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R Stouthamer

Publications and source records attributed to R Stouthamer.

18 recordsLinked to original sources

Genetics of female functional virginity in the parthenogenesis-Wolbachia infected parasitoid wasp Telenomus nawai (Hymenoptera: Scelionidae).

A lepidopteran egg parasitoid species Telenomus nawai consists of two distinct populations with different reproductive modes. One is a completely thelytokous population consisting of females only, whereas the other displays arrhenotokous reproduction where fertilized eggs develop into diploid females and unfertilized eggs into haploid males. Thelytoky in T. nawai is caused by a bacterial symbiont, the parthenogenesis-inducing (PI) Wolbachia. Recent theoretical studies have shown that when a PI-Wolbachia is spreading in a population, mutations that allow uninfected females to produce more male offspring will spread rapidly eventually becoming fixed. The consequence of such a mutation is that sexual reproduction is no longer successful in infected females. Here we determine the genetic basis of the females' inability to reproduce sexually by introgressing the genome of a thelytokous line into an arrhenotokous line. The results suggest that the mutations are recessive and inherited either as a single-locus major gene with some modifiers, or as two partially linked loci.

Animals↗

Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps.

The intracellular bacterium Wolbachia is one of the most common symbionts in arthropods and, because of its manipulative effects on host reproduction, is assumed to be an important factor in several evolutionary processes. These bacteria are mainly vertically transmitted from mother to daughter through the egg cytoplasm, and horizontal transmission is generally assumed to be rare. Here, we show natural inter- and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia between parasitoid wasps of the genus Trichogramma. Horizontal transfer was observed when infected and uninfected larvae shared the same host egg. This is the first report, to our knowledge, on interspecific horizontal transfer of Wolbachia between closely related sympatric species. Some originally uninfected immature wasps acquired Wolbachia while inside the host egg, but not all of these newly infected females exhibited the parthenogenesis phenotype. In general, intraspecific horizontal transfer was more successful than interspecific transfer. Wolbachia underwent vertical transmission in the new species but the infection tended to be lost within several generations. Our results have important implications for understanding the evolution of Wolbachia-host associations.

Animals↗

Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae.

In Hymenoptera, complete parthenogenesis, that is thelytoky, is a common phenomenon where virgin females produce only daughters. Thelytoky is often induced by bacteria of the genus Wolbachia, but can also be genetically determined by the insect itself, as in the genus Trichogramma where both forms exist. In order to compare these two forms of thelytoky, chromosome behaviour analysis in young eggs and genetic analysis of microsatellite markers were carried out in the wasp Trichogramma cacoeciae, where thelytoky is genetically determined. Microscopic studies revealed that during female gamete formation meiotic cells undergo only a single equational division followed by the expulsion of a single polar body. This absence of meiotic recombination and reduction corresponds well with the high levels of heterozygosity observed in females collected from the field and a nonsegregation pattern in the offspring of heterozygous females. We therefore concluded that diploidy in T. cacoeciae is maintained through an apomictic cloning mechanism and that the incidence of thelytoky under genetic control of the wasp differs entirely from the mechanism induced by Wolbachia infection, where thelytoky is restored through gamete duplication.

Animals↗

Diversity, distribution and specificity of WO phage infection in Wolbachia of four insect species.

The bacteriophage WO was recently characterized in Wolbachia, a strictly intracellular bacterium that causes several reproductive alterations in its arthropod hosts. To gain insights into the phage-Wolbachia relationships, we studied the phage presence among Wolbachia infecting four insect species sharing several Wolbachia strains, two Drosophila and two of their parasitoid wasps. Based on the phage sequence of ORF7, we identified five different phages in six Wolbachia strains. Among these five bacteriophages, some are specific for a given bacterial strain whereas others are not, but globally phage infection appears stable on a large geographical scale and across insect generations. Their specificity contrasts with the absence of congruence between Wolbachia and phage phylogenies, suggesting phage exchanges between different Wolbachia lineages.

Animals↗

Selfish element maintains sex in natural populations of a parasitoid wasp.

Genomic conflicts between heritable elements with different modes of inheritance are important in the maintenance of sex and in the evolution of sex ratio. Generally, we expect sexual populations to exhibit a 1:1 sex ratio. However, because of their biology, parasitoid wasps often exhibit a female-biased sex ratio. Sex-ratio distorters can further alter this optimum, sometimes leading to the complete loss of sexual reproduction. In the parasitoid wasp Trichogramma kaykai ca. 4-26% of females in field populations are infected with a bacterial sex-ratio distorter, Wolbachia, allowing virgin mothers to produce daughters. In some micro-Hymenoptera these infections have led to the complete loss of sex, but in field populations of T. kaykai the proportion of individuals infected remains relatively stable. We tested several hypotheses to explain this low infection level, including inefficient and horizontal transmission of Wolbachia, suppressor genes negating the effect of Wolbachia and the presence of male-biasing sex-ratio distorters. Here, a male-biasing sex-ratio distorter, a parasitic B chromosome, causing females to produce only sons, keeps the frequency of Wolbachia low. The male-biasing factor of T. kaykai is the second known case of a B chromosome manipulating the reproduction of a parasitoid wasp.

Animals↗

How does infection with parthenogenesis-inducing Wolbachia reduce the fitness of Trichogramma?

We analyzed the survival rate of the immature stages of Trichogramma species and lines that differed in their mode of reproduction. Specifically, we compared the mortality of arrhenotokous (W(-)), irrevertable thelytokous (W(-)), and Wolbachia-associated thelytokous (W(+)) forms. The embryonic mortality of the W(+) strains was significantly higher than that of the W(-) lines. The embryonic mortality was negligible for the arrhenotokous Trichogramma evanescens and the thelytokous Trichogramma cacoeciae, which is not infected with Wolbachia. Only 30% of the eggs of the Wolbachia-infected strains developed to adults, while the emergence rate of the Wolbachia-free strains was more than 78%, irrespective of the origin of the strains. More than 78% of the overall mortality in W(+) strains happened during the early stages of development. About 35% of embryos of W(+) strains remain in the mitotic stage even 48 h after oviposition. Most embryos of W(-) strains had already developed to cellular blastoderm after 6 h, regardless of strains. The mortality of immature stages in W(+) strains was mainly caused by the failure of the mitotic divisions.

Animals↗

Infectious parthenogenesis.

Parthenogenesis-inducing Wolbachia bacteria are reproductive parasites that cause infected female wasps to produce daughters without mating. This manipulation of the host's reproduction enhances the transmission of Wolbachia to future generations because the bacteria are passed on vertically only from mothers to daughters. Males are dead ends for cytoplasmically inherited bacteria: they do not pass them on to their offspring. Vertical transmission of Wolbachia has been previously considered to be the main mode of transmission. Here we report frequent horizontal transmission from infected to uninfected wasp larvae sharing a common food source. The transferred Wolbachia are then vertically transmitted to the new host's offspring. This natural and unexpectedly frequent horizontal transfer of parthenogensis-inducing Wolbachia intraspecifically has important implications for the co-evolution of Wolbachia and their host.

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Cross-order transfer of Wolbachia from Muscidifurax uniraptor (Hymenoptera: Pteromalidae) to Drosophila simulans (Diptera: Drosophilidae).

Bacteria of the genus Wolbachia are widespread in arthropods and can induce different effects on the host such as cytoplasmic incompatibility (CI), thelytoky (T) or feminization (F). In some Wolbachia-infected hosts, no effect (N) has been found. Successful transfer of Wolbachia by microinjection from one host to an uninfected one has been established with CI, F, N-Wolbachia but not with T-Wolbachia. In this paper a transfer experiment of T-Wolbachia from the parasitoid Muscidifurax uniraptor to Drosophila simulans is described. The infection could be detected in the new host for several generations by polymerase chain reaction (PCR). However, no specific effects on the host were detected, and the bacteria were not stably maintained.

Alphaproteobacteria↗

Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria.

Male-killing bacteria, which are inherited through the female line and kill male progeny only, are known from five different orders of insect. Our knowledge of the incidence of these elements has stemmed from discovery of their phenotype in different species. Our estimate of the frequency with which insects have been invaded by these elements therefore depends on each observation of the male-killing phenotype within a species being associated with a single microorganism. We here record an example of a single insect species being infected with two taxonomically distinct male-killing bacteria. Western European populations of the two-spot ladybird, Adalia bipunctata, have previously been shown to bear a male-killing Rickettsia. However, we here show that the majority of the male-killing lines tested from Central and Eastern Europe do not bear this bacterium. Rather, 16S rDNA sequence analysis suggests male-killing is associated with a member of the genus Spiroplasma. We discuss this conclusion in relation to the evolutionary genetics of male-killing bacteria, and the evolution of male-killing behaviour in the eubacteria.

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Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene.

Bacteria of the genus Wolbachia (Rickettsiae) are widespread in arthropods and can induce cytoplasmic incompatibility (CI), thelytoky (T) or feminization (F) in their host. Recent research on the wsp gene of mainly CI inducing Wolbachia has shown that this gene evolves at a much faster rate than previously sequenced genes such as 16S or ftsZ. As a result this gene appears to be very useful in subdividing the Wolbachia and twelve groups have been distinguished to date. Here we extend the Wolbachia wsp data set with fifteen T-Wolbachia, one F-Wolbachia and three other CI-Wolbachia strains. The results showed: (i) the addition of seven groups; (ii) no relation between host phenotype and Wolbachia phylogenetic position; and (iii) possible horizontal Wolbachia transfer between the moth Ephestia kuehniella and its parasitoid Trichogramma spp.

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Spacer 2 region and 5S rDNA variation of Wolbachia strains involved in cytoplasmic incompatibility or sex-ratio distortion in arthropods.

Bacteria in the genus Wolbachia are widespread in arthropods and can induce sex-ratio distortion or cytoplasmic incompatibility in their hosts. The phylogeny of Wolbachia has been studied using 16S rDNA and the cell cycle gene ftsZ, but sequence variation of those genes is limited. The spacer 2 region (SR2) was amplified to determine whether this region would improve phylogenetic resolution. The SR2 of Wolbachia is 66 bp long, shows higher variation than ftsZ and has very low homology with closely related bacteria. Due to the small length of SR2 of Wolbachia, little phylogenetic information could be retrieved.

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Wolbachia pipientis: microbial manipulator of arthropod reproduction.

The alpha-proteobacterium Wolbachia pipientis is a very common cytoplasmic symbiont of insects, crustaceans, mites, and filarial nematodes. To enhance its transmission, W. pipientis has evolved a large scale of host manipulations: parthenogenesis induction, feminization, and male killing. W. pipientis's most common effect is a crossing incompatibility between infected males and uninfected females. Little is known about the genetics and biochemistry of these symbionts because of their fastidious requirements. The affinity of W. pipientis for the microtubules associated with the early divisions in eggs may explain some of their effects. Such inherited microorganisms are thought to have been major factors in the evolution of sex determination, eusociality, and speciation. W. pipientis isolates are also of interest as vectors for the modification of wild insect populations, in the improvement of parasitoid wasps in biological pest control, and as a new method for interfering with diseases caused by filarial nematodes.

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Microtubule organization during the early development of the parthenogenetic egg of the hymenopteran Muscidifurax uniraptor.

The origin of the zygotic centrosome is an important step in developmental biology. It is generally thought that sperm at fertilization plays a central role in forming the functional centrosome which subsequently organizes the first mitotic spindle. However, this view is not applicable in the case of parthenogenetic eggs which develop without the sperm contribution. To clarify the problem of the origin of the zygotic centrosome during parthenogenetic development, we studied a hymenopteran, Muscidifurax uniraptor. Antitubulin antibody revealed that after activation several asters assembled in the egg cytoplasm. The number of asters varied in relation to the cell cycle. They became visible from anaphase of the first meiotic division and increased in number as meiosis progressed, reaching a maximum at the first mitosis. From anaphase-telophase of the first mitosis they decreased in number and were no longer found during the third mitotic division. To elucidate the nature of these asters we performed an ultrastructural study with transmission electron microscopy and immunofluorescence with antibodies against anti-gamma-tubulin and CP190. In this way we showed the presence in these asters of centrosomal components and centrioles. Our observations suggest that the cytoplasm of Muscidifurax eggs contains a pool of inactive centrosomal precursor proteins becoming able to nucleate microtubules into well-defined asters containing centrioles after activation.

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Horizontal transmission of parthenogenesis-inducing microbes in Trichogramma wasps.

Complete parthenogenesis (thelytoky) in species of the parasitic wasp Trichogramma is usually caused by the cytoplasmically inherited bacterium Wolbachia. This symbiont induces gamete duplication, which, in these haplodiploid organisms, results in all-female broods. Antibiotic treatment "cures' this condition, restoring normal sexual reproduction. Phylogenetic analysis of Wolbachia has shown that, in contrast with the strains in other host organisms (where the symbiont also induces different reproductive alterations), those in Trichogramma form a monophyletic group. This might be an indication of symbiont-host cocladogenesis. To test this, we performed comparative molecular phylogenetics on 20 parthenogenetic Trichogramma cultures and their Wolbachiae. We conclude that there is, in fact, little evidence for cocladogenesis. Instead, the phylogenetic distribution of the symbionts appears to result from occasional horizontal transmission, which probably takes place inside the hosts of Trichogramma parasitoids (usually lepidopteran eggs). This study therefore suggests that parthenogenesis is not only curable, it can sometimes be contagious also.

Alphaproteobacteria↗

Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata).

A cytoplasmically inherited microorganism associated with male killing in the two-spot ladybird beetle, Adalia bipunctata, is shown to be closely related to bacteria in the genus Rickettsia. Sequencing of a PCR-amplified product of the 16S genes coding for rRNA (16S rDNA) shows the organism associated with male killing in ladybirds to share a common ancestry with the Rickettsias relative to other genera (e.g., Anaplasma, Ehrlichia, and Cowdria). The rickettsial 16S rDNA product is found in four strains of ladybird beetle showing male embryo lethality and is absent from two uninfected strains and an antibiotic-cured strain. In addition, a revertant strain that had naturally lost the male-killing trait failed to amplify the rickettsial 16S rDNA product. Use of PCR primers for a 17-kDa protein antigen which is found only in rickettsias also resulted in an amplified product from infected strains. Uninfected, cured, and revertant strains and insect species infected with related bacteria (cytoplasmic-incompatibility bacteria from Nasonia wasps) failed to amplify the product. Discovery of a close relative of rickettsias associated with sex ratio distortion in insects has implications for the evolution and population dynamics of this bacterial genus.

Animals↗

Molecular identification of microorganisms associated with parthenogenesis.

Cytoplasmically interited microorganisms are widespread in insects and have been implicated as causes of female parthenogenesis (females developing from unfertilized eggs) and cytoplasmic incompatibility. Normal sexual reproduction can be restored by treatment with antibiotics. Sequence analysis of the DNA encoding 16S ribosomal RNA has shown that cytoplasmic incompatibility bacteria from diverse insect taxa are closely related (they share >95% sequence sililarity) and belong to the alpha subdivision of Proteobacteria. Here we show that parthenogenesis-associated bacteria from parasitoid Hymenoptera also fall into this bacterial group, having up to 99% sequence similarity to some incompatibility microorganisms. Both incompatibility and parthenogenesis microorganisms alter host chromosome behaviour during early mitotic divisions of the egg. Incompatibility bacteria act by interfering with paternal chromosome incorporation in fertilized eggs, whereas parthenogenesis bacteria prevent segregation of chromosomes in unfertilized eggs. These traits are adaptive for the microorganisms. On the basis of their sequence similarities, we conclude that parthenogenesis bacteria and cytoplasmic incompatibility bacteria form a monophyletic group of microorganisms that 'specialize' in manipulating chromosome behaviour and reproduction of insects.

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Phylogeny of cytoplasmic incompatibility micro-organisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences.

Cytoplasmic incompatibility results in embryo mortality in diploids, or all male offspring in haplodiploids, when individuals carrying different cytoplasmic factors are crossed. Cytoplasmic factors have been identified as intracellular micro-organisms. Microbe-induced cytoplasmic incompatibility is found in many insect taxa and may play a role in reproductive isolation between populations. Such micro-organisms cause bidirectional incompatibility between species of the parasitoid wasp genus Nasonia. The phylogenetic relationship of cytoplasmic incompatibility microorganisms (CIM) of different Nasonia species was analysed using their 16S ribosomal DNA (rDNA) sequence. Two 16S rDNA operons were detected in the CIM of each Nasonia species. Sequence analysis indicates that the Nasonia CIM are closely related and belong to the alpha group of the Proteobacteria.

Animals↗

Antibiotics cause parthenogenetic Trichogramma (Hymenoptera/Trichogrammatidae) to revert to sex.

Completely parthenogenetic Trichogramma wasps can be rendered permanently bisexual by treatment with three different antibiotics or high temperatures. The evidence strongly suggests that maternally inherited microorganisms cause parthenogenesis in these wasps. Theories predict female-biased sex ratio in offspring under the influence of maternally inherited symbionts, but extreme sex ratios of 100% females were never considered because the lack of males would prevent the host's reproduction.

Journal Article↗