Dataset Information

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

ABSTRACT: 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 3-4 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.

SUBMITTER: O'Connor O

PROVIDER: S-EPMC8259877 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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

O'Connor Olivia O Ou Tey Putita TP Aubry Fabien F Dabo Stéphanie S Russet Sylvie S Girault Dominique D In Saraden S Minier Marine M Lequime Sebastian S Hoem Thavry T Boyer Sébastien S Dussart Philippe P Pocquet Nicolas N Burtet-Sarramegna Valérie V Lambrechts Louis L Duong Veasna V Dupont-Rouzeyrol Myrielle M

Emerging microbes & infections 20211201 1

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 3-4 replacement in 2005-2007, both followed by a massive dengue outbreak. However, their underlying evolutionary drivers have not been eluc ...[more]

PMID: 34139961

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Project description:BackgroundBecause no dengue vaccine or antiviral therapy is commercially available, controlling the primary mosquito vector, Aedes aegypti, is currently the only means to prevent dengue outbreaks. Traditional models of Ae. aegypti assume that population dynamics are regulated by density-dependent larval competition for food and little affected by oviposition behavior. Due to direct impacts on offspring survival and development, however, mosquito choice in oviposition site can have important consequences for population regulation that should be taken into account when designing vector control programs.Methodology/principal findingsWe examined oviposition patterns by Ae. aegypti among 591 naturally occurring containers and a set of experimental containers in Iquitos, Peru. Using larval starvation bioassays as an indirect measure of container food content, we assessed whether females select containers with the most food for their offspring. Our data indicate that choice of egg-laying site is influenced by conspecific larvae and pupae, container fill method, container size, lid, and sun exposure. Although larval food positively influenced oviposition, our results did not support the hypothesis that females act primarily to maximize food for larvae. Females were most strongly attracted to sites containing immature conspecifics, even when potential competitors for their progeny were present in abundance.Conclusion/significanceDue to strong conspecific attraction, egg-laying behavior may contribute more to regulating Ae. aegypti populations than previously thought. If highly infested containers are targeted for removal or larvicide application, females that would have preferentially oviposited in those sites may instead distribute their eggs among other suitable, previously unoccupied containers. Strategies that kill mosquitoes late in their development (i.e., insect growth regulators that kill pupae rather than larvae) will enhance vector control by creating "egg sinks," treated sites that exploit conspecific attraction of ovipositing females, but reduce emergence of adult mosquitoes via density-dependent larval competition and late acting insecticide.

Project description:BackgroundDengue virus type 3 genotype III (DENV3/III) is associated with increased number of severe infections when it emerged in the Americas and Asia. We had previously demonstrated that the DENV3/III was introduced into Malaysia in the late 2000s. We investigated the genetic diversity of DENV3/III strains recovered from Malaysia and examined their phylogenetic relationships against other DENV3/III strains isolated globally.ResultsPhylogenetic analysis revealed at least four distinct DENV3/III lineages. Two of the lineages (DENV3/III-B and DENV3/III-C) are current actively circulating whereas the DENV3/III-A and DENV3/III-D were no longer recovered since the 1980s. Selection pressure analysis revealed strong evidence of positive selection on a number of amino acid sites in PrM, E, NS1, NS2a, NS2b, NS3, NS4a, and NS5. The Malaysian DENV3/III isolates recovered in the 1980s (MY.59538/1987) clustered into DENV3/III-B, which was the lineage with cosmopolitan distribution consisting of strains actively circulating in the Americas, Africa, and Asia. The Malaysian isolates recovered after the 2000s clustered within DENV3/III-C. This DENV3/III-C lineage displayed a more restricted geographical distribution and consisted of isolates recovered from Asia, denoted as the Asian lineage. Amino acid variation sites in NS5 (NS5-553I/M, NS5-629 T, and NS5-820E) differentiated the DENV3/III-C from other DENV3 viruses. The codon 629 of NS5 was identified as a positively selected site. While the NS5-698R was identified as unique to the genome of DENV3/III-C3. Phylogeographic results suggested that the recent Malaysian DENV3/III-C was likely to have been introduced from Singapore in 2008 and became endemic. From Malaysia, the virus subsequently spread into Taiwan and Thailand in the early part of the 2010s and later reintroduced into Singapore in 2013.ConclusionsDistinct clustering of the Malaysian old and new DENV3/III isolates suggests that the currently circulating DENV3/III in Malaysia did not descend directly from the strains recovered during the 1980s. Phylogenetic analyses and common genetic traits in the genome of the strains and those from the neighboring countries suggest that the Malaysian DENV3/III is likely to have been introduced from the neighboring regions. Malaysia, however, serves as one of the sources of the recent regional spread of DENV3/III-C3 within the Asia region.

Project description:BackgroundVector surveillance provides critical data for decision-making to ensure that malaria control programmes remain effective and responsive to any threats to a successful control and elimination programme. The quality and quantity of data collected is dependent on the sampling tools and laboratory techniques used which may lack the sensitivity required to collect relevant data for decision-making. Here, 40 vector control experts were interviewed to assess the benefits and limitations of the current vector surveillance tools and techniques. In addition, experts shared ideas on "blue sky" indicators which encompassed ideas for novel methods to monitor presently used indicators, or to measure novel vector behaviours not presently measured. Algorithms for deploying surveillance tools and priorities for understanding vector behaviours are also needed for collecting and interpreting vector data.ResultsThe available tools for sampling and analysing vectors are often hampered by high labour and resource requirements (human and supplies) coupled with high outlay and operating costs and variable tool performance across species and geographic regions. The next generation of surveillance tools needs to address the limitations of present tools by being more sensitive, specific and less costly to deploy to enable the collection and use of epidemiologically relevant vector data to facilitate more proactive vector control guidance. Ideas and attributes for Target Product Profiles (TPPs) generated from this analysis provide targets for research and funding to develop next generation tools.ConclusionsMore efficient surveillance tools and a more complete understanding of vector behaviours and populations will provide a basis for more cost effective and successful malaria control. Understanding the vectors' behaviours will allow interventions to be deployed that target vulnerabilities in vector behaviours and thus enable more effective control. Through defining the strengths and weaknesses of the current vector surveillance methods, a foundation and initial framework was provided to define the TPPs for the next generation of vector surveillance methods. The draft TTPs presented here aim to ensure that the next generation tools and technologies are not encumbered by the limitations of present surveillance methods and can be readily deployed in low resource settings.

Dataset Information

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

Publications

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

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