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Ancient gene linkages support ctenophores as sister to other animals

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  • Darrin T. Schultz

    (University of Vienna
    Monterey Bay Aquarium Research Institute
    University of California)

  • Steven H. D. Haddock

    (Monterey Bay Aquarium Research Institute
    University of California)

  • Jessen V. Bredeson

    (University of California)

  • Richard E. Green

    (University of California)

  • Oleg Simakov

    (University of Vienna)

  • Daniel S. Rokhsar

    (University of California
    Okinawa Institute of Science and Technology Graduate University
    Chan Zuckerberg Biohub)

Abstract

A central question in evolutionary biology is whether sponges or ctenophores (comb jellies) are the sister group to all other animals. These alternative phylogenetic hypotheses imply different scenarios for the evolution of complex neural systems and other animal-specific traits1–6. Conventional phylogenetic approaches based on morphological characters and increasingly extensive gene sequence collections have not been able to definitively answer this question7–11. Here we develop chromosome-scale gene linkage, also known as synteny, as a phylogenetic character for resolving this question12. We report new chromosome-scale genomes for a ctenophore and two marine sponges, and for three unicellular relatives of animals (a choanoflagellate, a filasterean amoeba and an ichthyosporean) that serve as outgroups for phylogenetic analysis. We find ancient syntenies that are conserved between animals and their close unicellular relatives. Ctenophores and unicellular eukaryotes share ancestral metazoan patterns, whereas sponges, bilaterians, and cnidarians share derived chromosomal rearrangements. Conserved syntenic characters unite sponges with bilaterians, cnidarians, and placozoans in a monophyletic clade to the exclusion of ctenophores, placing ctenophores as the sister group to all other animals. The patterns of synteny shared by sponges, bilaterians, and cnidarians are the result of rare and irreversible chromosome fusion-and-mixing events that provide robust and unambiguous phylogenetic support for the ctenophore-sister hypothesis. These findings provide a new framework for resolving deep, recalcitrant phylogenetic problems and have implications for our understanding of animal evolution.

Suggested Citation

  • Darrin T. Schultz & Steven H. D. Haddock & Jessen V. Bredeson & Richard E. Green & Oleg Simakov & Daniel S. Rokhsar, 2023. "Ancient gene linkages support ctenophores as sister to other animals," Nature, Nature, vol. 618(7963), pages 110-117, June.
  • Handle: RePEc:nat:nature:v:618:y:2023:i:7963:d:10.1038_s41586-023-05936-6
    DOI: 10.1038/s41586-023-05936-6
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    Citations

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    Cited by:

    1. Minjun Jin & Wanqing Li & Zhongyu Ji & Guotao Di & Meng Yuan & Yifan Zhang & Yunsi Kang & Chengtian Zhao, 2024. "Coordinated cellular behavior regulated by epinephrine neurotransmitters in the nerveless placozoa," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Lauren E. Vandepas & Caroline Stefani & Phillip P. Domeier & Nikki Traylor-Knowles & Frederick W. Goetz & William E. Browne & Adam Lacy-Hulbert, 2024. "Extracellular DNA traps in a ctenophore demonstrate immune cell behaviors in a non-bilaterian," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Zhijun Dong & Fanghan Wang & Yali Liu & Yongxue Li & Haiyan Yu & Saijun Peng & Tingting Sun & Meng Qu & Ke Sun & Lei Wang & Yuanqing Ma & Kai Chen & Jianmin Zhao & Qiang Lin, 2024. "Genomic and single-cell analyses reveal genetic signatures of swimming pattern and diapause strategy in jellyfish," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Wenxiu Wang & Weizhi Song & Marwan E. Majzoub & Xiaoyuan Feng & Bu Xu & Jianchang Tao & Yuanqing Zhu & Zhiyong Li & Pei-Yuan Qian & Nicole S. Webster & Torsten Thomas & Lu Fan, 2024. "Decoupling of strain- and intrastrain-level interactions of microbiomes in a sponge holobiont," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Mario Ivanković & Jeremias N. Brand & Luca Pandolfini & Thomas Brown & Martin Pippel & Andrei Rozanski & Til Schubert & Markus A. Grohme & Sylke Winkler & Laura Robledillo & Meng Zhang & Azzurra Codin, 2024. "A comparative analysis of planarian genomes reveals regulatory conservation in the face of rapid structural divergence," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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