Impact of daily temperature fluctuations on dengue virus transmission by Aedes aegypti

Abstract

Most studies on the ability of insect populations to transmit pathogens consider only constant temperatures and do not account for realistic daily temperature fluctuations that can impact vectorpathogen interactions. Here, we show that diurnal temperature range (DTR) affects two important parameters underlying dengue virus (DENV) transmission by Aedes aegypti. In two independent experiments using different DENV serotypes, mosquitoes were less susceptible to virus infection and died faster under larger DTR around the same mean temperature. Large DTR (20°C) decreased the probability of midgut infection, but not duration of the virus extrinsic incubation period (EIP), compared with moderate DTR (10°C) or constant temperature. A thermodynamic model predicted that at mean temperatures <18°C, DENV transmission increases as DTR increases, whereas at mean temperatures >18°C, larger DTR reduces DENV transmission. The negative impact of DTR on Ae. aegypti survival indicates that large temperature fluctuations will reduce the probability of vector survival through EIP and expectation of infectious life. Seasonal variation in the amplitude of daily temperature fluctuations helps to explain seasonal forcing of DENV transmission at locations where average temperature does not vary seasonally and mosquito abundance is not associated with dengue incidence. Mosquitoes lived longer and were more likely to become infected under moderate temperature fluctuations, which is typical of the high DENV transmission season than under large temperature fluctuations, which is typical of the low DENV transmission season. Our findings reveal the importance of considering short-term temperature variations when studying DENV transmission dynamics.arbovirus | climate | vectorial capacity I ncidence, seasonal variation, and global distribution of vectorborne diseases are known to be influenced by climate (1). What is controversial is exactly how climatic factors-and thus climate change-impact the intrinsic transmission intensity of most vector-borne pathogens (1-5). Part of the problem derives from the interplay of multiple factors, such as spatial heterogeneity (6) or differing socioeconomic and demographic backgrounds (3, 7) that combine with climate to influence overall transmission dynamics. In addition, our ability to accurately define the impact of climatic factors on the risk of vector-borne disease is limited by poor understanding of the mechanistic link between environmental variables, such as temperature, and the vectorial capacity of insect vector populations (1,(8)(9)(10)(11)(12).Vectorial capacity captures key components of an insect's role in pathogen transmission, which is influenced by many environmental, ecological, behavioral, and molecular factors (13). Mathematically, it can be described by:where m is vector density per person, a is daily probability of a vector biting a human host, p is daily probability of vector survival, n is duration in days of the pathogen extrinsic incubation period (EIP) in the vector, and b is vector ...

Abbreviations and acronyms

“…The VC has shown to be affected by temperature, which impacts biological processes of mosquitoes including their interaction with viruses (Watts et al, 1987;Lambrechts et al, 2011). Chepkorir et al (2014) demonstrated a significantly higher infection rate at high temperatures for mosquitoes collected in Nairobi and Kilifi (Kenya), which is consistent with previous results (Watts et al, 1987).…”

“…aegypti is also a vector of Wuchereria bancrofti and Brugia malayi, both of which cause lymphatic filariasis or elephantiasis (Service, 2012; Consequently, Ae. aegypti has been the subject of numerous vector competence and population genetic studies (Aitken, Downs and Shope, 1977;Gubler et al, 1979;Tabachnick and Powell, 1979;Rosen et al, 1985;Tabachnick et al, 1985;Tardieux et al, 1990;Miller and Mitchell, 1991;Apostol, Reiter and Miller, 1996;Bosio and Beaty, 1998;Vazeille-Falcoz et al, 1999;Bosio, Fulton and Salasek, 2000;Bennett et al, 2002b;Gorrochotegui-Escalante et al, 2002;Mercado-Curiel, Black and Muñoz, 2008;Lozano-Fuentes et al, 2009;Sylla et al, 2009;Lambrechts, 2011;Lambrechts et al, 2011;Guo et al, 2013;Muñoz et al, 2013b;Chepkorir et al, 2014;Diagne et al, 2014;Dickson et al, 2014;Gonçalves et al, 2014;Vega-Rúa et al, 2014).…”

Impact of Climate and Mosquito Vector Abundance on Sylvatic Arbovirus Circulation Dynamics in Senegal

“…Temperature has been shown to directly affect the force of infection for arboviruses by changing the EIP 5 and viral replication rates. 6,7 In general, EIP is inversely associated with temperature, with increasing temperatures leading to shorter EIPs. Lambrechts and others 7 found a moderate association between diurnal temperature range and vector competence for DENV, with larger diurnal temperature range being associated with lower midgut infection and dissemination rates.…”

“…First, the extrinsic incubation period (EIP), defined as the time interval between vector infection and transmission, is influenced by temperature 5 and directly affects the force of infection for DENV. [6][7][8] The EIP for DENV ranges from 15 days at 25 C to 6.5 days at 30 C 9 and from 4 days at 37 to more than 30 days at 18 for YFV. 10 Second, higher temperatures result in higher viral replication of DENV in Aedes.…”

Invasiveness ofAedes aegyptiandAedes albopictusand Vectorial Capacity for Chikungunya Virus

“…Temperature is recognized to have a stronger influence on A. albopictus abundance than precipitation [49], but low rainfall levels may lead to an extinction of the A. albopictus population [50]. In a study that evaluated the impact of diurnal temperature range, A. aegypti lived longer and was more likely to become infected under moderate temperature fluctuations, typical of the high DENV transmission season, than under large temperature fluctuations, typical of the low DENV transmission season [51]. Temperature also may affect critical components of VC, such as mosquito developmental time and consequent population density, survivorship, blood feeding, fecundity, and the EIP.…”