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Transgenerational effect of infection in Plasmodium-infected mosquitoes.

ABSTRACT: Transgenerational effects of infection have a huge potential to influence the prevalence and intensity of infections in vectors and, by extension, disease epidemiology. These transgenerational effects may increase the fitness of offspring through the transfer of protective immune factors. Alternatively, however, infected mothers may transfer the costs of infection to their offspring. Although transgenerational immune protection has been described in a dozen invertebrate species, we still lack a complete picture of the incidence and importance of transgenerational effects of infection in most invertebrate groups. The existence of transgenerational infection effects in mosquito vectors is of particular interest because of their potential for influencing parasite prevalence and intensity and, by extension, disease transmission. Here we present what we believe to be the first study on transgenerational infection effects in a mosquito vector infected with malaria parasites. The aim of this experiment was to quantify both the benefits and the costs of having an infected mother. We find no evidence of transgenerational protection in response to a Plasmodium infection. Having an infected mother does, however, entail considerable fecundity costs for the offspring: fecundity loss is three times higher in infected offspring issued from infected mothers than in infected offspring issued from uninfected mothers. We discuss the implications of our results and we call for more studies looking at transgenerational effects of infection in disease vectors.

SUBMITTER: Pigeault R

PROVIDER: S-EPMC4387496 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Transgenerational effect of infection in Plasmodium-infected mosquitoes.

Pigeault R R Vézilier J J Nicot A A Gandon S S Rivero A A

Biology letters 20150301 3

Transgenerational effects of infection have a huge potential to influence the prevalence and intensity of infections in vectors and, by extension, disease epidemiology. These transgenerational effects may increase the fitness of offspring through the transfer of protective immune factors. Alternatively, however, infected mothers may transfer the costs of infection to their offspring. Although transgenerational immune protection has been described in a dozen invertebrate species, we still lack a ...[more]

PMID: 25762571

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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:In vitro studies of sexual blood stages of the most fatal malaria species, Plasmodium falciparum, have revealed key processes by which gametocytes develop and transmit infection from humans to anopheline mosquitoes. However, most malaria cases outside sub-Saharan Africa are caused by other Plasmodium spp., frequently Plasmodium vivax and Plasmodium knowlesi, a zoonotic parasite of macaque monkeys. Gametocytes of P. vivax and P. knowlesi exhibit distinct morphology, faster development, and a shorter life span compared with gametocytes of P. falciparum, reflecting the evolutionary separation and biological differences of these species. Unlike P. falciparum, P. vivax cannot be cultivated in vitro, necessitating access to infected primates for laboratory studies. In contrast, P. knowlesi asexual stages have been successfully adapted to cultures in macaque and human red blood cells, but these stages have not been reported to produce gametocytes infective to mosquitoes. Here, we show that gametocyte production and sporadic, low-level mosquito infectivity of a P. knowlesi strain was not improved by application of a "crash" method commonly used to induce gametocytes in P. falciparum cultures. However, Percoll-gradient purified schizonts from this strain yielded highly synchronised populations that, in three of six experiments, produced infections at an average rate of 0.97-9.1 oocysts in Anopheles dirus mosquitoes. Oocyst counts were most abundant in mosquitoes that were fed from the synchronised cultures 36 h after schizont purification. Gametocytes in these cultures occurred at low prevalence and were difficult to observe. Transcription from orthologs of P. falciparum gametocyte-specific markers did not correlate with infectivity of the P. knowlesi parasites to mosquitoes. The ability to infect mosquitoes from in vitro-cultivated P. knowlesi will support research on the unique features of this emerging pathogen and facilitate comparative studies of transmission by the different human malarias.

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Transgenerational effect of infection in Plasmodium-infected mosquitoes.

Publications

Transgenerational effect of infection in Plasmodium-infected mosquitoes.

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