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Cited by 7Evolution and Genetic DynamicsChromosomal and Genetic VariationsRNA and protein synthesis mechanisms

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Recurrent evolution of selfishness from an essential tRNA synthetase in Caenorhabditis tropicalis

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Tikanova, Polina, Ross, James Julian, Hagmüller, Andreas, Pühringer, Florian, Pliota, Pinelopi, Krogull, Daniel, Stefania, Valeria, Hunold, Manuel, Koreshova, Alevtina, Koller, Anja, Ostapchuk, Ivanna, Okweri, Jacqueline, Gokcezade, Joseph, Duchek, Peter, Dong, Gang, Ben-David, Eyal, Burga, Alejandro·2025·Nature Ecology & Evolution
DOI 10.1038/s41559-025-02894-2PMC PMC12680543

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Abstract

No genome on Earth is free of selfish genes. This reflects both their ability to subvert the laws of inheritance and their de novo emergence from host genes. Yet, despite their ubiquity and key role in driving innovation, the mechanisms responsible for their genesis remain largely unexplored. Here we report the discovery of three toxin–antidote elements in the nematode Caenorhabditis tropicalis . Toxin–antidote elements are selfish genes that increase their frequency in populations by poisoning non-carrier individuals. We find that all three novel toxins— klmt-1 , pzl-1 and hyde-1 —arose via gene duplication from fars-3 , an essential subunit of the phenylalanyl tRNA synthetase. Their antidotes—KSS proteins—are rapidly evolving F-box proteins that degrade toxins via the SCF ubiquitin–ligase complex. Our phylogenetic and genomic analyses strongly suggest that the ancestor of all extant KSS antidotes fortuitously acquired affinity for FARS-3, much like ‘self’ proteins are targeted in autoimmune disease. This interaction neutralized the toxicity of future paralogues before it arose (presuppression), allowing otherwise deleterious mutant alleles to persist and ultimately evolve into selfish genes—consistent with the theory of constructive neutral evolution.

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Metadata

Authors
Tikanova, P., Ross, J. J., Hagmüller, A., Pühringer, F., Pliota, P., Krogull, D., Stefania, V., Hunold, M., Koreshova, A., Koller, A., Ostapchuk, I., Okweri, J., Gokcezade, J., Duchek, P., Dong, G., Ben-David, E., & Burga, A.
Affiliations
  • Institute of Molecular Biotechnology (AT)
  • Max Perutz Labs (AT)
Corresponding author
Burga, Alejandro
ORCID
Venue
Nature Ecology & Evolution
Publisher
Springer Science and Business Media LLC
Published
2025-11-17
Volume
9
Issue
12
Pages
2374-2390
ISSN
2397-334X (ISSN-L)
DOI
10.1038/s41559-025-02894-2
PMC
PMC12680543
OpenAlex
W4416299124
Cited by
7
References
6
Citations by year
2026: 4 · 2025: 1
FWCI
2.94
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Ecology & Evolution (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion, cc-by)
Funders
  • Österreichischen Akademie der Wissenschaften
  • Austrian Science Fund
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
Keywords
selfish genes, toxin-antidote system, phenylalanyl-tRNA synthetase, gene duplication, F-box protein, SCF ubiquitin ligase, parasexuality, autoimmune disease
MeSH terms
Animals, Caenorhabditis, Phenylalanine-tRNA Ligase, Phylogeny, Evolution, Molecular, Gene Duplication

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