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Human-aided dispersal and population bottlenecks facilitate parasitism escape in the most invasive mosquito species

Maxime Girard, Edwige Martin, Laurent Vallon, Van Trân Van, Camille Da Silva Carvalho, Justine Sack, Zélia Bontemps, Julie Balteneck, Florence Colin, Pénélope Duval, Simon Malassigné, Ian Hennessee, Lucrecia Vizcaino, Yamila Romer, Nsa Dada, Khan Ly Huynh Kim, Trang Huynh Thi Thuy, Christophe Bellet, Grégory L’Ambert, Fara Nantenaina Raharimalala, Natapong Jupatanakul, Clément Goubert, Matthieu Boulesteix, Patrick Mavingui, Emmanuel Desouhant, Patricia Luis, Rémy Cazabet, Anne‐Emmanuelle Hay, Claire Valiente Moro, Guillaume Minard

2024PNAS Nexus10 citationsDOIOpen Access PDF

Abstract

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 A. taiwanensis infection in natural A. albopictus populations. We showed that A. 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.

Topics & Concepts

Biological dispersalBiologyAedes albopictusInvasive speciesEcologyParasitismPopulationParasite hostingRange (aeronautics)Introduced speciesVector (molecular biology)LarvaZoologyHost (biology)Aedes aegyptiDemographyBiochemistryRecombinant DNAMaterials scienceWorld Wide WebSociologyComputer scienceGeneComposite materialMosquito-borne diseases and controlInsect symbiosis and bacterial influencesMalaria Research and Control
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