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. 2019;8(1):1265-1279.
doi: 10.1080/22221751.2019.1657785.

Evolution and biological significance of flaviviral elements in the genome of the arboviral vector Aedes albopictus

Vincent Houé  1   2 , Gaelle Gabiane  1 , Catherine Dauga  3 , Marie Suez  4 , Yoann Madec  5 , Laurence Mousson  1 , Michele Marconcini  6 , Pei-Shi Yen  1 , Xavier de Lamballerie  7   8 , Mariangela Bonizzoni  6 , Anna-Bella Failloux  1
Affiliations

Evolution and biological significance of flaviviral elements in the genome of the arboviral vector Aedes albopictus

Vincent Houé et al. Emerg Microbes Infect. 2019.

Abstract

Since its genome details are publically available, the mosquito Aedes albopictus has become the central stage of attention for deciphering multiple biological and evolutionary aspects at the root of its success as an invasive species. Its genome of 1,967 Mb harbours an unusual high number of non-retroviral integrated RNA virus sequences (NIRVS). NIRVS are enriched in piRNA clusters and produce piRNAs, suggesting an antiviral effect. Here, we investigated the evolutionary history of NIRVS in geographically distant Ae. albopictus populations by comparing genetic variation as derived by neutral microsatellite loci and seven selected NIRVS. We found that the evolution of NIRVS was far to be neutral with variations both in their distribution and sequence polymorphism among Ae. albopictus populations. The Flaviviral elements AlbFlavi2 and AlbFlavi36 were more deeply investigated in their association with dissemination rates of dengue virus (DENV) and chikungunya virus (CHIKV) in Ae. albopictus at both population and individual levels. Our results show a complex association between NIRVS and DENV/CHIKV opening a new avenue for investigating the functional role of NIRVS as antiviral elements shaping vector competence of mosquitoes to arboviruses.

Keywords: NIRVS; arboviral diseases; genetic structure; vector competence.

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Conflict of interest statement

No potential conflict of interest was reported by the authors.

Figures

Figure 1.
Figure 1.
Estimated population structure of 363 individuals (19 populations) using 10 microsatellite markers. Map with sampling sites of populations with colour pie charts showing genotype frequencies, according to Cluster 1 (red) and Cluster 2, which the latest subdivided into 4 subclusters (blue, green, yellow and orange), deduced from the ΔK curve obtained (Supplementary Figure 1(A–C)).
Figure 2.
Figure 2.
NIRVS variability among Aedes albopictus populations. The frequency of AlbFlavi1 (A), AlbFlavi2 (B), AlbFlavi4 (C), AlbFlavi10 (D), AlbFlavi36 (E), AlbFlavi41 (F) and CSA (G and H) was assessed for 20 individuals in each Ae. albopictus population (except the Rio population with 19 individuals). Populations were clustered according to their continent of origin. Oahu and Foshan correspond to laboratory colonies. The variability of CSA was assessed using two sets of primers: CSA-NS3 (G) and CSA-JJL (H).
Figure 3.
Figure 3.
Aedes albopictus population clustering based on microsatellite and NIRVS loci. (A) Dendrogram of Ae. albopictus populations based on the analysis of 8 microsatellite loci of 12 Aedes albopictus populations using Cavalli-Sforza & Edwards’s genetic distance and Neighbour-Joining method. Bootstrap values were indicated when >50%. (B) Dendrogram of Ae. albopictus populations based on Bray Curtis distance representing dissimilarities between NIRVS composition and abundances.
Figure 4.
Figure 4.
Divergence of AlbFlavi2 among Aedes albopictus individuals. Phylogram of AlbFlavi2 sequences based on parsimony with gaps considered as 5th nucleotides. Each node was found in 98–100% of the trees obtained through NNI rearrangements. Significant bootstrap values were indicated at nodes. hmwb: high molecular weight band Values; in brackets: alignment coordinates of deletion. The same result was obtained by parsimony without gap as 5th nucleotide, except for the sequence cluster of mosquitoes from Morocco.
Figure 5.
Figure 5.
Pilot analysis showing the association between frequencies of AlbFlavi2/AlbFlavi36 and DENV/CHIKV dissemination efficiencies (DE) in Aedes albopictus populations. The Foshan colony and the Tibati population (Cameroon, generation F1) were used for the analysis. (A) Presence/absence of AlbFlavi2 and DEs to DENV and CHIKV obtained for the Foshan colony. (B) Presence/absence of AlbFlavi36 and DEs to DENV and CHIKV obtained for the Foshan colony. (C) Presence/absence of AlbFlavi2 and DEs to DENV and CHIKV obtained for the Tibati population. (D) Presence/absence of AlbFlavi36 and DEs to DENV and CHIKV obtained for the Tibati population. DEs were obtained for both viruses at 14 days post-infection. In total, 191 and 122 individuals were examined for presence of AlbFlavi2/AlbFlavi36 after infection DENV and CHIKV, respectively. Interactions of populations and frequencies of AlbFlavi2/AlbFlavi36 with DEs were tested using logistic regression models.
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Grants and funding

This study was supported by the Institut Pasteur, the French Government’s Investissement d’Avenir program, Laboratoire d’Excellence “Integrative Biology of Emerging Infectious Diseases” (grant number ANR-10-LABX-62-IBEID to A-BF), the European Union’s Horizon 2020 research and innovation program, ZIKAlliance program under ZIKAlliance grant agreement no. 734548 to A-BF, and the European Research Council, NIRV_HOST_INT Council (grant agreement number 682394 – NIRV_HOST_INT to VH and MB).

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