Ambient temperature and dietary supplementation interact to shape mosquito vector competence for malaria

Abstract

The extent to which environmental factors influence the ability of Anopheles mosquitoes to transmit malaria parasites remains poorly explored. Environmental variation, such as change in ambient temperature, will not necessarily influence the rates of host and parasite processes equivalently, potentially resulting in complex effects on infection outcomes. As proof of principle, we used Anopheles stephensi and the rodent malaria parasite, Plasmodium yoelii, to examine the effects of a range of constant temperatures on one aspect of host defense (detected as alterations in expression of nitric oxide synthase gene – NOS) to parasite infection. We experimentally boosted mosquito midgut immunity to infection through dietary supplementation with the essential amino acid L-Arginine (L-Arg), which increases midgut NO levels by infection-induced NOS catalysis in A. stephensi. At intermediate temperatures, supplementation reduced oocyst prevalence, oocyst intensity, and sporozoite prevalence suggesting that the outcome of parasite infection was potentially dependent upon the rate of NOS-mediated midgut immunity. At low and high temperature extremes, however, infection was severely constrained irrespective of supplementation. The effects of L-Arg appeared to be mediated by NO-dependent negative feedback on NOS expression, as evidenced by depressed NOS expression in L-Arg treated groups at temperatures where supplementation decreased parasite infection. These results suggest the need to consider the direct (e.g. effects of mosquito body temperature on parasite physiology) and indirect effects (e.g. mediated through changes in mosquito physiology / immunity) of environmental factors on mosquito-malaria interactions in order to understand natural variation in vector competence.

Zika and chikungunya: mosquito‐borne viruses in a changing world

“…[52][53][54][55][56][57][58][59][60][61] Temperature has clear impacts on vector-borne diseases through effects on the insect vectors; mosquitoes are ectotherms and their internal body temperature varies considerably with variation in ambient temperature. Mosquito physiology (e.g., immunity), [62][63][64] life history (e.g., development, survival, reproduction, biting rates), 40,[65][66][67] and arbovirus fitness (e.g., vector competence and extrinsic incubation periods) [68][69][70][71][72] are all directly affected by temperature variation. Future climate change will likely alter the climate conditions that mosquito vectors experience, but it remains unclear how mosquito vectors will respond.…”

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

“…Dependence on the external environment for body temperature control has significant impacts on insect physiological functioning (Chown & Nicolson, 2004) and, subsequently, life‐history traits (Ciota, Matacchiero, Kilpatrick, & Kramer, 2014; Clissold & Simpson, 2015; Lachenicht, Clusella‐Trullas, Boardman, Le Roux, & Terblanche, 2010). Temperature effects may be particularly important when considering the immune system, as responses to temperature variation can have direct consequences for both pathogen infection and host survival (Alto & Bettinardi, 2013; Murdock, Blanford, Luckhart, & Thomas, 2014; Pamminger, Steier, & Tragust, 2016; Pounds et al., 2006; Richards, Anderson, Lord, & Tabachnick, 2012; Wolinska & King, 2009). …”

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

“…This could impact the vectorial capacity of insect vectors of malaria and other pathogens. In [95], it was demonstrated that ambient temperature influences the expression of immune genes that can regulate the intensity of Plasmodium yoelii infection in An. stephensi mosquitoes.…”