Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes

Aboagye-Antwi, Fred; Guindo, Amadou; Traoré, Amadou S; Hurd, Hilary; Coulibaly, Mamadou B.; Traorè, Sékou F.; Tripet, Frédéric

doi:10.1186/1475-2875-9-243

Cited by 31 publications

(31 citation statements)

References 46 publications

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“…Given that most parasitic infections exert energetic costs to their host vectors [19, 20], with resultant loss of reproductive potential and reduced lifespan [21–25], it is possible that the malaria vector’s quest for increased probing is to meet its own metabolic demands and that of the growing oocyst. Studies on the effect of Plasmodium infection on vector longevity are conflicting, with majority showing vector survival is unaffected, but some showing reduced vector survival [24].…”

Section: Discussionmentioning

confidence: 99%

Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake

et al. 2014

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Summary Plasmodium parasites are known to manipulate the behaviour of their vectors so as to enhance transmission [1–4]. From an evolutionary standpoint, behaviour manipulation by the parasite should expose the vector to limited risk of early mortality while ensuring sufficient energy supply for both it and the vector [5, 6]. However, it is unknown if this vector manipulation also affects vector-plant interaction and sugar uptake. Here, we show that the attraction of Anopheles gambiae s.s. to plant odours increased by 30% and 24% following infection with oocyst- and sporozoite-stages of Plasmodium falciparum respectively, while probing activity increased by 77% and 80% respectively, when the vectors were infected with the two stages of the parasite. Our data also revealed an increased sugar uptake at oocyst-stage which decreased at the sporozoite-stage of infection compared to uninfected An. gambiae, with depletion of lipid reserves at the sporozoite-stage. These results point to a possible physiological adjustment by An. gambiae to P. falciparum infection or behaviour manipulation of An. gambiae by P. falciparum to enhance transmission. We conclude that the nectar seeking behaviour of P. falciparum-infected An. gambiae appears to be modified in a manner governed by the vector’s fight for survival and the parasite’s need to advance its transmission.

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Section: Discussionmentioning

confidence: 99%

Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake

et al. 2014

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“…Aboagye-Antwi et al [47] caught An. gambiae in Mali and studied survival of mosquitoes with or without naturally occurring P. falciparum infections.…”

Section: Discussionmentioning

confidence: 99%

Using infective mosquitoes to challenge monkeys with Plasmodium knowlesi in malaria vaccine studies

Murphy

Weiss

Fryauff

et al. 2014

Malar J

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BackgroundWhen rhesus monkeys (Macaca mulatta) are used to test malaria vaccines, animals are often challenged by the intravenous injection of sporozoites. However, natural exposure to malaria comes via mosquito bite, and antibodies can neutralize sporozoites as they traverse the skin. Thus, intravenous injection may not fairly assess humoral immunity from anti-sporozoite malaria vaccines. To better assess malaria vaccines in rhesus, a method to challenge large numbers of monkeys by mosquito bite was developed.MethodsSeveral species and strains of mosquitoes were tested for their ability to produce Plasmodium knowlesi sporozoites. Donor monkey parasitaemia effects on oocyst and sporozoite numbers and mosquito mortality were documented. Methylparaben added to mosquito feed was tested to improve mosquito survival. To determine the number of bites needed to infect a monkey, animals were exposed to various numbers of P. knowlesi-infected mosquitoes. Finally, P. knowlesi-infected mosquitoes were used to challenge 17 monkeys in a malaria vaccine trial, and the effect of number of infectious bites on monkey parasitaemia was documented.ResultsAnopheles dirus, Anopheles crascens, and Anopheles dirus X (a cross between the two species) produced large numbers of P. knowlesi sporozoites. Mosquito survival to day 14, when sporozoites fill the salivary glands, averaged only 32% when donor monkeys had a parasitaemia above 2%. However, when donor monkey parasitaemia was below 2%, mosquitoes survived twice as well and contained ample sporozoites in their salivary glands. Adding methylparaben to sugar solutions did not improve survival of infected mosquitoes. Plasmodium knowlesi was very infectious, with all monkeys developing blood stage infections if one or more infected mosquitoes successfully fed. There was also a dose-response, with monkeys that received higher numbers of infected mosquito bites developing malaria sooner.ConclusionsAnopheles dirus, An. crascens and a cross between these two species all were excellent vectors for P. knowlesi. High donor monkey parasitaemia was associated with poor mosquito survival. A single infected mosquito bite is likely sufficient to infect a monkey with P. knowlesi. It is possible to efficiently challenge large groups of monkeys by mosquito bite, which will be useful for P. knowlesi vaccine studies.

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“…To our knowledge, however, the existence of a physiological trade-off between fecundity and longevity in mosquitoes has never been formally demonstrated. Indeed, none of the longevity studies reviewed by Ferguson & Read [3] or published since [9][10][11] has measured the effects of Plasmodium on fecundity and longevity in the same individual.…”

Section: Introductionmentioning

confidence: 99%

Plasmodium infection decreases fecundity and increases survival of mosquitoes

et al. 2012

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Long-lived mosquitoes maximize the chances of Plasmodium transmission. Yet, in spite of decades of research, the effect of Plasmodium parasites on mosquito longevity remains highly controversial. On the one hand, many studies report shorter lifespans in infected mosquitoes. On the other hand, parallel (but separate) studies show that Plasmodium reduces fecundity and imply that this is an adaptive strategy of the parasite aimed at redirecting resources towards longevity. No study till date has, however, investigated fecundity and longevity in the same individuals to see whether this prediction holds. In this study, we follow for both fecundity and longevity in Plasmodium-infected and uninfected mosquitoes using a novel, albeit natural, experimental system. We also explore whether the genetic variations that arise through the evolution of insecticide resistance modulate the effect of Plasmodium on these two life-history traits. We show that (i) a reduction in fecundity in Plasmodium-infected mosquitoes is accompanied by an increase in longevity; (ii) this increase in longevity arises through a trade-off between reproduction and survival; and (iii) in insecticide-resistant mosquitoes, the slope of this trade-off is steeper when the mosquito is infected by Plasmodium (cost of insecticide resistance).

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Hydric stress-dependent effects of Plasmodium falciparum infection on the survival of wild-caught Anopheles gambiae female mosquitoes

Cited by 31 publications

References 46 publications

Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake

Plasmodium falciparum Infection Increases Anopheles gambiae Attraction to Nectar Sources and Sugar Uptake

Using infective mosquitoes to challenge monkeys with Plasmodium knowlesi in malaria vaccine studies

Plasmodium infection decreases fecundity and increases survival of mosquitoes

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