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Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies

Author

Listed:
  • Francesco Cicconardi

    (Bristol University
    University of Cambridge)

  • Edoardo Milanetti

    (Sapienza University
    Italian Institute of Technology)

  • Erika C. Pinheiro de Castro

    (University of Cambridge)

  • Anyi Mazo-Vargas

    (Cornell University)

  • Steven M. Van Belleghem

    (University of Puerto Rico
    KU Leuven)

  • Angelo Alberto Ruggieri

    (University of Puerto Rico)

  • Pasi Rastas

    (University of Helsinki)

  • Joseph Hanly

    (The George Washington University
    Smithsonian Tropical Research Institute)

  • Elizabeth Evans

    (University of Puerto Rico)

  • Chris D. Jiggins

    (University of Cambridge)

  • W. Owen McMillan

    (Smithsonian Tropical Research Institute)

  • Riccardo Papa

    (University of Puerto Rico
    University of Puerto Rico
    University of Puerto Rico)

  • Daniele Di Marino

    (Polytechnic University of Marche
    Mario Negri Institute for Pharmacological Research-IRCCS
    National Biodiversity Future Center (NBFC))

  • Arnaud Martin

    (The George Washington University)

  • Stephen H. Montgomery

    (Bristol University
    Smithsonian Tropical Research Institute)

Abstract

Heliconius butterflies, a speciose genus of Müllerian mimics, represent a classic example of an adaptive radiation that includes a range of derived dietary, life history, physiological and neural traits. However, key lineages within the genus, and across the broader Heliconiini tribe, lack genomic resources, limiting our understanding of how adaptive and neutral processes shaped genome evolution during their radiation. Here, we generate highly contiguous genome assemblies for nine Heliconiini, 29 additional reference-assembled genomes, and improve 10 existing assemblies. Altogether, we provide a dataset of annotated genomes for a total of 63 species, including 58 species within the Heliconiini tribe. We use this extensive dataset to generate a robust and dated heliconiine phylogeny, describe major patterns of introgression, explore the evolution of genome architecture, and the genomic basis of key innovations in this enigmatic group, including an assessment of the evolution of putative regulatory regions at the Heliconius stem. Our work illustrates how the increased resolution provided by such dense genomic sampling improves our power to generate and test gene-phenotype hypotheses, and precisely characterize how genomes evolve.

Suggested Citation

  • Francesco Cicconardi & Edoardo Milanetti & Erika C. Pinheiro de Castro & Anyi Mazo-Vargas & Steven M. Van Belleghem & Angelo Alberto Ruggieri & Pasi Rastas & Joseph Hanly & Elizabeth Evans & Chris D. , 2023. "Evolutionary dynamics of genome size and content during the adaptive radiation of Heliconiini butterflies," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41412-5
    DOI: 10.1038/s41467-023-41412-5
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    References listed on IDEAS

    as
    1. 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.
    2. Qiang Lin & Shaohua Fan & Yanhong Zhang & Meng Xu & Huixian Zhang & Yulan Yang & Alison P. Lee & Joost M. Woltering & Vydianathan Ravi & Helen M. Gunter & Wei Luo & Zexia Gao & Zhi Wei Lim & Geng Qin , 2016. "The seahorse genome and the evolution of its specialized morphology," Nature, Nature, vol. 540(7633), pages 395-399, December.
    3. Lukas Gerasimavicius & Benjamin J. Livesey & Joseph A. Marsh, 2022. "Loss-of-function, gain-of-function and dominant-negative mutations have profoundly different effects on protein structure," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Antoine Couto & Fletcher J. Young & Daniele Atzeni & Simon Marty & Lina Melo‐Flórez & Laura Hebberecht & Monica Monllor & Chris Neal & Francesco Cicconardi & W. Owen McMillan & Stephen H. Montgomery, 2023. "Rapid expansion and visual specialisation of learning and memory centres in the brains of Heliconiini butterflies," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. Joe Parker & Georgia Tsagkogeorga & James A. Cotton & Yuan Liu & Paolo Provero & Elia Stupka & Stephen J. Rossiter, 2013. "Genome-wide signatures of convergent evolution in echolocating mammals," Nature, Nature, vol. 502(7470), pages 228-231, October.
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    Cited by:

    1. Xinhua Fu & Xinlei Zhu, 2024. "Key homeobox transcription factors regulate the development of the firefly’s adult light organ and bioluminescence," Nature Communications, Nature, vol. 15(1), pages 1-18, December.

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