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Dengue virus infection modifies mosquito blood-feeding behavior to increase transmission to the host.

ABSTRACT: Mosquito blood-feeding behavior is a key determinant of the epidemiology of dengue viruses (DENV), the most-prevalent mosquito-borne viruses. However, despite its importance, how DENV infection influences mosquito blood-feeding and, consequently, transmission remains unclear. Here, we developed a high-resolution, video-based assay to observe the blood-feeding behavior of Aedes aegypti mosquitoes on mice. We then applied multivariate analysis on the high-throughput, unbiased data generated from the assay to ordinate behavioral parameters into complex behaviors. We showed that DENV infection increases mosquito attraction to the host and hinders its biting efficiency, the latter resulting in the infected mosquitoes biting more to reach similar blood repletion as uninfected mosquitoes. To examine how increased biting influences DENV transmission to the host, we established an in vivo transmission model with immuno-competent mice and demonstrated that successive short probes result in multiple transmissions. Finally, to determine how DENV-induced alterations of host-seeking and biting behaviors influence dengue epidemiology, we integrated the behavioral data within a mathematical model. We calculated that the number of infected hosts per infected mosquito, as determined by the reproduction rate, tripled when mosquito behavior was influenced by DENV infection. Taken together, this multidisciplinary study details how DENV infection modulates mosquito blood-feeding behavior to increase vector capacity, proportionally aggravating DENV epidemiology. By elucidating the contribution of mosquito behavioral alterations on DENV transmission to the host, these results will inform epidemiological modeling to tailor improved interventions against dengue.

SUBMITTER: Wei Xiang BW

PROVIDER: S-EPMC8785958 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Dengue virus infection modifies mosquito blood-feeding behavior to increase transmission to the host.

Wei Xiang Benjamin Wong BW Saron Wilfried A A WAA Stewart James C JC Hain Arthur A Walvekar Varsha V Missé Dorothée D Thomas Fréderic F Kini R Manjunatha RM Roche Benjamin B Claridge-Chang Adam A St John Ashley L AL Pompon Julien J

Proceedings of the National Academy of Sciences of the United States of America 20220101 3

Mosquito blood-feeding behavior is a key determinant of the epidemiology of dengue viruses (DENV), the most-prevalent mosquito-borne viruses. However, despite its importance, how DENV infection influences mosquito blood-feeding and, consequently, transmission remains unclear. Here, we developed a high-resolution, video-based assay to observe the blood-feeding behavior of <i>Aedes aegypti</i> mosquitoes on mice. We then applied multivariate analysis on the high-throughput, unbiased data generated ...[more]

PMID: 35012987

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Project description:BackgroundThe Madagascar National Strategic Plan for Malaria Control 2018 (NSP) outlines malaria control pre-elimination strategies that include detailed goals for mosquito control. Primary surveillance protocols and mosquito control interventions focus on indoor vectors of malaria, while many potential vectors feed and rest outdoors. Here we describe the application of tools that advance our understanding of diversity, host choice, and Plasmodium infection in the Anopheline mosquitoes of the Western Highland Fringe of Madagascar.Methodology/principal findingsWe employed a modified barrier screen trap, the QUadrant Enabled Screen Trap (QUEST), in conjunction with the recently developed multiplex BLOOdmeal Detection Assay for Regional Transmission (BLOODART). We captured a total of 1252 female Anopheles mosquitoes (10 species), all of which were subjected to BLOODART analysis. QUEST collection captured a heterogenous distribution of mosquito density, diversity, host choice, and Plasmodium infection. Concordance between Anopheles morphology and BLOODART species identifications ranged from 93-99%. Mosquito feeding behavior in this collection frequently exhibited multiple blood meal hosts (single host = 53.6%, two hosts = 42.1%, three hosts = 4.3%). The overall percentage of human positive bloodmeals increased between the December 2017 and the April 2018 timepoints (27% to 44%). Plasmodium positivity was frequently observed in the abdomens of vectors considered to be of secondary importance, with an overall prevalence of 6%.Conclusions/significanceThe QUEST was an efficient tool for sampling exophilic Anopheline mosquitoes. Vectors considered to be of secondary importance were commonly found with Plasmodium DNA in their abdomens, indicating a need to account for these species in routine surveillance efforts. Mosquitoes exhibited multiple blood feeding behavior within a gonotrophic cycle, with predominantly non-human hosts in the bloodmeal. Taken together, this complex feeding behavior could enhance the role of multiple Anopheline species in malaria transmission, possibly tempered by zoophilic feeding tendencies.

Project description:BackgroundAlthough American crows are a key indicator species for West Nile virus (WNV) and mount among the highest viremias reported for any host, the importance of crows in the WNV transmission cycle has been called into question because of their consistent underrepresentation in studies of Culex blood meal sources. Here, we test the hypothesis that this apparent underrepresentation could be due, in part, to underrepresentation of crow nesting habitat from mosquito sampling designs. Specifically, we examine how the likelihood of a crow blood meal changes with distance to and timing of active crow nests in a Davis, California, population.MethodsSixty artificial mosquito resting sites were deployed from May to September 2014 in varying proximity to known crow nesting sites, and Culex blood meal hosts were identified by DNA barcoding. Genotypes from crow blood meals and local crows (72 nestlings from 30 broods and 389 local breeders and helpers) were used to match mosquito blood meals to specific local crows.ResultsAmong the 297 identified Culex blood meals, 20 (6.7%) were attributable to crows. The mean percentage of blood meals of crow origin was 19% in the nesting period (1 May-18 June 2014), but 0% in the weeks after fledging (19 June-1 September 2014), and the likelihood of a crow blood meal increased with proximity to an active nest: the odds that crows hosted a Culex blood meal were 38.07 times greater within 10 m of an active nest than > 10 m from an active nest. Nine of ten crow blood meals that could be matched to a genotype of a specific crow belonged to either nestlings in these nests or their mothers. Six of the seven genotypes that could not be attributed to sampled birds belonged to females, a sex bias likely due to mosquitoes targeting incubating or brooding females.ConclusionData herein indicate that breeding crows serve as hosts for Culex in the initial stages of the WNV spring enzootic cycle. Given their high viremia, infected crows could thereby contribute to the re-initiation and early amplification of the virus, increasing its availability as mosquitoes shift to other moderately competent later-breeding avian hosts.

Project description:Tsetse flies are the notorious transmitters of African trypanosomiasis, a disease caused by the Trypanosoma parasite that affects humans and livestock on the African continent. Metacyclic infection rates in natural tsetse populations with Trypanosoma brucei, including the two human-pathogenic subspecies, are very low, even in epidemic situations. Therefore, the infected fly/host contact frequency is a key determinant of the transmission dynamics. As an obligate blood feeder, tsetse flies rely on their complex salivary potion to inhibit host haemostatic reactions ensuring an efficient feeding. The results of this experimental study suggest that the parasite might promote its transmission through manipulation of the tsetse feeding behavior by modifying the saliva composition. Indeed, salivary gland Trypanosoma brucei-infected flies display a significantly prolonged feeding time, thereby enhancing the likelihood of infecting multiple hosts during the process of a single blood meal cycle. Comparison of the two major anti-haemostatic activities i.e. anti-platelet aggregation and anti-coagulation activity in these flies versus non-infected tsetse flies demonstrates a significant suppression of these activities as a result of the trypanosome-infection status. This effect was mainly related to the parasite-induced reduction in salivary gland gene transcription, resulting in a strong decrease in protein content and related biological activities. Additionally, the anti-thrombin activity and inhibition of thrombin-induced coagulation was even more severely hampered as a result of the trypanosome infection. Indeed, while naive tsetse saliva strongly inhibited human thrombin activity and thrombin-induced blood coagulation, saliva from T. brucei-infected flies showed a significantly enhanced thrombinase activity resulting in a far less potent anti-coagulation activity. These data clearly provide evidence for a trypanosome-mediated modification of the tsetse salivary composition that results in a drastically reduced anti-haemostatic potential and a hampered feeding performance which could lead to an increase of the vector/host contact and parasite transmission in field conditions.

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Dengue virus infection modifies mosquito blood-feeding behavior to increase transmission to the host.

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Dengue virus infection modifies mosquito blood-feeding behavior to increase transmission to the host.

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