The shutting down of the insulin pathway: a developmental window for Wolbachia load and feminization

Benjamin Herran,Sandrine Geniez,Barton Slatko,Jérôme Lesobre,Maryline Raimond,Carine Delaunay,Joanne Bertaux,Pierre Grève

doi:10.1038/s41598-020-67428-1

Abstract

Using the isopod Armadillidium vulgare as a case study, we review the significance of the "bacterial dosage model", which connects the expression of the extended phenotype to the rise of the Wolbachia load. In isopods, the Insulin-like Androgenic Gland hormone (IAG) induces male differentiation: Wolbachia feminizes males through insulin resistance, presumably through defunct insulin receptors. This should prevent an autocrine development of the androgenic glands so that females differentiate instead: feminization should translate as IAG silencing and increased Wolbachia load in the same developmental window. In line with the autocrine model, uninfected males expressed IAG from the first larval stage on, long before the androgenic gland primordia begin to differentiate, and exponentially throughout development. In contrast in infected males, expression fully stopped at stage 4 (juvenile), when male differentiation begins. This co-occurred with the only significant rise in the Wolbachia load throughout the life-stages. Concurrently, the raw expression of the bacterial Secretion Systems co-increased, but they were not over-expressed relative to the number of bacteria. The isopod model leads to formulate the "bacterial dosage model" throughout extended phenotypes as the conjunction between bacterial load as the mode of action, timing of multiplication (pre/post-zygotic), and site of action (soma vs. germen).

Highlights

Using the isopod Armadillidium vulgare as a case study, we review the significance of the "bacterial dosage model", which connects the expression of the extended phenotype to the rise of the Wolbachia load
Inter-individual variability was likely inflated by fluctuations of the Wolbachia load during the reproductive cycle, for example when Wolbachia accumulates in the ovaries: more oocytes get infected as ovaries mature[38]
The only effective increase in the bacterial load coincided with the time of sexual differentiation: in isopods, the gonads start to differentiate at stage 4, at stage 5 the external sex characters begin to appear in m ales[36]

Summary

Introduction

Using the isopod Armadillidium vulgare as a case study, we review the significance of the "bacterial dosage model", which connects the expression of the extended phenotype to the rise of the Wolbachia load. Wolbachia are likely the most widespread endosymbionts on Earth, infecting arthropods such as insects, mites, spiders and crustaceans, and parasitic n ematodes[1] These maternally transmitted endosymbionts proliferate by manipulating the reproduction of their host through four main extended phenotypes (male-killing, parthenogenesis, Cytoplasmic Incompatibility (CI), feminization) or by developing an obligate interaction with their partner[2,3]. In Muscidifurax uniraptor, the Wolbachia-induced production of diploid females through parthenogenesis is altered in a dose-dependent manner by rifampicin treatments of the mothers, that result in a decrease of the bacterial load: the higher the dose of rifampicin, the higher the proportion of haploid males[15] And in both cases, the proper execution of the extended phenotypes is conditioned by the bacterial load at a pre-zygotic level, as depleting the generation N-1 hampers their expression. Bacterial titres increase dramatically between the first and the fifth instar stages, correlatively to the essential role of Wolbachia for embryonic d evelopment[22]

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Results

Conclusion