Quantifying the effects of temperature on mosquito and parasite traits that determine the transmission potential of human malaria

Abstract

Malaria transmission is known to be strongly impacted by temperature. The current understanding of how temperature affects mosquito and parasite life history traits derives from a limited number of empirical studies. These studies, some dating back to the early part of last century, are often poorly controlled, have limited replication, explore a narrow range of temperatures, and use a mixture of parasite and mosquito species. Here, we use a single pairing of the Asian mosquito vector, An. stephensi and the human malaria parasite, P. falciparum to conduct a comprehensive evaluation of the thermal performance curves of a range of mosquito and parasite traits relevant to transmission. We show that biting rate, adult mortality rate, parasite development rate, and vector competence are temperature sensitive. Importantly, we find qualitative and quantitative differences to the assumed temperature-dependent relationships. To explore the overall implications of temperature for transmission, we first use a standard model of relative vectorial capacity. This approach suggests a temperature optimum for transmission of 29°C, with minimum and maximum temperatures of 12°C and 38°C, respectively. However, the robustness of the vectorial capacity approach is challenged by the fact that the empirical data violate several of the model’s simplifying assumptions. Accordingly, we present an alternative model of relative force of infection that better captures the observed biology of the vector–parasite interaction. This model suggests a temperature optimum for transmission of 26°C, with a minimum and maximum of 17°C and 35°C, respectively. The differences between the models lead to potentially divergent predictions for the potential impacts of current and future climate change on malaria transmission. The study provides a framework for more detailed, system-specific studies that are essential to develop an improved understanding on the effects of temperature on malaria transmission.

Hemocyte-targeted gene expression in the female malaria mosquito using thehemolectinpromoter fromDrosophila

“…At permissive temperatures (18°C to 20°C), Gal80ts binds to Gal4 and inhibits Gal4 activity, while at restrictive temperatures (28 to 30°C), it no longer binds to Gal4, allowing Gal4-dependent transgene expression. This system would also be suitable for studying Plasmodium falciparum development in transgenic mosquitoes as the human malaria parasite, contrary to the rodent parasite, Plasmodium berghei, can develop within temperatures ranging from 21 up to 34°C, with most studies analyzing malaria infection in Anopheles at 24 to 28°C (Shapiro, Whitehead et al 2017). The hml-gal4 line presented here was initially designed to carry, in tandem with hml-gal4, the gal80ts sequence under the control of a second and identical hml promoter.…”

Spatial heterogeneity in the abundance and fecundity of Arctic mosquitoes

“…Aquatic habitats are subject to changes in temperature and precipitation, the evaporative balance of which determines aquatic habitat duration, stability, and the extent of crowding, which can impact immature mortality (Sota et al 1994, Ros a et al 2014, Marini et al 2016) and adult size (Chaves et al 2011, Mulatti et al 2014. In the terrestrial environment, adult mosquito longevity (Shapiro et al 2017), reproduction (Reisen et al 2010), and abundance (Hoshi et al 2017) are influenced by temperature. In the terrestrial environment, adult mosquito longevity (Shapiro et al 2017), reproduction (Reisen et al 2010), and abundance (Hoshi et al 2017) are influenced by temperature.…”

“…Furthermore, temperature dictates mosquito growth rates and stage-specific phenology , which can impact immature survival (Loetti et al 2011, Ciota et al 2014, Culler et al 2015 and adult size (Lyimo et al 1992, Christiansen-Jucht et al 2015. In the terrestrial environment, adult mosquito longevity (Shapiro et al 2017), reproduction (Reisen et al 2010), and abundance (Hoshi et al 2017) are influenced by temperature. In the absence of autogeny, reproduction may be further impacted by the availability of vertebrate hosts (Wekesa et al 1996).…”

Exploring the lower thermal limits for transmission of human malaria, Plasmodium falciparum

“…Similar historic studies either lacked temperature 61 control, adequate sampling, or did not use P. falciparum parasites (e.g. [10][11][12][13] Mosquitoes were reared at 27°C following standard protocols [15]. P. falciparum (NF54) 75 parasite cultures were either provided by the Johns Hopkins Malaria Institute Core 76 Facility, or produced in our lab following protocols described in [15].…”

“…[10][11][12][13] Mosquitoes were reared at 27°C following standard protocols [15]. P. falciparum (NF54) 75 parasite cultures were either provided by the Johns Hopkins Malaria Institute Core 76 Facility, or produced in our lab following protocols described in [15]. In all cases 77 gametocyte cultures reached approximately 2-4% mature gametocytemia and were 78 between 14-17 days post gametocyte induction when cultures were fed to 3-5 day old 79 mosquitoes.…”