Journal Article Ahead of print
PubMed: 41802010 DOI: 10.1371/journal.ppat.1014034
Mutualism in disguise: A mosquito parasite with mixed transmission mode displays mutualistic traits promoting oogenesis.
PLoS Pathog 22(3):e1014034
Authors: Maxime Girard, Mathieu Laÿs, Edwige Martin, Laurent Vallon, An-Nah Chanfi, Mélanie Bretton, Aurélien Vigneron, Séverine Balmand, Patricia Luis, Anne-Emmanuelle Hay, Claire Valiente Moro, Guillaume Minard
Affiliations
- Universite Claude Bernard Lyon 1, Laboratoire d'Ecologie Microbienne, UMR CNRS 5557, UMR INRAE 1418, VetAgro Sup, Villeurbanne, France.
- INSA Lyon, INRAE, BF2I, UMR 203, Villeurbanne, France.
Abstract
Mutualistic traits are frequently associated with vertically transmitted symbionts, in part because repeated interactions can align host and symbiont fitness. However, how such traits emerge in symbionts combining vertical and horizontal transmission remains unclear. Here we show that Ascogregarina taiwanensis, previously described as a weak horizontally transmitted parasite of the Asian tiger mosquito (Aedes albopictus), also displays mutualistic traits that enhance mosquito reproduction. Infected females show improved embryogenesis and an extended egg-laying period, while most pseudo-vertically transmit oocysts to their progeny at oviposition sites. This interaction ultimately produces larger larvae that are more frequently infected by As. taiwanensis. Dual transcriptomic analyses further reveal that early oogenesis in infected females involves increased nitrogen metabolism in both partners, enhanced detoxification of blood waste, and activation of egg development pathways. These changes improve assimilation of blood proteins essential for egg production. Together, our results illustrate how physiological coupling during reproduction, combined with mother-biased transmission, can generate mutualistic traits within an interaction that also retains parasitic features, blurring the boundary between parasitism and mutualism.
MeSH
Reproduction, Blood, Ovum, Oogenesis, Parasites