Influence of Vectors' Risk-Spreading Strategies and Environmental Stochasticity on the Epidemiology and Evolution of Vector-Borne Diseases: The Example of Chagas' Disease

Insects are known to display strategies that spread the risk of encountering unfavorable conditions, thereby decreasing the extinction probability of genetic lineages in unpredictable environments. To what extent these strategies influence the epidemiology and evolution of vector-borne diseases in stochastic environments is largely unknown. In triatomines, the vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas' disease, juvenile development time varies between individuals and such variation most likely decreases the extinction risk of vector populations in stochastic environments. We developed a simplified multi-stage vector-borne SI epidemiological model to investigate how vector risk-spreading strategies and environmental stochasticity influence the prevalence and evolution of a parasite. This model is based on available knowledge on triatomine biodemography, but its conceptual outcomes apply, to a certain extent, to other vector-borne diseases. Model comparisons between deterministic and stochastic settings led to the conclusion that environmental stochasticity, vector risk-spreading strategies (in particular an increase in the length and variability of development time) and their interaction have drastic consequences on vector population dynamics, disease prevalence, and the relative short-term evolution of parasite virulence. Our work shows that stochastic environments and associated risk-spreading strategies can increase the prevalence of vector-borne diseases and favor the invasion of more virulent parasite strains on relatively short evolutionary timescales. This study raises new questions and challenges in a context of increasingly unpredictable environmental variations as a result of global climate change and human interventions such as habitat destruction or vector control.Centro de Estudios Parasitológicos y de Vectore

Influence of Vectors' Risk-Spreading Strategies and Environmental Stochasticity on the Epidemiology and Evolution of Vector-Borne Diseases: The Example of Chagas' Disease

Insects are known to display strategies that spread the risk of encountering unfavorable conditions, thereby decreasing the extinction probability of genetic lineages in unpredictable environments. To what extent these strategies influence the epidemiology and evolution of vector-borne diseases in stochastic environments is largely unknown. In triatomines, the vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas' disease, juvenile development time varies between individuals and such variation most likely decreases the extinction risk of vector populations in stochastic environments. We developed a simplified multi-stage vector-borne SI epidemiological model to investigate how vector risk-spreading strategies and environmental stochasticity influence the prevalence and evolution of a parasite. This model is based on available knowledge on triatomine biodemography, but its conceptual outcomes apply, to a certain extent, to other vector-borne diseases. Model comparisons between deterministic and stochastic settings led to the conclusion that environmental stochasticity, vector risk-spreading strategies (in particular an increase in the length and variability of development time) and their interaction have drastic consequences on vector population dynamics, disease prevalence, and the relative short-term evolution of parasite virulence. Our work shows that stochastic environments and associated risk-spreading strategies can increase the prevalence of vector-borne diseases and favor the invasion of more virulent parasite strains on relatively short evolutionary timescales. This study raises new questions and challenges in a context of increasingly unpredictable environmental variations as a result of global climate change and human interventions such as habitat destruction or vector control.Centro de Estudios Parasitológicos y de Vectore

Influence of Vectors' Risk-Spreading Strategies and Environmental Stochasticity on the Epidemiology and Evolution of Vector-Borne Diseases: The Example of Chagas' Disease

Insects are known to display strategies that spread the risk of encountering unfavorable conditions, thereby decreasing the extinction probability of genetic lineages in unpredictable environments. To what extent these strategies influence the epidemiology and evolution of vector-borne diseases in stochastic environments is largely unknown. In triatomines, the vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas' disease, juvenile development time varies between individuals and such variation most likely decreases the extinction risk of vector populations in stochastic environments. We developed a simplified multi-stage vector-borne SI epidemiological model to investigate how vector risk-spreading strategies and environmental stochasticity influence the prevalence and evolution of a parasite. This model is based on available knowledge on triatomine biodemography, but its conceptual outcomes apply, to a certain extent, to other vector-borne diseases. Model comparisons between deterministic and stochastic settings led to the conclusion that environmental stochasticity, vector risk-spreading strategies (in particular an increase in the length and variability of development time) and their interaction have drastic consequences on vector population dynamics, disease prevalence, and the relative short-term evolution of parasite virulence. Our work shows that stochastic environments and associated risk-spreading strategies can increase the prevalence of vector-borne diseases and favor the invasion of more virulent parasite strains on relatively short evolutionary timescales. This study raises new questions and challenges in a context of increasingly unpredictable environmental variations as a result of global climate change and human interventions such as habitat destruction or vector control.Centro de Estudios Parasitológicos y de Vectore

Rôle des compromis évolutifs dans la spécialisation et la coexistence d'espèces compétitrices. Développements théoriques et expérimentaux chez les insectes parasitoïdes.

Trade-offs have a central place in the evolution of life-history traits since they bound the universe of possibilities. Trade-offs in energy allocation toward reproduction and maintenance are essentially linked, in parasitoid insects, to the host and food availability of the environment and to the number of eggs carried by females. Our experiments in behavioural ecology and eco-physiology show, in the parasitoid Venturia canescens, that (i) environmental characteristics select for a differential energy allocation toward egg manufacture and energy storage during the larval stage; and (ii) that an adjustment of the energy allocation strategies in response to the host availability takes place during the adult stage. Our theoretical investigations put forward that food quality has a central role in the evolution of the trade-off between host and food searching, and suggest its importance in the structuring of parasitoid communities.Les compromis évolutifs ou trade-offs occupent une place centrale dans l'évolution des traits d'histoire de vie car ils contraignent l'univers des possibles. Les trade-offs dans l'allocation d'énergie vers la reproduction et la maintenance sont essentiellement liés, chez les insectes parasitoïdes, à la disponibilité en hôtes et en nourriture de l'environnement et au nombre d'œufs dont disposent les femelles. Nos expériences relevant de l'écologie comportementale et de l'éco-physiologie démontrent, chez le parasitoïde Venturia canescens, (i) que les caractéristiques de l'environnement sélectionnent une allocation différentielle des ressources vers la fabrication des œufs et la mise en place des réserves énergétiques pendant la phase larvaire ; et (ii) qu'un ajustement des stratégies d'allocation d'énergie en réponse à la disponibilité en hôtes existe pendant la phase adulte. Nos travaux théoriques révèlent le rôle central de la qualité de la nourriture dans l'évolution du trade-off entre recherche d'hôtes et de nourriture, et suggère son importance dans la structuration des communautés de parasitoïdes

Role of trade-offs in the specialisation and coexistence of competing species : Theoretical and empirical developments in parasitoid insects.

Trade-offs have a central place in the evolution of life-history traits since they bound the universe of possibilities. Trade-offs in energy allocation toward reproduction and maintenance are essentially linked, in parasitoid insects, to the host and food availability of the environment and to the number of eggs carried by females. Our experiments in behavioural ecology and eco-physiology show, in the parasitoid Venturia canescens, that (i) environmental characteristics select for a differential energy allocation toward egg manufacture and energy storage during the larval stage; and (ii) that an adjustment of the energy allocation strategies in response to the host availability takes place during the adult stage. Our theoretical investigations put forward that food quality has a central role in the evolution of the trade-off between host and food searching, and suggest its importance in the structuring of parasitoid communities.Les compromis évolutifs ou trade-offs occupent une place centrale dans l évolution des traits d histoire de vie car ils contraignent l univers des possibles. Les trade-offs dans l allocation d énergie vers la reproduction et la maintenance sont essentiellement liés, chez les insectes parasitoïdes, à la disponibilité en hôtes et en nourriture de l environnement et au nombre d œufs dont disposent les femelles. Nos expériences relevant de l écologie comportementale et de l éco-physiologie démontrent, chez le parasitoïde Venturia canescens, (i) que les caractéristiques de l environnement sélectionnent une allocation différentielle des ressources vers la fabrication des œufs et la mise en place des réserves énergétiques pendant la phase larvaire ; et (ii) qu un ajustement des stratégies d allocation d énergie en réponse à la disponibilité en hôtes existe pendant la phase adulte. Nos travaux théoriques révèlent le rôle central de la qualité de la nourriture dans l évolution du trade-off entre recherche d hôtes et de nourriture, et suggère son importance dans la structuration des communautés de parasitoïdesLYON1-BU.Sciences (692662101) / SudocSudocFranceF

Does synovigeny confer reproductive plasticity upon a parasitoid wasp that is faced with variability in habitat richness?

Understanding the factors that constrain the reproductive success of animals and their demographics requires detailed insight into the processes of resource acquisition and allocation in relation to habitat richness. Parasitoid wasp females are valuable models in this respect because their lifetime reproductive success is closely tied to host availability. Parasitoids that manufacture eggs throughout adult life (i.e. ‘synovigenic’ species) and characteristically acquire nutrients via feeding are predicted to be plastic in their allocation to egg manufacture. Using the synovigenic parasitoid wasp Venturia canescens, we tested whether this prediction holds when females are faced with variation in the availability of both hosts and food. Laboratory experiments were conducted to determine how environmental variation affects parasitoid reproductive success and the lifetime dynamics of egg load and of major nutrient types. Our results, surprisingly, show that female V. canescens lacks a significant degree of reproductive plasticity under our experimental conditions. In particular, allocation of resources to reproduction was high irrespective of host availability. We attribute this lack of flexibility to the low energy content of V. canescens' eggs and to features peculiar to the ecology of this species. Our findings shed new light on the physiological factors that constrain parasitoid lifetime reproductive success

Fuelling flight in a parasitic wasp: Which energetic substrate to use?

1. Flight is an energy-demanding behaviour in insects. In parasitic wasps, strategies of nutrient acquisition and allocation, resulting life-history trade-offs and relationships with foraging strategies and resource availability have received much attention. However, despite the ecological importance of dispersal between host and food patches, and the great impact energy diverted to flight should have on lifetime reproductive success, the eco-physiology of flight in parasitoids is poorly understood. 2. The objective of this study is to (i) identify the energetic resources used to fuel flight, and (ii) relate nutrient type and rate of utilisation to selective pressures in terms of resource availability posed by the environment. 3. Using a flight mill and biochemical assays, we compared flight performance and nutrient dynamics during flight between two reproductive modes of the parasitoid Venturia canescens Gravenhorst, which is known to thrive preferentially in contrasted environments (i.e. natural vs. anthropogenic habitat), differing notably in host and food distribution. 4. Biochemical analyses of different nutrient types showed that glycogen is the flight fuel used by this species, yet no significant differences in its dynamics in flight were found between the two reproductive modes. 5. Results suggest that both glycogen quantity and flight performance are related to the diverging ecological conditions experienced by thelytokous and arrhenotokous strains. © 2012 The Royal Entomological Society

Influence of vectors' risk-spreading strategies and environmental stochasticity on the epidemiology and evolution of vector-borne diseases: the example of Chagas' disease.

Insects are known to display strategies that spread the risk of encountering unfavorable conditions, thereby decreasing the extinction probability of genetic lineages in unpredictable environments. To what extent these strategies influence the epidemiology and evolution of vector-borne diseases in stochastic environments is largely unknown. In triatomines, the vectors of the parasite Trypanosoma cruzi, the etiological agent of Chagas' disease, juvenile development time varies between individuals and such variation most likely decreases the extinction risk of vector populations in stochastic environments. We developed a simplified multi-stage vector-borne SI epidemiological model to investigate how vector risk-spreading strategies and environmental stochasticity influence the prevalence and evolution of a parasite. This model is based on available knowledge on triatomine biodemography, but its conceptual outcomes apply, to a certain extent, to other vector-borne diseases. Model comparisons between deterministic and stochastic settings led to the conclusion that environmental stochasticity, vector risk-spreading strategies (in particular an increase in the length and variability of development time) and their interaction have drastic consequences on vector population dynamics, disease prevalence, and the relative short-term evolution of parasite virulence. Our work shows that stochastic environments and associated risk-spreading strategies can increase the prevalence of vector-borne diseases and favor the invasion of more virulent parasite strains on relatively short evolutionary timescales. This study raises new questions and challenges in a context of increasingly unpredictable environmental variations as a result of global climate change and human interventions such as habitat destruction or vector control

Schematic representation of the one-parasite-strain version of the model.

<p>Because vectors are divided into two stages (juvenile and adult), and that both stages can get and transmit the parasite, we present first a simplified vector-borne epidemiological model with only one stage for vectors (panel a) and then the vector life-cycle (panel b). Hosts are represented with dashed lines and vectors with solid lines (a) Susceptible hosts <i>H_s</i> get infected through contacts with infected vectors <i>V_i</i> with probability <i>Φ_h</i>, and susceptible vectors <i>V_s</i> through contacts with infected hosts <i>H_i</i> with probability <i>Φ_v</i>. Susceptible and infected vectors and hosts give birth to susceptible vectors and hosts. Infected host survival <i>S_hi</i> is a function of parasite virulence <i>α</i>. Environmental stochasticity is applied to vector survival (only adults, see below) with intensity <i>ε_s</i>. (b) Susceptible and infected adult vectors <i>V_as</i> and <i>V_ai</i> give birth to susceptible juvenile vectors <i>V_js</i>. Susceptible and infected juvenile vectors <i>V_js</i> and <i>V_ji</i> remain in the juvenile stage with probability <i>P_j</i> and mature into adults with probability (1-<i>P_j</i>). Only adult survival <i>S_va</i> is submitted to stochasticity with intensity <i>ε_s</i>. See text, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0070830#pone-0070830-t001" target="_blank">Table 1</a>, Appendix S1 in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0070830#pone.0070830.s003" target="_blank">File S1</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0070830#pone.0070830.s001" target="_blank">Fig. S1</a> for further details.</p