Friend or foe: A mosquito parasite with mixed transmission mode displays mutualistic traits promoting oogenesis.

Abstract

Mutualism is often selected in vertically transmitted symbionts due to their fitness interdependence with hosts. However, the evolution of mutualism remains unclear in symbionts using both vertical and horizontal transmission. In this study, we show that Ascogregarina taiwanensis, previously known as a weak horizontally transmitted parasite of the Asian tiger mosquito (Aedes albopictus), exhibits mutualistic traits that enhance mosquito reproduction. The symbiont improves embryogenesis and extends the egg-laying period while most females are pseudo-vertically transmitting symbiont oocysts to their progeny at oviposition sites. Dual transcriptomic analyses 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 lead to improved assimilation of blood proteins essential for egg production. Our findings provide rare empirical evidence of a symbiont displaying both parasitic and mutualistic traits, offering new insights into the evolutionary dynamics of mixed-mode transmission symbioses. Significance StatementHow mutualism evolves from parasitism remains a central question in evolutionary biology, particularly for symbionts that combine vertical and horizontal transmission. We show that Ascogregarina taiwanensis, an Apicomplexan parasite previously known to be costly for developing Aedes albopictus mosquitoes, is also pseudo-vertically transmitted: most females release oocysts into the water during oviposition, exposing their offspring. Surprisingly, infection enhances host reproduction by promoting oogenesis through protein assimilation, leading to the production of larger larvae. Dual transcriptomic analyses reveal coordinated shifts in host and parasite metabolism, especially in nitrogen assimilation. Our findings provide rare evidence that mutualistic traits can emerge in a symbiont with mixed-mode transmission, offering new insights into the evolutionary transitions shaping host-microbe interactions.