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.

Philippe Christe,Olivier Glaizot,Jessica Delhaye,Consolée Aletti

doi:10.1186/s13071-016-1905-7

Philippe Christe, Olivier Glaizot + Show 2 more

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https://doi.org/10.1186/s13071-016-1905-7

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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.

Highlights

The 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
Laying probability increased with blood meal size (Table 2, Fig. 1) and tended to decrease with increasing exposure level (P = 0.064): females under high exposure had lower probability to lay than females under low exposure (P = 0.010) but there was a marginally significant difference between females under high exposure and unexposed females due to higher variation in the unexposed group (P = 0.066, Table 2, Fig. 2a)
Even though our data do not provide a terminal measurement of reproductive success of the females and do not allow us to conclude about the underlying mechanism, these results showed a positive link between investment in immune defences and fecundity

Summary

Introduction

The 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. Exposure is associated with vitellogenesis disruption, apoptosis and egg resorption in the ovaries [11, 29,30,31,32] that can lead to delayed reproduction and/or decreased fecundity [33] This highlights a second trade-off between fight against the parasite and reproduction [34]. This trade-off has been suggested to originate from the amino acid (arginine) requirement needed for both immune response [21] and egg production [35] It may originate from the antioxidant requirement needed for both self-maintenance during the fight against the parasite and reproduction. Following the intake of a Plasmodium-infected blood meal, mosquitoes should suffer costs from the exposure even if the parasite does not develop

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