Multiple Wolbachia determinants control the evolution of cytoplasmic incompatibilities in Culex pipiens mosquito populations

Atyame, Célestine M.; Duron, Olivier; Tortosa, Pablo; Pasteur, Nicole; Fort, Philippe; Weill, Mylène

doi:10.1111/j.1365-294x.2010.04937.x

Cited by 50 publications

(75 citation statements)

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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%

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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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Section: Discussionsupporting

confidence: 86%

“…This situation is reminiscent of our recent study of Cx. pipiens populations on Réunion Island, in which closely related Wolbachia were found to encode a variety of resc functions in addition to the one involved in their self-compatibility [16].…”

Section: Discussionmentioning

confidence: 99%

Rapid evolution ofWolbachiaincompatibility types

et al. 2012

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“…Interestingly, very low Wolbachia diversity was found in natural populations of Cx . quinquefasciatus in the five investigated islands of south-western Indian Ocean (SWIO), namely La Réunion Island, Madagascar, Mayotte, Mauritius and Grande Glorieuse: all identified Wolbachia strains belonged to the w Pip-I group [4, 31]; thus suggesting that a single incompatible Wolbachia may be used for the control of all regional populations. Laboratory crossing experiments identified the Wolbachia w Pip(Is) strain (from the w Pip-IV group) as a good candidate for IIT in the islands of the SWIO.…”

Section: Introductionmentioning

confidence: 99%

“…quinquefasciatus in the islands of SWIO, where this species is considered as the main vector for lymphatic filarial and Rift Valley Fever virus [32], and exhibits high levels of insecticides resistance [33, 34]. As the efficacy of IIT may be impaired by the co-circulation of several distinct CI phenotypes in natural populations [31, 35], we first examined CI properties of the LR[ w Pip(Is)] line in reciprocal crosses involving field mosquitoes sampled as larvae in 19 distinct localities on La Réunion Island. We then assessed incompatible males’ competitiveness under semi field conditions, an investigation that is required prior to open field release since these conditions are more closely related to mosquitoes’ natural habitat.…”

Section: Introductionmentioning

confidence: 99%

Wolbachia-Based Population Control Strategy Targeting Culex quinquefasciatus Mosquitoes Proves Efficient under Semi-Field Conditions

et al. 2015

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In mosquitoes, the maternally inherited bacterial Wolbachia induce a form of embryonic lethality called cytoplasmic incompatibility (CI). This property can be used to reduce the density of mosquito field populations through inundative releases of incompatible males in order to sterilize females (Incompatible Insect Technique, or IIT, strategy). We have previously constructed the LR[wPip(Is)] line representing a good candidate for controlling field populations of the Culex quinquefasciatus mosquito in the islands of the south-western Indian Ocean. The main purpose of the present study was to fill the gap between laboratory experiments and field implementation, i.e. assessing mating competitiveness of these incompatible males under semi-field conditions. In a first set of experiments, we analyzed crossing relationships between LR[wPip(Is)] males and La Réunion field females collected as larvae in 19 distinct localities throughout the island. This investigation revealed total embryonic mortality, confirming the strong sterilizing capacity of LR[wPip(Is)] males. Subsequently, mating competitiveness of LR[wPip(Is)] males was assessed under semi-field conditions in the presence of field males and females from La Réunion. Confrontations were carried out in April and December using different ratios of LR[wPip(Is)] to field males. The results indicated that the LR[wPip(Is)] males successfully compete with field males in mating with field females, displaying even higher competitiveness than field males in April. Our results support the implementation of small-scale field tests in order to assess the feasibility of IIT against Cx. quinquefasciatus in the islands of southwestern Indian Ocean where this mosquito species is a proven competent vector for human pathogens.

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“…In this classical study system, the complexity and variability of incompatibility patterns have long been recognized (Laven 1967). The hypothesis that host nuclear variation could be responsible for such complexity, although appealing and theoretically sound (Rousset et al 1991), has been repeatedly ruled out by empirical data (Ghelelovitch 1952;Laven 1953Laven , 1957Laven , 1967Barr 1966;Irving-Bell 1983;Duron et al 2006Duron et al , 2012Walker et al 2009;Atyame et al 2011; but see Sinkins et al 2005). Figure 2 shows the compatibility matrix between 19 C. pipiens lines compiled from earlier studies (Duron et al 2006(Duron et al , 2007.…”

Section: Introductionmentioning

confidence: 99%

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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Multiple Wolbachia determinants control the evolution of cytoplasmic incompatibilities in Culex pipiens mosquito populations

Cited by 50 publications

References 67 publications

Rapid evolution ofWolbachiaincompatibility types

Rapid evolution ofWolbachiaincompatibility types

Wolbachia-Based Population Control Strategy Targeting Culex quinquefasciatus Mosquitoes Proves Efficient under Semi-Field Conditions

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

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