Maintenance of adaptive differentiation by Wolbachia induced bidirectional cytoplasmic incompatibility: the importance of sib-mating and genetic systems

<p>Abstract</p> <p>Background</p> <p>Bacteria of the genus <it>Wolbachia </it>are reproductive parasites widespread among arthropods. The most common effect arising from the presence of <it>Wolbachia </it>in a population is Cytoplasmic Incompatibility (CI), whereby postmating reproductive isolation occurs in crosses between an infected male and an uninfected female, or when a male is infected with a different strain of <it>Wolbachia </it>to that of the female (bidirectional CI). Previous theoretical models have demonstrated that bidirectional CI can contribute to the genetic divergence of populations in haploid and diploid organisms. However, haplodiploid organisms were not considered in these models even though they include <it>Nasonia </it>parasitoid wasps – the best example of the implication of <it>Wolbachia </it>in ongoing speciation. Moreover, previous work did not investigate inbreeding mating systems, which are frequently observed in arthropod species.</p> <p>Results</p> <p>We developed a stochastic two-island model which simulated three genetic scenarios, diploidy, haploidy, and haplodiploidy, with two CI phenotypes being considered for the latter: (1) male development of female progeny; and (2) mortality of fertilized eggs. We also investigated the effect of varying the proportion of sib mating. In the model each allopatric population was initially fixed for a single allele at a nuclear locus under positive selection and infected with one strain of <it>Wolbachia</it>. Each simulation presupposed that the two populations were fixed for a different allele and a different strain of <it>Wolbachia</it>. The degree of genetic differentiation observed in the locus under selection due to bidirectional CI was much lower for the two haplodiploid phenotypes than for either diploids or haploids. Furthermore, we demonstrated that sib-mating may compensate for the lower efficiency of bidirectional CI in haplodiploids by maintaining genetic divergence.</p> <p>Conclusion</p> <p>Our model suggests that maintenance of genetic differentiation facilitated by <it>Wolbachia </it>is more likely to occur in diploids and haploids than in haplodiploids. However, increasing the level of sib-mating may compensate for the weak effect of bidirectional CI in haplodiploids. Our work therefore gives a potential explanation for why the haplodiploid <it>Nasonia </it>species, which are infected with bidirectionally incompatible <it>Wolbachia </it>strains and undergo sib-mating, have differentiated genetically and maintained this differentiation without premating isolation.</p

Les bactéries symbiotiques d'arthropodes et de nématodes De nouvelles alliées dans le contrôle des maladies infectieuses Endosymbionts of arthropods and nematodes: allies to fight infectious diseases?

International audienceArthropods and nematodes are important protagonists in human health because either they act as vectors of pathogens (bacteria, protozoa, viruses or fungus), or are themselves parasites. Fighting infectious diseases is based essentially on vaccination (prevention) or chemotherapeutic (curative) approaches in human, but one can envisage as an alternative to reduce the number of vectors or limit their ability to spread pathogens. Such strategies controling dissemination will undoubtedly benefit from the knowledge accumumulated by recent works on powerful mechanisms developped by symbiotic insect bacteria such as Wolbachia to popagate in arthropods and nematods. This review summarizes these recent data, and indicate how these mechanisms can be manipulated to reduce the dissemination of insect vectors propagating human diseases

Intragenomic conflict in populations infected by Parthenogenesis Inducing Wolbachia ends with irreversible loss of sexual reproduction

<p>Abstract</p> <p>Background</p> <p>The maternally inherited, bacterial symbiont, parthenogenesis inducing (PI) <it>Wolbachia</it>, causes females in some haplodiploid insects to produce daughters from both fertilized and unfertilized eggs. The symbionts, with their maternal inheritance, benefit from inducing the production of exclusively daughters, however the optimal sex ratio for the nuclear genome is more male-biased. Here we examine through models how an infection with PI-<it>Wolbachia </it>in a previously uninfected population leads to a genomic conflict between PI-<it>Wolbachia </it>and the nuclear genome. In most natural populations infected with PI-<it>Wolbachia </it>the infection has gone to fixation and sexual reproduction is impossible, specifically because the females have lost their ability to fertilize eggs, even when mated with functional males.</p> <p>Results</p> <p>The PI <it>Wolbachia </it>infection by itself does not interfere with the fertilization process in infected eggs, fertilized infected eggs develop into biparental infected females. Because of the increasingly female-biased sex ratio in the population during a spreading PI-<it>Wolbachia </it>infection, sex allocation alleles in the host that cause the production of more sons are rapidly selected. In haplodiploid species a reduced fertilization rate leads to the production of more sons. Selection for the reduced fertilization rate leads to a spread of these alleles through both the infected and uninfected population, eventually resulting in the population becoming fixed for both the PI-<it>Wolbachia </it>infection and the reduced fertilization rate. Fertilization rate alleles that completely interfere with fertilization ("virginity alleles") will be selected over alleles that still allow for some fertilization. This drives the final resolution of the conflict: the irreversible loss of sexual reproduction and the complete dependence of the host on its symbiont.</p> <p>Conclusions</p> <p>This study shows that dependence among organisms can evolve rapidly due to the resolution of the conflicts between cytoplasmic and nuclear genes, and without requiring a mutualism between the partners.</p

Wolbachia Interferes with Ferritin Expression and Iron Metabolism in Insects

Wolbachia is an intracellular bacterium generally described as being a facultative reproductive parasite. However, Wolbachia is necessary for oogenesis completion in the wasp Asobara tabida. This dependence has evolved recently as a result of interference with apoptosis during oogenesis. Through comparative transcriptomics between symbiotic and aposymbiotic individuals, we observed a differential expression of ferritin, which forms a complex involved in iron storage. Iron is an essential element that is in limited supply in the cell. However, it is also a highly toxic precursor of Reactive Oxygen Species (ROS). Ferritin has also been shown to play a key role in host–pathogen interactions. Measuring ferritin by quantitative RT-PCR, we confirmed that ferritin was upregulated in aposymbiotic compared to symbiotic individuals. Manipulating the iron content in the diet, we showed that iron overload markedly affected wasp development and induced apoptotic processes during oogenesis in A. tabida, suggesting that the regulation of iron homeostasis may also be related to the obligate dependence of the wasp. Finally, we demonstrated that iron metabolism is influenced by the presence of Wolbachia not only in the obligate mutualism with A. tabida, but also in facultative parasitism involving Drosophila simulans and in Aedes aegypti cells. In these latter cases, the expression of Wolbachia bacterioferritin was also increased in the presence of iron, showing that Wolbachia responds to the concentration of iron. Our results indicate that Wolbachia may generally interfere with iron metabolism. The high affinity of Wolbachia for iron might be due to physiological requirement of the bacterium, but it could also be what allows the symbiont to persist in the organism by reducing the labile iron concentration, thus protecting the cell from oxidative stress and apoptosis. These findings also reinforce the idea that pathogenic, parasitic and mutualistic intracellular bacteria all use the same molecular mechanisms to survive and replicate within host cells. By impacting the general physiology of the host, the presence of a symbiont may select for host compensatory mechanisms, which extends the possible consequences of persistent endosymbiont on the evolution of their hosts

Parasite-Parasite Interactions in the Wild: How To Detect Them?

International audienceInter-specific interactions between parasites impact on parasite intra-hostdynamics, host health, and disease management. Identifying and understandinginteraction mechanisms in the wild is crucial for wildlife disease management.It is however complex because several scales are interlaced. Parasite–parasite interactions are likely to occur via mechanisms at the within-host level,but also at upper levels (host population and community). Furthermore, interactionsoccurring at one level of organization spread to upper levels throughcascade effects. Even if cascade effects are important confounding factors, weargue that we can also benefit from them because upper scales often provide away to survey a wider range of parasites at lower cost. New protocols andtheoretical studies (especially across scales) are necessary to take advantage ofthis opportunity

Influence of the Virus LbFV and of Wolbachia in a Host-Parasitoid Interaction

Symbionts are widespread and might have a substantial effect on the outcome of interactions between species, such as in host-parasitoid systems. Here, we studied the effects of symbionts on the outcome of host-parasitoid interactions in a four-partner system, consisting of the parasitoid wasp Leptopilina boulardi, its two hosts Drosophila melanogaster and D. simulans, the wasp virus LbFV, and the endosymbiotic bacterium Wolbachia. The virus is known to manipulate the superparasitism behavior of the parasitoid whereas some Wolbachia strains can reproductively manipulate and/or confer pathogen protection to Drosophila hosts. We used two nuclear backgrounds for both Drosophila species, infected with or cured of their respective Wolbachia strains, and offered them to L. boulardi of one nuclear background, either infected or uninfected by the virus. The main defence mechanism against parasitoids, i.e. encapsulation, and other important traits of the interaction were measured. The results showed that virus-infected parasitoids are less frequently encapsulated than uninfected ones. Further experiments showed that this viral effect involved both a direct protective effect against encapsulation and an indirect effect of superparasitism. Additionally, the Wolbachia strain wAu affected the encapsulation ability of its Drosophila host but the direction of this effect was strongly dependent on the presence/absence of LbFV. Our results confirmed the importance of heritable symbionts in the outcome of antagonistic interactions.Peer reviewe

Impact of Wolbachia on oxidative stress sensitivity in the parasitic wasp Asobara japonica

International audienceThe oxidative homeostasis is the balance between reactive oxygen species and antioxidant molecules. In addition to be considered as a key factor underlying life-history traits evolution, the oxidative homeostasis has been shown to be involved in many host–symbiont associations. Previous studies suggest an interaction between the bacterial endosymbiont Wolba-chia and the oxidative homeostasis of some insect hosts. This interaction is likely to exert a strong influence on the host evolution, as it has been proposed in the wasp Asobara tabida, whose dependence upon Wolbachia is due to the evolutionary loss of its ability to regulate the oxidative homeostasis in the absence of the symbiont. Although such cases of complete dependence are rare, cases of insects having lost only a part of their autonomy over the control of the oxidative homeostasis might be more common. If so, one can expect that insects having coevolved with Wolbachia will be more sensitive to oxidative stress when cured of their symbionts. We tested this hypothesis by studying the effects of an experimentally-induced oxidative stress on various life-history traits of Asobara japonica, a species closely related to A. tabida. For most of the life-history traits studied, the sensitivity of the wasps to oxidative stress did not correlate with their infection status. The only exception was the parasitic success. However, contrarily to our expectation, the sensitivity to oxidative stress was increased, rather than decreased, when Wolbachia was present. This result suggests that Wolbachia does not participate to mitigate oxidative stress in A. japonica, and that on the contrary its presence might still be costly in stressful environments

Influence of Microbial Symbionts on Plant–Insect Interactions

International audienceThere is growing evidence that microorganisms are important ‘hidden players’ in insect–plant interactions. Insect symbionts can directly affect these interactions by providing insects with key nutrients or by interfering with the plant to modulate food provisioning to insects and plant defences. Insect symbionts can also have indirect cascading ecological consequences at the community level through insect- and plant-mediated effects that include their impact on insect reproduction, on natural enemies of herbivores or on plant-associated microorganisms. Identification of symbiotic communities associated with insects, characterization of transmission and acquisition patterns as well as understanding of molecular mechanisms underlying these plant–insect–microbe interactions have important ecological and evolutionary consequences. This review highlights the excitement that surrounds these investigations and the promise they hold for a better understanding of the functional, ecological and evolutionary impacts of symbionts on plant–insect interactions, with implications and relevance for both applied and fundamental researches