Abstract

Rift Valley fever virus (RVFV) causes morbidity and mortality in humans and domestic ungulates in sub-Saharan Africa, Egypt, and the Arabian Peninsula. Mosquito vectors transmit RVFV between vertebrates by bite, and also vertically to produce infectious progeny. Arrival of RVFV into the United States by infected mosquitoes or humans could result in significant impacts on food security, human health, and wildlife health. Elucidation of the vectors involved in the post-introduction RVFV ecology is paramount to rapid implementation of vector control. We performed vector competence experiments in which field-collected mosquitoes were orally exposed to an epidemic strain of RVFV via infectious blood meals. We targeted floodwater Aedes species known to feed on cattle, and/or deer species (Aedes melanimon Dyar, Aedes increpitus Dyar, Aedes vexans [Meigen]). Two permanent-water-breeding species were targeted as well: Culiseta inornata (Williston) of unknown competence considering United States populations, and Culex tarsalis Coquillett as a control species for which transmission efficiency is known. We tested the potential for midgut infection, midgut escape (dissemination), ovarian infection (vertical transmission), and transmission by bite (infectious saliva). Tissues were assayed by plaque assay and RT-qPCR, to quantify infectious virus and confirm virus identity. Tissue infection data were analyzed using a within-host model under a Bayesian framework to determine the probabilities of infection outcomes (midgut-limited infection, disseminated infection, etc.) while estimating barriers to infection between tissues. Permanent-water-breeding mosquitoes (Cx. tarsalis and Cs. inornata) exhibited more efficient horizontal transmission, as well as potential for vertical transmission, which is contrary to the current assumptions of RVFV ecology. Barrier estimates trended higher for Aedes spp., suggesting systemic factors in the differences between these species and Cx. tarsalis and Cs. inornata. These data indicate higher potential for vertical transmission than previously appreciated, and support the consensus of RVFV transmission including a broad range of potential vectors.

Highlights

  • Rift Valley fever virus (RVFV) is a mosquito-borne virus (Order: Bunyavirales, Family: Phenuiviridae, Genus: Phlebovirus) endemic to sub-Saharan Africa that affects both humans and domestic ungulates [1]

  • Preliminary evidence for vertical transmission has been demonstrated under laboratory conditions using a colonized line of Culex tarsalis Coquillett [6]; the implications for vertical transmission by a permanent-water ovipositing mosquito are unclear for the epidemiology of RVFV

  • We included Aedes increpitus Dyar based on high abundances in our sampling sites, and Cx. tarsalis to confirm previously demonstrated high transmission rates, while providing a positive control species. For each of these species, we investigated the progression of virus infection throughout mosquito bodies, as well as potential for vertical transmission of RVFV using infection of ovaries as a proxy

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Summary

Introduction

Rift Valley fever virus (RVFV) is a mosquito-borne virus (Order: Bunyavirales, Family: Phenuiviridae, Genus: Phlebovirus) endemic to sub-Saharan Africa that affects both humans and domestic ungulates [1]. In addition to horizontal transmission by mosquitoes, there is strong evidence for vertical transmission by some floodwater Aedes spp. mosquitoes [3,4]. These species oviposit dessication-resistant eggs which may be able to harbor virus throughout periods with little to no rainfall. This persistence in the mosquito population is thought to be a mechanism of viral maintenance, allowing the virus to survive long interepidemic periods in mosquito egg populations, which can hatch following periods of high rainfall [3,5]. Vertical transmission of viruses in the vector is well-documented throughout the order Bunyavirales [7]

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