Life and death of selfish genes: comparative genomics reveals the dynamic evolution of cytoplasmic incompatibility

Martinez, J. , Klasson, L., Welch, J. J. and Jiggins, F. M. (2021) Life and death of selfish genes: comparative genomics reveals the dynamic evolution of cytoplasmic incompatibility. Molecular Biology and Evolution, 38(1), pp. 2-15. (doi: 10.1093/molbev/msaa209) (PMID:32797213) (PMCID:PMC7783169)

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Cytoplasmic incompatibility is a selfish reproductive manipulation induced by the endosymbiont Wolbachia in arthropods. In males Wolbachia modifies sperm, leading to embryonic mortality in crosses with Wolbachia-free females. In females, Wolbachia rescues the cross and allows development to proceed normally. This provides a reproductive advantage to infected females, allowing the maternally transmitted symbiont to spread rapidly through host populations. We identified homologs of the genes underlying this phenotype, cifA and cifB, in 52 of 71 new and published Wolbachia genome sequences. They are strongly associated with cytoplasmic incompatibility. There are up to seven copies of the genes in each genome, and phylogenetic analysis shows that Wolbachia frequently acquires new copies due to pervasive horizontal transfer between strains. In many cases, the genes have subsequently acquired loss-of-function mutations to become pseudogenes. As predicted by theory, this tends to occur first in cifB, whose sole function is to modify sperm, and then in cifA, which is required to rescue the cross in females. Although cif genes recombine, recombination is largely restricted to closely related homologs. This is predicted under a model of coevolution between sperm modification and embryonic rescue, where recombination between distantly related pairs of genes would create a self-incompatible strain. Together, these patterns of gene gain, loss, and recombination support evolutionary models of cytoplasmic incompatibility.

Item Type:Articles
Glasgow Author(s) Enlighten ID:Martinez, Dr Julien
Authors: Martinez, J., Klasson, L., Welch, J. J., and Jiggins, F. M.
College/School:College of Medical Veterinary and Life Sciences > School of Infection & Immunity > Centre for Virus Research
Journal Name:Molecular Biology and Evolution
Publisher:Oxford University Press
ISSN (Online):1537-1719
Published Online:14 August 2020
Copyright Holders:Copyright © 2020 The Authors
First Published:First published in Molecular Biology and Evolution 38(1): 2-15
Publisher Policy:Reproduced under a Creative Commons License

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
168419Wolbachia as a defence against RNA viruses in insects. Wellcome Trust (094664/Z/10/Z)Alain KohlWellcome Trust (WELLCOTR)094664/Z/10/Z- RG61077III-MRC-GU Centre for Virus Research
173477Wolbachia-mediated arbovirus inhibition in mosquitoesSteven SinkinsWellcome Trust (WELLCOTR)202888/Z/16/ZIII-MRC-GU Centre for Virus Research