Human-aided dispersal facilitates parasitism escape in the most invasive mosquito species

Abstract

During biological invasion process, species encounter new environments and partially escape some ecological constraints they faced in their native range, while they face new ones. The Asian tiger mosquito Aedes albopictus is one of the most iconic invasive species introduced in every inhabited continent due to international trade. It has also been shown to be infected by a prevalent yet disregarded microbial entomoparasite Ascogregarina taiwanensis. In this study, we aimed at deciphering the factors that shape the global dynamics of As. taiwanensis infection in natural Ae. albopictus populations. We showed that Ae. albopictus populations are highly colonized by several parasite genotypes but recently introduced ones are escaping it. We further performed experiments based on the invasion process to explain such pattern. To that end, we hypothesized that (i) mosquito passive dispersal (i.e. human-aided egg transportation) may affect the parasite infectiveness, (ii) founder effects (i.e. population establishment by a small number of mosquitoes) may influence the parasite dynamics and (iii) unparasitized mosquitoes are more prompt to found new populations through active flight dispersal. The two first hypotheses were supported as we showed that parasite infection decreases over time when dry eggs are stored and that experimental increase in mosquitoes density improves the parasite horizontal transmission to larvae. Surprisingly, parasitized mosquitoes tend to be more active than their unparasitized relatives. Finally, this study highlights the importance of global trade as a driver of biological invasion of the most invasive arthropod vector species. SignificanceGlobal trade expansion has facilitated the introduction of invasive species such as the Asian tiger mosquito Aedes albopictus. Eventually, invasive species might escape their natural enemies and this phenomenon exemplifies their invasion success. In this study, we combined field observations and laboratory experiments to decipher the ecological consequences of the invasion process on the interaction dynamics between Ae. albopictus and its most prevalent natural parasite As. taiwanensis. We observed a decrease in parasitism in recently introduced populations and provide experimental evidence to explain how human-aided mosquito transportation and mosquito population bottlenecks were a burden for the parasite.