W., Zhang, X., Sun, Z., Lan, X., Han, J., Chen, H., Bradley, D. G., Jiang, Y., & Lei, C.
Affiliations
  • Northwest A&F University (CN)
  • Northwestern Polytechnical University (CN)
  • Yunnan University (CN)
  • Qinghai University (CN)
  • Ningxia University (CN)
  • Henan Academy of Agricultural Sciences (CN)
  • Anhui Academy of Agricultural Sciences (CN)
  • National Beef Cattle Industrial Technology System (CN)
  • State Key Laboratory of Herbage Improvement and Grassland Agro-ecosystems (CN)
  • Yunnan Agricultural University (CN)
  • Kunming Institute of Zoology (CN)
  • Chinese Academy of Agricultural Sciences (CN)
  • Trinity College Dublin (IE)
Corresponding author
  • Jiang, Yu
  • Lei, Chuzhao
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2018-06-14
Volume
9
Issue
1
Pages
2337-2337
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-018-04737-0
PMC
PMC6002414
OpenAlex
W2805177757
Cited by
403
References
60
Citations by year
2026: 26 · 2025: 49 · 2024: 66 · 2023: 56 · 2022: 52 · 2021: 74 · 2020: 38 · 2019: 29 · 2018: 12
FWCI
23.77
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Lanzhou University Institutional Repository (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • CGSPace A Repository of Agricultural Research Outputs (Consultative Group for International Agricultural Research) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Trinity's Access to Research Output (TARA) (Trinity College Dublin) (submittedVersion)
Funders
  • Natural Science Foundation of Qinghai Province of China
  • National Natural Science Foundation of China (31501918)
  • Yunnan Modern Agriculture Beef Cattle Industry Technology System
  • National Thousand Youth Talents Plan
  • National Beef Cattle and Yak Industrial Technology System
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and phenotypic traits in livestock
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Forensic and Genetic Research
Keywords
cattle domestication, population ancestry, adaptive introgression, banteng, yak, Y-chromosome haplotypes
MeSH terms
Domestication, Animals, Breeding, Cattle, China, Chromosomes, Female, Genetics, Population, Geography, Haplotypes, Male, Mitochondria, Phylogeny, Species Specificity, Genetic Variation, Models, Statistical, Genome, Tibet, Polymorphism, Single Nucleotide

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