Abstract

BackgroundThe life cycles of many insect species include an obligatory or facultative diapause stage with arrested development and low metabolic activity as an overwintering strategy. Diapause is characterised by profound physiological changes in endocrine activity, cell proliferation and nutrient metabolism. However, little is known regarding host-microbiome interactions during diapause, despite the importance of bacterial symbionts for host nutrition and development. In this work, we investigated (i) the role of the microbiome for host nutrient allocation during diapause and (ii) the impact of larval diapause on microbiome dynamics in the parasitoid wasp Nasonia vitripennis, a model organism for host-microbiome interactions.ResultsOur results demonstrate that the microbiome is essential for host nutrient allocation during diapause in N. vitripennis, as axenic diapausing larvae had consistently lower glucose and glycerol levels than conventional diapausing larvae, especially when exposed to cold temperature. In turn, microbiome composition was altered in diapausing larvae, potentially due to changes in the surrounding temperature, host nutrient levels and a downregulation of host immune genes. Importantly, prolonged larval diapause had a transstadial effect on the adult microbiome, with unknown consequences for host fitness. Notably, the most dominant microbiome member, Providencia sp., was drastically reduced in adults after more than 4 months of larval diapause, while potential bacterial pathogens increased in abundance.ConclusionThis work investigates host-microbiome interactions during a crucial developmental stage, which challenges both the insect host and its microbial associates. The impact of diapause on the microbiome is likely due to several factors, including altered host regulatory mechanisms and changes in the host environment.8eXiSqX1W-a7vPRfczqREZVideo .

Highlights

  • The life cycles of many insect species include an obligatory or facultative diapause stage with arrested development and low metabolic activity as an overwintering strategy

  • Larval diapause induction and termination in N. vitripennis As previously shown [44, 45], N. vitripennis females exposed to diapause-inducing conditions produced non-diapausing offspring in the first days of adult life before “switching” to the production of only diapause-destined offspring for the rest of their lifespan (Fig. 1)

  • All larvae were reared at 25°C for 7 days until the last larval instar. Both types of larvae have generally entirely ingested the fly host and stop feeding, as the non-diapausing larvae will soon pupate, and the diapause-destined larvae go into diapause

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Summary

Introduction

The life cycles of many insect species include an obligatory or facultative diapause stage with arrested development and low metabolic activity as an overwintering strategy. Despite an increased interest in the regulatory and physiological aspects of insect diapause [1, 5,6,7,8,9,10,11,12,13,14], the dynamics of host-microbiome interactions during diapause remain underexplored (but see [15,16,17,18]) This contrasts with a growing body of research on hibernating mammals, demonstrating a seasonal remodelling of the gut microbiome between the hibernating and active phases in various species [19,20,21,22]. The gut microbiota interacts with the JH and the IIS pathways, which are likely key hormonal regulators of diapause induction and metabolic remodelling in diverse insects [6, 9, 12, 13]

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