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。     

From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila

Wolbachia are maternally inherited bacteria that commonly spread through host populations by causing cytoplasmic incompatibility, often expressed as reduced egg hatch when uninfected females mate with infected males. Infected females are frequently less fecund as a consequence of Wolbachia infection. However, theory predicts that because of maternal transmission, these "parasites" will tend to evolve towards a more mutualistic association with their hosts. Drosophila simulans in California provided the classic case of a Wolbachia infection spreading in nature. Cytoplasmic incompatibility allowed the infection to spread through individual populations within a few years and from southern to northern California (more than 700 km) within a decade, despite reducing the fecundity of infected females by 15%-20% under laboratory conditions. Here we show that the Wolbachia in California D. simulans have changed over the last 20 y so that infected females now exhibit an average 10% fecundity advantage over uninfected females in the laboratory. Our data suggest smaller but qualitatively similar changes in relative fecundity in nature and demonstrate that fecundity-increasing Wolbachia variants are currently polymorphic in natural populations.     

A genetic test of the mechanism of Wolbachia-induced cytoplasmic incompatibility in Drosophila

Cytoplasmic bacteria of the genus Wolbachia are best known as the cause of cytoplasmic incompatibility (CI): many uninfected eggs fertilized by Wolbachia-modified sperm from infected males die as embryos. In contrast, eggs of infected females rescue modified sperm and develop normally. Although Wolbachia cause CI in at least five insect orders, the mechanism of CI remains poorly understood. Here I test whether the target of Wolbachia-induced sperm modification is the male pronucleus (e.g., DNA or pronuclear proteins) or some extranuclear factor from the sperm required for embryonic development (e.g., the paternal centrosome). I distinguish between these hypotheses by crossing gynogenetic Drosophila melanogaster females to infected males. Gynogenetic females produce diploid eggs whose normal development requires no male pronucleus but still depends on extranuclear paternal factors. I show that when gynogenetic females are crossed to infected males, uniparental progeny with maternally derived chromosomes result. This finding shows that Wolbachia impair the male pronucleus but no extranuclear component of the sperm.     

Wolbachia affects oviposition and mating behaviour of its spider mite host

Wolbachia bacteria are transmitted from mother to offspring via the cytoplasm of the egg. When mated to males infected with Wolbachia bacteria, uninfected females produce unviable offspring, a phenomenon called cytoplasmic incompatibility (CI). Current theory predicts that ‘sterilization’ of uninfected females by infected males confers a fitness advantage to Wolbachia in infected females. When the infection is above a threshold frequency in a panmictic population, CI reduces the fitness of uninfected females below that of infected females and, consequently, the proportion of infected hosts increases. CI is a mechanism that benefits the bacteria but, apparently, not the host. The host could benefit from avoiding incompatible mates. Parasite load and disease resistance are known to be involved in mate choice. Can Wolbachia also be implicated in reproductive behaviour? We used the two‐spotted spider mite – Wolbachia symbiosis to address this question. Our results suggest that uninfected females preferably mate to uninfected males while infected females aggregate their offspring, thereby promoting sib mating. Our data agrees with other results that hosts of Wolbachia do not necessarily behave as innocent bystanders – host mechanisms that avoid CI can evolve.     

Can cytoplasmic incompatibility inducing Wolbachia promote the evolution of mate preferences?

The maternally inherited bacterium, Wolbachia pipientis, manipulates host reproduction by rendering uninfected females reproductively incompatible with infected males (cytoplasmic incompatibility, CI). Hosts may evolve mechanisms, such as mate preferences, to avoid fitness costs of Wolbachia infection. Despite the potential importance of mate choice for Wolbachia population dynamics, this possibility remains largely unexplored. Here we model the spread of an allele encoding female mate preference for uninfected males alongside the spread of CI inducing Wolbachia. Mate preferences can evolve but the spread of the preference allele depends on factors associated with both Wolbachia infection and the preference allele itself. Incomplete maternal transmission of Wolbachia, fitness costs and low CI, improve the spread of the preference allele and impact on the population dynamics of Wolbachia. In addition, mate preferences are found in infected individuals. These results have important consequences for the fate of Wolbachia and studies addressing mate preferences in infected populations.     

Variable fitness effects of Wolbachia infection in Drosophila melanogaster

Maternally inherited Wolbachia bacteria are extremely widespread among insects and their presence is usually associated with parasitic modifications of host fitness. Wolbachia pipientis infects Drosophila melanogaster populations from all continents, but their persistence in this species occurs despite any strong parasitic effects. Here, we have investigated the symbiosis between Wolbachia and D. melanogaster and found that Wolbachia infection can have significant survival and fecundity effects. Relative to uninfected flies, infected females from three fly strains showed enhanced survival or fecundity associated with Wolbachia infection, one strain showed both and one strain responded positively to Wolbachia removal. We found no difference in egg hatch rates (cytoplasmic incompatibility) for crosses between infected males and uninfected females, although there were fecundity differences. Females from this cross consistently produced fewer eggs than infected females and these fecundity differences could promote the spread of infection just like cytoplasmic incompatibility. More surprising, we found that infected females often had the greatest fecundity when mated to uninfected males. This could also promote the spread of Wolbachia infection, though here the fitness benefits would also help to spread infection when Wolbachia are rare. We suggest that variable fitness effects, in both sexes, and which interact strongly with the genetic background of the host, could increase cytoplasmic drive rates in some genotypes and help explain the widespread persistence of Wolbachia bacteria in D. melanogaster populations. These interactions may further explain why many D. melanogaster populations are polymorphic for Wolbachia infection. We discuss our results in the context of host-symbiont co-evolution.     

Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis

The aim of this study is to examine the expression of cytoplasmic incompatibility and investigate the distribution and population frequencies of Wolbachia pipientis strains in Drosophila simulans. Nucleotide sequence data from 16S rDNA and a Wolbachia surface protein coding sequence and cytoplasmic incompatibility assays identify four distinct Wolbachia strains: wHa, wRi, wMa, and wAu. The levels of cytoplasmic incompatibility between six lines carrying these strains of bacteria and three control lines without bacteria are characterized. Flies infected with wHa and wRi are bidirectionally incompatible, and males that carry either strain can only successfully produce normal numbers of offspring with females carrying the same bacterial strain. Males infected with wAu do not express incompatibility. Males infected with the wMa strain express intermediate incompatibility when mated to females with no bacteria and no incompatibility with females with any other Wolbachia strain. We conduct polymerase chain reaction/restriction fragment length polymorphism assays to distinguish the strain of Wolbachia and the mitochondrial haplotype to survey populations for each type and associations between them. Drosophila simulans is known to have three major mitochondrial haplotypes (siI, sill, and siIII) and two subtypes (siIIA and siIIB). All infected lines of the sil haplotype carry wHa, wNo, or both; wMa and wNo are closely related and it is not clear whether they are distinct strains or variants of the same strain. Infected lines with the silIA haplotype harbor wRi and the siIIB haplotype carries wAu. The wMa infection is found in siIII haplotype lines. The phenotypic expression of cytoplasmic incompatibility and its relation to between-population differences in frequencies of Wolbachia infection are discussed.     

Wolbachia plays no role in the one-way reproductive incompatibility between the hybridizing field crickets Gryllus firmus and G. pennsylvanicus

Wolbachia are cytoplasmically inherited alpha-proteobacteria that can cause cytoplasmic incompatibility (CI) in insects. This incompatibility between sperm and egg is evident when uninfected females mate with infected males. Wolbachia-driven reproductive incompatibilities are of special interest because they may play a role in speciation. However, the presence of Wolbachia does not always imply incompatibility. The field crickets Gryllus firmus and G. pennsylvanicus exhibit a very clear unidirectional incompatibility and have been cited as a possible example of Wolbachia-induced CI. Here, we conduct curing experiments, intra- and interspecific crosses, cytological examination of Wolbachia in testes and Wolbachia quantifications through real-time PCR. All of our data strongly suggest that Wolbachia are not involved in the reproductive incompatibility between G. firmus and G. pennsylvanicus.     

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.     

Dynamics of double and single Wolbachia infections in Drosophila simulans from New Caledonia

The bacterial symbiont Wolbachia can cause cytoplasmic incompatibility in Drosophila simulans flies: if an infected male mates with an uninfected female, or a female with a different strain of Wolbachia, there can be a dramatic reduction in the number of viable eggs produced. Here we explore the dynamics associated with double and single Wolbachia infections in New Caledonia. Doubly infected females were compatible with all males in the population, explaining the high proportion of doubly infected flies. In this study, males that carry only wHa or wNo infections showed reduced incompatibility when mated to uninfected females, compared with previous reports. These data suggest that either the DNA of these bacterial isolates have diverged from those previously collected, or the genetic background of the host has lead to a reduction in the phenotype of incompatibility. Mitochondrial sequence polymorphism at two sites within the host genome was assayed to investigate population structure related to infection types. There was no correlation between sequence polymorphism and infection type suggesting that double infections are the stable type, with singly infected and uninfected flies arising from stochastic segregation of bacterial strains. Finally, we discuss the nomenclature of Wolbachia strain designation.     

Increased male mating rate in Drosophila is associated with Wolbachia infection

The maternally inherited bacterium Wolbachia pipientis infects 25-75% of arthropods and manipulates host reproduction to improve its transmission. One way Wolbachia achieves this is by inducing cytoplasmic incompatibility (CI), where crosses between infected males and uninfected females are inviable. Infected males suffer reduced fertility through CI and reduced sperm production. However, Wolbachia induce lower levels of CI in nonvirgin males. We examined the impact of Wolbachia on mating behaviour in male Drosophila melanogaster and D. simulans, which display varying levels of CI, and show that infected males mate at a higher rate than uninfected males in both species. This may serve to increase the spread of Wolbachia, or alternatively, may be a behavioural adaptation employed by males to reduce the level of CI. Mating at high rate restores reproductive compatibility with uninfected females resulting in higher male reproductive success thus promoting male promiscuity. Increased male mating rates also have implications for the transmission of Wolbachia.     

Genetic diversity of Costa Rican populations of the rice planthopper Tagosodes orizicolus (Homoptera: Delphacidae)

Tagosodes orizicolus (Homoptera: Delphacidae) is one of the main constraints of the rice production in the Neotropics. This planthopper produces severe damages as a phloem feeder, causes mechanical injury during oviposition and vectors the rice hoja blanca virus (RHBV). The main objective of this study was to determine the genetic diversity of T. orizicolus populations from three rice growing regions of Costa Rica, using RAPDs. Individuals from Guanacaste, Parrita, San Carlos and Cali-Colombia, as outgroup, were analyzed using the random primers. Phenetic relationships revealed that the Costa Rican populations were clearly separated from Cali-Colombia, sharing less than 25% similarity. Costa Rican populations were divided into two main branches separated at 30% similarity. The first branch included Guanacaste and San Carlos and the second displayed Parrita. In relation to similarity indexes within groups, the Guanacaste cluster showed the highest (over 50%) and Cali-Colombia was the most diverse (28%). The correspondence analysis confirmed the clusters of the phenogram and showed close interactions between the Parrita and San Carlos populations. The genetic separation observed could be the result of the geographic isolation among populations, but it could also be explained by the infection with the rickettsia Wolbachia pipientis. This bacterium causes cytoplasmic incompatibility in its host, which results in non-viable progeny when infected males mate with non-infected females, or when insects hosting different strains of Wolbachia mate. Then, a search for Wolbachia in previously described populations of T orizicolus was initiated. The presence of the bacteria was analyzed by PCR with 16S rDNA-specific primers for Wolbachia. The PCR analyses revealed infections of 86% in the population of San Carlos, 96% in Guanacaste, 37% in Parrita and 100% in Cali-Colombia. Crosses between individuals of T. orizicolus from Parrita and Guanacaste were performed for testing cytoplasmic incompatibility. When infected males were crossed with non-infected females within the same population, a significant reduction in progeny number was obtained as well as when crosses between infected individuals belonging to different populations were performed. These experiments showed cytoplasmic incompatibility not only caused by the presence of Wolbachia within the population, but also by the presence of different strains of the bacteria between populations.     

Cytoplasmic Incompatibility in Drosophila Simulans: Dynamics and Parameter Estimates from Natural Populations

In Drosophila simulans, cytoplasmically transmitted Wolbachia microbes cause reduced egg hatch when infected males mate with uninfected females. A Wolbachia infection and an associated mtDNA variant have spread northward through California since 1986. PCR assays show that Wolbachia infection is prevalent throughout the continental US and Central and South America, but some lines from Florida and Ecuador that are PCR-positive for Wolbachia do not cause incompatibility. We estimate from natural populations infection frequencies and the transmission and incompatibility parameter values that affect the spread of the infection. On average, infected females from nature produce 3-4% uninfected ova. Infected females with relatively low fidelity of maternal transmission show partial incompatibility with very young infected laboratory males. Nevertheless, crosses between infected flies in nature produce egg-hatch rates indistinguishable from those produced by crosses between uninfected individuals. Incompatible crosses in nature produce hatch rates 30-70% as high as those from compatible crosses. Wild-caught infected and uninfected females are equally fecund in the laboratory. Incompatibility decreases with male age, and age-specific incompatibility levels suggest that males mating in nature may often be 2 or 3 weeks old. Our parameter estimates accurately predict the frequency of Wolbachia infection in California populations.     

Wolbachia-induced 'hybrid breakdown' in the two-spotted spider mite Tetranychus urticae Koch

The most common post-zygotic isolation mechanism between populations of the phytophagous mite Tetranychus urticae is 'hybrid breakdown', i.e. when individuals from two different populations are crossed, F1 hybrid females are produced, but F2 recombinant male offspring suffer increased mortality. Two-spotted spider mites collected from two populations, one on rose and the other on cucumber plants, were infected with Wolbachia bacteria. These bacteria may induce cytoplasmic incompatibility in their hosts: uninfected (U) females become reproductively incompatible with infected (W) males. We report on the effect of Wolbachia infections in intra- and interstrain crosses on (i) F1 mortality and sex ratios (a test for cytoplasmic incompatibility), and (ii) the number of haploid offspring and mortality in clutches of F1 virgins (a test for hybrid breakdown). U x W crosses within the rose strain exhibited partial cvtoplasmic incompatibility. More interestingly, F2 males suffered increased mortality, a result identical to the hybrid breakdown phenomenon. The experiments were repeated using females from the cucumber strain. In interstrain U x W and U x U crosses, hybrid breakdown was much stronger in the former (80 versus 26%). This is the first report of a Wolbachia infection causing a hybrid breakdown phenotype. Our results show that Wolbhachia infections can contribute to reproductive incompatibility between populations of T. urticae.     

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

Wolbachia are maternally inherited endosymbionts that can invade arthropod populations through manipulation of their reproduction. In mosquitoes, Wolbachia induce embryonic death, known as cytoplasmic incompatibility (CI), whenever infected males mate with females either uninfected or infected with an incompatible strain. Although genetic determinants of CI are unknown, a functional model involving the so-called mod and resc factors has been proposed. Natural populations of Culex pipiens mosquito display a complex CI relationship pattern associated with the highest Wolbachia (wPip) genetic polymorphism reported so far. We show here that C. pipiens populations from La Réunion, a geographically isolated island in the southwest of the Indian Ocean, are infected with genetically closely related wPip strains. Crossing experiments reveal that these Wolbachia are all mutually compatible. However, crosses with genetically more distant wPip strains indicate that Wolbachia strains from La Réunion belong to at least five distinct incompatibility groups (or crossing types). These incompatibility properties which are strictly independent from the nuclear background, formally establish that in C. pipiens, CI is controlled by several Wolbachia mod/resc factors.     

Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans

The effects of high temperatures, antibiotics, nutrition and larval density on cytoplasmic incompatibility caused by a Wolbachia infection were investigated in Drosophila simulans. Exposure of larvae from an infected stock to moderate doses of tetracycline led to complete incompatibility when treated females were crossed to infected males; the same doses only caused a partial restoration of compatibility when treated males were crossed to uninfected females. In crosses with treated females, there was a strong correlation between dose effects on hatch rates and infection levels in embryos produced by these females. Ageing and rearing males at a high temperature led to increased compatibility. However, exposing infected females to a high temperature did not influence their compatibility with infected males. Male temperature effects depended on conditions experienced at the larval stage but not the pupal stage. Exposure to 25 °C reduced the density of Wolbachia in embryos compared with a 19 °C treatment. Low levels of nutrition led to increased compatibility, but no effect of larval crowding was detected. These findings show the ways environmental factors can influence the expression of cytoplasmic incompatibility and suggest that environmental effects may be mediated by bacterial density.     

Population dynamics of noncytoplasmic incompatibility-inducing Wolbachia in Nilaparvata lugens and its effects on host adult life span and female fitness

Wolbachia are bacteria that live intracellularly in a wide variety of arthropods. They are maternally inherited and can affect both reproduction and fitness of its host. When infected males mate with uninfected females or females infected by a different Wolbachia strain, there is often a failure of karyogamy, which is usually attributed to cytoplasmic incompatibility (CI). We measured the strength of CI induced by Wolbachia and the fitness effects in three Chinese populations of the brown planthopper Nilaparvata lugens from Hainan, Yunnan, and Guangxi provinces, respectively. No evidence for CI was found in any of the populations, whereas an enhanced fecundity and shortened longevity were observed only in the Hainan population. The infection density was significantly higher in the Hainan population than in the Guangxi population. The Wolbachia strain infecting the three populations appeared to be the same based on the nucleotide sequence of the wsp gene. Therefore, the variable effects of Wolbachia on host fitness seem to be the result of differences in the host genetic background and Wolbachia infection density. The ability of the non-CI-inducing Wolbachia to maintain themselves in their hosts may be attributed to their positive effects on host fecundity and efficient maternal transmission.     

Wolbachia and reproductive conflict in Exorista sorbillans

Many arthropods harbour endosymbiotic bacteria of the genus Wolbachia. These endosymbionts are transmitted vertically from one generation to the next and are obligatory in several Dipterans that have been studied to date. These bacteria induce an array of reproductive isolation mechanisms that are implicated in pest management to evolutionary biology of respective hosts. The uzifly, Exorista sorbillans, a tachinid endoparasitoid of the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae), causes enormous losses to the silk industry; now it is known that it harbours Wolbachia endobacteria. The elimination of Wolbachia by antibiotics interrupts embryogenesis and causes various reproductive conflicts such as (1) a reduction of fecundity of uninfected female, (2) cytoplasmic incompatibility in the uninfected females crossed with infected males, (3) genomic incompatibility in crosses between males and females from uninfected population, and (4) sex-ratio distortion in uninfected females irrespective of the presence of Wolbachia in males. These results suggest that the relationship of Wolbachia with its uzifly host is one of mutual symbiosis as it controls the reproductive physiology of its host.     

Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences

Abstract.— Until now, only two Wolbachia-mediated cytoplasmic incompatibility (CI) types have been described in haplodiploid species, the first in Nasonia (Insect) and the second in Tetranychus (Acari). They both induce a malebiased sex ratio in the incompatible cross. In Nasonia, CI does not reduce fertility since incompatible eggs develop as haploid males, whereas in Tetranychus CI leads to a partial mortality of incompatible eggs, thus reducing the fertility of females. Here, we study Wolbachia infection in a Drosophila parasitoid, Leptopilina heterotoma (Hymenoptera: Figitidae). A survey of Wolbachia infection shows that all natural populations tested are totally infected. Crosses between infected males and cured females show complete incompatibility: almost no females are produced. Moreover, incompatible eggs die early during their development, unlike Nasonia. This early death allows the parasitized Drosophila larva to achieve its development and to emerge. Thus, uninfected females crossed with infected males have reduced offspring production consisting only of males. Evidence of this CI type in insects demonstrates that the difference in CI types of Nasonia and Tetranychus is not due to specific factors of insects or acari. Using theoretical models, we compare the invasion processes of different strategies of Wolbachia: CI in diploid species, the two CI types in haplodiploid species, and parthenogenesis (the classical effect in haplodiploid species). Models show that CI in haplodiploid species is less efficient than in diploid ones. However, the Leptopilina type is advantageous compared to the Nasonia type. Parthenogenesis may be more or less advantageous, depending on the infection cost and on the proportion of fertilized eggs. Finally, we can propose different processes of Wolbachia strategy evolution in haplodiploid species from Nasonia CI type to Leptopilina CI type or parthenogenesis.