Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia

In haplodiploid species, Wolbachia-induced cytoplasmic incompatibility (CI) can be expressed in one of two ways: as a "conversion" of diploid fertilized eggs into haploid males or as embryonic mortality. Here we describe CI-type variation within the parasitic wasp genus Nasonia and genetically analyze the basis of this variation. We reach four main conclusions: (i) CI is expressed primarily as conversion in N. vitripennis, but as embryonic mortality in the sibling species N. giraulti and N. longicornis; (ii) the difference in CI type between N. giraulti (mortality) and N. vitripennis (conversion) is determined by host nuclear genotype rather than by Wolbachia differences; (iii) N. vitripennis "conversion genes" are recessive in hybrid females; and (iv) a difference in CI level between the sibling species N. giraulti and N. longicornis is due to the different Wolbachia infections in the species rather than to the host genotype. These results show that host nuclear genes can influence the type of CI present in a species. On the basis of these findings, we propose a model for how different CI types evolve in haplodiploids due to selection on nuclear genes modifying CI.     

Contrasting effects of Wolbachia on cytoplasmic incompatibility and fecundity in the haplodiploid mite Tetranychus urticae

Recent studies on Wolbachia‐induced incompatibility in haplodiploid insects and mites have revealed a diversity of cytoplasmic incompatibility (CI) patterns among host species. Here, we report intraspecific diversity in CI expression among four strains of the arrhenotokous mite Tetranychus urticae and in T. turkestani. Variability of CI expression within T. urticae ranged from no CI to complete CI, and included either female embryonic mortality or male conversion types of CI. A fecundity cost attributed to the infection with the high‐CI Wolbachia strain was the highest ever recorded for Wolbachia (?80 to ?100% decrease). Sequence polymorphism at a 550‐bp‐portion of Wolbachia wsp gene revealed two clusters distant by 21%, one of which included three Wolbachia strains infecting mite populations sampled from the same host‐plant species, but showing distinct CI patterns. These data are discussed in the light of theoretical predictions on the evolutionary pathways followed in this symbiotic interaction.     

Wolbachia and cytoplasmic incompatibility in mosquitoes

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.     

Wolbachia symbiont infections induce strong cytoplasmic incompatibility in the tsetse fly Glossina morsitans

Tsetse flies are vectors of the protozoan parasite African trypanosomes, which cause sleeping sickness disease in humans and nagana in livestock. Although there are no effective vaccines and efficacious drugs against this parasite, vector reduction methods have been successful in curbing the disease, especially for nagana. Potential vector control methods that do not involve use of chemicals is a genetic modification approach where flies engineered to be parasite resistant are allowed to replace their susceptible natural counterparts, and Sterile Insect technique (SIT) where males sterilized by chemical means are released to suppress female fecundity. The success of genetic modification approaches requires identification of strong drive systems to spread the desirable traits and the efficacy of SIT can be enhanced by identification of natural mating incompatibility. One such drive mechanism results from the cytoplasmic incompatibility (CI) phenomenon induced by the symbiont Wolbachia. CI can also be used to induce natural mating incompatibility between release males and natural populations. Although Wolbachia infections have been reported in tsetse, it has been a challenge to understand their functional biology as attempts to cure tsetse of Wolbachia infections by antibiotic treatment damages the obligate mutualistic symbiont (Wigglesworthia), without which the flies are sterile. Here, we developed aposymbiotic (symbiont-free) and fertile tsetse lines by dietary provisioning of tetracycline supplemented blood meals with yeast extract, which rescues Wigglesworthia-induced sterility. Our results reveal that Wolbachia infections confer strong CI during embryogenesis in Wolbachia-free (Gmm(Apo)) females when mated with Wolbachia-infected (Gmm(Wt)) males. These results are the first demonstration of the biological significance of Wolbachia infections in tsetse. Furthermore, when incorporated into a mathematical model, our results confirm that Wolbachia can be used successfully as a gene driver. This lays the foundation for new disease control methods including a population replacement approach with parasite resistant flies. Alternatively, the availability of males that are reproductively incompatible with natural populations can enhance the efficacy of the ongoing sterile insect technique (SIT) applications by eliminating the need for chemical irradiation.     

Natural Wolbachia infections in the Drosophila yakuba species complex do not induce cytoplasmic incompatibility but fully rescue the wRi modification

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.     

Wolbachia与昆虫精卵细胞质不亲和

Wolbachia是广泛分布在昆虫体内的一类共生菌,能通过多种机制调节宿主的生殖方式,包括诱导宿主精卵细胞质不亲和(CI)、孤雌生殖、雌性化、杀雄等,其中细胞质不亲和为最普遍的表型,即感染Wolbachia的雄性和未感染或感染不同品系Wolbachia的雌性宿主交配后,受精卵不能正常发育,在胚胎期死亡。多数CI胚胎在第1次分裂时,来自父本的染色质浓缩缺陷,导致父本遗传物质无法正常分配到子细胞中,因而引起胚胎死亡。守门员模型认为,产生CI可能需要有两种因子,其中之一使得精子发生修饰改变,导致受精后雄性原核发育滞后。第2种因子可能与Wolbachia的原噬菌体有关,在胚胎发育后期导致胚胎死亡。近期的研究已发现,在Wolbachia感染的宿主中,一些与生殖细胞发生和繁殖相关基因的表达发生了显著改变,Wolbachia可能因此对宿主的生殖产生重大影响,进而导致CI的产生。本文主要综述了CI的细胞学表型、解释CI的模型及其分子机理,向读者展示一个小小的细菌是如何通过精妙的策略影响昆虫宿主的繁殖,从而实现其自身的生存和传播的。     

Infection polymorphism and cytoplasmic incompatibility in Hymenoptera-Wolbachia associations

Most cases of Wolbachia infection so far documented in haplodiploid Hymenoptera are associated with parthenogenesis induction. Only three examples of Wolbachia-mediated cytoplasmic incompatibility (CI) have been reported, resulting either in haploidisation of fertilised eggs, which develop into viable males, or in their death. To better document this variability, we studied two new Wolbachia-wasp associations involving Drosophila parasitoids. In Trichopria cf. drosophilae, individuals are infected by two different Wolbachia variants, populations are nearly totally infected, and Wolbachia induces incomplete CI resulting in death of the fertilised eggs. On the other hand, Pachycrepoideus dubius harbours only one bacterial variant, populations are polymorphic for infection, and Wolbachia has no detectable effect. These two cases show that the range of variation in Wolbachia's effects in Hymenoptera is as wide as in diploids, extending from complete CI to an undetectable effect. Cases so far studied show some parallel between the strength of incompatibility, the number of Wolbachia variants infecting each wasp, and the natural infection frequency. These empirical data support theoretical models predicting evolution of CI towards lower levels, resulting in the decline and ultimate loss of infection, and place multiple infections as being an important factor in the evolution of host-Wolbachia associations.     

Induced paternal effects mimic cytoplasmic incompatibility in Drosophila

Wolbachia is an intracellular microbe found in a wide diversity of arthropod and filarial nematode hosts. In arthropods these common bacteria are reproductive parasites that manipulate central elements of their host's reproduction to increase their own maternal transmission in one of several ways. Cytoplasmic incompatibility (CI) is one such manipulation where sperm are somehow modified in infected males and this modification must be rescued by the presence of the same bacterial strain in the egg for normal development to proceed. The molecular mechanisms involved in the expression of CI are unknown. Here we show that Wolbachia infection results in increased mRNA and protein expression of the Drosophila simulans nonmuscle myosin II gene zipper. Induced overexpression of zipper in Wolbachia-free transgenic D. melanogaster males results in paternal-effect lethality that mimics the fertilization defects associated with CI. Likewise, overexpression of the tumor suppressor gene, lethal giant larvae [l(2)gl], results in egg lethality and a CI phenotype. Stoichiometric levels of zipper and l(2)gl are required for proper segregation of cellular determinants during neuroblast stem cell division. Taken together these results form the basis of a working hypothesis whereby Wolbachia induces paternal effects in sperm by manipulating the expression of key regulators of cytoskeletal activity during spermatogenesis.     

Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan

Wolbachia are a group of maternally inherited bacteria that infect a wide range of arthropods. Wolbachia infections are known to result in the expression of various abnormal reproductive phenotypes, the best known being cytoplasmic incompatibility. The first systematic survey of 42 spider mite species in Japan revealed that seven species (16.7%) were infected with Wolbachia. Wolbachia in the spider mites were grouped into three subgroups in supergroup B by phylogenetic analyses of the wsp gene. Most spider mites did not show cytoplasmic incompatibility when infected males were crossed with uninfected females. However, all infected populations of Panonychus mori and Oligonychus gotohi (five and four populations, respectively) possessed modification-positive strains of Wolbachia, and the cytoplasmic incompatibility decreased egg hatchability and female ratio of the spider mites. Thus, some Wolbachia strains cause sex ratio distortion in their hosts.     

Modified SLCA algorithm for full-sib reconstruction of haplodiploid species

Full-sib reconstruction from molecular marker data in the absence of parental information is an active research area. Such analyses can provide useful information for studies of mating systems and gene flow, and for estimating effective population size in the wild. Although various methods have been proposed, but their estimation accuracies for some applications are not known. Here we propose a modified version of Shared Loci Correspondence Analysis (mSLCA) to reconstruct full-sib families of haplodiploid species. We ran simulations to compare the accuracies of the original SLCA and mSLCA. mSLCA outperformed SLCA at various data settings. mSLCA produced accurate estimates of the number of full-sib families when the numbers of loci and alleles per locus were equal to or more than eight. We also used actual DNA data of commercial Bombus terrestris colonies to verify the validity of estimates with an increasing number of colonies. mSLCA outperformed SLCA at various colony sizes with slight underestimation.     

Hybridization and cytoplasmic incompatibility among alfalfa weevil strains

Cross-matings were conducted among eastern, western, and Egyptian alfalfa weevil strains. Fully viable progenies were produced in reciprocal crosses between eastern and Egyptian weevils. The cross between western males and females of eastern or Egyptian strains was incompatible, producing infertile eggs, while the reciprocal cross yielded viable progeny but with a distorted sex ratio, predominantly female. The cause of incompatibility is due to the presence in the western weevil of a rickettsia, which is transmitted through the female parent. Of eight weevil populations surveyed, only the western weevil and a weevil population from the Netherlands harbored the rickettsiae. We conclude that all alfalfa weevil populations in the United States belong to the same species, Hypera postica (Gyllenhal), and that they are potentially interbreeding populations.

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Résumé Des croisements ont été effectués entre 3 lignées d'H. postica et H. brunneipennis. Des descendants totalement viables ont été obtenus par croisements réciproques entre H. postica de Beltsville et H. brunneipennis. Les croisements entre mâles de H. postica de Logan et femelles de H. postica de Beltsville ou de H. brunneipennis ont été incompatibles, produisant des oeufs stériles, tandis que les croisements réciproques donnaient une descendance viable, mais avec un taux sexuel modifié avec prédominance de femelles. La cause de l'incompatibilité est due à la présence d'une rickettsia dans les H. postica de Logan, transmise par la femelle. Des 8 populations examinées, seule celle de Logan et 1 des pays Bas hébergeaient des rickettsia. Nous en concluons que toutes les populations des USA appartiennent à H. postica Gyllenhal, et qu'elles sont toutes potentiellement interfécondes.

     

Cardinium symbionts cause cytoplasmic incompatibility in spider mites

Intracellular symbiotic bacteria belonging to the Cytophaga-Flavobacterium-Bacteroides lineage have recently been described and are widely distributed in arthropod species. The newly discovered bacteria, named Cardinium sp, cause the expression of various reproductive alterations in their arthropod hosts, including cytoplasmic incompatibility (CI), induction of parthenogenesis and feminization of genetic males. We detected 16S ribosomal DNA sequences similar to those of Cardinium from seven populations of five spider mite species, suggesting a broad distribution of infection of Cardinium in spider mites. To clarify the effect of Cardinium on the reproductive traits of the infected spider mites, infected mites were crossed with uninfected mites for each population. In one of the populations, Eotetranychus suginamensis, CI was induced when infected males were crossed with uninfected females. The other six populations of four species showed no reproductive abnormalities in the F(1) generation, but the possibility of CI effects in the F(2) generation remains to be tested. One species of spider mite, Tetranychus pueraricola, harbored both Cardinium and Wolbachia, but these symbionts seemed to have no effect on the reproduction of the host, even when the host was infected independently with each symbiont.     

The etiological agent of cytoplasmic incompatibility in Culex pipiens

All individuals of Culex pipiens (wide sense) which have been examined were infected with Wolbachia pipientis. Larvae reared in tetracycline were freed of these symbiotes and remained free (aposymbiotic) in future generations. When males were freed of their symbiotes, they no longer displayed incompatibility. Aposymbiotic males were compatible with all females, whether infected or not. Aposymbiotic females, on the other hand, laid fertile eggs after mating with aposymbiotic males, but not after mating with normal males. Most eggs laid by aposymbiotic females after mating with normal males showed no development at all, even though the females had been inseminated.     

Sperm chromatin remodelling and Wolbachia-induced cytoplasmic incompatibility in Drosophila.

Wolbachia pipientis is an obligate bacterial endosymbiont, which has successfully invaded approximately 20% of all insect species by manipulating their normal developmental patterns. Wolbachia-induced phenotypes include parthenogenesis, male killing, and, most notably, cytoplasmic incompatibility. In the future these phenotypes might be useful in controlling or modifying insect populations but this will depend on our understanding of the basic molecular processes underlying insect fertilization and development. Wolbachia-infected Drosophila simulans express high levels of cytoplasmic incompatibility in which the sperm nucleus is modified and does not form a normal male pronucleus when fertilizing eggs from uninfected females. The sperm modification is somehow rescued in eggs infected with the same strain of Wolbachia. Thus, D. simulans has become an excellent model organism for investigating the manner in which endosymbionts can alter reproductive programs in insect hosts. This paper reviews the current knowledge of Drosophila early development and particularly sperm function. Developmental mutations in Drosophila that are known to affect sperm function will also be discussed.incompatibility.     

Wolbachia segregation dynamics and levels of cytoplasmic incompatibility in Drosophila sechellia

In Drosophila sechellia, the endocellular bacterium Wolbachia induces cytoplasmic incompatibility (CI): in crosses involving infected males, a partial or complete embryonic mortality occurs unless the female bears the same Wolbachia. D. sechellia is known to harbour two Wolbachia variants, namely wSh and wSn, closely related to wHa and wNo, respectively, two strains infecting the populations of D. simulans from the Seychelles archipelago and New Caledonia. Strikingly, the two species show similar infection patterns: in D. sechellia, wSh can be present on its own or in double infection with wSn, but individuals carrying wSn only do not occur; in D. simulans, wHa can be present on its own or in double infection with wNo, but individuals carrying wNo only do not occur, or occur at very low frequency. Previous experiments on D. simulans showed that lines singly infected by wNo can be obtained by segregation, and stably maintained. Here we investigate this issue in D. sechellia through an 18 generation experiment, and show that wSn and wSh singly infected lines can arise by segregation. Using singly infected lines obtained in this experiment, we estimate the CI intensities of wSh and wSn in D. sechellia, and compare these to the CI intensities of the same Wolbachia injected into D. simulans. Our results do not suggest any consistent effect of the host species on the CI induced by wSh. On the contrary, it seems that wSn expression is repressed by host factors in D. sechellia.     

Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: mainland-island model

Bacteria of the genus Wolbachia are among the most common endosymbionts in the world. In many insect species these bacteria induce a sperm-egg incompatibility between the gametes of infected males and uninfected females, commonly called unidirectional cytoplasmic incompatibility (CI). It is generally believed that unidirectional CI cannot promote speciation in hosts because infection differences between populations will be unstable and subsequent gene flow will eliminate genetic differences between diverging populations. In the present study we investigate this question theoretically in a mainland-island model with migration from mainland to island. Our analysis shows that (a) the infection polymorphism is stable below a critical migration rate, (b) an (initially) uninfected "island" can better maintain divergence at a selected locus (e.g. can adapt locally) in the presence of CI, and (c) unidirectional CI selects for premating isolation in (initially) uninfected island populations if they receive migration from a Wolbachia-infected mainland. Interestingly, premating isolation is most likely to evolve if levels of incompatibility are intermediate and if either the infection causes fecundity reductions or Wolbachia transmission is incomplete. This is because under these circumstances an infection pattern with an infected mainland and a mostly uninfected island can persist in the face of comparably high migration. We present analytical results for all three findings: (a) a lower estimation of the critical migration rate in the presence of local adaptation, (b) an analytical approximation for the gene flow reduction caused by unidirectional CI, and (c) a heuristic formula describing the invasion success of mutants at a mate preference locus. These findings generally suggest that Wolbachia-induced unidirectional CI can be a factor in divergence and speciation of hosts.     

A re-examination of Wolbachia-induced cytoplasmic incompatibility in California Drosophila simulans

Background

In California Drosophila simulans, the maternally inherited Riverside strain Wolbachia infection (wRi) provides a paradigm for rapid spread of Wolbachia in nature and rapid evolutionary change. wRi induces cytoplasmic incompatibility (CI), where crosses between infected males and uninfected females produce reduced egg-hatch. The three parameters governing wRi infection-frequency dynamics quantify: the fidelity of maternal transmission, the level of cytoplasmic incompatibility, and the relative fecundity of infected females. We last estimated these parameters in nature in 1993. Here we provide new estimates, under both field and laboratory conditions. Five years ago, we found that wRi had apparently evolved over 15 years to enhance the fecundity of infected females; here we examine whether CI intensity has also evolved.

Methodology/Principal Findings

New estimates using wild-caught flies indicate that the three key parameters have remained relatively stable since the early 1990s. As predicted by our three-parameter model using field-estimated parameter values, population infection frequencies remain about 93%. Despite this relative stability, laboratory data based on reciprocal crosses and introgression suggest that wRi may have evolved to produce less intense CI (i.e., higher egg hatch from incompatible crosses). In contrast, we find no evidence that D. simulans has evolved to lower the susceptibility of uninfected females to CI.

Conclusions/Significance

Evolution of wRi that reduces CI is consistent with counterintuitive theoretical predictions that within-population selection on CI-causing Wolbachia does not act to increase CI. Within taxa, CI is likely to evolve mainly via pleiotropic effects associated with the primary targets of selection on Wolbachia, i.e., host fecundity and transmission fidelity. Despite continuous, strong selection, D. simulans has not evolved appreciably to suppress CI. Our data demonstrate a lack of standing genetic variation for CI resistance in the host.