Exploring the Evolution of Wolbachia Compatibility Types

Charlat, Sylvain; Calmet, Claire; Andrieu, Olivier; Merçot, Hervé

doi:10.1534/genetics.103.015198

Cited by 26 publications

(44 citation statements)

References 32 publications

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“…The presence of several Key factors in each strain, on the other hand, is not compatible with allelic variation and must be interpreted as being (at least partly) the result of variation in gene content. Interestingly, this interpretation is compatible with current theory for the evolution of CI types (Charlat et al 2001(Charlat et al , 2005Engelstädter et al 2006) and a model of evolution in which new Lock or Key types arise by point mutations, whereas new genes are created by duplication events. In order to understand the evolution of incompatibility under this model, consider a randomly mating host population fixed for CI bacteria containing a single pair of Lock and Key loci {Lock 1 , Key 1 }.…”

Section: Discussionsupporting

confidence: 87%

On the Genetic Architecture of Cytoplasmic Incompatibility: Inference from Phenotypic Data

Nor¹,

Engelstädter²,

Duron³

et al. 2013

The American Naturalist

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JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. abstract: Numerous insects carry intracellular bacteria that manipulate the insects' reproduction and thus facilitate their own spread. Cytoplasmic incompatibility (CI) is a common form of such manipulation, where a (currently uncharacterized) bacterial modification of male sperm induces the early death of embryos unless the fertilized eggs carry the same bacteria, inherited from the mother. The death of uninfected embryos provides an indirect selective advantage to infected ones, thus enabling the spread of the bacteria. Here we use and expand recently developed algorithms to infer the genetic architecture underlying the complex incompatibility data from the mosquito Culex pipiens. We show that CI requires more genetic determinants than previously believed and that quantitative variation in gene products potentially contributes to the observed CI patterns. In line with population genetic theory of CI, our analysis suggests that toxin factors (those inducing embryo death) are present in fewer copies in the bacterial genomes than antitoxin factors (those ensuring that infected embryos survive). In combination with comparative genomics, our approach will provide helpful guidance to identify the genetic basis of CI and more generally of other toxin/antitoxin systems that can be conceptualized under the same framework.

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Section: Discussionsupporting

confidence: 87%

On the Genetic Architecture of Cytoplasmic Incompatibility: Inference from Phenotypic Data

Nor¹,

Engelstädter²,

Duron³

et al. 2013

The American Naturalist

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“…Each new CI type observed here resulted from the gain of a new resc function with no apparent change in its mod function. This supports the notion that the mod and resc functions vary independently, in agreement with the fact that these functions are encoded by different genes of the Wolbachia genome [8,11,12,15,16].…”

Section: Discussionsupporting

confidence: 86%

“…In this study, we showed that changes in CI properties of Wolbachia infecting Cx. pipiens can be observed on a laboratory time scale, and support the notion that complexity of the mod -resc system allows a more gradual transition [32,33]. Within 5 years, new CI types emerged independently in two Cx.…”

Section: Discussionsupporting

confidence: 69%

Rapid evolution ofWolbachiaincompatibility types

et al. 2012

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In most insects, the endosymbiont Wolbachia induces cytoplasmic incompatibility (CI), an embryonic mortality observed when infected males mate either with uninfected females or with females infected by an incompatible Wolbachia strain. Although the molecular mechanism of CI remains elusive, it is classically viewed as a modification -rescue model, in which a Wolbachia mod function disables the reproductive success of the sperm of infected males, unless eggs are infected and express a compatible resc function. The extent to which the modification -rescue model can predict highly complex CI pattern remains a challenging issue. Here, we show the rapid evolution of the mod -resc system in the Culex pipiens mosquito. We have surveyed four incompatible laboratory isofemale lines over 50 generations and observed in two of them that CI has evolved from complete to partial incompatibility (i.e. the production of a mixture of compatible and incompatible clutches). Emergence of the new CI types depends only on Wolbachia determinants and can be simply explained by the gain of new resc functions. Evolution of CI types in Cx. pipiens thus appears as a gradual process, in which one or several resc functions can coexist in the same individual host in addition to the ones involved in the self-compatibility. Our data identified CI as a very dynamic process. We suggest that ancestral and mutant Wolbachia expressing distinct resc functions can co-infect individual hosts, opening the possibility for the mod functions to evolve subsequently. This gives a first clue towards the understanding of how Wolbachia reached highly complex CI pattern in host populations.

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“…A likely explanation for the lack of CI induction by Wolbachia-infected males is that the Wolbachia strain has the mod À phenotype that does not modify sperm (Bourtzis et al, 1998;Merçot and Poinsot, 1998;Charlat et al, 2001;Vala et al, 2002;Zabalou et al, 2004). Males infected with mod À strains are phenotypically indistinguishable from uninfected males; they are compatible with infected as well as uninfected females.…”

Section: Discussionmentioning

confidence: 99%

The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni

Ros

Breeuwer

2009

Heredity

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Many arthropods are infected with vertically transmitted, intracellular bacteria manipulating their host's reproduction. Cytoplasmic incompatibility (CI) is commonly observed and is expressed as a reduction in the number of offspring in crosses between infected males and uninfected females (or females infected with a different bacterial strain). CI is often related to the presence of Wolbachia, but recent findings indicate that a second reproductive parasite, Cardinium, is also capable of inducing CI. Although both Wolbachia and Cardinium occur in arthropods and may infect the same host species, little is known about their interactions. We observed Wolbachia and Cardinium in the sexual spider mite Bryobia sarothamni (Acari: Tetranychidae) and investigated the effects of both bacteria on reproduction. We performed all possible crossing combinations using naturally infected strains, and show that Cardinium induces strong CI, expressed as an almost complete female mortality. B. sarothamni is the third host species in which Cardiniuminduced CI is observed, and this study reveals the strongest CI effect found so far. Wolbachia, however, did not induce CI. Even so, CI was not induced by doubly infected males, and neither singly Wolbachia-infected nor doubly infected females could rescue CI induced by Cardinium-infected males. Possibly, this is related to the differences between Cardinium strains infecting singly and doubly infected individuals. We found a cost of infection in single infected individuals, but not in doubly infected individuals. We show that infection frequencies in field populations ranged from completely uninfected to a polymorphic state. In none of the populations infections were fixed.

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Exploring the Evolution of Wolbachia Compatibility Types

Cited by 26 publications

References 32 publications

On the Genetic Architecture of Cytoplasmic Incompatibility: Inference from Phenotypic Data

On the Genetic Architecture of Cytoplasmic Incompatibility: Inference from Phenotypic Data

Rapid evolution ofWolbachiaincompatibility types

The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni

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