Complex effects of temperature on mosquito immune function

Abstract

Over the last 20 years, ecological immunology has provided much insight into how environmental factors shape host immunity and host–parasite interactions. Currently, the application of this thinking to the study of mosquito immunology has been limited. Mechanistic investigations are nearly always conducted under one set of conditions, yet vectors and parasites associate in a variable world. We highlight how environmental temperature shapes cellular and humoral immune responses (melanization, phagocytosis and transcription of immune genes) in the malaria vector, Anopheles stephensi. Nitric oxide synthase expression peaked at 30°C, cecropin expression showed no main effect of temperature and humoral melanization, and phagocytosis and defensin expression peaked around 18°C. Further, immune responses did not simply scale with temperature, but showed complex interactions between temperature, time and nature of immune challenge. Thus, immune patterns observed under one set of conditions provide little basis for predicting patterns under even marginally different conditions. These quantitative and qualitative effects of temperature have largely been overlooked in vector biology but have significant implications for extrapolating natural/transgenic resistance mechanisms from laboratory to field and for the efficacy of various vector control tools.

Responses to a warming world: Integrating life history, immune investment, and pathogen resistance in a model insect species

“…Based on previous studies (Bauerfeind & Fischer, 2014; Murdock et al., 2012; Triggs & Knell, 2012), hemocyte density was expected to decrease at the higher temperature treatments. Instead, we saw numbers increase linearly with increasing temperature, something that has previously only been shown in Plodia when larvae are under additional environmental stressors (Triggs & Knell, 2012).…”

“…While increasing temperature tends to increase the rate of biochemical processes, this does not necessarily extend to all aspects of physiology, and increasing temperature may not positively correlate with improved immune competence (Angilletta, Huey, & Frazier, 2010; Murdock et al., 2012; Suwanchaichinda & Paskewitz, 1998). …”

Genetic and phenotypic relationships between immune defense, melanism and life-history traits at different temperatures and sexes in Tenebrio molitor

“…Effects of temperature on immune and life-history traits Previous studies both from evolutionary ecology and biological pest control have, in general, shown that even a modest rise in temperature makes the hosts more resistant to infections by microbes and parasites (Thomas andBlanford, 2003, Adamo andLovett, 2011), although the response is not necessarily linear, highlighting the significance of measurements done in a range of temperatures (Murdock et al, 2012). In our study, the encapsulation responses of beetles reared at 18 1C were the highest, and the encapsulation ability was the lowest at the highest temperature.…”

Climate, environmental and socio-economic change: weighing up the balance in vector-borne disease transmission

“…Temperature has been shown to affect immune responses in a variety of insects, including beetles, crickets, butterflies and Drosophila (fruit flies). Focusing on mosquito vectors, a few studies have investigated the effect of temperature on mosquito immune responses; Suwanchaichinda & Paskewitz [93] showed that the melanization response in Anopheles gambiae progressively decreases as temperatures increase, while Murdock et al [94] investigated the response of cellular and humoral immunity to changes in temperature. In the latter study, a complex picture emerged, with melanization, phagocytosis and an antimicrobial peptide (AMP) defensin expression peaking at 188C, whereas nitric oxide synthase expression peaked at 308C.…”

“…B 370: 20130551 response to changes in ambient temperature. The study in reference [94] demonstrates how the immune gene profile of a vector at one ambient temperature can be completely altered at a different temperature. This could impact the vectorial capacity of insect vectors of malaria and other pathogens.…”