# Mutualism in disguise: A mosquito parasite with mixed transmission mode displays mutualistic traits promoting oogenesis

## TL;DR

A mosquito parasite boosts host reproduction while spreading to offspring, showing traits of both mutualism and parasitism.

## Contribution

Reveals how a horizontally and pseudo-vertically transmitted parasite can develop mutualistic traits during reproduction.

## Key findings

- Infected mosquitoes produce larger eggs and larvae, with extended egg-laying periods.
- Parasite transmission is biased toward offspring via oocysts released at oviposition sites.
- Transcriptomic analysis shows enhanced nitrogen metabolism and blood waste detoxification in infected females.

## 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.

Mosquitoes host a wide diversity of microorganisms that can profoundly influence their biology, and their effects on mosquito physiology and reproduction are often more complex than expected. In this study, we examined the interaction between the Asian tiger mosquito Aedes albopictus, a major invasive disease vector, and its common gregarine parasite Ascogregarina taiwanensis. We show that this parasite spreads in two ways: unrelated interindividual transmission can occur through breeding sites, but its transmission is also biased toward the offspring of infected females because parasites are released into the water at egg-laying sites. Rather than acting solely as a cost to the host, infection was associated with changes in reproductive physiology: parasitized females produced larger eggs, laid them over a longer period, and gave rise to larger larvae, despite ingesting similar amounts of blood as uninfected females. Transcriptomic and physiological analyses indicate that these effects are linked to enhanced processing of blood-derived nutrients, particularly nitrogen, during oogenesis. These findings suggest that physiological responses to infection during reproduction can generate host benefits that also favor parasite transmission, illustrating how mutualistic traits may emerge as by-products of adaptation within predominantly parasitic interactions.