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Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy.

ABSTRACT: Field populations of arthropods are often polymorphic for Wolbachia but the factors maintaining intermediate Wolbachia frequencies are generally not understood. In Drosophila melanogaster, Wolbachia frequencies are highly variable across the globe. We document the persistence of a Wolbachia infection frequency cline in D. melanogaster populations from eastern Australia across at least 20 years, with frequencies generally high in the tropics but lower in cool temperate regions. The results are interpreted using a model of frequency dynamics incorporating cytoplasmic incompatibility (CI), imperfect maternal transmission and Wolbachia effects on fitness. Clinal variation is less pronounced in eastern North America which may reflect annual recolonization at higher latitudes. Limited samples from Africa from latitudes matching our tropical and subtropical samples from Australia and North America show comparably high infection frequencies, but some equatorial samples show lower frequencies. Adult dormancy across cold periods may contribute to the Australian Wolbachia cline. Infected flies exposed to cold conditions for an extended period had reduced fecundity and viability, an effect not evident in unexposed controls. These fitness costs may contribute to the relatively low Wolbachia frequencies in Australian temperate areas; whereas different processes, including CI induced by young males, may contribute to higher frequencies in tropical locations.

SUBMITTER: Kriesner P

PROVIDER: S-EPMC4874875 | biostudies-literature | 2016 May

REPOSITORIES: biostudies-literature

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Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy.

Kriesner Peter P Conner William R WR Weeks Andrew R AR Turelli Michael M Hoffmann Ary A AA

Evolution; international journal of organic evolution 20160505 5

Field populations of arthropods are often polymorphic for Wolbachia but the factors maintaining intermediate Wolbachia frequencies are generally not understood. In Drosophila melanogaster, Wolbachia frequencies are highly variable across the globe. We document the persistence of a Wolbachia infection frequency cline in D. melanogaster populations from eastern Australia across at least 20 years, with frequencies generally high in the tropics but lower in cool temperate regions. The results are in ...[more]

PMID: 27076356

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Project description:In models extensively used in studies of aging and extended lifespan, such as C. elegans and Drosophila, adult senescence is regulated by gene networks that are likely to be similar to ones that underlie lifespan extension during dormancy. These include the evolutionarily conserved insulin/IGF, TOR and germ line-signaling pathways. Dormancy, also known as dauer stage in the larval worm or adult diapause in the fly, is triggered by adverse environmental conditions, and results in drastically extended lifespan with negligible senescence. It is furthermore characterized by increased stress resistance and somatic maintenance, developmental arrest and reallocated energy resources. In the fly Drosophila melanogaster adult reproductive diapause is additionally manifested in arrested ovary development, improved immune defense and altered metabolism. However, the molecular mechanisms behind this adaptive lifespan extension are not well understood.A genome wide analysis of transcript changes in diapausing D. melanogaster revealed a differential regulation of more than 4600 genes. Gene ontology (GO) and KEGG pathway analysis reveal that many of these genes are part of signaling pathways that regulate metabolism, stress responses, detoxification, immunity, protein synthesis and processes during aging. More specifically, gene readouts and detailed mapping of the pathways indicate downregulation of insulin-IGF (IIS), target of rapamycin (TOR) and MAP kinase signaling, whereas Toll-dependent immune signaling, Jun-N-terminal kinase (JNK) and Janus kinase/signal transducer and activator of transcription (JAK/STAT) pathways are upregulated during diapause. Furthermore, we detected transcriptional regulation of a large number of genes specifically associated with aging and longevity.We find that many affected genes and signal pathways are shared between dormancy, aging and lifespan extension, including IIS, TOR, JAK/STAT and JNK. A substantial fraction of the genes affected by diapause have also been found to alter their expression in response to starvation and cold exposure in D. melanogaster, and the pathways overlap those reported in GO analysis of other invertebrates in dormancy or even hibernating mammals. Our study, thus, shows that D. melanogaster is a genetically tractable model for dormancy in other organisms and effects of dormancy on aging and lifespan.

Project description:BackgroundWolbachia are bacterial endosymbionts of many arthropod species in which they manipulate reproductive functions. The distribution of these bacteria in the Drosophila ovarian cells at different stages of oogenesis has been amply described. The pathways along which Wolbachia influences Drosophila oogenesis have been, so far, little studied. It is known that Wolbachia are abundant in the somatic stem cell niche of the Drosophila germarium. A checkpoint, where programmed cell death, or apoptosis, can occur, is located in region 2a/2b of the germarium, which comprises niche cells. Here we address the question whether or not the presence of Wolbachia in germarium cells can affect the frequency of cyst apoptosis in the checkpoint.ResultsOur current fluorescent microscopic observations showed that the wMel and wMelPop strains had different effects on female germline cells of D. melanogaster. The Wolbachia strain wMel did not affect the frequency of apoptosis in cells of the germarium. The presence of the Wolbachia strain wMelPop in the D. melanogasterw1118 ovaries increased the number of germaria where cells underwent apoptosis in the checkpoint. Based on the appearance in the electron microscope, there was no difference in morphological features of apoptotic cystocytes between Wolbachia-infected and uninfected flies. Bacteria with normal ultrastructure and large numbers of degenerating bacteria were found in the dying cyst cells.ConclusionsOur current study demonstrated that the Wolbachia strain wMelPop affects the egg chamber formation in the D. melanogaster ovaries. This led to an increase in the number of germaria containing apoptotic cells. It is suggested that Wolbachia can adversely interfere either with the cystocyte differentiation into the oocyte or with the division of somatic stem cells giving rise to follicle cells and, as a consequence, to improper ratio of germline cells to follicle cells and, ultimately, to apoptosis of cysts. There was no similar adverse effect in D. melanogaster Canton S infected with the Wolbachia strain wMel. This was taken to mean that the observed increase in frequency of apoptosis was not the general effect of Wolbachia on germline cells of D. melanogaster, it was rather induced by the virulent Wolbachia strain wMelPop.

Dataset Information

Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy.

Publications

Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy.

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