Abstract

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.

Highlights

  • Environmental stochasticity is a major factor responsible for fluctuations in the density of populations, and possibly their extinction, and on an evolutionary timescale it strongly influences organisms’ life histories [1,2]

  • This result held for stochastic environments, provided that the intensity of the stochasticity was relatively low, or that vector life-history traits such as adult survival and fecundity were high enough to allow a high persistence of vector populations (Fig. 2d, black lines)

  • We showed that vector riskspreading strategy in stochastic environments, defined here as an increase in the inter-individual variability in vector development time, can enhance parasite prevalence among both vectors and hosts, but does not affect the long-term evolution of parasite virulence

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Summary

Introduction

Environmental stochasticity is a major factor responsible for fluctuations in the density of populations, and possibly their extinction, and on an evolutionary timescale it strongly influences organisms’ life histories [1,2]. Several theoretical works have investigated the influence of different sources of random variability on the epidemiology and evolution of diseases. Climate-based transmission models that integrate explicit relationships between climatic factors and insect life-history traits such as development time have been developed to investigate the effect of climatic variations on the population dynamics of vectors and, in turn, on the epidemiology of vector-borne diseases [12,13,14,15]. To our knowledge, the possible impacts of environmental stochasticity on the evolution of vector-borne diseases have never been investigated

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