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Rapid chromosome evolution and acquisition of thermosensitive stochastic sex determination in nematode androdioecious hermaphrodites

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  • Kohta Yoshida

    (Max Planck Institute for Biology Tübingen
    National Institute of Genetics
    Niigata University)

  • Hanh Witte

    (Max Planck Institute for Biology Tübingen)

  • Ryo Hatashima

    (Institute of Science Tokyo)

  • Simo Sun

    (The University of Tokyo)

  • Taisei Kikuchi

    (The University of Tokyo)

  • Waltraud Röseler

    (Max Planck Institute for Biology Tübingen)

  • Ralf J. Sommer

    (Max Planck Institute for Biology Tübingen)

Abstract

The factors contributing to evolution of androdioecy, the coexistence of hermaphrodites and males such as in Caenorhabditis elegans, remains poorly known. However, nematodes exhibit androdioecy in at last 13 genera with the predatory genus Pristionchus having seven independent transitions towards androdioecy. Nonetheless, associated genomic architecture and sex determination mechanisms are largely known from Caenorhabditis. Here, studying 47 Pristionchus species, we observed repeated chromosome evolution which abolished the ancestral XX/XO sex chromosome system. Two phylogenetically unrelated androdioecious Pristionchus species have no genomic differences between sexes and mating hermaphrodites with males resulted in hermaphroditic offspring only. We demonstrate that stochastic sex determination is influenced by temperature in P. mayeri and P. entomophagus, and CRISPR engineering indicated a conserved role of the transcription factor TRA-1 in P. mayeri. Chromosome-level genome assemblies and subsequent genomic analysis of related Pristionchus species revealed stochastic sex determination to be derived from XY sex chromosome systems through sex chromosome-autosome fusions. Thus, rapid karyotype evolution, sex chromosome evolution and evolvable sex determination mechanisms are general features of this genus, and represent a dynamic background against which androdioecy has evolved recurrently. Future studies might indicate that stochastic sex determination is more common than currently appreciated.

Suggested Citation

  • Kohta Yoshida & Hanh Witte & Ryo Hatashima & Simo Sun & Taisei Kikuchi & Waltraud Röseler & Ralf J. Sommer, 2024. "Rapid chromosome evolution and acquisition of thermosensitive stochastic sex determination in nematode androdioecious hermaphrodites," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53854-6
    DOI: 10.1038/s41467-024-53854-6
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    1. Ryoji Shinya & Simo Sun & Mehmet Dayi & Isheng Jason Tsai & Atsushi Miyama & Anthony Fu Chen & Koichi Hasegawa & Igor Antoshechkin & Taisei Kikuchi & Paul W. Sternberg, 2022. "Possible stochastic sex determination in Bursaphelenchus nematodes," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
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