Effect of Constant Temperatures on Culicoides sonorensis Midge Physiology and Vesicular Stomatitis Virus Infection

SIMPLE SUMMARY: Culicoides biting midges are nuisance pests of livestock and well-known vectors of veterinary arboviruses, such as vesicular stomatitis virus (VSV). Female midges ingest viruses when feeding on blood to obtain protein for egg-laying. After ingesting a VSV-infected blood meal, the environmental temperature of the resting location mediates the rates at which blood is digested, eggs are laid, and virus particles are replicated inside the midge. VSV transmission will occur if the timing of virus amplification aligns with the next feeding–egg-laying cycle. We evaluated the impact of constant environmental temperatures on midge physiology (lifespan and reproduction), vector competence for VSV (infection and dissemination), and thermal resting preference. Our results indicate that after ingesting a blood meal, most midges prefer to rest in areas that fall within their preferred physiological range regardless of the temperatures at which they were being maintained. These preferred temperatures maximized their survival, the number of egg-laying cycles, and the likelihood of VSV transmission. Our temperature approach shows that in the Culicoides–VSV system, the preferred resting temperature selected by blood-fed midges is beneficial for both insect and virus transmission. ABSTRACT: Culicoides midges play an important role in vesicular stomatitis virus (VSV) transmission to US livestock. After VSV-blood feeding, blood digestion followed by oviposition occurs while ingested virus particles replicate and disseminate to salivary glands for transmission during subsequent blood-feeding events. Changes to environmental temperature may alter the feeding–oviposition–refeeding cycles, midge survival, VSV infection, and overall vector capacity. However, the heterothermic midge may respond rapidly to environmental changes by adjusting their thermal behavior to resting in areas closer to their physiological range. Here we investigated the effects of four constant environmental temperatures (20, 25, 30, and 35 °C) on C. sonorensis survival, oviposition, and VSV infection, as well as resting thermal preferences after blood-feeding. We found that most midges preferred to rest in areas at 25–30 °C. These two constant temperatures (25 and 30 °C) allowed an intermediate fitness performance, with a 66% survival probability by day 10 and oviposition cycles occurring every 2–3 days. Additionally, VSV infection rates in bodies and heads with salivary glands were higher than in midges held at 20 °C and 35 °C. Our results provide insight into the implications of temperature on VSV–Culicoides interactions and confirm that the range of temperature preferred by midges can benefit both the vector and the arbovirus.