留言板

尊敬的读者、作者、审稿人, 关于本刊的投稿、审稿、编辑和出版的任何问题, 您可以本页添加留言。我们将尽快给您答复。谢谢您的支持!

姓名
邮箱
手机号码
标题
留言内容
验证码

Genome-wide analysis reveals signatures of complex introgressive gene flow in macaques (genus Macaca)

Yang Song Cong Jiang Kun-Hua Li Jing Li Hong Qiu Megan Price Zhen-Xin Fan Jing Li

Yang Song, Cong Jiang, Kun-Hua Li, Jing Li, Hong Qiu, Megan Price, Zhen-Xin Fan, Jing Li. Genome-wide analysis reveals signatures of complex introgressive gene flow in macaques (genus Macaca). Zoological Research, 2021, 42(4): 433-449. doi: 10.24272/j.issn.2095-8137.2021.038
Citation: Yang Song, Cong Jiang, Kun-Hua Li, Jing Li, Hong Qiu, Megan Price, Zhen-Xin Fan, Jing Li. Genome-wide analysis reveals signatures of complex introgressive gene flow in macaques (genus Macaca). Zoological Research, 2021, 42(4): 433-449. doi: 10.24272/j.issn.2095-8137.2021.038

全基因组分析揭示猕猴属物种间复杂的渐渗基因流

doi: 10.24272/j.issn.2095-8137.2021.038

Genome-wide analysis reveals signatures of complex introgressive gene flow in macaques (genus Macaca)

Funds: This work was supported by the National Natural Science Foundation of China (31530068, 31770415) and Fundamental Research Funds for the Central Universities (SCU2021D006)
More Information
  • 摘要: 猕猴属物种分化时间较短(约500万年),经历了快速的适应辐射,是物种形成和渐渗基因流研究的理想模型。为了更全面、深入的阐释猕猴属进化过程中的种间基因流,我们对4个猕猴(2个红面猴和2个藏酋猴)进行了全基因组重测序,并结合已报道的猕猴属全基因组数据,我们共分析了14个猕猴个体基因组,覆盖了亚洲猕猴的所有种组。研究结果表明猕猴属中存在着广泛的种间基因流信号,最强的信号出现在fascicularissilenus种组之间。其中尤其是食蟹猴与南豚尾猴之间的基因流信号最为显著,结合多种基因组分析方法,食蟹猴与与南豚尾猴之间可能存在双向的基因流;且二者因种间基因流而共享的基因组片段占基因组的6.19%。同时也检测到一些岛屿物种(如苏拉威西猕猴和日本猴)与其他猕猴间存在基因流,这可能在很大程度上归因于近缘物种间基因组的相似性或祖先谱系间的杂交事件。此外,我们也发现同一物种(红面猴、恒河猴、食蟹猴、南豚尾猴和藏酋猴)的不同种群个体间存在不一致的基因流信号,表明这些基因流发生在不同的种群分化之后。种群历史动态分析显示所有的亚洲猕猴在500万年前都经历了一次瓶颈,此后,不同物种表现出了不同的种群历史动态,表明猕猴属在进化过程中经历了复杂的环境与气候变化。综上,该研究从全基因组的角度揭示了亚洲猕猴进化过程中复杂的种间基因流。
  • Figure  1.  Local evolutionary history of macaques at individual level

    A: Each bar represents a chromosome, in terms of M. mulatta genome. Colored bands represent tree topologies of each 100 kb window. Colors correspond to topologies in (B). B: Ten most common trees. Values at top left corner are percentage of all 100 kb windows that recover that topology. Colors correspond to colored bands in (A), with gray and black regions showing other topologies and missing data.

    Figure  2.  MSC (multispecies coalescent) tree

    All node support values are 100%. A: MSC species tree generated from ASTRAL and MP-EST based on 26 633 SNV-fragments. B: Species tree with divergence time. Topology and divergence time were both estimated in SNAPP based on 20 000 SNV sites. This tree shows a conflict of Mfas_1 position with (A). Numbers on nodes indicate divergence time. Purple bars on nodes represent 95% confidence interval of divergence time. C: MSC tree at species level.

    Figure  3.  Consensus network of 26 633 SNV-fragment trees with 11% threshold

    Cuboid structures mainly occur in fascicularis and sinica species groups, indicating phylogenetic conflicts in these two species groups and potential interspecific gene flow. There is no cuboid structure in the net center, indicating that the evolutionary relationship of ancestral macaques is relatively clear.

    Figure  4.  Gene flow signals in macaques

    A: Gene flow identified by D statistic (corrected P<0.001) at individual level. Numbers in grids represent D values, with higher values indicating higher introgression level. Grids without numbers indicate that no gene flow signal was detected. Redder colors indicate higher D statistics. Maximum D value of each individual pair was used for drawing. B: Gene flow identified by D statistic (corrected P<0.001) at species level. The meanings of color and number in grid are the same as that in (A). Maximum D value of each species pair was used for drawing. C: Species tree of macaques with directional gene flow signals. Only signals confirmed by both D and DFOIL statistics are shown here. Arrows indicate direction of gene flow.

    Figure  5.  Proportion of genome shared through gene flow estimated by fd statistic at (A) individual level and (B) species level

    Number in grid is value of fd. Grids without numbers indicate that no gene flow signal was detected. The fd values of species pairs between fascicularis and silenus species groups were higher than that of other species pairs, with M. fascicularis and M. nemestrina species pair showing highest fd value. In addition, M. fascicularis and M. mulatta species pair showed a high fd value.

    Figure  6.  Rooted network of macaques

    A: Rooted network of macaques with four reticulations inferred by PhyloNetworks based on 26 633 SNV-fragments. Hybrid edges are annotated with their inheritance values, which measure proportion of genes inherited via gene flow. B: Network scores based on different maximum number of reticulations (0–6). We estimated networks with a different maximum number of reticulations, and each generated a network score, with lower scores indicating better networks. However, networks with five and six reticulations could not be re-rooted by P. anubis due to hybrid edges on the P. anubis branch. Therefore, only the network with four reticulations is shown here.

    Figure  7.  Distribution of top 5% of windows with strongest introgression signals according to fd across chromosome 18

    Species of species pairs belong to fascicularis and silenus species groups. Results showed that top 5% of windows with strongest introgression signals for different species pairs had similar genomic distributions.

    Figure  8.  Genome-wide heterozygosity and demographic history

    A: Genome-wide heterozygosity estimated from non-overlapping 1 Mb windows. B–D: Historical effective population sizes (Ne) of fascicularis, silenus, and sinica species groups. X-axis represents time; Y-axis represents Ne. Plots were scaled using a mutation rate (μ) of 0.58×10-8 bp-1 generation-1 and a generation time (g) of 10.

    Table  1.   Information on samples and genomic data

    Scientific nameCommon nameSample IDNCBI accession No.SexSample originSequencing platformNo. of bases (Gb)Depth*
    M. arctoides Stump-tailed macaque Marc_R02 This study, SAMN15194901 Male Yunnan, China Illumina 152.0 ~47.0×
    Marc_R19 This study, SAMN15194902 Female Guangxi, China Illumina 112.2 ~34.7×
    M. assamensis Assamese macaque Mass SRR2981114 Male Yunnan, China Illumina 154.0 ~47.6×
    M. fascicularis Crab-eating macaque Mfas_1 SRR8194877 Female Unknown (in captivity in China) Illumina 92.1 ~28.5×
    Mfas_Mau ERS629711 Male Mauritius Illumina 61.6 ~19.0×
    M. fuscata Japanese macaque Mfus DRR002234 Unknown Japan Illumina 142.5 ~44.0×
    M. mulatta Rhesus macaque Mmul_Chi SRR1944102 Female China Illumina 144.5 ~44.7×
    Mmul_Ind SRR1952166 Female India Illumina 131.3 ~40.6×
    M. nemestrina Southern pig-tailed macaque Mnem_1 SRR1698391, SRR1698394, SRR1698403, SRR1698405 Female Unknown Illumina 152.7 ~47.2×
    Mnem_2 SRR5947292 Male Borneo, Malaysia Illumina 140.7 ~43.5×
    M. nigra Black crested macaque Mnig SRR5947294 Female Sulawesi, Indonesia Illumina 135.8 ~42.0×
    M. thibetana Tibetan macaque Mthi_HT1 This study, SAMN15194903 Female Anhui, China Illumina 93.7 ~29.0×
    Mthi_R25 This study, SAMN15194904 Female Guangxi, China Illumina 113.9 ~35.2×
    M. tonkeana Tonkean macaque Mton SRR5947293 Male Sulawesi, Indonesia Illumina 135.4 ~41.8×
    P. anubis Olive baboon Panu SRR8723580 Female Unknown Illumina 137.9 ~42.6×
    For individual macaque genome samples, scientific name, common name, sample ID, NCBI accession No., sex, sample origin, sequencing platform, No. of bases, and sequencing depth are shown. New whole-genome sequences of this study are marked in bold. *: Calculations were based on total length of M. mulatta genome assembly Mmul_8.0.1, 3 236 224 332 bp.
    下载: 导出CSV

    Table  2.   SNV information for each analyzed macaque

    SampleFilteredDownsampled (~15×)
    SNVsHomoHetCallable sitesHetHeterozygosityTsTvTs/Tv
    Marc_R027 271 2755 383 3711 887 9042 555 381 3323 782 7130.001 48010 682 0134 949 0532.16
    Marc_R197 000 6095 675 9531 324 6562 553 354 8582 644 1710.001 03610 334 3434 762 6142.17
    Mass7 926 4684 560 0393 366 4292 519 264 1306 121 1310.002 43010 831 1125 023 8432.16
    Mfas_16 909 0523 101 4133 807 6392 562 592 8127 612 4410.002 97110 058 2784 638 5712.17
    Mfas_Mau6 773 3773 895 5602 877 8172 549 849 9255 881 3160.002 30710 190 9364 659 3002.19
    Mfus4 805 3723 403 3381 402 0342 562 072 2752 619 7780.001 0237 074 7873 279 2162.16
    Mmul_Chi5 192 0052 071 9813 120 0242 556 851 6195 748 6080.002 2487 168 2593 273 7522.19
    Mmul_Ind4 058 5271 370 6382 687 8892 550 406 2185 072 9520.001 9895 723 4952 602 7822.20
    Mnem_18 733 0294 860 2523 872 7772 559 986 4847 267 8110.002 83912 211 4365 571 8072.19
    Mnem_28 568 0744 907 7253 660 3492 557 580 2977 210 5730.002 81912 310 8455 636 7982.18
    Mnig7 743 3846 043 2241 700 1602 553 652 5843 353 0470.001 31311 259 3205 250 2642.14
    Mthi_HT16 133 3365 691 120442 2162 488 747 849903 3960.000 3639 401 2834 277 3212.20
    Mthi_R256 858 2495 921 203937 0462 552 204 0591 886 2870.000 73910 137 4094 730 6512.14
    Mton8 229 8735 597 6162 632 2572 555 184 6605 168 7710.002 02311 872 7555 501 5802.16
    Panu17 507 27115 461 1422 046 1292 529 072 2363 620 0490.001 43125 935 87111 112 1782.33
    For individual macaque genome samples, short ID, total number of single nucleotide variants (SNVs), number of heterozygous SNVs (Het), number of homozygous SNVs (Homo), and transitions/transversions (Ts/Tv) are shown.
    下载: 导出CSV

    Table  3.   Statistics on top 5% of windows with strongest introgression signals based on fd for species pairs between fascicularis and silenus species groups

    Species pairNo. of top 5% windowsNo. of shared windowsPercentage of shared windowsNo. of specific windowsPercentage of specific window
    M. fascicularis-silenus group speciesM. fascicularis-
    M. nemestrina
    2 9201 75660.1437812.95
    M. fascicularis-
    M. nigra
    2 58567.932258.70
    M. fascicularis-
    M. tonkeana
    2 81462.402579.13
    M. nemestrina-fascicularis group speciesM. fascicularis-
    M. nemestrina
    2 9201 38247.3337812.95
    M. fuscata-
    M. nemestrina
    3 01545.8464621.43
    M. mulatta-
    M. nemestrina
    2 99946.0844614.87
    For M. fascicularis-silenus group species pairs, 60.14%–67.93% of top 5% of windows were shared, and this proportion for M. nemestrina-fascicularis group species pairs was 45.84%–47.33%. Windows specific to each species pair only accounted for 8.70%–21.43%.
    下载: 导出CSV
  • [1] Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N, et al. 2013. Hybridization and speciation. Journal of Evolutionary Biology, 26(2): 229−246. doi: 10.1111/j.1420-9101.2012.02599.x
    [2] Ang A, Boonratana R, Choudhury A, Supriatna J. 2020. Macaca nemestrina. The IUCN Red List of Threatened Species 2020: e.T12555A181324867.
    [3] Árnason U, Lammers F, Kumar V, Nilsson MA, Janke A. 2018. Whole-genome sequencing of the blue whale and other rorquals finds signatures for introgressive gene flow. Science Advances, 4(4): eaap9873. doi: 10.1126/sciadv.aap9873
    [4] Arnold ML, Meyer A. 2006. Natural hybridization in primates: one evolutionary mechanism. Zoology (Jena), 109(4): 261−276. doi: 10.1016/j.zool.2006.03.006
    [5] Baiz MD, Tucker PK, Mueller JL, Cortés-Ortiz L. 2020. X-linked signature of reproductive isolation in humans is mirrored in a howler monkey hybrid zone. Journal of Heredity, 111(5): 419−428. doi: 10.1093/jhered/esaa021
    [6] Barley AJ, de Oca ANM, Reeder TW, Manríquez-Morán NL, Monroy JCA, Hernández-Gallegos O, et al. 2019. Complex patterns of hybridization and introgression across evolutionary timescales in Mexican whiptail lizards (Aspidoscelis). Molecular Phylogenetics and Evolution, 132: 284−295. doi: 10.1016/j.ympev.2018.12.016
    [7] Bernsteil IS. 1966. Naturally occurring primate hybrid. Science, 154(3756): 1559−1560. doi: 10.1126/science.154.3756.1559
    [8] Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH, Xie D, et al. 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology, 10(4): e1003537. doi: 10.1371/journal.pcbi.1003537
    [9] Bryant D, Bouckaert R, Felsenstein J, Rosenberg NA, RoyChoudhury A. 2012. Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Molecular Biology and Evolution, 29(8): 1917−1932. doi: 10.1093/molbev/mss086
    [10] Bunlungsup S, Kanthaswamy S, Oldt RF, Smith DG, Houghton P, Hamada Y, et al. 2017. Genetic analysis of samples from wild populations opens new perspectives on hybridization between long-tailed (Macaca fascicularis) and rhesus macaques (Macaca mulatta). American Journal of Primatology, 79(12): e22726. doi: 10.1002/ajp.22726
    [11] Chen SF, Zhou YQ, Chen YR, Gu J. 2018. Fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17): i884−i890. doi: 10.1093/bioinformatics/bty560
    [12] Chu JH, Lin YS, Wu HY. 2007. Evolution and dispersal of three closely related macaque species, Macaca mulatta, M. cyclopis, and M. fuscata, in the Eastern Asia. Molecular Phylogenetics and Evolution, 43(2): 418−429. doi: 10.1016/j.ympev.2006.11.022
    [13] Ciani AC, Stanyon R, Scheffrahn W, Sampurno B. 1989. Evidence of gene flow between Sulawesi macaques. American Journal of Primatology, 17(4): 257−270. doi: 10.1002/ajp.1350170402
    [14] Cortés-Ortiz L, Duda Jr TF, Canales-Espinosa D, García-Orduña F, Rodríguez-Luna E, Bermingham E. 2007. Hybridization in large-bodied new world primates. Genetics, 176(4): 2421−2425. doi: 10.1534/genetics.107.074278
    [15] Deinard A, Smith DG. 2001. Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. Journal of Human Evolution, 41(1): 45−59. doi: 10.1006/jhev.2001.0480
    [16] Delson E. 1980. Fossil macaques, phyletic relationships and a scenario of deployment. In: Lindburg DG. The Macaques: Studies in Ecology, Behavior and Evolution. New York: Van Nostrand Reinhold.
    [17] DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genetics, 43(5): 491−498. doi: 10.1038/ng.806
    [18] Edelman NB, Frandsen PB, Miyagi M, Clavijo B, Davey J, Dikow RB, et al. 2019. Genomic architecture and introgression shape a butterfly radiation. Science, 366(6465): 594−599. doi: 10.1126/science.aaw2090
    [19] Eudey A, Kumar A, Singh M, Boonratana R. 2020. Macaca fascicularis (Errata Version Published in 2021). The IUCN Red List of Threatened Species 2020: e.T12551A195354635.
    [20] Evans BJ, Tosi AJ, Zeng K, Dushoff J, Corvelo A, Melnick DJ. 2017. Speciation over the edge: gene flow among non-human primate species across a formidable biogeographic barrier. Royal Society Open Science, 4(10): 170351. doi: 10.1098/rsos.170351
    [21] Fan PF, Liu Y, Zhang ZC, Zhao C, Li C, Liu WL, et al. 2017. Phylogenetic position of the white-cheeked macaque (Macaca leucogenys), a newly described primate from southeastern Tibet. Molecular Phylogenetics and Evolution, 107: 80−89. doi: 10.1016/j.ympev.2016.10.012
    [22] Fan ZX, Zhao G, Li P, Osada N, Xing JC, Yi Y, et al. 2014. Whole-genome sequencing of Tibetan macaque (Macaca thibetana) provides new insight into the macaque evolutionary history. Molecular Biology and Evolution, 31(6): 1475−1489. doi: 10.1093/molbev/msu104
    [23] Fan ZX, Zhou AB, Osada N, Yu JQ, Jiang J, Li P, et al. 2018. Ancient hybridization and admixture in macaques (genus Macaca) inferred from whole genome sequences. Molecular Phylogenetics and Evolution, 127: 376−386. doi: 10.1016/j.ympev.2018.03.038
    [24] Felsenstein J. 1989. PHYLIP - phylogeny inference package (Version 3.2). Cladistics, 5(2): 164−166.
    [25] Figueiro HV, Li G, Trindade FJ, Assis J, Pais F, Fernandes G, et al. 2017. Genome-wide signatures of complex introgression and adaptive evolution in the big cats. Science Advances, 3(7): e1700299. doi: 10.1126/sciadv.1700299
    [26] Fooden J. 1976. Provisional classification and key to living species of macaques (primates: Macaca). Folia Primatologica, 25(2–3): 225−236.
    [27] Gante HF, Matschiner M, Malmstrom M, Jakobsen KS, Jentoft S, Salzburger W. 2016. Genomics of speciation and introgression in princess cichlid fishes from Lake Tanganyika. Molecular Ecology, 25(24): 6143−6161. doi: 10.1111/mec.13767
    [28] Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, et al. 2010. A draft sequence of the neandertal genome. Science, 328(5979): 710−722. doi: 10.1126/science.1188021
    [29] Groves C. 2001. Primate Taxonomy. Washington: Smithsonian Institution Press.
    [30] Hamada Y, San AM, Malaivijitnond S. 2016. Assessment of the hybridization between rhesus (Macaca mulatta) and long-tailed macaques (M. fascicularis) based on morphological characters. American Journal of Physical Anthropology, 159(2): 189−198. doi: 10.1002/ajpa.22862
    [31] Hamada Y, Yamamoto A, Kunimatsu Y, Tojima S, Mouri T, Kawamoto Y. 2012. Variability of tail length in hybrids of the Japanese macaque (Macaca fuscata) and the taiwanese macaque (Macaca cyclopis). Primates, 53(4): 397−411. doi: 10.1007/s10329-012-0317-3
    [32] Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. 2018. UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution, 35(2): 518−522. doi: 10.1093/molbev/msx281
    [33] Holbourn AE, Kuhnt W, Clemens SC, Kochhann KGD, Jöhnck J, Lübbers J, et al. 2018. Late Miocene climate cooling and intensification of southeast Asian winter monsoon. Nature Communications, 9(1): 1584. doi: 10.1038/s41467-018-03950-1
    [34] Ito T, Kanthaswamy S, Bunlungsup S, Oldt RF, Houghton P, Hamada Y, et al. 2020. Secondary contact and genomic admixture between rhesus and long-tailed macaques in the Indochina Peninsula. Journal of Evolutionary Biology, 33(9): 1164−1179. doi: 10.1111/jeb.13681
    [35] Ito T, Lee YJ, Nishimura TD, Tanaka M, Woo JY, Takai M. 2018. Phylogenetic relationship of a fossil macaque (Macaca cf. robusta) from the Korean peninsula to Extant species of macaques based on zygomaxillary morphology. Journal of Human Evolution, 119: 1−13. doi: 10.1016/j.jhevol.2018.02.002
    [36] Jiang J, Yu JQ, Li J, Li P, Fan ZX, Niu LL, et al. 2016. Mitochondrial genome and nuclear markers provide new insight into the evolutionary history of macaques. PLoS One, 11(5): e0154665. doi: 10.1371/journal.pone.0154665
    [37] Junier T, Zdobnov EM. 2010. The newick utilities: high-throughput phylogenetic tree processing in the UNIX shell. Bioinformatics, 26(13): 1669−1670. doi: 10.1093/bioinformatics/btq243
    [38] Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods, 14(6): 587−589. doi: 10.1038/nmeth.4285
    [39] Kubisch HM, Falkenstein KP, Deroche CB, Franke DE. 2012. Reproductive efficiency of captive Chinese- and Indian-origin rhesus macaque (Macaca mulatta) females. American Journal of Primatology, 74(2): 174−184. doi: 10.1002/ajp.21019
    [40] Kuhlwilm M, Han S, Sousa VC, Excoffier L, Marques-Bonet T. 2019. Ancient admixture from an extinct ape lineage into bonobos. Nature Ecology & Evolution, 3(6): 957−965.
    [41] Kumar V, Lammers F, Bidon T, Pfenninger M, Kolter L, Nilsson MA, et al. 2017. The evolutionary history of bears is characterized by gene flow across species. Scientific Reports, 7: 46487. doi: 10.1038/srep46487
    [42] Lambert SM, Streicher JW, Fisher-Reid MC, de la Cruz FRM, Martinez-Méndez N, García-Vázquez UO, et al. 2019. Inferring introgression using RADseq and DFOIL: Power and pitfalls revealed in a case study of spiny lizards (Sceloporus). Molecular Ecology Resources, 19(4): 818−837. doi: 10.1111/1755-0998.12972
    [43] Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with bowtie 2. Nature Methods, 9(4): 357−359. doi: 10.1038/nmeth.1923
    [44] Lewis PO. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology, 50(6): 913−925. doi: 10.1080/106351501753462876
    [45] Lexer C, Widmer A. 2008. Review. The genic view of plant speciation: recent progress and emerging questions. Philosophical transactions of the Royal Society B, 363(1506): 3023−3036. doi: 10.1098/rstb.2008.0078
    [46] Li H. 2011. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics, 27(21): 2987−2993. doi: 10.1093/bioinformatics/btr509
    [47] Li H, Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature, 475(7357): 493−496. doi: 10.1038/nature10231
    [48] Li J, Han K, Xing JC, Kim HS, Rogers J, Ryder OA, et al. 2009. Phylogeny of the macaques (Cercopithecidae: Macaca) based on Alu elements. Gene, 448(2): 242−249. doi: 10.1016/j.gene.2009.05.013
    [49] Li QQ, Zhang YP. 2005. Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), Inferred from mitochondrial DNA sequences. Biochemical Genetics, 43(7–8): 375−386.
    [50] Liu L, Yu LL, Edwards SV. 2010. A maximum pseudo-likelihood approach for estimating species trees under the coalescent model. BMC Evolutionary Biology, 10: 302. doi: 10.1186/1471-2148-10-302
    [51] Liu ZJ, Tan XX, Orozco-terWengel P, Zhou XM, Zhang LY, Tian SL, et al. 2018. Population genomics of wild Chinese rhesus macaques reveals a dynamic demographic history and local adaptation, with implications for biomedical research. GigaScience, 7(9): giy106.
    [52] Louys J, Turner A. 2012. Environment, preferred habitats and potential refugia for Pleistocene Homo in southeast Asia. Comptes Rendus Palevol, 11(2–3): 203−211.
    [53] Malinsky M, Matschiner M, Svardal H. 2021. Dsuite - fast D-statistics and related admixture evidence from VCF files. Molecular Ecology Resources, 21(2): 584−595. doi: 10.1111/1755-0998.13265
    [54] Martin SH, Davey JW, Jiggins CD. 2015. Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Molecular Biology and Evolution, 32(1): 244−257. doi: 10.1093/molbev/msu269
    [55] Martin SH, Jiggins CD. 2017. Interpreting the genomic landscape of introgression. Current Opinion in Genetics & Development, 47: 69−74.
    [56] Matsudaira K, Hamada Y, Bunlungsup S, Ishida T, San AM, Malaivijitnond S. 2018. Whole mitochondrial genomic and Y-chromosomal phylogenies of burmese long-tailed macaque (Macaca fascicularis aurea) suggest ancient hybridization between fascicularis and sinica species groups. Journal of Heredity, 109(4): 360−371. doi: 10.1093/jhered/esx108
    [57] Meijaard E. 2003. Mammals of south-east Asian islands and their Late Pleistocene environments. Journal of Biogeography, 30(8): 1245−1257. doi: 10.1046/j.1365-2699.2003.00890.x
    [58] Nakhleh L. 2013. Computational approaches to species phylogeny inference and gene tree reconciliation. Trends in Ecology & Evolution, 28(12): 719−728.
    [59] Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution, 32(1): 268−274. doi: 10.1093/molbev/msu300
    [60] Nosil P. 2008. Speciation with gene flow could be common. Molecular Ecology, 17(9): 2103−2106. doi: 10.1111/j.1365-294X.2008.03715.x
    [61] Osada N, Matsudaira K, Hamada Y, Malaivijitnond S. 2021. Testing sex-biased admixture origin of macaque species using autosomal and x-chromosomal genomic sequences. Genome Biology and Evolution, 13(1): evaa209.
    [62] Pabijan M, Zieliński P, Dudek K, Stuglik M, Babik W. 2017. Isolation and gene flow in a speciation continuum in newts. Molecular Phylogenetics and Evolution, 116: 1−12. doi: 10.1016/j.ympev.2017.08.003
    [63] Pease JB, Hahn MW. 2015. Detection and polarization of introgression in a five-taxon phylogeny. Systematic Biology, 64(4): 651−662. doi: 10.1093/sysbio/syv023
    [64] Prado-Martinez J, Sudmant PH, Kidd JM, Li H, Kelley JL, Lorente-Galdos B, et al. 2013. Great ape genetic diversity and population history. Nature, 499(7459): 471−475. doi: 10.1038/nature12228
    [65] Reimand J, Kull M, Peterson H, Hansen J, Vilo J. 2007. g:Profiler—a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Research, 35(S2): W193−W200.
    [66] Rogers J, Raveendran M, Harris RA, Mailund T, Leppälä K, Athanasiadis G, et al. 2019. The comparative genomics and complex population history of Papio baboons. Science Advances, 5(1): eaau6947. doi: 10.1126/sciadv.aau6947
    [67] Roos C, Boonratana R, Supriatna J, Fellowes JR, Groves CP, Nash SD, et al. 2014. An updated taxonomy and conservation status review of Asian primates. Asian Primates Journal, 4(1): 2−38.
    [68] Roos C, Kothe M, Alba DM, Delson E, Zinner D. 2019. The radiation of macaques out of Africa: evidence from mitogenome divergence times and the fossil record. Journal of Human Evolution, 133: 114−132. doi: 10.1016/j.jhevol.2019.05.017
    [69] Rovie-Ryan JJ, Khan FAA, Abdullah MT. 2021. Evolutionary pattern of Macaca fascicularis in southeast Asia inferred using y-chromosomal gene. BMC Ecology and Evolution, 21(1): 26. doi: 10.1186/s12862-021-01757-1
    [70] Schliep KP. 2011. Phangorn: phylogenetic analysis in R. Bioinformatics, 27(4): 592−593. doi: 10.1093/bioinformatics/btq706
    [71] Sniderman JMK, Woodhead JD, Hellstrom J, Jordan GJ, Drysdale RN, Tyler JJ, et al. 2016. Pliocene reversal of late Neogene aridification. Proceedings of the National Academy of Sciences of the United States of America, 113(8): 1999−2004. doi: 10.1073/pnas.1520188113
    [72] Solís-Lemus C, Bastide P, Ané C. 2017. PhyloNetworks: a package for phylogenetic networks. Molecular Biology and Evolution, 34(12): 3292−3298. doi: 10.1093/molbev/msx235
    [73] Stange M, Sánchez-Villagra MR, Salzburger W, Matschiner M. 2018. Bayesian divergence-time estimation with genome-wide single-nucleotide polymorphism data of sea catfishes (Ariidae) supports Miocene closure of the Panamanian isthmus. Systematic Biology, 67(4): 681−699. doi: 10.1093/sysbio/syy006
    [74] Stevison LS, Kohn MH. 2009. Divergence population genetic analysis of hybridization between rhesus and Cynomolgus macaques. Molecular Ecology, 18(11): 2457−2475. doi: 10.1111/j.1365-294X.2009.04212.x
    [75] Tarailo-Graovac M, Chen NS. 2009. Using repeatmasker to identify repetitive elements in genomic sequences. Current Protocols in Bioinformatics, 25(1): 4−10.
    [76] Tosi AJ, Coke CS. 2007. Comparative phylogenetics offer new insights into the biogeographic history of Macaca fascicularis and the origin of the mauritian macaques. Molecular Phylogenetics and Evolution, 42(2): 498−504. doi: 10.1016/j.ympev.2006.08.002
    [77] Tosi AJ, Disotell TR, Morales JC, Melnick DJ. 2003a. Cercopithecine y-chromosome data provide a test of competing morphological evolutionary hypotheses. Molecular Phylogenetics and Evolution, 27(3): 510−521. doi: 10.1016/S1055-7903(03)00024-1
    [78] Tosi AJ, Morales JC, Melnick DJ. 2000. Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Molecular Phylogenetics and Evolution, 17(2): 133−144. doi: 10.1006/mpev.2000.0834
    [79] Tosi AJ, Morales JC, Melnick DJ. 2003b. Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution, 57(6): 1419−1435. doi: 10.1111/j.0014-3820.2003.tb00349.x
    [80] Trask JAS, Garnica WT, Smith DG, Houghton P, Lerche N, Kanthaswamy S. 2013. Single-nucleotide polymorphisms reveal patterns of allele sharing across the species boundary between rhesus (Macaca mulatta) and cynomolgus (M. fascicularis) macaques. American Journal of Primatology, 75(2): 135−144. doi: 10.1002/ajp.22091
    [81] Vanderpool D, Minh BQ, Lanfear R, Hughes D, Murali S, Harris RA, et al. 2020. Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression. PLoS Biology, 18(12): e3000954. doi: 10.1371/journal.pbio.3000954
    [82] Wang RJ, Thomas GWC, Raveendran M, Harris RA, Doddapaneni H, Muzny DM, et al. 2020. Paternal age in rhesus macaques is positively associated with germline mutation accumulation but not with measures of offspring sociability. Genome Research, 30(6): 826−834. doi: 10.1101/gr.255174.119
    [83] Wen DQ, Yu Y, Zhu JF, Nakhleh L. 2018. Inferring phylogenetic networks using PhyloNet. Systematic Biology, 67(4): 735−740. doi: 10.1093/sysbio/syy015
    [84] Woodruff DS. 2010. Biogeography and conservation in southeast Asia: how 2.7 million years of repeated environmental fluctuations affect today’s patterns and the future of the remaining refugial-phase biodiversity. Biodiversity and Conservation, 19(4): 919−941. doi: 10.1007/s10531-010-9783-3
    [85] Xue C, Raveendran M, Harris RA, Fawcett GL, Liu XM, White S, et al. 2016. The population genomics of rhesus macaques (Macaca mulatta) based on whole-genome sequences. Genome Research, 26(12): 1651−1662. doi: 10.1101/gr.204255.116
    [86] Yan GM, Zhang GJ, Fang XD, Zhang YF, Li C, Ling F, et al. 2011. Genome sequencing and comparison of two nonhuman primate animal models, the cynomolgus and Chinese rhesus macaques. Nature Biotechnology, 29(11): 1019−1023. doi: 10.1038/nbt.1992
    [87] Yang FT, Shi LM. 1994. Studies of the miotic chromosomes, meiosis and spermatogenesis of a macaque hybrid. Acta Genetica Sinica, 21(1): 24−29. (in Chinese)
    [88] Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(8): 1586−1591. doi: 10.1093/molbev/msm088
    [89] Zhang C, Rabiee M, Sayyari E, Mirarab S. 2018. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinformatics, 19(S6): 153. doi: 10.1186/s12859-018-2129-y
    [90] Zhang DZ, Song G, Gao B, Cheng YL, Qu YH, Wu SY, et al. 2017. Genomic differentiation and patterns of gene flow between two long-tailed tit species (Aegithalos). Molecular Ecology, 26(23): 6654−6665. doi: 10.1111/mec.14383
    [91] Zhou XM, Meng XH, Liu ZJ, Chang J, Wang BS, Li MZ, et al. 2016. Population genomics reveals low genetic diversity and adaptation to hypoxia in snub-nosed monkeys. Molecular Biology and Evolution, 33(10): 2670−2681. doi: 10.1093/molbev/msw150
    [92] Ziegler T, Abegg C, Meijaard E, Perwitasari-Farajallah D, Walter L, Hodges JK, et al. 2007. Molecular phylogeny and evolutionary history of southeast Asian macaques forming the M. silenus group. Molecular Phylogenetics and Evolution, 42(3): 807−816. doi: 10.1016/j.ympev.2006.11.015
    [93] Zinner D, Arnold ML, Roos C. 2011. The strange blood: natural hybridization in primates. Evolutionary Anthropology: Issues, News, and Reviews, 20(3): 96−103. doi: 10.1002/evan.20301
  • ZR-2021-038Supplementary Materials.zip
  • 加载中
图(8) / 表(3)
计量
  • 文章访问数:  1530
  • HTML全文浏览量:  696
  • PDF下载量:  288
  • 被引次数: 0
出版历程
  • 收稿日期:  2021-04-19
  • 录用日期:  2021-05-20
  • 网络出版日期:  2021-06-09
  • 刊出日期:  2021-07-18

目录

    /

    返回文章
    返回