Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings

Olivia O'Connor (1) , Tey Putita Ou (2) , Fabien Aubry (3) , Stéphanie Dabo (3) , Sylvie Russet (1) , Dominique Girault (1) , Saraden In (2) , Marine Minier (4) , Thavry Hoem (2) , Sébastien Boyer (5) , Philippe Dussart (2) , Nicolas Pocquet (4) , Valérie Burtet-Sarramegna (6) , Louis A Lambrechts (3) , Veasna Duong (4) , Myrielle Dupont-Rouzeyrol (1)

1 URE-DA - Dengue et Arbovirose
2 Unité de Virologie / Virology Unit [Phnom Penh]
3 IVI - Interactions Virus-Insectes - Insect-Virus Interactions
4 URE-EM - Entomologie médicale [Nouméa, Nouvelle-Calédonie]
5 Medical and Veterinary Entomology - Entomologie médciale et vétérinaire [Phnom Penh, Cambodia]
6 ISEA - Institut de sciences exactes et appliquées

Dengue virus (DENV) evolutionary dynamics are characterized by frequent DENV genotype/lineage replacements, potentially associated with changes in disease severity and human immunity. New Caledonia (NC) and Cambodia, two contrasted epidemiological settings, respectively experienced a DENV-1 genotype IV to I replacement in 2012 and a DENV-1 genotype I lineage 3 to 4 replacement in 2005-2007, both followed by a massive dengue outbreak. However, their underlying evolutionary drivers have not been elucidated. Here, we tested the hypothesis that these genotype/lineage switches reflected a higher transmission fitness of the replacing DENV genotype/lineage in the mosquito vector using in vivo competition experiments. For this purpose, field-derived Aedes aegypti from NC and Cambodia were orally challenged with epidemiologically relevant pairs of four DENV-1 genotype I and IV strains from NC or four DENV-1 genotype I lineage 3 and 4 strains from Cambodia, respectively. The relative transmission fitness of each DENV-1 genotype/lineage was measured by quantitative RT-PCR for infection, dissemination, and transmission rates. Results showed a clear transmission fitness advantage of the replacing DENV-1 genotype I from NC within the vector. A similar but more subtle pattern was observed for the DENV-1 lineage 4 replacement in Cambodia. Our results support the hypothesis that vector-driven selection contributed to the DENV-1 genotype/lineage replacements in these two contrasted epidemiological settings, and reinforce the idea that natural selection taking place within the mosquito vector plays an important role in DENV short-term evolutionary dynamics.

Mots clés: Dengue virus; genotype/lineage replacement; Aedes aegypti; transmission fitness; competition assay

Domaines: Virologie

Olivia O'Connor, Tey Putita Ou, Fabien Aubry, Stéphanie Dabo, Sylvie Russet, et al.. Potential role of vector-mediated natural selection in dengue virus genotype/lineage replacements in two epidemiologically contrasted settings. Emerging microbes & infections, 2021, 10 (1), pp.1346-1357. ⟨10.1080/22221751.2021.1944789⟩. ⟨pasteur-03265221⟩