Wolbachia variability and host effects on crossing type in Culex mosquitoes

Sinkins, Steven P.; Walker, Thomas; Lynd, Amy; Steven, Andrew; Makepeace, Ben L.; Godfray, H. Charles J.; Parkhill, Julian

doi:10.1038/nature03629

Cited by 140 publications

(170 citation statements)

References 28 publications

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“…Besides, the implication of Wolbachia variants in the establishment of CI does not preclude the influence of others factors like nuclear genes, in particular restorer genes Sinkins et al 2005). Construction of strains harbouring distinct Wolbachia variants in a same nuclear genetic background is currently underway to address this latter issue.…”

Section: Discussionmentioning

confidence: 99%

“…Sanogo & Dobson (2004) delineated three wPip variants among 11 laboratory strains by analysis of the variability of orf7 copy number in the WO prophage. Sinkins et al (2005) described two wPip variants based on polymorphism of ankyrin-repeat encoding genes ( pk genes) associated with a prophage region. We identified previously five distinct wPip strains from 531 mosquitoes by analysing the polymorphism of Tr1, an apparently functional transposable element of the IS5 family (Duron et al 2005).…”

Section: Introductionmentioning

confidence: 99%

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Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens

2005

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Wolbachia are maternally inherited endosymbiotic bacteria that infect many arthropod species and may induce cytoplasmic incompatibility (CI) resulting in abortive embryonic development. Among all the described host species, mosquitoes of the Culex pipiens complex display the highest variability of CI crossing types. Paradoxically, searches for polymorphism in Wolbachia infecting strains and field populations hitherto failed or produced very few markers. Here, we show that an abundant source of the long-sought polymorphism lies in WO prophage sequences present in multiple copies dispersed in the genome of Wolbachia infecting C. pipiens (wPip). We identified up to 66 different Wolbachia variants in C. pipiens strains and field populations and no occurrence of superinfection was observed. At least 49 different Wolbachia occurred in Southern Europe C. pipiens populations, and up to 10 different Wolbachia were even detected in a single population. This is in sharp contrast with North African and Cretan samples, which exhibited only six variants. The WO polymorphism appeared stable over time, and was exclusively transferred maternally. Interestingly, we found that the CI pattern previously described correlates with the variability of Gp15, a prophage protein similar to a bacterial virulence protein. WO prophage sequences thus represent variable markers that now open routes for approaching the molecular basis of CI, the host effects, the structure and dynamics of Wolbachia populations.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens

2005

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“…pipiens complex appears to have been recent; how could this multitude of crossing types evolve in such a short evolutionary time period? It is possible that genetic differences in mosquito host factors are partially responsible; such factors have recently been implicated in modifying CI phenotype in Culex (Sinkins et al 2005) and in other insects (Bordenstein et al 2003;Mercot & Charlat 2004). Alternatively or in concert with host related factors, mobile genetic entities in Wolbachia, such as phages (Sinkins et al 2005;Duron et al 2006) or transposable elements (Bordenstein & Wernegreen 2004;Sanogo & Dobson 2004;Wu et al 2004;Duron et al 2005) could facilitate rapid evolution by causing mutations from insertion/transposition and/or by acting as a mechanism for horizontal transfer of genetic material between Wolbachia strains (Sinkins et al 2005).…”

Section: Discussionmentioning

confidence: 99%

Evolutionary history of a mosquito endosymbiont revealed through mitochondrial hitchhiking

2006

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Due to cytoplasmic inheritance, spread of maternally inherited Wolbachia symbionts can result in reduction of mitochondrial variation in populations. We examined sequence diversity of the mitochondrial NADH dehydrogenase subunit 4 (ND4 ) gene in Wolbachia-infected (South Africa (SA), California and Thailand) and uninfected (SA) Culex pipiens complex populations. In total, we identified 12 haplotypes (A-L). In infected populations, 99% of individuals had haplotype K. In the uninfected SA population, 11 haplotypes were present, including K. Nuclear allozyme diversity was similar between infected and uninfected SA populations. Analysis of nuclear DNA sequences suggested that haplotype K presence in uninfected SA Cx. pipiens was probably due to a shared ancestral polymorphism rather than hybrid introgression. These data indicate that Wolbachia spread has resulted in drastic reduction of mitochondrial variability in widely separated Cx. pipiens complex populations. In contrast, the uninfected SA population is probably a cryptic species where Wolbachia introgression has been prevented by reproductive isolation, maintaining ancestral levels of mitochondrial diversity. Molecular clock analyses suggest that the Wolbachia sweep occurred within the last 47 000 years. The effect of Wolbachia on mitochondrial dynamics can provide insight on the potential for Wolbachia to spread transgenes into mosquito populations to control vector-borne diseases.

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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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Wolbachia variability and host effects on crossing type in Culex mosquitoes

Cited by 140 publications

References 28 publications

Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens

Hypervariable prophage WO sequences describe an unexpected high number of Wolbachia variants in the mosquito Culex pipiens

Evolutionary history of a mosquito endosymbiont revealed through mitochondrial hitchhiking

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

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