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

Author:

Girard Maxime1ORCID,Martin Edwige1,Vallon Laurent1,Tran Van Van1,Da Silva Carvalho Camille1ORCID,Sack Justine1,Bontemps Zélia12ORCID,Balteneck Julie13,Colin Florence1,Duval Pénélope1,Malassigné Simon1ORCID,Hennessee Ian4,Vizcaino Lucrecia5,Romer Yamila6,Dada Nsa78ORCID,Ly Huynh Kim Khan9,Huynh Thi Thuy Trang9ORCID,Bellet Christophe10,Lambert Gregory11,Nantenaina Raharimalala Fara12,Jupatanakul Natapong13ORCID,Goubert Clement14ORCID,Boulesteix Matthieu15,Mavingui Patrick16,Desouhant Emmanuel15ORCID,Luis Patricia1ORCID,Cazabet Rémy17ORCID,Hay Anne-Emmanuelle1ORCID,Valiente Moro Claire1ORCID,Minard Guillaume1ORCID

Affiliation:

1. University of Lyon, Université Claude Bernard Lyon 1, CNRS, INRAe, VetAgro Sup, UMR Ecologie Microbienne , F-69622 Villeurbanne , France

2. Department of Medical Biochemistry and Microbiology, Science for Life Laboratories, Uppsala University , 752 37 Uppsala , Sweden

3. Université de Lyon, INSA Lyon, Université Claude Bernard Lyon 1, CNRS, UMR 5240 MAP, Microbiologie, Adaptation, Pathogénie , F-69622 Villeurbanne , France

4. Rollins School of Public Health, Emory University , Atlanta, GA 30322 , USA

5. Entomology Branch, Division of Parasitic Diseases and Malaria, Center for Global Health, US Centers for Disease Control and Prevention , Atlanta, GA 30333 , USA

6. Emory College of Arts and Science, Emory University , Atlanta, GA 30322 , USA

7. Centre de Recherche pour la lutte contre les Maladies Infectieuses Tropicales/Tropicales Infectious Diseases Research Centre, Université d’Abomey-Calavi , Cotonou , Benin

8. School of Life Sciences, Arizona State University , Tempe, AZ 85281 , USA

9. Department of Medical Entomology and Zoonotics, Pasteur Institute , 722700 Ho Chi Minh City , Vietnam

10. Entente Interdépartementale Rhône-Alpes pour la Démoustication , 73310 Chindrieux , France

11. Entente Interdépartementale de Démoustication du Littoral Méditerranéen , 34000 Montpellier , France

12. Pasteur Institute , Antananarivo , Madagascar

13. National Center for Genetic Engineering and Biotechnology (BIOTEC) , 12120 Pathum Thani , Thailand

14. Canadian Centre for Computational Genomics, McGill Genome Centre, Human Genetics, McGill University , QC H3A0G1 Montreal , Canada

15. Laboratoire de Biométrie et de Biologie Evolutive, Université de Lyon, Université Claude Bernard Lyon 1, UMR CNRS 5558, VetAgro Sup , F-69622 Villeurbanne , France

16. UMR PIMIT, Processus Infectieux en Milieu Insulaire Tropical, CNRS 9192, INSERM U1187, IRD 249, Université de La Réunion, 97490 Sainte-Clotilde , La Réunion , France

17. Univ de Lyon, CNRS, Université Lyon 1, LIRIS, UMR5205 , F-69622 Villeurbanne , France

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.

Funder

French National Research Program for Environmental and Occupational Health of Anses

Thailand Program Management Unit for Human Resources & Institutional Development, Research and Innovation

Publisher

Oxford University Press (OUP)

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