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Feminising Wolbachia disrupt Armadillidium vulgare insulin-like signalling pathway
Benjamin Herran1, Camille Houdelet1, Maryline Raimond1
1UMR CNRS 7267 Écologie et Biologie des Interactions, Université de Poitiers, Poitiers, France.
Abstract:
The endosymbiont Wolbachia feminises male isopods by making them refractory to the insulin-like masculinising hormone, which shunts the autocrine development of the androgenic glands. It was, therefore, proposed that Wolbachia silences the IR receptors, either by preventing their expression or by inactivating them. We describe here the two IR paralogs of Armadillidium vulgare. They displayed a conventional structure and belonged to a family widespread among isopods. Av-IR1 displayed an ubiquist expression, whereas the expression of Av-IR2 was restricted to the gonads. Both were constitutively expressed in males and females and throughout development. However, upon silencing, altered gland physiology and gene expression therein suggested antagonistic roles for Av-IR1 (androinhibiting) and Av-IR2 (androstimulating). They may function in tandem with regulating neurohormones, as a conditional platform that conveys insulin signalling. Wolbachia infection did not alter their expression patterns: leaving the IRs unscathed, the bacteria would suppress the secretion of the neurohormones, thus inducing body-wide IR deactivation and feminisation. Adult males injected with Wolbachia acquired an intersexed physiology. Their phenotypes and gene expressions mirrored the silencing of Av-IR1 only, suggesting that imperfect feminisation stems from a flawed invasion of the androstimulating centre, whereas in fully feminised males invasion would be complete in early juveniles. TAKE AWAY: Two antagonistic Insulin Receptors were characterised in Armadillidium vulgare. The IRs were involved in androstimulating and androinhibiting functions. Wolbachia-induced feminisation did not prevent the expression of the IRs. Imperfectly feminised intersexes phenocopied the silencing of Av-IR1 only. Wolbachia would deactivate the IRs by suppressing neurosecretory co-factors.
Insights
The endosymbiont Wolbachia feminizes male isopods by altering insulin signaling. Two antagonistic insulin receptors (IRs) were identified, with Wolbachia suppressing neurohormones to deactivate IRs and induce feminization.
Area of Science:
- Endocrinology
- Molecular Biology
- Reproductive Biology
Background:
- Wolbachia endosymbionts are known to feminize male isopods.
- This feminization is hypothesized to involve the silencing of insulin receptors (IRs).
- The specific mechanisms by which Wolbachia affects IRs and masculinization remain unclear.
Purpose of the Study:
- To characterize the insulin receptor (IR) paralogs in the isopod Armadillidium vulgare.
- To investigate the roles of these IR paralogs in sexual development and hormone signaling.
- To elucidate the mechanism by which Wolbachia induces feminization in male isopods.
Main Methods:
- Identification and structural analysis of two IR paralogs (Av-IR1 and Av-IR2) in Armadillidium vulgare.
- Analysis of IR expression patterns in males and females throughout development.
- Functional characterization of IRs through silencing experiments and observation of effects on androgenic gland physiology and gene expression.
- Experimental injection of adult males with Wolbachia to observe phenotypic and gene expression changes.
Main Results:
- Two IR paralogs, Av-IR1 and Av-IR2, were identified with conventional structures and widespread family distribution.
- Av-IR1 showed ubiquitous expression, while Av-IR2 expression was restricted to the gonads; both were constitutively expressed in both sexes.
- Silencing experiments revealed antagonistic roles: Av-IR1 is androinhibiting, and Av-IR2 is androstimulating, potentially regulating neurohormones and insulin signaling.
- Wolbachia infection did not alter IR expression but suppressed neurohormone secretion, leading to body-wide IR deactivation and feminization.
- Adult males injected with Wolbachia exhibited intersex physiology, mirroring Av-IR1 silencing, suggesting incomplete feminization results from flawed invasion of the androstimulating center.
Conclusions:
- Two antagonistic insulin receptors (IRs) with distinct roles in sexual physiology were characterized in Armadillidium vulgare.
- Wolbachia-induced feminization operates by suppressing neurosecretory co-factors, leading to IR deactivation, rather than by altering IR expression.
- The degree of feminization correlates with the completeness of Wolbachia invasion, impacting the androstimulating center and leading to varied intersex phenotypes.
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