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Life and Death of Selfish Genes: Comparative Genomics Reveals the Dynamic Evolution of Cytoplasmic Incompatibility.

Accepted version
Peer-reviewed

Type

Article

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Authors

Martinez, Julien 
Klasson, Lisa 
Welch, John J 
Jiggins, Francis M 

Abstract

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.

Description

Keywords

Wolbachia, cif genes evolution, cytoplasmic incompatibility, Animals, Drosophila, Evolution, Molecular, Female, Genome, Bacterial, Host-Pathogen Interactions, Male, Repetitive Sequences, Nucleic Acid, Spermatozoa, Wolbachia

Journal Title

Mol Biol Evol

Conference Name

Journal ISSN

0737-4038
1537-1719

Volume Title

38

Publisher

Oxford University Press (OUP)

Rights

All rights reserved
Sponsorship
Wellcome Trust (094664/Z/10/Z)
European Research Council (281668)
Wellcome Trust grant number WT094664MA - Wellcome Trust grant number WT202888/Z/16/Z - ERC grant 281668