Exposure of the mosquito vector Culex pipiens to the malaria parasite Plasmodium relictum: effect of infected blood intake on immune and antioxidant defences, fecundity and survival

Abstract

BackgroundThe intake of a Plasmodium-infected blood meal may affect mosquito physiology and a series of trade-offs may occur, in particular between immune defences, reproduction and self-maintenance. We evaluated the cost of exposure to Plasmodium in the mosquito vector by investigating the effect of exposure on fecundity and survival and the implication of immune and antioxidant defences in mediating this cost.MethodsWe used the natural Culex pipiens-Plasmodium relictum association. We exposed female mosquitoes to increasing levels of parasites by allowing them to feed either on uninfected canaries, Serinus canaria, (unexposed mosquitoes) or on infected canaries with low (low exposure) or high (high exposure) parasitaemia. We recorded blood meal size, fecundity (laying probability and clutch size) and survival. We quantified the expression of genes involved in immune and antioxidant defences (nitric oxide synthase, NOS; superoxide dismutase, SOD; glucose-6-phosphate dehydrogenase, G6PDH).ResultsWe found that the laying probability of exposed females decreased with increasing exposure to the parasite and with increasing SOD expression. Clutch size of exposed females was higher compared to unexposed ones for similar blood meal size and was positively correlated to the NOS expression. We found no effect of exposure on survival. After blood meal intake, SOD increased in the three groups, NOS increased in exposed females and G6PDH increased in highly exposed females only.ConclusionsOur results illustrated a trade-off between fight against the parasite and reproduction and a cost of exposure which might be mediated by the investment in immune and/or antioxidant defences. They also showed that this trade-off could lead to opposed outcome, potentially depending on the vector physiological status. Finally, they highlighted that the ingestion of a Plasmodium-infected blood meal may affect mosquito life history traits in a complex way.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-016-1905-7) contains supplementary material, which is available to authorized users.

Long-term pathogenic response to Plasmodium relictum infection in Culex pipiens mosquito

“…In accordance with previous studies in several malaria systems [ 9 , 10 , 15 , 16 ] but see [ 18 ], we observed a negative impact of Plasmodium on mosquito fecundity in the first GC following an infected blood meal. However, the cost payed by infected females was relatively low ( Fig 2 ).…”

“…Although the Plasmodium effect on fecundity has been studied in many mosquito/parasite systems [ 9 , 10 , 15 , 16 ], most articles have focused only on the first gonotrophic cycle which is defined as a blood meal followed by an oviposition event [ 6 , 7 , 9 – 11 , 17 , 18 ]. However, during their lifetime, female mosquitoes take several blood meals, which raises the question of whether they may be able to compensate the fecundity costs induced by an infected blood meal during the following gonotrophic cycles.…”

The effect of dietary antioxidant supplementation in a vertebrate host on the infection dynamics and transmission of avian malaria to the vector

“…Vertebrates can be dead end hosts for Plasmodium parasites if the parasites are not transmitted to a vector in which they undergo their sexual reproduction (Valkiunas 2005 ). The parasite intensity in the blood has been shown to affect life history traits of vectors (Delhaye et al 2016b ) and has been associated to the transmission probability to the vector, measured as oocyst prevalence and oocyst burden (Vezilier et al 2010 ; Pigeault et al 2015 ). It has also been shown that oocyst prevalence and oocyst burden depend on mosquito blood meal size (Pigeault et al 2015 ).…”

Enhanced Attraction of Arthropod Vectors to Infected Vertebrates: A Review of Empirical Evidence

“…Using lab-bred Culex pipiens and Plasmodium relictum, infection was shown to decrease mosquito fecundity (Vézilier et al, 2012;Pigeault and Villa, 2018) and to increase their survival under ad libitum food conditions (Vézilier et al, 2012). On the opposite, using mosquitoes reared from egg rafts collected in the field, the same infection was shown to slightly increase fecundity (Delhaye et al, 2016) and to decrease survival under a food restriction regime (Lalubin et al, 2014). Independently of the systems used, most of these studies did not find an effect of the infection on host longevity when food was given ad libitum (Lalubin et al, 2014;Delhaye et al, 2016;Pigeault and Villa, 2018).…”

“…On the opposite, using mosquitoes reared from egg rafts collected in the field, the same infection was shown to slightly increase fecundity (Delhaye et al, 2016) and to decrease survival under a food restriction regime (Lalubin et al, 2014). Independently of the systems used, most of these studies did not find an effect of the infection on host longevity when food was given ad libitum (Lalubin et al, 2014;Delhaye et al, 2016;Pigeault and Villa, 2018). Moreover, Plasmodium falciparum increases fecundity and do not reduce survival in Anopheles gambiae (Alout et al, 2016).…”