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Jin-Wu He, Ru Zhang, Jie Yang, Zhou Chang, Li-Xin Zhu, Si-Han Lu, Fei-Ang Xie, Jun-Lai Mao, Zhi-Wei Dong, Gui-Chun Liu, Ping Hu, Yan Dong, Wen-Ting Wan, Ruo-Ping Zhao, Tian-Zhu Xiong, Jorge L. León-Cortés, Chu-Yang Mao, Wei Zhang, Shuai Zhan, Jun Li, Lei Chen, Wen Wang, Xue-Yan Li. High-quality reference genomes of swallowtail butterflies provide insights into their coloration evolution. Zoological Research, 2022, 43(3): 367-379. doi: 10.24272/j.issn.2095-8137.2021.303
Citation: Jin-Wu He, Ru Zhang, Jie Yang, Zhou Chang, Li-Xin Zhu, Si-Han Lu, Fei-Ang Xie, Jun-Lai Mao, Zhi-Wei Dong, Gui-Chun Liu, Ping Hu, Yan Dong, Wen-Ting Wan, Ruo-Ping Zhao, Tian-Zhu Xiong, Jorge L. León-Cortés, Chu-Yang Mao, Wei Zhang, Shuai Zhan, Jun Li, Lei Chen, Wen Wang, Xue-Yan Li. High-quality reference genomes of swallowtail butterflies provide insights into their coloration evolution. Zoological Research, 2022, 43(3): 367-379. doi: 10.24272/j.issn.2095-8137.2021.303


doi: 10.24272/j.issn.2095-8137.2021.303

High-quality reference genomes of swallowtail butterflies provide insights into their coloration evolution

Funds: This work was supported by the National Natural Science Foundation of China (31621062 to W.W., 32070482 to X.Y.L.), Chinese Academy of Sciences (“Light of West China” to X.Y.L., XDB13000000 to W.W.), Yunnan Provincial Science and Technology Department (Talent Project of Yunnan: 202105AC160039), and Biodiversity Conservation Program of the Ministry of Ecology and Environment, China (China BON-Butterflies)
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  • 摘要: 凤蝶(凤蝶科)具有多彩的翅膀图案、丰富的形态多样性、重要的系统发育地位(是所有其他蝴蝶的姐妹类群)等,是历史上备受关注的蝴蝶类群。这一类群在生态适应、系统发育、遗传学和进化等领域都被广泛研究。值得注意的是,它们含有一类独特的色素类型,即凤蝶色素,这有助于颜色多样性的形成和各种生物学功能的发挥,如躲避捕食者和择偶。然而,到目前为止,系统发育和遗传的背景下,它们颜色多样性和凤蝶色素起源的基因组和遗传基础仍未可知。该研究使用长读长测序技术,解析了11种凤蝶的高质量参考基因组。结合之前发表的蝴蝶基因组,克服了不完全谱系分选和基因流等挑战,构建了族水平稳定的系统发育树。系统的基因组分析表明,模式基因和转运体/辅助因子等编码基因的凤蝶科特异的保守非外显子元件和转录因子结合位点的进化,以及转运体/辅因子的快速进化,可能促进了凤蝶色素的起源与进化。这些结果不仅为了解颜色多样性的基因组基础尤其是凤蝶色素的起源提供了新见解,而且为探索蝴蝶的进化、生态学和保护提供了重要的数据资源。
    #Authors contributed equally to this work
  • Figure  1.  Phylogeny of swallowtail butterflies

    A: Maximum-likelihood (ML) phylogenetic tree from ~45 Mb of syntenic whole-genome alignment (WGA) sequences of 17 swallowtail butterfly species (Papilionidae) and Kallima inachus (outgroup). One hundred bootstraps were used to compute node support, with all nodes showing 100% support. B: Superimposed ultrametric gene trees in a consensus DensiTree plot. Window-based gene trees (WGTs) and multispecies coalescent simulated gene trees are shown as observed and simulated, respectively.

    Figure  2.  Evolution of conserved non-exonic elements (CNEs) among swallowtail butterfly genomes

    A: Length and number of CNEs and Papilionidae-specific CNEs (PSCNEs). B: Location distribution of CNEs and PSCNEs in different genomic regions. C: KEGG enrichment (P<0.05) of neighboring genes physically associated with transcription factor binding sites (TFBSs) in PSCNEs. We selected top 20 KEGG terms ranked by count in PSCNEs. Pathways possibly related to color diversity in butterflies are highlighted in bold.

    Figure  3.  Schematic of papiliochrome biosynthesis

    Firstly, spatiotemporal expression of papiliochromes is mediated by different transcription factors (TFs) and patterning genes (above). Effector genes include two major categories. Enzymes (bottom left) that control biochemical synthesis of papiliochrome precursors. Transporters (such as ATP-binding cassette (ABC) transmembrane transporters and small G-proteins (Rab GTPases)) and their cofactors (bottom right) possibly contribute to the transport of pigment precursors to pigment granules, where different pigment precursors meet to combine into papiliochromes. art1/art2, two copies of aristaless; abd-A, abdominal A; en/inv paralogous genes engrailed and invected; wg, wingless; ABCGs, subfamily of ABC; GEF, guanine nucleotide exchange factor; GAP, GTPase-activating protein; E3, E3 ubiquitin ligase.

    Figure  4.  Evolution of papiliochrome biosynthesis-related genes

    A: Syntenic relationships of orthologous patterning genes (en/inv: engrailed and invected) among Lepidoptera were identified and visualized using MCScan. Species abbreviations with light blue and light brown backgrounds in tree represent species in Papilionidae (ingroups) and outgroups, respectively (same in panels B and D). B: Evolution of PSCNEs and Papilionidae-conserved TFBSs in upstream region (0–5 kb) of patterning gene (en). C: Phylogenetic tree of effector genes (small GTPases: Rab family). Papilio bianor and Drosophila melanogaster represent whole ingroup species (Papilionidae) and outgroup species, respectively. Genes labeled with gene ID evolved into Papilionidae-specific TFBSs in their upstream regions, or evolved Papilionidae-specific positively selected sites in their coding regions. Red arrow indicates Lepidoptera-specific (Lep) clade. REG, rapidly evolving gene; PSG, positively selected gene. D: Evolution of positively selected effector gene (Rab: Pb_06387) in Papilionidae. E: Network of patterning and effector genes in pigmentation and predicted TFs in their upstream regulatory regions. Size of different nodes is related to number of connections among nodes. Hub genes (number of connection nodes exceeding 10) in gene regulatory network are highlighted in red.

    Table  1.   Genome assembly and quality estimation of swallowtail butterflies

    SubfamilyTribeSpeciesK-merGenome assemblyReads mapping ratio (%)
    Estimated size
    Assembly size
    Scaffold N50
    Complete BUSCO
    ratio (%)
    ParnassiinaeParnassiniParnassius orleans1 1151 1763.292.098.396
    LuehdorfiiniLuehdorfia chinensis6786562.390.498.993
    ZerynthiniSericinus montelus5715675.595.897.588.4
    Bhutanitis thaidina44944914.89899.199
    PapilioninaeLeptocirciniLamproptera curius5505952.589.995.885.8
    TeinopalpiniTeinopalpus imperialis53550412.595.897.193.0
    TroidiniTroides helena33633010.596.697.478.1
    Byasa hedistus2712889.298.193.498.5
    PapilioniniMeandrusa payeni40639212.596.398.897.5
    Papilio demoleus2402409.197.597.899.0
    Papilio protenor2142465.497.497.798.7
    下载: 导出CSV
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  • 收稿日期:  2022-01-09
  • 录用日期:  2022-03-30
  • 网络出版日期:  2022-03-31
  • 刊出日期:  2022-05-18