The Experts below are selected from a list of 324 Experts worldwide ranked by ideXlab platform
Seth R Bordenstein - One of the best experts on this subject based on the ideXlab platform.
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symbiont mediated Cytoplasmic Incompatibility what have we learned in 50 years
2020Co-Authors: Dylan J Shropshire, Brittany Leigh, Seth R BordensteinAbstract:Cytoplasmic Incompatibility (CI) is the most common symbiont-induced reproductive manipulation. Specifically, symbiont-induced sperm modifications cause catastrophic mitotic defects in the fertilized embryo and ensuing lethality in crosses between symbiotic males and either aposymbiotic females or females harboring a different symbiont strain. However, if the female carries the same symbiont strain, then embryos develop properly, thereby imparting a relative fitness benefit to symbiont-transmitting mothers. Thus, CI drives maternally-transmitted bacteria to high frequencies in arthropods worldwide. In the past two decades, CI experienced a boom in interest due to its (i) deployment in worldwide efforts to curb mosquito-borne diseases, (ii) causation by bacteriophage genes, cifA and cifB, that modify sexual reproduction, and (iii) important impacts on arthropod speciation. This review serves as a gateway to experimental, conceptual, and quantitative themes of CI and outlines significant gaps in understanding CI's mechanism that are ripe for investigation from diverse subdisciplines in the life sciences.
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paternal grandmother age affects the strength of wolbachia induced Cytoplasmic Incompatibility in drosophila melanogaster
Mbio, 2019Co-Authors: Emily M. Layton, Seth R Bordenstein, Jessamyn I. Perlmutter, Dylan J ShropshireAbstract:ABSTRACT Wolbachia are obligate intracellular bacteria that are globally distributed in half of all arthropod species. As the most abundant maternally inherited microbe in animals, Wolbachia manipulate host reproduction via reproductive parasitism strategies, including Cytoplasmic Incompatibility (CI). CI manifests as embryonic death when Wolbachia-modified sperm fertilize uninfected eggs but not maternally infected eggs. Thus, CI can provide a relative fitness advantage to Wolbachia-infected females and drive the infection through a population. In the genetic model Drosophila melanogaster, the Wolbachia strain wMel induces variable CI, making mechanistic studies in D. melanogaster cumbersome. Here, we demonstrate that sons of older paternal D. melanogaster grandmothers induce stronger CI than sons of younger paternal grandmothers, and we term this relationship the “paternal grandmother age effect” (PGAE). Moreover, the embryos and adult sons of older D. melanogaster grandmothers have higher Wolbachia densities, correlating with their ability to induce stronger CI. In addition, we report that Wolbachia density positively correlates with female age and decreases after mating, suggesting that females transmit Wolbachia loads that are proportional to their own titers. These findings reveal a transgenerational impact of age on wMel-induced CI, elucidate Wolbachia density dynamics in D. melanogaster, and provide a methodological advance to studies aimed at understanding wMel-induced CI in the D. melanogaster model. IMPORTANCE Unidirectional Cytoplasmic Incompatibility (CI) results in a postfertilization Incompatibility between Wolbachia-infected males and uninfected females. CI contributes to reproductive isolation between closely related species and is used in worldwide vector control programs to drastically lower arboviral vector population sizes or to replace populations that transmit arboviruses with those resistant to transmission. Despite decades of research on the factors that influence CI, penetrance is often variable under controlled laboratory conditions in various arthropods, suggesting that additional variables influence CI strength. Here, we demonstrate that paternal D. melanogaster grandmother age influences the strength of CI induced by their sons. Older D. melanogaster females have higher Wolbachia densities and produce offspring with higher Wolbachia densities that associate with stronger CI. This work reveals a multigenerational impact of age on CI and expands our understanding of host-Wolbachia interactions and the biology of CI induced by the Wolbachia strain infecting the most widely used arthropod model, D. melanogaster.
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one prophage wo gene rescues Cytoplasmic Incompatibility in drosophila melanogaster
Proceedings of the National Academy of Sciences of the United States of America, 2018Co-Authors: Dylan J Shropshire, Emily M. Layton, Helen Zhou, Seth R BordensteinAbstract:Wolbachia are maternally inherited, intracellular bacteria at the forefront of vector control efforts to curb arbovirus transmission. In international field trials, the Cytoplasmic Incompatibility (CI) drive system of wMel Wolbachia is deployed to replace target vector populations, whereby a Wolbachia-induced modification of the sperm genome kills embryos. However, Wolbachia in the embryo rescue the sperm genome impairment, and therefore CI results in a strong fitness advantage for infected females that transmit the bacteria to offspring. The two genes responsible for the wMel-induced sperm modification of CI, cifA and cifB, were recently identified in the eukaryotic association module of prophage WO, but the genetic basis of rescue is unresolved. Here we use transgenic and cytological approaches to demonstrate that maternal cifA expression independently rescues CI and nullifies embryonic death caused by wMel Wolbachia in Drosophila melanogaster. Discovery of cifA as the rescue gene and previously one of two CI induction genes establishes a “Two-by-One” model that underpins the genetic basis of CI. Results highlight the central role of prophage WO in shaping Wolbachia phenotypes that are significant to arthropod evolution and vector control.
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A single prophage WO gene rescues Cytoplasmic Incompatibility in Drosophila melanogaster
2018Co-Authors: J. Dylan Shropshire, Emily M. Layton, Helen Zhou, Seth R BordensteinAbstract:Wolbachia are maternally-inherited, intracellular bacteria at the forefront of vector control efforts to curb arbovirus transmission. In international field trials, the Cytoplasmic Incompatibility (CI) drive system of wMel Wolbachia is deployed to replace target vector populations, whereby a Wolbachia-induced modification of the sperm genome kills embryos. However, Wolbachia in the embryo rescue the sperm genome impairment, and therefore CI results in a strong fitness advantage for infected females that transmit the bacteria to offspring. The two genes responsible for the wMel-induced sperm modification of CI, cifA and cifB, were recently identified in the eukaryotic association module of prophage WO, but the genetic basis of rescue is unresolved. Here we use transgenic and cytological approaches to demonstrate that cifA independently rescues CI and nullifies embryonic death caused by wMel Wolbachia in Drosophila melanogaster. Discovery of cifA as the rescue gene and previously one of two CI induction genes establishes a new "Two-by-One" model that underpins the genetic basis of CI. Results highlight the central role of prophage WO in shaping Wolbachia phenotypes that are significant to arthropod evolution and vector control.
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Prophage WO genes recapitulate and enhance Wolbachia-induced Cytoplasmic Incompatibility
Nature, 2017Co-Authors: Daniel P. Lepage, Jason A. Metcalf, Sarah R. Bordenstein, Jessamyn I. Perlmutter, J. Dylan Shropshire, Emily M. Layton, Lisa J. Funkhouser-jones, John F. Beckmann, Seth R BordensteinAbstract:The discovery of two genes encoded by prophage WO from Wolbachia that functionally recapitulate and enhance Cytoplasmic Incompatibility in arthropods is the first inroad in solving the genetic basis of reproductive parasitism. The genus Wolbachia is an archetype of maternally inherited intracellular bacteria that infect the germline of numerous invertebrate species worldwide. They can selfishly alter arthropod sex ratios and reproductive strategies to increase the proportion of the infected matriline in the population. The most common reproductive manipulation is Cytoplasmic Incompatibility, which results in embryonic lethality in crosses between infected males and uninfected females. Females infected with the same Wolbachia strain rescue this lethality. Despite more than 40 years of research^ 1 and relevance to symbiont-induced speciation^ 2 , 3 , as well as control of arbovirus vectors^ 4 , 5 , 6 and agricultural pests^ 7 , the bacterial genes underlying Cytoplasmic Incompatibility remain unknown. Here we use comparative and transgenic approaches to demonstrate that two differentially transcribed, co-diverging genes in the eukaryotic association module of prophage WO^ 8 from Wolbachia strain w Mel recapitulate and enhance Cytoplasmic Incompatibility. Dual expression in transgenic, uninfected males of Drosophila melanogaster crossed to uninfected females causes embryonic lethality. Each gene additively augments embryonic lethality in crosses between infected males and uninfected females. Lethality associates with embryonic defects that parallel those of wild-type Cytoplasmic Incompatibility and is notably rescued by w Mel-infected embryos in all cases. The discovery of Cytoplasmic Incompatibility factor genes cifA and cifB pioneers genetic studies of prophage WO-induced reproductive manipulations and informs the continuing use of Wolbachia to control dengue and Zika virus transmission to humans. Bacteria from the genus Wolbachia infect many arthropods, including the mosquitoes that are vectors for many viruses that infect humans. Wolbachia infection causes 'Cytoplasmic Incompatibility', which means that crosses between infected males and uninfected females lead to embryonic death, increasing the proportion of infected females in the population. The molecular basis for this effect has been unknown. Here, Seth Bordenstein and colleagues use comparative and transgenic approaches to identify two genes encoded by the prophage WO from Wolbachia that recapitulate Cytoplasmic Incompatibility. The discovery of these Cytoplasmic Incompatibility factors could lead to the genetic manipulation of WO-induced reproductive alterations, and may feed into efforts to control the transmission of arthropod-borne viruses to humans.
Steven Sinkins - One of the best experts on this subject based on the ideXlab platform.
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Wolbachia transinfections in Culex quinquefasciatus generate Cytoplasmic Incompatibility
Insect Molecular Biology, 2019Co-Authors: Thomas Ant, Annabella Failloux, C. Herd, Faustine Louis, Steven SinkinsAbstract:Culex quinquefasciatus is an important mosquito vector of a number of viral and protozoan pathogens of humans and animals, and naturally carries the endosymbiont Wolbachia pipientis, strain wPip. Wolbachia are being used in two distinct vector control strategies: firstly, population suppression caused by mating incompatibilities between mass‐released transinfected males and wild females; and secondly, the spread of pathogen transmission‐blocking strains through populations. Using embryonic microinjection, two novel Wolbachia transinfections were generated in Cx. quinquefasciatus using strains native to the mosquito Aedes albopictus: a wAlbB single infection, and a wPip plus wAlbA superinfection. The wAlbB infection showed full bi‐directional Cytoplasmic Incompatibility (CI) with wild‐type Cx. quinquefasciatus in reciprocal crosses. The wPipwAlbA superinfection showed complete unidirectional CI, and therefore population invasion potential. While the wAlbB strain showed comparatively low overall densities, similar to the native wPip, the wPipwAlbA superinfection reached over 400‐fold higher densities in the salivary glands compared to the native wPip, suggesting it may be a candidate for pathogen transmission blocking.
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transcriptional regulation of culex pipiens mosquitoes by wolbachia influences Cytoplasmic Incompatibility
PLOS Pathogens, 2013Co-Authors: Sofia B Pinto, Kirsty Stainton, Simon R Harris, Zakaria Kambris, Elizabeth R Sutton, Michael B Bonsall, Julian Parkhill, Steven SinkinsAbstract:Cytoplasmic Incompatibility (CI) induced by the endosymbiont Wolbachia pipientis causes complex patterns of crossing sterility between populations of the Culex pipiens group of mosquitoes. The molecular basis of the phenotype is yet to be defined. In order to investigate what host changes may underlie CI at the molecular level, we examined the transcription of a homolog of the Drosophila melanogaster gene grauzone that encodes a zinc finger protein and acts as a regulator of female meiosis, in which mutations can cause sterility. Upregulation was observed in Wolbachia-infected C. pipiens group individuals relative to Wolbachia-cured lines and the level of upregulation differed between lines that were reproductively incompatible. Knockdown analysis of this gene using RNAi showed an effect on hatch rates in a Wolbachia infected Culex molestus line. Furthermore, in later stages of development an effect on developmental progression in CI embryos occurs in bidirectionally incompatible crosses. The genome of a wPip Wolbachia strain variant from Culex molestus was sequenced and compared with the genome of a wPip variant with which it was incompatible. Three genes in inserted or deleted regions were newly identified in the C. molestus wPip genome, one of which is a transcriptional regulator labelled wtrM. When this gene was transfected into adult Culex mosquitoes, upregulation of the grauzone homolog was observed. These data suggest that Wolbachia-mediated regulation of host gene expression is a component of the mechanism of Cytoplasmic Incompatibility.
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wolbachia strain wmel induces Cytoplasmic Incompatibility and blocks dengue transmission in aedes albopictus
Proceedings of the National Academy of Sciences of the United States of America, 2012Co-Authors: Marcus S C Blagrove, Camilo Ariasgoeta, Annabella Failloux, Steven SinkinsAbstract:Wolbachia inherited bacteria are able to invade insect populations using Cytoplasmic Incompatibility and provide new strategies for controlling mosquito-borne tropical diseases, such as dengue. The overreplicating wMelPop strain was recently shown to strongly inhibit the replication of dengue virus when introduced into Aedes aegypti mosquitoes, as well as to stimulate chronic immune up-regulation. Here we show that stable introduction of the wMel strain of Drosophila melanogaster into Aedes albopictus, a vector of dengue and other arboviruses, abolished the transmission capacity of dengue virus-challenged mosquitoes. Immune up-regulation was observed in the transinfected line, but at a much lower level than that previously found for transinfected Ae. aegypti. Transient infection experiments suggest that this difference is related to Ae. albopictus immunotolerance of Wolbachia, rather than to the Wolbachia strain used. This study provides an example of strong pathogen inhibition in a naturally Wolbachia-infected mosquito species, demonstrating that this inhibition is not limited to naturally naive species, and suggests that the Wolbachia strain is more important than host background for viral inhibition. Complete bidirectional Cytoplasmic Incompatibility was observed with WT strains infected with the naturally occurring Ae. albopictus Wolbachia, and this provides a mechanism for introducing wMel into natural populations of this species.
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Wolbachia and Cytoplasmic Incompatibility in mosquitoes
Insect biochemistry and molecular biology, 2004Co-Authors: Steven SinkinsAbstract:Wolbachia are maternally inherited bacteria that induce Cytoplasmic Incompatibility in mosquitoes, and are able to use these patterns of sterility to spread themselves through populations. For this reason they have been proposed as a gene drive system for mosquito genetic replacement, as well as for the reduction of population size or for modulating population age structure in order to reduce disease transmission. Here, recent progress in the study of mosquito Wolbachia is reviewed. We now have much more comprehensive estimates of the parameters that can affect the spread of Wolbachia through natural populations from low starting frequencies, and for waves of spread to be maintained in the face of partial barriers to gene flow. In Aedes albopictus these dynamics are extremely favourable, with very high maternal transmission fidelity and levels of Incompatibility recorded. Correspondence between measurements taken in the lab and field is much better than in the Drosophila simulans model system. Important research goals are also discussed, including Wolbachia transformation, interspecific transfer and the elucidation of the mechanisms of Incompatibility and rescue; all will be aided by a wealth of new Wolbachia genome information.
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wolbachia pipientis bacterial density and unidirectional Cytoplasmic Incompatibility between infected populations of aedes albopictus
Experimental Parasitology, 1995Co-Authors: Steven Sinkins, Henk R. Braig, Scott Leslie OneillAbstract:Unidirectional Cytoplasmic Incompatibility is seen when certain Wolbachia-infected insect populations are crossed. Two hypotheses might explain this phenomenon: superinfections with mutually incompatible strains of Wolbachia producing Incompatibility when crossed to individuals infected with only a single bacterial strain or, alternatively, a bacterial dosage model, with differences in Wolbachia densities responsible for the Incompatibility. A quantitative PCR assay was set up as a general method to compare Wolbachia densities between populations. Using this assay in unidirectionally incompatible stocks of the mosquito Aedes albopictus, we have determined that densities are significantly higher in Houston than in the Mauritius and Koh Samui stocks. This is consistent with a dosage model for the observed crossing patterns, but does not rule out the possibility that superinfection is the primary cause of the Incompatibility.
Stephen L. Dobson - One of the best experts on this subject based on the ideXlab platform.
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Fitness advantage and Cytoplasmic Incompatibility in Wolbachia single- and superinfected Aedes albopictus
Heredity, 2004Co-Authors: Stephen L. Dobson, Wanchai Rattanadechakul, Eric J. MarslandAbstract:Wolbachia are obligate, maternally inherited, intracellular bacteria that infect numerous insects and other invertebrates. Wolbachia infections have evolved multiple mechanisms to manipulate host reproduction and facilitate invasion of naive host populations. One such mechanism is Cytoplasmic Incompatibility (CI) that occurs in many insect species, including Aedes albopictus (Asian tiger mosquito). The multiple Wolbachia infections that occur naturally in A. albopictus make this mosquito a useful system in which to study CI. Here, experiments employ mosquito strains that have been introgressed to provide genetically similar strains that harbor differing Wolbachia infection types. Cytoplasmic Incompatibility levels, host longevity, egg hatch rates, and fecundity are examined. Crossing results demonstrate a pattern of additive unidirectional Cytoplasmic Incompatibility. Furthermore, relative to uninfected females, infected females are at a reproductive advantage due to both Cytoplasmic Incompatibility and a fitness increase associated with Wolbachia infection. In contrast, no fitness difference was observed in comparisons of single- and superinfected females. We discuss the observed results in regard to the evolution of the Wolbachia / A. albopictus symbiosis and the observed pattern of Wolbachia infection in natural populations.
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Fitness advantage and Cytoplasmic Incompatibility in Wolbachia single- and superinfected Aedes albopictus.
Heredity, 2004Co-Authors: Stephen L. Dobson, Wanchai Rattanadechakul, Eric J. MarslandAbstract:Fitness advantage and Cytoplasmic Incompatibility in Wolbachia single- and superinfected Aedes albopictus
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EVOLUTION OF WOLBACHIA Cytoplasmic Incompatibility TYPES
Evolution; international journal of organic evolution, 2004Co-Authors: Stephen L. DobsonAbstract:The success of obligate endosymbiotic Wolbachia infections in insects is due in part to Cytoplasmic Incompatibility (CI), whereby Wolbachia bacteria manipulate host reproduction to promote their invasion and persistence within insect populations. The observed diversity of CI types raises the question of what the evolutionary pathways are by which a new CI type can evolve from an ancestral type. Prior evolutionary models assume that Wolbachia exists within a host individual as a clonal infection. While endosymbiotic theory predicts a general trend toward clonality, Wolbachia provides an exception in which there is selection to maintain diversity. Here, evolutionary trajectories are discussed that assume that a novel Wolbachia variant will co-exist with the original infection type within a host individual as a superinfection. Relative to prior models, this assumption relaxes requirements and allows additional pathways for the evolution of novel CI types. In addition to describing changes in the Wolbachia infection frequency associated with the hypothesized evolutionary events, the predicted impact of novel CI variants on the host population is also described. This impact, resulting from discordant evolutionary interests of symbiont and host, is discussed as a possible cause of Wolbachia loss from the host population or host population extinction. The latter is also discussed as the basis for an applied strategy for the suppression of insect pest populations. Model predictions are discussed relative to a recently published Wolbachia genome sequence and prior characterization of CI in naturally and artificially infected insects.
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The effect of Wolbachia-induced Cytoplasmic Incompatibility on host population size in natural and manipulated systems
Proceedings. Biological sciences, 2002Co-Authors: Stephen L. Dobson, Charles W. Fox, Francis M. JigginsAbstract:Obligate, intracellular bacteria of the genus Wolbachia often behave as reproductive parasites by manipulating host reproduction to enhance their vertical transmission. One of these reproductive manipulations, Cytoplasmic Incompatibility, causes a reduction in egg-hatch rate in crosses between individuals with differing infections. Applied strategies based upon Cytoplasmic Incompatibility have been proposed for both the suppression and replacement of host populations. As Wolbachia infections occur within a broad range of invertebrates, these strategies are potentially applicable to a variety of medically and economically important insects. Here, we examine the interaction between Wolbachia infection frequency and host population size. We use a model to describe natural invasions of Wolbachia infections, artificial releases of infected hosts and releases of sterile males, as part of a traditional sterile insect technique programme. Model simulations demonstrate the importance of understanding the reproductive rate and intraspecific competition type of the targeted population, showing that releases of sterile or incompatible individuals may cause an undesired increase in the adult number. In addition, the model suggests a novel applied strategy that employs Wolbachia infections to suppress host populations. Releases of Wolbachia-infected hosts can be used to sustain artificially an unstable coexistence of multiple incompatible infections within a host population, allowing the host population size to be reduced, maintained at low levels, or eliminated.
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Wolbachia-Induced Cytoplasmic Incompatibility in Single- and Superinfected Aedes albopictus (Diptera: Culicidae)
Journal of medical entomology, 2001Co-Authors: Stephen L. Dobson, Eric J. Marsland, Wanchai RattanadechakulAbstract:Maternally inherited bacteria of the genus Volbachia can cause Cytoplasmic Incompatibility resulting in the developmental arrest of early embryos. Previous studies have shown that both single- and superinfections of Wolbachia naturally occur in populations of Aedes albopictus (Skuse). Here, we report crossing experiments using three infection types occurring in Ae. albopictus: uninfected, single-infected, and superinfected individuals. Crosses were monitored over the lifetime of adults to detect possible effects of host age on Cytoplasmic Incompatibility levels and infection virulence. Both single- and superinfections induced high levels of Cytoplasmic Incompatibility throughout the lifetime of Ae. albopictus, demonstrating that both the single- and superinfections are well adapted for invasion of Ae. albopictus populations. Superinfected females were the longest lived and had the highest oviposition rates, whereas in males, uninfected individuals were the longest lived. These latter results demonstrate the need for additional experiments to better elucidate Wolbachia effects on host fitness in addition to Cytoplasmic Incompatibility.
Eric J. Marsland - One of the best experts on this subject based on the ideXlab platform.
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Fitness advantage and Cytoplasmic Incompatibility in Wolbachia single- and superinfected Aedes albopictus
Heredity, 2004Co-Authors: Stephen L. Dobson, Wanchai Rattanadechakul, Eric J. MarslandAbstract:Wolbachia are obligate, maternally inherited, intracellular bacteria that infect numerous insects and other invertebrates. Wolbachia infections have evolved multiple mechanisms to manipulate host reproduction and facilitate invasion of naive host populations. One such mechanism is Cytoplasmic Incompatibility (CI) that occurs in many insect species, including Aedes albopictus (Asian tiger mosquito). The multiple Wolbachia infections that occur naturally in A. albopictus make this mosquito a useful system in which to study CI. Here, experiments employ mosquito strains that have been introgressed to provide genetically similar strains that harbor differing Wolbachia infection types. Cytoplasmic Incompatibility levels, host longevity, egg hatch rates, and fecundity are examined. Crossing results demonstrate a pattern of additive unidirectional Cytoplasmic Incompatibility. Furthermore, relative to uninfected females, infected females are at a reproductive advantage due to both Cytoplasmic Incompatibility and a fitness increase associated with Wolbachia infection. In contrast, no fitness difference was observed in comparisons of single- and superinfected females. We discuss the observed results in regard to the evolution of the Wolbachia / A. albopictus symbiosis and the observed pattern of Wolbachia infection in natural populations.
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Fitness advantage and Cytoplasmic Incompatibility in Wolbachia single- and superinfected Aedes albopictus.
Heredity, 2004Co-Authors: Stephen L. Dobson, Wanchai Rattanadechakul, Eric J. MarslandAbstract:Fitness advantage and Cytoplasmic Incompatibility in Wolbachia single- and superinfected Aedes albopictus
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Wolbachia-Induced Cytoplasmic Incompatibility in Single- and Superinfected Aedes albopictus (Diptera: Culicidae)
Journal of medical entomology, 2001Co-Authors: Stephen L. Dobson, Eric J. Marsland, Wanchai RattanadechakulAbstract:Maternally inherited bacteria of the genus Volbachia can cause Cytoplasmic Incompatibility resulting in the developmental arrest of early embryos. Previous studies have shown that both single- and superinfections of Wolbachia naturally occur in populations of Aedes albopictus (Skuse). Here, we report crossing experiments using three infection types occurring in Ae. albopictus: uninfected, single-infected, and superinfected individuals. Crosses were monitored over the lifetime of adults to detect possible effects of host age on Cytoplasmic Incompatibility levels and infection virulence. Both single- and superinfections induced high levels of Cytoplasmic Incompatibility throughout the lifetime of Ae. albopictus, demonstrating that both the single- and superinfections are well adapted for invasion of Ae. albopictus populations. Superinfected females were the longest lived and had the highest oviposition rates, whereas in males, uninfected individuals were the longest lived. These latter results demonstrate the need for additional experiments to better elucidate Wolbachia effects on host fitness in addition to Cytoplasmic Incompatibility.
Sylvain Charlat - One of the best experts on this subject based on the ideXlab platform.
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the toxin antidote model of Cytoplasmic Incompatibility genetics and evolutionary implications
Trends in Genetics, 2019Co-Authors: John F. Beckmann, Hervé Merçot, Mylène Weill, Hongli Chen, Mark Hochstrasser, Manon Bonneau, Denis Poinsot, Mathieu Sicard, Sylvain CharlatAbstract:Wolbachia bacteria inhabit the cells of about half of all arthropod species, an unparalleled success stemming in large part from selfish invasive strategies. Cytoplasmic Incompatibility (CI), whereby the symbiont makes itself essential to embryo viability, is the most common of these and constitutes a promising weapon against vector-borne diseases. After decades of theoretical and experimental struggle, major recent advances have been made toward a molecular understanding of this phenomenon. As pieces of the puzzle come together, from yeast and Drosophila fly transgenesis to CI diversity patterns in natural mosquito populations, it becomes clearer than ever that the CI induction and rescue stem from a toxin-antidote (TA) system. Further, the tight association of the CI genes with prophages provides clues to the possible evolutionary origin of this phenomenon and the levels of selection at play.
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The Toxin–Antidote Model of Cytoplasmic Incompatibility: Genetics and Evolutionary Implications
Trends in Genetics, 2019Co-Authors: John Beckmann, Mylène Weill, Hongli Chen, Mark Hochstrasser, Manon Bonneau, Denis Poinsot, Mathieu Sicard, Sylvain CharlatAbstract:Wolbachia bacteria inhabit the cells of about half of all arthropod species, an unparalleled success stemming in large part from selfish invasive strategies. Cytoplasmic Incompatibility (CI), whereby the symbiont makes itself essential to embryo viability, is the most common of these and constitutes a promising weapon against vector-borne diseases. After decades of theoretical and experimental struggle, major recent advances have been made toward a molecular understanding of this phenomenon. As pieces of the puzzle come together, from yeast and Drosophila fly transgenesis to CI diversity patterns in natural mosquito populations, it becomes clearer than ever that the CI induction and rescue stem from a toxin-antidote (TA) system. Further, the tight association of the CI genes with prophages provides clues to the possible evolutionary origin of this phenomenon and the levels of selection at play.
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Wolbachia Divergence and the Evolution of Cytoplasmic Incompatibility in Culex pipiens
PLoS ONE, 2014Co-Authors: Célestine Atyame Nten, Pierrick Labbe, Emilie Dumas, Pascal Milesi, Sylvain Charlat, Philippe Fort, Mylène WeillAbstract:Many insect species harbor Wolbachia bacteria that induce Cytoplasmic Incompatibility (CI), i.e. embryonic lethality in crosses between infected males and uninfected females, or between males and females carrying incompatible Wolbachia strains. The molecular mechanism of CI remains unknown, but the available data are best interpreted under a modification-rescue model, where a mod function disables the reproductive success of infected males' sperm, unless the eggs are infected and express a compatible resc function. Here we examine the evolution of CI in the mosquito Culex pipiens, harbouring a large number of closely related Wolbachia strains structured in five distinct phylogenetic groups. Specifically, we used a worldwide sample of mosquito lines to assess the hypothesis that genetic divergence should correlate with the divergence of CI properties on a low evolutionary scale. We observed a significant association of Wolbachia genetic divergence with CI patterns. Most Wolbachia strains from the same group were compatible whereas those from different groups were often incompatible. Consistently, we found a strong association between Wolbachia groups and their mod-resc properties. Finally, lines from the same geographical area were rarely incompatible, confirming the conjecture that the spatial distribution of Wolbachia compatibility types should be constrained by selection. This study indicates a clear correlation between Wolbachia genotypes and CI properties, paving the way toward the identification of the molecular basis of CI through comparative genomics. Citation: Atyame CM, Labbé P, Dumas E, Milesi P, Charlat S, et al. (2014) Wolbachia Divergence and the Evolution of Cytoplasmic Incompatibility in Culex pipiens. PLoS ONE 9(1): e87336.
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On the genetic architecture of Cytoplasmic Incompatibility: inference from phenotypic data
American Naturalist, 2013Co-Authors: Igor Nor, Jan Engelstädter, Olivier Duron, Max Reuter, Marie-france Sagot, Sylvain CharlatAbstract: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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Natural Wolbachia infections in the Drosophila yakuba species complex do not induce Cytoplasmic Incompatibility but fully rescue the wRi modification.
Genetics, 2004Co-Authors: Sofia Zabalou, Androniki Nirgianaki, Hervé Merçot, Sylvain Charlat, Daniel Lachaise, Kostas BourtzisAbstract:In this study, we report data about the presence of Wolbachia in Drosophila yakuba, D. teissieri, and D. santomea. Wolbachia strains were characterized using their wsp gene sequence and Cytoplasmic Incompatibility assays. All three species were found infected with Wolbachia bacteria closely related to the wAu strain, found so far in D. simulans natural populations, and were unable to induce Cytoplasmic Incompatibility. We injected wRi, a CI-inducing strain naturally infecting D. simulans, into the three species and the established transinfected lines exhibited high levels of CI, suggesting that absence of CI expression is a property of the Wolbachia strain naturally present or that CI is specifically repressed by the host. We also tested the relationship between the natural infection and wRi and found that it fully rescues the wRi modification. This result was unexpected, considering the significant evolutionary divergence between the two Wolbachia strains.
