Ubiquitous Selfish Toxin-Antidote Elements in Caenorhabditis Species

Eyal Ben-David*, Pinelopi Pliota, Sonya A. Widen, Alevtina Koreshova, Tzitziki Lemus-Vergara, Philipp Verpukhovskiy, Sridhar Mandali, Christian Braendle, Alejandro Burga, Leonid Kruglyak

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

16 Scopus citations

Abstract

Toxin-antidote elements (TAs) are selfish genetic dyads that spread in populations by selectively killing non-carriers. TAs are common in prokaryotes, but very few examples are known in animals. Here, we report the discovery of maternal-effect TAs in both C. tropicalis and C. briggsae, two distant relatives of C. elegans. In C. tropicalis, multiple TAs combine to cause a striking degree of intraspecific incompatibility: five elements reduce the fitness of >70% of the F2 hybrid progeny of two Caribbean isolates. We identified the genes underlying one of the novel TAs, slow-1/grow-1, and found that its toxin, slow-1, is homologous to nuclear hormone receptors. Remarkably, although previously known TAs act during embryonic development, maternal loading of slow-1 in oocytes specifically slows down larval development, delaying the onset of reproduction by several days. Finally, we found that balancing selection acting on linked, conflicting TAs hampers their ability to spread in populations, leading to more stable genetic incompatibilities. Our findings indicate that TAs are widespread in Caenorhabditis species and target a wide range of developmental processes and that antagonism between them may cause lasting incompatibilities in natural populations. We expect that similar phenomena exist in other animal species. Ben-David et al. find that selfish toxin-antidote elements are common in nematodes, can spread in nature by targeting post-embryonic development, and may prevent gene flow between populations.

Original languageAmerican English
Pages (from-to)990-1001.e5
JournalCurrent Biology
Volume31
Issue number5
DOIs
StatePublished - 8 Mar 2021

Bibliographical note

Funding Information:
We thank members of the Burga and Kruglyak labs for their comments. E.B.-D. is supported by the Israel Science Foundation (grant no. 2023/20) and NIH grant K99-HG010369; C.B. is supported by the Centre National de la Recherche Scientifique (CNRS); A.B. is supported by the Austrian Federal Ministry of Education, Science and Research, the Austrian Academy of Sciences, the City of Vienna, and the European Research Council under the European Union's Horizon 2020 research and innovation programme (ERC-2019-StG-851470); and L.K. is supported by the Howard Hughes Medical Institute and NIH grant R01 HG004321. E.B.-D. P.P. S.A.W. A.K. T.L.-V. P.V. S.M. and A.B. performed experiments. C.B. provided samples. E.B.-D. and A.B. conceptualized the study. A.B. and L.K. supervised the work. E.B.-D. A.B. and L.K. wrote the manuscript; all authors discussed and agreed on the final version of the manuscript. The authors declare no competing interests.

Publisher Copyright:
© 2020 The Author(s)

Keywords

  • Caenorhabditis
  • gene drive
  • genetic incompatibility
  • natural genetic variation
  • selfish gene
  • speciation
  • toxin-antidote
  • toxin-antitoxin

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