Research Article

Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits

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Science  21 Jun 2019:
Vol. 364, Issue 6446, eaav6202
DOI: 10.1126/science.aav6202
  • Phylogeny and trait evolution of ruminants.

    The phylogenic tree of ruminants is presented with the species within same families and subfamilies collapsed. The ruminants have many textbook examples of distinct traits. The four-chambered stomach with omasum chamber is a key innovation evolved in pecoran ruminants. Headgear keratinous sheath only appear in Bovidae and Antilocapridae lineages. Many ruminants have evolved high-crowned or hypsodont teethes. The Antilocapridae and two bovid lineages are among the mammals with highest cursorial locomotion ability.

  • Fig. 1 Phylogeny of ruminants.

    (A) The maximum likelihood phylogenetic tree from whole-genome sequences of 51 ruminant species and 13 fossil calibrations. To compute the node supports, 200 bootstraps were used, and all nodes have 100% support. The origin and credit of the portraits of different species are listed in table S54. (B) Prevalent discordance among 10,000 random WGTs was observed across different families of ruminant.

  • Fig. 2 Population size history of ruminants.

    (A) The normalized effective population sizes (Ne) of Ruminantia shows a clear decline trend from 100,000 to 50,000 years ago, in sharp contrast to the normalized Ne of human, which expanded dramatically at the same time. The Ne of each species is inferred by using PSMC (23). The normalized Ne is calculated by dividing the estimated value of Ne for each species at each time point with its maximum value. After normalizing each species’s Ne, we put 20 Ne datum points along the time axis into a window. For ruminants, a gray shadowed bar indicates the variation interval of different species at a window, and the trend line (red) is plotted by using the “smooth.spline” function in the R package. (B) Species grouped into continents Africa (26 species), Asia (seven species), and North America (four species). The trend line (red) indicates the dynamics of normalized effective population sizes in each continent. ka, thousand years.

  • Fig. 3 Structural characteristics and evolution of ruminant genomes.

    (A) Goat (19) was used to represent Ruminantia-specific genomic rearrangements in comparisons with Primates (human), Perissodactyla (horse), Suina (pig), Tylopoda (camel), and Cetacea (Killer whale). Syntenic blocks are linked between genomes in a circos plot. The red number beside each circos quantifies the occurrences of rearrangement events per aligned megabase (Mb) sequence. The high-quality de novo assembly of the black muntjac was included for within-ruminant synteny inference. (B) The average genome sizes, TE sizes, and contents of different TE types of Primates (human, chimpanzee, gorilla, and orangutan), Carnivora (dog, cheetah, and polar bear), Perissodactyla (horse, przewalski’s horse, and rhinoceros), Tylopoda (dromedary camel, bactrian camel, and alpaca), Suina (pig), and Cetacea (minke whale, killer whale, beluga whale, sperm whale, and yangtze finless porpoise). Overall, the average genome size of Ruminantia is significantly (Student’s t test, P < 0.01) larger than those of Canivora, Perissodactyla, Tylopoda, Suina, and Cetacea. Tragulidae is marked with dashed lines because the genome assembly contains more gaps, which hindered the annotation of TEs. The proportions of LINE, SINE, LTR, and DNA transposons are presented in the stacked bar plot. LINE/BovB and LINE/L1 are highlighted here to present their dynamic changes among ruminants. ***P < 0.01. (C) The average contents of different SINE types are plotted in the stacked bar plot across mammalian orders and suborders of Cetartiodactyla, with different colors. (D) A large fragment insertion of 3,396,232 bp is observed in the goat genome, which is also validated in other ruminant families, containing a cluster of PAG genes, specifically containing 36 coding genes and 32 pseudogenes in goat.

  • Fig. 4 Newly evolved genes, expanded and contracted gene families, REGs, and PSGs in ruminants.

    (A) Positively selected genes (PSGs), rapidly evolving genes (REGs), expanded genes, and newly evolved genes are shown along the phylogenetic tree. PSGs and REGs are identified with PAML. Newly evolved genes are identified based on the synteny relationships, with goat used as a reference. Expanded gene families are identified for the pecoran families. Tragulidae are excluded because of the relatively low quality of the assembled tragulid genome. (B) Diagram of the process of leukocytes crossing blood vessels, highlighting PSGs (orange) and REGs (blue). The orange rectangles indicate PSGs, and the blue rectangles represent the REGs. The solid lines represent direct interaction, and the dotted lines represent indirect interactions. (C) Diagram of nutrient metabolism evolution in Ruminantia displaying genes involved in nutrition metabolism. Expanded gene families are marked red, PSGs are marked yellow, and REGs are marked blue in (C) and (D). (D) Expansion of the lysozyme c gene family throughout the Ruminantia. The different expanded copies are presented with colors. Each line corresponds to the order or family in (A), and we chose the best assembled species genome sequences to draw the region. The slashes on each line indicate the ends of scaffolds in the assembled genomes.

  • Fig. 5 Genomic features related to ruminant characteristics.

    (A) Pairwise Spearman correlations of gene expressions indicated that the omasum, rumen, and reticulum evolved as an extension of the esophagus, whereas the abomasum evolved as an extension of the duodenum. Although it is anatomically closer to the reticulum, the omasum has a more similar gene expression atlas with that of the rumen than the reticulum, which mirrors the similar functions between them. (B) Diagram of the convergent feature of keratinous sheath in the Bovidae and Antilocapridae. The two red amino acids indicate convergent mutations of the KRT82 between Antilocapridae and Bovidae, and the red dots indicate the included species of Antilocapridae and Bovidae. (C) Body size contrast among ruminants and 11 genes related with bone development that have at least four specific mutations in giraffe and are involved in TGF-β, Hedgehog, Notch, Wnt, and FGF pathways. (D) A total of 642 genes in GO related to the development of body size are retrieved, and we calculated the dN/dS ratios on the branches, leading to large, medium, and small body sizes, under the two-ratio branch model (model 2) of PAML. Background dN/dS ratios are calculated under one-ratio branch model (model 1) of PAML. The distribution densities of the dN/dS values are shown. A box plot of dN/dS values in different body size categories is shown. The mean dN/dS values at the branches of large body size and small body size are significantly larger than background. ***P < 0.01. (E) Antilocapridae and Antilopinae species are among the most mobile land mammals, and both of them have specific mutations in several genes of the mitochondrial electron transport chain.

  • Table 1 Assembly statistics of 44 ruminant species.

    SpeciesCommon nameScaffold N50
    (bp)
    Contig N50
    (bp)
    SpeciesCommon nameScaffold N50
    (bp)
    Contig N50
    (bp)
    Tragulus javanicusLesser mouse-deer243,2506286Redunca reduncaBohor reedbuck438,84517,874
    Antilocapra americanaPronghorn1,463,79261,696Syncerus cafferAfrican buffalo2,316,37611,115
    Okapia johnstoniOkapi3,620,11658,892Gazella thomsoniThomson gazelle1,581,71736,935
    Giraffa camelopardalisGiraffe3,197,40422,538Tragelaphus strepsicerosGreater kudu520,72016,623
    Muntiacus muntjakIndian muntjac1,398,59110,925Nanger grantiGrant’s gazelle520,1316041
    Muntiacus reevesiChinese muntjac1,253,71968,151Sylvicapra grimmiaCommon duiker541,1915209
    Elaphurus davidianusMilu3,040,53032,708Aepyceros melampusImpala343,69951,379
    Rangifer tarandusReindeer1,059,11391,805Madoqua kirkiiKirk’s dik-dik489,83526,372
    Muntiacus crinifronsBlack muntjacNA1,458,913Oreotragus oreotragusKlipspringer340,33513,019
    Gervus albirostrisWhite-lipped deer3,567,44822,599Antidorcas marsupialisSpringbok698,57510,778
    Moschus chrysogasterForest musk deer2,509,22557,721Tragelaphus imberbisLesser kudu1,774,6916545
    Oryx gazellaGemsbok1,583,97218,132Tragelaphus spekiiSitatunga78,9735410
    Litocranius walleriGerenuk3,128,64147,546Philantomba maxwelliiMaxwell’s duiker390,5524423
    Damaliscus lunatusTopi1,172,12525,829Raphicerus campestrisSteenbok474,0335764
    Ammotragus lerviaBarbary sheep1,263,98118,541Neotragus pygmaeusRoyal antelope365,7365931
    Pseudois nayaurBlue sheep2,076,30823,854Alcelaphus buselaphusHartebeest11,2584274
    Ovis ammonArgali5,734,77645,638Capra ibexIbex15,190,72024,835
    Kobus ellipsiprymnusDefassa waterbuck782,10220,722Neotragus moschatusSuni957,0228233
    Procapra przewalskiiPrzewalski’s gazelle5,152,91420,018Taurotragus oryxCommon elandno scaffold1262
    Connochaetes taurinusBlue wildebeest3,511,34146,638Tragelaphus buxtoniMountain nyalano scaffold1309
    Cephalophus harveyiHarvey’s duiker365,46239,715Tragelaphus eurycerosBongono scaffold1980
    Tragelaphus scriptusBushbuck890,5549965Ourebia ourebiOribino scaffold1259

Supplementary Materials

  • Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits

    Lei Chen, Qiang Qiu, Yu Jiang, Kun Wang, Zeshan Lin, Zhipeng Li, Faysal Bibi, Yongzhi Yang, Jinhuan Wang, Wenhui Nie, Weiting Su, Guichun Liu, Qiye Li, Weiwei Fu, Xiangyu Pan, Chang Liu, Jie Yang, Chenzhou Zhang, Yuan Yin, Yu Wang, Yue Zhao, Chen Zhang, Zhongkai Wang, Yanli Qin, Wei Liu, Bao Wang, Yandong Ren, Ru Zhang, Yan Zeng, Rute R. da Fonseca, Bin Wei, Ran Li, Wenting Wan, Ruoping Zhao, Wenbo Zhu, Yutao Wang, Shengchang Duan, Yun Gao, Yong E. Zhang, Chunyan Chen, Christina Hvilsom, Clinton W. Epps, Leona G. Chemnick, Yang Dong, Siavash Mirarab, Hans Redlef Siegismund, Oliver A. Ryder, M. Thomas P. Gilbert, Harris A. Lewin, Guojie Zhang, Rasmus Heller, Wen Wang

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

    Download Supplement
    • Materials and Methods
    • Figs. S1 to S54
    • Tables S1 to S9, S11 to S23, S26 to S34, S37 to S39, S41 to S50, S53, and S54
    • References
    Table S10
    Table S24
    Table S25
    Table S35
    Table S36
    Table S40
    Table S51
    Table S52

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