Abstract

Organisms with complex life cycles can differ markedly in their biology across developmental life stages. Consequently, distinct life stages can represent drastically different environments for parasites. This difference is especially striking with holometabolous insects, which have dramatically different larval and adult life stages, bridged by a complete metamorphosis. There is no a priori guarantee that a parasite infecting the larval stage would be able to persist into the adult stage. In fact, to our knowledge, transstadial transmission of extracellular pathogens has never been documented in a host that undergoes complete metamorphosis. We tested the hypothesis that a bacterial parasite originally sampled from an adult host could infect a larva, then survive through metamorphosis and persist into the adult stage. As a model, we infected the host Drosophila melanogaster with a horizontally transmitted, extracellular bacterial pathogen, Providencia rettgeri. We found that this natural pathogen survived systemic infection of larvae (L3) and successfully persisted into the adult host. We then discuss how it may be adaptive for bacteria to transverse life stages and even minimize virulence at the larval stage in order to benefit from adult dispersal.

Highlights

  • Organisms with complex life cycles can differ dramatically in their biology across developmental life stages

  • The transition between life stages may be challenging for the parasite and might serve as a block on parasite development and/or transmission. This could be relevant for extracellular parasites that are not transmitted vertically, yet to our knowledge, there has been no study investigating the possibility that a systemic infection by an extracellular, horizontally-transmitted pathogen can persist through metamorphosis, a phenomenon called transstadial transmission

  • Transstadial persistence of vertically transmitted intracellular (e.g. Wolbachia and microsporidian species) and extracellular (e.g. Spiroplasma species) bacteria has been described in holometabolous insects that undergo complete metamorphosis [3,4,5], but it is as yet untested whether the same phenomenon can occur in the context of horizontally acquired opportunistic infections

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Summary

Introduction

Organisms with complex life cycles can differ dramatically in their biology across developmental life stages. This could be relevant for extracellular parasites that are not transmitted vertically, yet to our knowledge, there has been no study investigating the possibility that a systemic infection by an extracellular, horizontally-transmitted pathogen can persist through metamorphosis, a phenomenon called transstadial transmission. Transstadial persistence of vertically transmitted intracellular (e.g. Wolbachia and microsporidian species) and extracellular (e.g. Spiroplasma species) bacteria has been described in holometabolous insects that undergo complete metamorphosis [3,4,5], but it is as yet untested whether the same phenomenon can occur in the context of horizontally acquired opportunistic infections.

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