Evidence for carry-over effects of predator exposure on pathogen transmission potential (original) (raw)
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ABSTRACTThe transmission of malaria parasites from mosquito to human is largely determined by the dietary specialization ofAnophelesmosquitoes to feed on humans. Few studies have explored the impact of blood meal sources on the fitness of both the parasite and the mosquito. Our study investigated the effects of 3-4 consecutive blood meals from one of four vertebrate species (human, cattle, sheep, or chicken) on several fitness traits, including mosquito feeding rate, blood meal size, susceptibility to wild isolates ofPlasmodium falciparum, survival, fecundity, F1 offspring development time, and size. Our findings revealed no significant effect on parasite development. Similarly, parasite exposure had no overall effects on mosquito fitness. However, blood meal type did have a strong impact on mosquito feeding rate, survival, lifetime fecundity, and offspring size. Specifically, mosquitoes that were fed successive chicken blood meals produced fewer eggs and fewer and smaller F1 adults...
Freshwater Biology, 2014
1. Predators can directly and indirectly influence host-parasite interactions by consuming infected individuals, by removing infectious parasite stages and by changing host traits (e.g. behaviour). Because such effects can affect infection positively or negatively, understanding the net effects of predation on pathogen transmission under natural conditions is important. 2. We conducted a mesocosm experiment to examine the effects of predators on interactions between tadpole hosts (Pseudacris regilla) and trematode parasites (Ribeiroia ondatrae). We manipulated the presence of (non-lethal, i.e., caged) predators of tadpoles (dragonfly larvae) and (potentially lethal) parasite predators (damselfly larvae) to evaluate their individual and combined effects on host infection. We expected that dragonflies would reduce tadpole activity and thereby increase parasite infection through a reduction in antiparasite behaviour. Because damselflies can consume parasites in the laboratory, we predicted that damselflies would lower infection by consuming parasites before they infected tadpoles. Our goal was to evaluate the net consequences of these predator-mediated effects for host/prey infection. 3. The presence of caged dragonflies reduced tadpole activity, resulting in a~50% increase in average infection load compared to treatments without predators. In contrast to our prediction that damselflies would reduce infection, damselflies elicited behavioural and morphological changes in hosts similar to dragonflies, with a comparable increase in parasite transmission. Thus, predatormediated effects were evident predominantly through changes in host/prey behaviour, rather than through changes in the abundance of parasites. The lack of a direct effect of predators on infection (i.e. via consumption of parasites) could be the result of the presence of alternative prey (zooplankton) or a mismatch in timing between visual predators feeding during the day and parasites released from the first intermediate host and infecting amphibians at night. 4. The presence of predators also stimulated morphological defences in their tadpole prey, including increased tail and body depth. Interestingly, we found that parasite infection also induced morphological changes in tadpole tail and body depth, similar to changes produced by (non-lethal) cues from predators. Parasites caused malformations in tadpoles, but there were no effects on tadpole growth or development from either parasites or predators. 5. This research has key implications for linking predation and infectious disease in aquatic ecosystems. Our results emphasise the importance of indirect effects of predators on infection and highlight possible trade-offs in mitigating the concurrent risks of predation and disease. Parasites can also alter host morphology through trait-mediated effects similar to predators, supporting a broader inclusion of parasites in the study of the ecology of natural enemies.
Co-evolution between mosquitoes and microsporidian transmission strategies
2021
Parasite and host impose strong selection on each other. The first causes damages and mortality to the host, while the second responds by reducing the detrimental effects and the intensity and/or success of infection. The resulting co-evolutionary dynamics are profoundly affected by the ecological conditions, for these may influence many aspects of host-parasite interactions including life history evolution, virulence and transmission. It is therefore essential to study and incorporate environmental variation in the field of parasitology to gain an exhaustive understanding of how host and parasite evolve. In this thesis, a single generation and an evolutionary experimental approach were used to investigate the impact of the ecological and epidemiological conditions on several aspects of host-parasite interactions, with the main focus on parasite transmission strategies. Firstly, it was examined the effect of the availability of resources for the host, timing of infection, and co-infection on the virulence and transmission success of two parasites with conflicting transmission strategy. Next, it was tested how the environment influenced the trade-off between vertical and horizontal transmission in a parasite with a mixed mode of transmission and it was assessed the genetic contribution of the host to its transmission mode. Whether the vertical and horizontal component of this parasite and the associated virulence responded to restriction opportunities, represented by different availability of resources over several generations, was investigated with an evolutionary experiment. Finally, the presence of a plastically parasite-induced response on the recombination rate of the host as a potential crossgenerational defence mechanism was explored. The experiments cover many key aspects of hostparasite interactions and emphasize the role of the ecological conditions on shaping these relationships. The results and their implications are discussed in detail throughout the thesis. Overall, this work highlights the dependence of crucial aspects of host-parasite interactions from the epidemiological and ecological conditions. Disentangling the various forces surrounding these interactions may help us to acquire a better knowledge of how a changing environment may drive the evolution of both host and parasite.
Larval nutritional stress affects vector life history traits and human malaria transmission
Scientific reports, 2016
Exposure to stress during an insect's larval development can have carry-over effects on adult life history traits and susceptibility to pathogens. We investigated the effects of larval nutritional stress for the first time using field mosquito vectors and malaria parasites. In contrast to previous studies, we show that larval nutritional stress may affect human to mosquito transmission antagonistically: nutritionally deprived larvae showed lower parasite prevalence for only one gametocyte carrier; they also had lower fecundity. However, they had greater survival rates that were even higher when infected. When combining these opposing effects into epidemiological models, we show that larval nutritional stress induced a decrease in malaria transmission at low mosquito densities and an increase in transmission at high mosquito densities, whereas transmission by mosquitoes from well-fed larvae was stable. Our work underscores the importance of including environmental stressors towar...
Avian malaria infection intensity influences mosquito feeding patterns
International journal for parasitology, 2017
Pathogen-induced host phenotypic changes are widespread phenomena that can dramatically influence host-vector interactions. Enhanced vector attraction to infected hosts has been reported in a variety of host-pathogen systems, and has given rise to the parasite manipulation hypothesis whereby pathogens may adaptively modify host phenotypes to increase transmission from host to host. However, host phenotypic changes do not always favour the transmission of pathogens, as random host choice, reduced host attractiveness and even host avoidance after infection have also been reported. Thus, the effects of hosts' parasitic infections on vector feeding behaviour and on the likelihood of parasite transmission remain unclear. Here, we experimentally tested how host infection status and infection intensity with avian Plasmodium affect mosquito feeding patterns in house sparrows (Passer domesticus). In separate experiments, mosquitoes were allowed to bite pairs containing (i) one infected a...
Ecology and evolutionary implications of malaria parasite virulence in mosquito vectors
2002
I Chapter 1: General introduction 4 1.1 Why study parasites?' 4 1.2 Importance of parasites in nature 4 1.3 Parasites and evolution 5 1.4 Evolution of virulence 6 1.5 Evolution and epidemiology of vector-borne disease 9 1.6 Malaria: natural history and epidemiology 11 1.6.1 Plasmodium life cycle 12 1.6.2 Anopheles life cycle 13 1.6.3 Epidemiology 13 1.7 Evolution of virulence in malaria 14 1.7.1 Vertebrate host mortality 16 1.7.2 Vertebrate host morbidity 17 1.7.3 Vertebrate host genotype 17 1.7.4 Vector fitness 18 1.8 Experimental system 19 1.8.1 The parasite 20 1.8.2 The vertebrate host 20 1.8.3 The vector 21 1.8.4 Generality of the model system 22 1.9 Thesis aims and overview 24 Chapter 2: What is the general impact of malaria parasites on mosquito survival? 26 2.1 Summary 26 2.2 Introduction 26 2.3 Methods 28 2.4 Results 33 2.4.1 Overall effect 33 2.4.2 Choice of species 35 2.4.3 Length of study 36 2.4.4 Dose effects 37 2.4.5 Environmental conditions 38 2.4.6 Choice of contr...
Predator diversity, intraguild predation, and indirect effects drive parasite transmission
Proceedings of the National Academy of Sciences of the United States of America, 2015
Humans are altering biodiversity globally and infectious diseases are on the rise; thus, there is interest in understanding how changes to biodiversity affect disease. Here, we explore how predator diversity shapes parasite transmission. In a mesocosm experiment that manipulated predator (larval dragonflies and damselflies) density and diversity, non-intraguild (non-IG) predators that only consume free-living cercariae (parasitic trematodes) reduced metacercarial infections in tadpoles, whereas intraguild (IG) predators that consume both parasites and tadpole hosts did not. This likely occurred because IG predators reduced tadpole densities and anticercarial behaviors, increasing per capita exposure rates of the surviving tadpoles (i.e., via density- and trait-mediated effects) despite the consumption of parasites. A mathematical model demonstrated that non-IG predators reduce macroparasite infections, but IG predation weakens this "dilution effect" and can even amplify pa...
Frontiers in Ecology and Evolution, 2015
Previous studies have shown that Plasmodium parasites can manipulate mosquito feeding behaviors such as motivation and avidity to feed on vertebrate hosts, in ways that increase the probability of parasite transmission. These studies, however, have been mainly carried out on non-natural and/or laboratory based model systems and hence may not reflect what occurs in the field. We now need to move closer to the natural setting, if we are to fully capture the ecological and evolutionary consequences of these parasite-induced behavioral changes. As part of this effort, we conducted a series of experiments to investigate the long and short-range behavioral responses to human stimuli in the mosquito Anopheles coluzzii during different stages of infection with sympatric field isolates of the human malaria parasite Plasmodium falciparum in Burkina Faso. First, we used a dual-port olfactometer designed to take advantage of the whole body odor to gauge mosquito long-range host-seeking behaviors. Second, we used a locomotor activity monitor system to assess mosquito short-range behaviors. Compared to control uninfected mosquitoes, P. falciparum infection had no significant effect neither on long-range nor on short-range behaviors both at the immature and mature stages. This study, using a natural mosquito-malaria parasite association, indicates that manipulation of vector behavior may not be a general phenomenon. We speculate that the observed contrasting phenotypes with model systems might result from coevolution of the human parasite and its natural vector. Future experiments, using other sympatric malaria mosquito populations or species are required to test this hypothesis. In conclusion, our results highlight the importance of following up discoveries in laboratory model systems with studies on natural parasite-mosquito interactions to accurately predict the epidemiological, ecological and evolutionary consequences of parasite manipulation of vector behaviors.
Ecological immunology of mosquito–malaria interactions
Trends in Parasitology, 2008
More than a century after the discovery of the complex life cycle of its causative agent, malaria remains a major health problem. Understanding mosquito-malaria interactions could lead to breakthroughs in malaria control. Novel strategies, such as the design of transgenic mosquitoes refractory to Plasmodium, or design of human vaccines emulating mosquito resistance to the parasite, require extensive knowledge of processes involved in immune responses and of microevolutionary mechanisms that create and maintain variation in immune responses in wild vector populations. The recent realization of how intimately and specifically mosquitoes and Plasmodium co-evolve in Nature is driving vector molecular biologists and evolutionary ecologists to move closer to the natural setting under the common umbrella of 'Ecological immunology'.
Proceedings of the Royal Society B: Biological Sciences, 2013
Previous studies have suggested that Plasmodium parasites can manipulate mosquito feeding behaviours such as probing, persistence and engorgement rate in order to enhance transmission success. Here, we broaden analysis of this ‘manipulation phenotype’ to consider proximate foraging behaviours, including responsiveness to host odours and host location. Using Anopheles stephensi and Plasmodium yoelii as a model system, we demonstrate that mosquitoes with early stage infections (i.e. non-infectious oocysts) exhibit reduced attraction to a human host, whereas those with late-stage infections (i.e. infectious sporozoites) exhibit increased attraction. These stage-specific changes in behaviour were paralleled by changes in the responsiveness of mosquito odourant receptors, providing a possible neurophysiological mechanism for the responses. However, we also found that both the behavioural and neurophysiological changes could be generated by immune challenge with heat-killed Escherichia co...