Dataset Information

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

ABSTRACT: The transmission of Plasmodium within a vertebrate host population is strongly associated with the life history traits of its vector. Therefore the effect of malaria infection on mosquito fecundity and longevity has traditionally received a lot of attention. Several species of malaria parasites reduce mosquito fecundity, nevertheless almost all of the studies have focused only on the first gonotrophic cycle. Yet, during their lifetime, female mosquitoes go through several gonotrophic cycles, which raises the question of whether they are able to compensate the fecundity costs induced by the parasite. The impact of Plasmodium infection on female longevity is not so clear and has produced conflicting results. Here we measured the impact of Plasmodium relictum on its vector's longevity and fecundity during three consecutive gonotrophic cycles. In accordance with previous studies, we observed a negative impact of Plasmodium infection on mosquito (Culex pipiens) fecundity in the first gonotrophic cycle. Interestingly, despite having taken two subsequent uninfected blood meals, the negative impact of malaria parasite persisted. Nevertheless no impact of infection on mosquito longevity was observed. Our results are not in line with the hypothesis that the reduction of fecundity observed in infected mosquitoes is an adaptive strategy of Plasmodium to increase the longevity of its vector. We discuss the different underlying mechanisms that may explain our results.

SUBMITTER: Pigeault R

PROVIDER: S-EPMC5798818 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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

Pigeault Romain R Villa Manon M

PloS one 20180205 2

The transmission of Plasmodium within a vertebrate host population is strongly associated with the life history traits of its vector. Therefore the effect of malaria infection on mosquito fecundity and longevity has traditionally received a lot of attention. Several species of malaria parasites reduce mosquito fecundity, nevertheless almost all of the studies have focused only on the first gonotrophic cycle. Yet, during their lifetime, female mosquitoes go through several gonotrophic cycles, whi ...[more]

PMID: 29401525

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Project description:BACKGROUND: The control of most vectors of malaria is threatened by the spread of insecticide resistance. One factor that has been hitherto largely overlooked is the potential effects of insecticide resistance on the ability of mosquitoes to transmit malaria: are insecticide-resistant mosquitoes as good vectors of Plasmodium as susceptible ones? The drastic physiological changes that accompany the evolution of insecticide resistance may indeed alter the ability of vectors to transmit diseases, a possibility that, if confirmed, could have major epidemiological consequences. METHODS: Using a novel experimental system consisting of the avian malaria parasite (Plasmodium relictum) and its natural vector (the mosquito Culex pipiens), two of the most common mechanisms of insecticide resistance (esterase overproduction and acetylcholinesterase modification) were investigated for their effect on mosquito infection rate and parasite burden. For this purpose two types of experiments were carried out using (i) insecticide-resistant and susceptible laboratory isogenic lines of Cx. pipiens and (ii) wild Cx. pipiens collected from a population where insecticide resistant and susceptible mosquitoes coexist in sympatry. RESULTS: The isogenic line and wild-caught mosquito experiments were highly consistent in showing no effect of either esterase overproduction or of acetylcholinesterase modification on either the infection rate or on the oocyst burden of mosquitoes. The only determinant of these traits was blood meal size, which was similar across the different insecticide resistant categories in both experiments. CONCLUSIONS: Insecticide resistance was found to have no effect on Plasmodium development within the mosquito. This is the first time this question has been addressed using a natural mosquito-Plasmodium combination, while taking care to standardize the genetic background against which the insecticide resistance genes operate. Infection rate and oocyst burden are but two of the factors that determine the vectorial capacity of mosquitoes. Other key determinants of parasite transmission, such as mosquito longevity and behaviour, or the parasite's incubation time, need to be investigated before concluding on whether insecticide resistance influences the ability of mosquitoes to transmit malaria.

Project description:BackgroundPlasmodium parasites that cause bird malaria occur in all continents except Antarctica and are primarily transmitted by mosquitoes in the genus Culex. Culex quinquefasciatus, the mosquito vector of avian malaria in Hawai'i, became established in the islands in the 1820s. While the deadly effects of malaria on endemic bird species have been documented for many decades, vector-parasite interactions in avian malaria systems are relatively understudied.MethodsTo evaluate the gene expression response of mosquitoes exposed to a Plasmodium infection intensity known to occur naturally in Hawai'i, offspring of wild-collected Hawaiian Cx. quinquefasciatus were fed on a domestic canary infected with a fresh isolate of Plasmodium relictum GRW4 from a wild-caught Hawaiian honeycreeper. Control mosquitoes were fed on an uninfected canary. Transcriptomes of five infected and three uninfected individual mosquitoes were sequenced at each of three stages of the parasite life cycle: 24 h post feeding (hpf) during ookinete invasion; 5 days post feeding (dpf) when oocysts are developing; 10 dpf when sporozoites are released and invade the salivary glands.ResultsDifferential gene expression analyses showed that during ookinete invasion (24 hpf), genes related to oxidoreductase activity and galactose catabolism had lower expression levels in infected mosquitoes compared to controls. Oocyst development (5 dpf) was associated with reduced expression of a gene with a predicted innate immune function. At 10 dpf, infected mosquitoes had reduced expression levels of a serine protease inhibitor, and further studies should assess its role as a Plasmodium agonist in C. quinquefasciatus. Overall, the differential gene expression response of Hawaiian Culex exposed to a Plasmodium infection intensity known to occur naturally in Hawai'i was low, but more pronounced during ookinete invasion.ConclusionsThis is the first analysis of the transcriptional responses of vectors to malaria parasites in non-mammalian systems. Interestingly, few similarities were found between the response of Culex infected with a bird Plasmodium and those reported in Anopheles infected with human Plasmodium. The relatively small transcriptional changes observed in mosquito genes related to immune response and nutrient metabolism support conclusions of low fitness costs often documented in experimental challenges of Culex with avian Plasmodium.

Project description:BackgroundParasites are recognized for their ability to modify host physiology and behaviours in ways that increase parasite fitness. Protozoan parasites of the genus Plasmodium are a group of widespread vector-borne parasites of vertebrates, causing disease to a wide range of hosts, but most notably to human and avian hosts.MethodsThe hypothesis that infection with the avian malaria, Plasmodium relictum (GRW4 lineage) impacts flight activity in one of their natural vectors, Culex quinquefasciatus, was tested using both parasites and mosquitoes colonized from local populations in East-Central Texas, USA. Groups of Cx. quinquefasciatus were allowed to feed directly on canaries with active P. relictum infections and control canaries with no P. relictum exposure history. Additionally, how P. relictum sporozoite invasion of mosquito salivary glands impacts mosquito flight activity behaviour was tested using a Locomotor Activity Monitor for both control and infected females. Generalized linear mixed models were used to evaluate the influence of infection status on the response variables of flight activity (continuous) and probability of flight occurring (binomial).ResultsInfection status was a significant predictor of flight activity and flight probability and interactions between infection status and experimental period of infection as well as infection status and dusk were statistically significant predictors of flight activity. Plasmodium relictum infected mosquitoes had a mean flight activity of 3.10 and control mosquitoes had an overall mean flight activity of 3.13.DiscussionBased on these results, avian malaria parasites increase the flight activity of these mosquitoes at hours known for peak host-seeking behaviour but decrease overall diel activity.ConclusionAlthough the ramifications of this behavioural change for P. relictum transmission are unclear, these results provide additional empirical evidence suggesting that avian malaria can influence mosquito behaviour and modulate transmission potential.

Dataset Information

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

Publications

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

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