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Effects of Wolbachia infection and ovarian tumor mutations on Sex-lethal germline functioning in Drosophila.

ABSTRACT: Wolbachia is a ubiquitous intracellular endosymbiont of invertebrates. Surprisingly, infection of Drosophila melanogaster by this maternally inherited bacterium restores fertility to females carrying ovarian tumor (cystocyte overproliferation) mutant alleles of the Drosophila master sex-determination gene, Sex-lethal (Sxl). We scanned the Drosophila genome for effects of infection on transcript levels in wild-type previtellogenic ovaries that might be relevant to this suppression of female-sterile Sxl mutants by Wolbachia. Yolk protein gene transcript levels were most affected, being reduced by infection, but no genes showed significantly more than a twofold difference. The yolk gene effect likely signals a small, infection-induced delay in egg chamber maturation unrelated to suppression. In a genetic study of the Wolbachia-Sxl interaction, we established that germline Sxl controls meiotic recombination as well as cystocyte proliferation, but Wolbachia only influences the cystocyte function. In contrast, we found that mutations in ovarian tumor (otu) interfere with both Sxl germline functions. We were led to otu through characterization of a spontaneous dominant suppressor of the Wolbachia-Sxl interaction, which proved to be an otu mutation. Clearly Sxl and otu work together in the female germline. These studies of meiosis in Sxl mutant females revealed that X chromosome recombination is considerably more sensitive than autosomal recombination to reduced Sxl activity.

SUBMITTER: Sun S

PROVIDER: S-EPMC2666500 | biostudies-literature | 2009 Apr

REPOSITORIES: biostudies-literature

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Effects of Wolbachia infection and ovarian tumor mutations on Sex-lethal germline functioning in Drosophila.

Sun Sha S Cline Thomas W TW

Genetics 20090126 4

Wolbachia is a ubiquitous intracellular endosymbiont of invertebrates. Surprisingly, infection of Drosophila melanogaster by this maternally inherited bacterium restores fertility to females carrying ovarian tumor (cystocyte overproliferation) mutant alleles of the Drosophila master sex-determination gene, Sex-lethal (Sxl). We scanned the Drosophila genome for effects of infection on transcript levels in wild-type previtellogenic ovaries that might be relevant to this suppression of female-steri ...[more]

PMID: 19171941

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Project description:Reinforcement refers to the evolution of increased mating discrimination against heterospecific individuals in zones of geographic overlap and can be considered a final stage in the speciation process. One the factors that may affect reinforcement is the degree to which hybrid matings result in the permanent loss of genes from a species' gene pool. Matings between females of Drosophila subquinaria and males of D. recens result in high levels of offspring mortality, due to interspecific cytoplasmic incompatibility caused by Wolbachia infection of D. recens. Such hybrid inviability is not manifested in matings between D. recens females and D. subquinaria males. Here we ask whether the asymmetrical hybrid inviability is associated with a corresponding asymmetry in the level of reinforcement. The geographic ranges of D. recens and D. subquinaria were found to overlap across a broad belt of boreal forest in central Canada. Females of D. subquinaria from the zone of sympatry exhibit much stronger levels of discrimination against males of D. recens than do females from allopatric populations. In contrast, such reproductive character displacement is not evident in D. recens, consistent with the expected effects of unidirectional cytoplasmic incompatibility. Furthermore, there is substantial behavioral isolation within D. subquinaria, because females from populations sympatric with D. recens discriminate against allopatric conspecific males, whereas females from populations allopatric with D. recens show no discrimination against any conspecific males. Patterns of general genetic differentiation among populations are not consistent with patterns of behavioral discrimination, which suggests that the behavioral isolation within D. subquinaria results from selection against mating with Wolbachia-infected D. recens. Interspecific cytoplasmic incompatibility may contribute not only to post-mating isolation, an effect already widely recognized, but also to reinforcement, particularly in the uninfected species. The resulting reproductive character displacement not only increases behavioral isolation from the Wolbachia-infected species, but may also lead to behavioral isolation between populations of the uninfected species. Given the widespread occurrence of Wolbachia among insects, it thus appears that there are multiple ways by which these endosymbionts may directly and indirectly contribute to reproductive isolation and speciation.

Project description:BACKGROUND: Sex determining mechanisms are evolutionarily labile and related species often use different primary signals and gene regulatory networks. This is well illustrated by the sex determining cascade of Drosophila fruitflies, which have recruited Sex-lethal as the master switch and cellular memory of sexual identity, a role performed in other insects by the gene transformer. Here we investigate the evolutionary change in the coding sequences of sex determining genes associated with the recruitment of Sex-lethal. We analyze sequences of Sex-lethal itself, its Drosophila paralogue sister-or-Sex-lethal and downstream targets transformer and doublesex. RESULTS: We find that the recruitment of sister-or-Sex-lethal was associated with a number of adaptive amino acid substitutions, followed by a tightening of purifying selection within the Drosophila clade. Sequences of the paralogue sister-or-Sex-lethal, in contrast, show a signature of rampant positive selection and relaxation of purifying selection. The recruitment of Sex-lethal as top regulator and memory gene is associated with a significant release from purifying selection in transformer throughout the Drosophila clade. In addition, doublesex shows a signature of positive selection and relaxation of purifying selection in the Drosophila clade. A similar pattern is seen in sequences from the sister Tephritidae clade. CONCLUSIONS: The pattern of molecular evolution we observe for Sex-lethal and its paralogue sister-or-Sex-lethal is not characteristic of a duplication followed by neo-functionalization. Rather, evidence suggests a sub-functionalization scenario achieved through the evolution of sophisticated splicing. As expected, we find that transformer evolves under relaxed purifying selection after the recruitment of Sex-lethal in Drosophila. Finally, the observation of doublesex adaptation in both Drosophila and Tephritidae suggests that these changes are due to ongoing adaptation of downstream sex-specific regulation, rather than being associated the recruitment of Sex-lethal and the resulting change in the topology of the sex determining cascade.

Dataset Information

Effects of Wolbachia infection and ovarian tumor mutations on Sex-lethal germline functioning in Drosophila.

Publications

Effects of Wolbachia infection and ovarian tumor mutations on Sex-lethal germline functioning in Drosophila.

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