Genome-wide analysis reveals signatures of complex introgressive gene flow in macaques (genus Macaca)
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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fascicularis和silenus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。Abstract: The genus Macaca serves as an ideal research model for speciation and introgressive gene flow due to its short period of diversification (about five million years ago) and rapid radiation of constituent species. To understand evolutionary gene flow in macaques, we sequenced four whole genomes (two M. arctoides and two M. thibetana) and combined them with publicly available macaque genome data for genome-wide analyses. We analyzed 14 individuals from nine Macaca species covering all Asian macaque species groups and detected extensive gene flow signals, with the strongest signals between the fascicularis and silenus species groups. Notably, we detected bidirectional gene flow between M. fascicularis and M. nemestrina. The estimated proportion of the genome inherited via gene flow between the two species was 6.19%. However, the introgression signals found among studied island species, such as Sulawesi macaques and M. fuscata, and other species were largely attributed to the genomic similarity of closely related species or ancestral introgression. Furthermore, gene flow signals varied in individuals of the same species (M. arctoides, M. fascicularis, M. mulatta, M. nemestrina and M. thibetana), suggesting very recent gene flow after the populations split. Pairwise sequentially Markovian coalescence (PSMC) analysis showed all macaques experienced a bottleneck five million years ago, after which different species exhibited different fluctuations in demographic history trajectories, implying they have experienced complicated environmental variation and climate change. These results should help improve our understanding of the complicated evolutionary history of macaques, particularly introgressive gene flow.
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Key words:
- Macaca /
- Whole genome /
- Introgression /
- Gene flow /
- Demographic history
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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 name Common name Sample ID NCBI accession No. Sex Sample origin Sequencing platform No. 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. Table 2. SNV information for each analyzed macaque
Sample Filtered Downsampled (~15×) SNVs Homo Het Callable sites Het Heterozygosity Ts Tv Ts/Tv Marc_R02 7 271 275 5 383 371 1 887 904 2 555 381 332 3 782 713 0.001 480 10 682 013 4 949 053 2.16 Marc_R19 7 000 609 5 675 953 1 324 656 2 553 354 858 2 644 171 0.001 036 10 334 343 4 762 614 2.17 Mass 7 926 468 4 560 039 3 366 429 2 519 264 130 6 121 131 0.002 430 10 831 112 5 023 843 2.16 Mfas_1 6 909 052 3 101 413 3 807 639 2 562 592 812 7 612 441 0.002 971 10 058 278 4 638 571 2.17 Mfas_Mau 6 773 377 3 895 560 2 877 817 2 549 849 925 5 881 316 0.002 307 10 190 936 4 659 300 2.19 Mfus 4 805 372 3 403 338 1 402 034 2 562 072 275 2 619 778 0.001 023 7 074 787 3 279 216 2.16 Mmul_Chi 5 192 005 2 071 981 3 120 024 2 556 851 619 5 748 608 0.002 248 7 168 259 3 273 752 2.19 Mmul_Ind 4 058 527 1 370 638 2 687 889 2 550 406 218 5 072 952 0.001 989 5 723 495 2 602 782 2.20 Mnem_1 8 733 029 4 860 252 3 872 777 2 559 986 484 7 267 811 0.002 839 12 211 436 5 571 807 2.19 Mnem_2 8 568 074 4 907 725 3 660 349 2 557 580 297 7 210 573 0.002 819 12 310 845 5 636 798 2.18 Mnig 7 743 384 6 043 224 1 700 160 2 553 652 584 3 353 047 0.001 313 11 259 320 5 250 264 2.14 Mthi_HT1 6 133 336 5 691 120 442 216 2 488 747 849 903 396 0.000 363 9 401 283 4 277 321 2.20 Mthi_R25 6 858 249 5 921 203 937 046 2 552 204 059 1 886 287 0.000 739 10 137 409 4 730 651 2.14 Mton 8 229 873 5 597 616 2 632 257 2 555 184 660 5 168 771 0.002 023 11 872 755 5 501 580 2.16 Panu 17 507 271 15 461 142 2 046 129 2 529 072 236 3 620 049 0.001 431 25 935 871 11 112 178 2.33 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. 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 pair No. of top 5% windows No. of shared windows Percentage of shared windows No. of specific windows Percentage of specific window M. fascicularis-silenus group species M. fascicularis-
M. nemestrina2 920 1 756 60.14 378 12.95 M. fascicularis-
M. nigra2 585 67.93 225 8.70 M. fascicularis-
M. tonkeana2 814 62.40 257 9.13 M. nemestrina-fascicularis group species M. fascicularis-
M. nemestrina2 920 1 382 47.33 378 12.95 M. fuscata-
M. nemestrina3 015 45.84 646 21.43 M. mulatta-
M. nemestrina2 999 46.08 446 14.87 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%. -
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ZR-2021-038Supplementary Materials.zip
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