Biology subjects

Pigeault, R.

Publications and source records attributed to Pigeault, R..

9 recordsLinked to original sources

bioRxiv2024

Impact of vertebrate host parasitaemia on Plasmodium development within mosquitoes

BackgroundIn vector-borne diseases, invertebrate hosts are exposed to highly variable quantities of parasites during their blood meal. This heterogeneity may partly explain the overdispersed distribution of parasites within the vector population, as well as the variability in the extrinsic incubation period (EIP) of the parasite. Indeed, the quantity of parasites ingested is often considered as a good predictor of the quantity of parasites that will develop within the vectors, as well as the speed at which they will develop (EIP). However, density-dependent processes can strongly influence the relationship between parasite burden in the vertebrate host and in vectors, making this relationship not always clear. MethodsHere, we used the avian malaria system to investigate whether the proportion of red blood cells infected by sexual and/or asexual stages of malaria parasite influences the intensity of malaria infection and the EIP of Plasmodium within the invertebrate vectors. For this purpose, we have experimentally infected twelve vertebrate hosts in order to generate a range of intensity of infection. More than a thousand mosquitoes took a blood meal on these hosts and the development of Plasmodium within the vectors was followed for more than 20 days. ResultsThe main finding presented in this study reveals a negative relationship between the intensity of infection in the vertebrate host and the EIP. Four days were sufficient for 10% of infected mosquitoes fed on the most infected hosts to become infectious. However, the number of transmissible stages did not significantly vary according to the vertebrate host intensity of infection. ConclusionWhile the quantity of ingested parasites had no impact on the density of transmissible stages in infectious mosquitoes, the EIP was affected. Studies have demonstrated that small changes in the EIP can have a significant effect on the number of mosquitoes living long enough to transmit parasites. Here, we observed a difference of 4-6 days in the detection of the first transmissible stages, depending on the intensity of infection of the bitten vertebrate host. Considering that a gonotrophic cycle lasts 3-4 days, the shortened EIP observed here may have significant effects on Plasmodium transmission.

pathology↗

bioRxiv2024

Within-host environmental heterogeneity is associated with phenotypic but not genomic diversity in Wolbachia endosymbionts

The mechanisms underlying within-host diversification in parasite populations are poorly understood. Yet, phenotypic and genotypic variation in parasites can shape their evolutionary trajectories and have important epidemiological consequences. Our aim was to determine whether the constraints associated with infecting different host tissues lead to the emergence and coexistence of multiple parasite sub-populations with distinct phenotypes. We tested this hypothesis using the most widespread bacterial endosymbiont, Wolbachia. We injected Wolbachia bacteria isolated from three tissues of the common pill-bug (Armadillidium vulgare) into uninfected individuals and monitored the growth rate and virulence of each bacterial sub-population in the new hosts. Our results highlight that within-host tissue heterogeneity leads to diverse Wolbachia phenotypes. High-depth genome re-resequencing of Wolbachia sub-populations revealed that this polymorphism was not due to genomic variation but was more likely a result of phenotypic plasticity. Indeed, we found no recurrent tissue-specific genomic variation among infected individuals. Our single nucleotide polymorphism (SNP) filtration pipeline, developed to ensure SNP validity, detected only one substitution. This Wolbachia variant, observed in one female, was present in all three bacterial sub-populations, with frequencies ranging from 24% to 58% depending on the tissue. Overall, our results support the stability of the Wolbachia genome with respect to the rarity of point mutations, in agreement with reports from other symbiotic systems. From a methodological perspective, our study highlights the need for considerable caution when detecting variants in endosymbiont populations, as our conservative approach led us to exclude more than 99.5% of the initially called variants.

evolutionary biology↗

bioRxiv2023

Spring reproductive success influences autumnal malarial load in a passerine bird

Although avian haemosporidian parasites are widely used as model organisms to study fundamental questions in evolutionary and behavorial ecology of host-parasite interactions, some of their basic characteristics, such as seasonal variations in within-host density, are still mostly unknown. In addition, their interplay with host reproductive success in the wild seems to depend on the interaction of many factors, starting with host and parasite species and the temporal scale under study. Here, we monitored the parasitemia of two haemosporidian parasites - Plasmodium relictum (lineage SGS1) and P. homonucleophilum (lineage SW2) - in two wild populations of great tits (Parus major) in Switzerland over three years, to characterize their dynamics. We also collected data on birds reproductive output - laying date, clutch size, fledging success - to determine whether they were associated with parasitemia before (winter), during (spring) and after (autumn) breeding season. Parasitemia of both species dramatically increased in spring, in a way that was correlated to parasitemia in winter. Parasitemia before and during breeding season did not explain reproductive success. However, the birds which fledged the more chicks had higher parasitemia in autumn, which was not associated with their parasitemia in previous spring. Our results tend to indicate that high haemosporidian parasite loads do not impair reproduction in great tits, but high resource allocation into reproduction can leave birds less able to maintain low parasitemia over the following months.

ecology↗

bioRxiv2021

Predator avoidance and foraging for food shape synchrony and response to perturbations in trophic metacommunities

The response of species to perturbations strongly depends on spatial aspects in populations connected by dispersal. Asynchronous fluctuations in biomass among populations lower the risk of simultaneous local extinctions and thus reduce the regional extinction risk. However, dispersal is often seen as passive diffusion that balances species abundance between distant patches, whereas ecological constraints, such as predator avoidance or foraging for food, trigger the movement of individuals. Here, we propose a model in which dispersal rates depend on the abundance of the species interacting with the dispersing species (e.g., prey or predators) to determine how density-dependent dispersal shapes spatial synchrony in trophic metacommunities in response to stochastic perturbations. Thus, unlike those with passive dispersal, this model with density-dependent dispersal bypasses the classic vertical transmission of perturbations due to trophic interactions and deeply alters synchrony patterns. We show that the species with the highest coefficient of variation of biomass governs the dispersal rate of the dispersing species and determines the synchrony of its populations. In addition, we show that this mechanism can be modulated by the relative impact of each species on the growth rate of the dispersing species. Species affected by several constraints disperse to mitigate the strongest constraints (e.g., predation), which does not necessarily experience the highest variations due to perturbations. Our approach can disentangle the joint effects of several factors implied in dispersal and provides a more accurate description of dispersal and its consequences on metacommunity dynamics.

ecology↗

bioRxiv2021

Determinants of haemosporidian single and co-infections risks in western paleartic birds

Co-infections with multiple pathogens are common in the wild and may act as a strong selective pressure on both host and parasite evolution. Yet, contrary to single infection, the factors that shape co-infection risk are largely under-investigated. Here, we explored the extent to which bird ecology and phylogeny impact single and co-infection probabilities by haemosporidian parasites using large datasets from museum collections and a Bayesian phylogenetic modelling framework. While both phylogeny and species attributes (e.g. size of the geographic range, life-history strategy, migration) were relevant predictors of co-infection risk, these factors were less pertinent in predicting the probability of being single infected. Our study suggests that co-infection risk is under a stronger deterministic control than single-infection risk. These results underscore the combined influence of host evolutionary history and species attributes in determining single and co-infection pattern providing new avenues regarding our ability to predict infection risk in the wild.

ecology↗

bioRxiv2020

Gene regulation of the avian malaria parasite Plasmodium relictum, during the different stages within the mosquito vector

The malaria parasite Plasmodium relictum is one of the most widespread species of avian malaria. As is the case in its human counterparts, bird Plasmodium undergoes a complex life cycle infecting two hosts: the arthropod vector and the vertebrate host. In this study, we examine the transcriptome of P. relictum (SGS1) during crucial timepoints within its natural vector, Culex pipiens quinquefasciatus. Differential gene-expression analyses identified genes linked to the parasites life-stages at: i) a few minutes after the blood meal is ingested, ii) during peak oocyst production phase, iii) during peak sporozoite phase and iv) during the late-stages of the infection. A large amount of genes coding for functions linked to host-immune invasion and multifunctional genes was active throughout the infection cycle. One gene associated with a conserved Plasmodium membrane protein with unknown function was upregulated throughout the parasite development in the vector, suggesting an important role in the successful completion of the sporogonic cycle. Transcript annotation further revealed novel genes, which were significantly differentially expressed during the infection in the vector as well as upregulation of reticulocyte-binding proteins, which raises the possibility of the multifunctionality of these RBPs. We establish the existence of highly stage-specific pathways being overexpressed during the infection. This first study of gene-expression of a non-human Plasmodium species in its natural vector provides a comprehensive insight into the molecular mechanisms of the common avian malaria parasite P. relictum and provides essential information on the evolutionary diversity in gene regulation of the Plasmodiums vector stages.

evolutionary biology↗

bioRxiv2020

Last-come, best served? Mosquito biting order and Plasmodium transmission

A pervasive characteristic of malaria parasite infection in mosquito vector populations is their tendency to be overdispersed. Understanding the mechanisms underlying the overdispersed distribution of parasites is of key importance as it may drastically impact the transmission dynamics of the pathogen. The small fraction of heavily infected individuals might serve as superspreaders and cause a disproportionate number of subsequent infections. Although multiple factors ranging from environmental stochasticity to inter-individual heterogeneity may explain parasite overdispersion, Plasmodium infection has also been observed to be highly overdispersed in inbred mosquito population maintained under standardized laboratory conditions, suggesting that other mechanisms may be at play. Here, we show that the aggregated distribution of Plasmodium within mosquito vectors is partially explained by a temporal heterogeneity in parasite infectivity triggered by the bites of blood-feeding mosquitoes. Several experimental blocks carried out with three different Plasmodium isolates have consistently shown that the transmission of the parasite increases progressively with the order of mosquito bites. Surprisingly the increase in transmission is not associated with an increase in Plasmodium replication rate or higher investment in the production of the transmissible stage (gametocyte). Adjustment of the physiological state of the gametocytes could be, however, an adaptive strategy to respond promptly to mosquito bites. Overall our data show that malaria parasite appears to be able to respond to the bites of mosquitoes to increase its own transmission at a much faster pace than initially thought (hours rather than days). Further work needs to be carried out to elucidate whether these two strategies are complementary and, particularly, what are their respective underlaying mechanisms. Understanding the processes underlying the temporal fluctuations in Plasmodium infectivity throughout vertebrate host-to-mosquito transmission is essential and could lead to the development of new approaches to control malaria transmission. Author summaryPlasmodium parasites are known for being the etiological agents of malaria and for the devastating effects they cause on human populations. A pervasive characteristic of Plasmodium infection is their tendency to be overdispersed in mosquito vector populations: the majority of mosquitoes tend to harbour few or no parasites while a few individuals harbor the vast majority of the parasite population. Understanding the mechanisms underlying Plasmodium overdispersed distribution is of key importance as it may drastically impact the transmission dynamics of the pathogen. Here, we show that the aggregated distribution of Plasmodium parasites within mosquito vectors is partially explained by a temporal heterogeneity in Plasmodium infectivity triggered by the bites of blood-feeding mosquitoes. In other words, mosquitoes that bite at the beginning of a 3h feeding session have significantly fewer parasites than those that bite towards the end. Malaria parasite is therefore capable of responding to the bites of mosquitoes to increase its own transmission at a much faster pace than thought (hours rather than days). Understanding the processes underlying the temporal fluctuations in Plasmodium infectivity throughout vertebrate host-to-mosquito transmission is essential and could lead to the development of new approaches to control malaria transmission.

microbiology↗

bioRxiv2019

Opening Pandora’s Box: Distribution of Plasmodium gametocytes in bloodstream

Malaria, a vector borne disease caused by Plasmodium spp., remains a major global cause of morbidity and mortality. Optimization of the disease control strategies requires a thorough understanding of the fundamental processes underlying parasite transmission. Although the number of transmissible stages of Plasmodium (gametocyte) in human blood is frequently used as an indicator of human-to-mosquito transmission potential, this relationship is not always clear. Important efforts have been made to develop molecular tools to fine-tune gametocyte densities estimation and therefore improve the prediction of mosquito infection rates, but a significant level of uncertainty around this estimate remains. Here we show with both human and avian malaria system that the within-vertebrate host distribution of gametocytes could explain much of this uncertainty. By comparing gametocyte densities in bloodstream between different body parts, we found a difference by nearly 50% in humans and by more than 15% in birds. An estimation of gametocyte density from only one blood sample, as is usually the case, could therefore drastically over- or underestimated the infectivity of gametocyte carriers. This might have important consequences on the epidemiology of the disease since we show, using the avian malaria system, that this variation influences the transmission of the parasite to the mosquito vector. In the light of our results, we argue that it is essential to consider the heterogeneous distribution of gametocyte to improve human diagnosis, identify infectious reservoirs and to test new malaria control strategies.

evolutionary biology↗

bioRxiv2018

Timing malaria transmission with mosquito fluctuations

Temporal variations in the activity of arthropod vectors can dramatically affect the epidemiology and evolution of vector-borne pathogens. Here we explore the \"Hawking hypothesis\" stating that these pathogens may evolve the ability to time investment in transmission to match the activity of their vectors. First, we use a theoretical model to identify the conditions promoting the evolution of time-varying transmission strategies in pathogens. Second, we experimentally test the \"Hawking hypothesis\" by monitoring the within-host dynamics of Plasmodium relictum throughout the acute and the chronic phases of the bird infection. To explore the periodicity in the host parasite density, we develop a new methodology to correct for non-stationarities in the host parasitaemia. We detect a periodic increase of parasitaemia and mosquito infection in the late afternoon that coincides with an increase in the biting activity of its natural vector. We also detect a positive effect of mosquito bites on Plasmodium replication in the birds both in the acute and in the chronic phases of the infection. This study highlights that Plasmodium parasites use two different strategies to increase the match between transmission potential and vector availability. We discuss the adaptive nature of these unconditional and plastic transmission strategies with respect to the time-scale and the predictability of the fluctuations in the activity of the vector.\n\nImpact SummarySeasonal and daily fluctuations in the environment affect the abundance and the activity of vectors and may therefore have profound consequences on the transmission of infectious diseases. Here we show that, in accord with evolutionary theory, malaria parasites have evolved two different and complementary strategies to cope with fluctuations in mosquito availability. First, Plasmodium relictum adopts an unconditional strategy whereby within-host parasitaemia and mosquito infection increases in the afternoon and in the evening, when its vector, the Culex pipiens mosquito, is most active. Second, we find evidence for a plastic strategy allowing the parasitaemia to rapidly increase after exposure to mosquito bites.

evolutionary biology↗