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Adaptive expansion of ERVK solo-LTRs is associated with Passeriformes speciation events

Author

Listed:
  • Guangji Chen

    (University of Chinese Academy of Sciences
    Zhejiang University School of Medicine
    BGI Research)

  • Dan Yu

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Yu Yang

    (Huaqiao University)

  • Xiang Li

    (Chinese Academy of Sciences)

  • Xiaojing Wang

    (Chinese Academy of Sciences)

  • Danyang Sun

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Yanlin Lu

    (Zhejiang University School of Medicine
    Zhejiang University School of Medicine)

  • Rongqin Ke

    (Huaqiao University)

  • Guojie Zhang

    (Zhejiang University School of Medicine
    Zhejiang University)

  • Jie Cui

    (Fudan University
    Qingdao Marine Science and Technology Center
    Shanghai Sci-Tech Inno Center for Infection & Immunity
    Fudan University)

  • Shaohong Feng

    (Zhejiang University School of Medicine
    Zhejiang University
    Zhejiang University School of Medicine)

Abstract

Endogenous retroviruses (ERVs) are ancient retroviral remnants integrated in host genomes, and commonly deleted through unequal homologous recombination, leaving solitary long terminal repeats (solo-LTRs). This study, analysing the genomes of 362 bird species and their reptilian and mammalian outgroups, reveals an unusually higher level of solo-LTRs formation in birds, indicating evolutionary forces might have purged ERVs during evolution. Strikingly in the order Passeriformes, and especially the parvorder Passerida, endogenous retrovirus K (ERVK) solo-LTRs showed bursts of formation and recurrent accumulations coinciding with speciation events over past 22 million years. Moreover, our results indicate that the ongoing expansion of ERVK solo-LTRs in these bird species, marked by high transcriptional activity of ERVK retroviral genes in reproductive organs, caused variation of solo-LTRs between individual zebra finches. We experimentally demonstrated that cis-regulatory activity of recently evolved ERVK solo-LTRs may significantly increase the expression level of ITGA2 in the brain of zebra finches compared to chickens. These findings suggest that ERVK solo-LTRs expansion may introduce novel genomic sequences acting as cis-regulatory elements and contribute to adaptive evolution. Overall, our results underscore that the residual sequences of ancient retroviruses could influence the adaptive diversification of species by regulating host gene expression.

Suggested Citation

  • Guangji Chen & Dan Yu & Yu Yang & Xiang Li & Xiaojing Wang & Danyang Sun & Yanlin Lu & Rongqin Ke & Guojie Zhang & Jie Cui & Shaohong Feng, 2024. "Adaptive expansion of ERVK solo-LTRs is associated with Passeriformes speciation events," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47501-3
    DOI: 10.1038/s41467-024-47501-3
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    References listed on IDEAS

    as
    1. Shaohong Feng & Josefin Stiller & Yuan Deng & Joel Armstrong & Qi Fang & Andrew Hart Reeve & Duo Xie & Guangji Chen & Chunxue Guo & Brant C. Faircloth & Bent Petersen & Zongji Wang & Qi Zhou & Mark Di, 2020. "Dense sampling of bird diversity increases power of comparative genomics," Nature, Nature, vol. 587(7833), pages 252-257, November.
    2. Jianhua Wang & Guan-Zhu Han, 2023. "Genome mining shows that retroviruses are pervasively invading vertebrate genomes," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Joel Armstrong & Glenn Hickey & Mark Diekhans & Ian T. Fiddes & Adam M. Novak & Alden Deran & Qi Fang & Duo Xie & Shaohong Feng & Josefin Stiller & Diane Genereux & Jeremy Johnson & Voichita Dana Mari, 2020. "Progressive Cactus is a multiple-genome aligner for the thousand-genome era," Nature, Nature, vol. 587(7833), pages 246-251, November.
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