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.

已知昆虫可演化出分散不利环境遭遇风险的策略，从而降低不可预测环境中遗传谱系的灭绝概率。目前学界尚未明确，这类策略在随机环境中对虫媒传染病的流行病学特征与演化过程的影响程度究竟如何。作为恰加斯病（Chagas’ disease）病原体克氏锥虫（Trypanosoma cruzi）的传播媒介，锥蝽（triatomines）的若虫发育时长存在个体差异，这类差异大概率可降低随机环境中媒介种群的灭绝风险。我们构建了简化的多阶段虫媒易感-感染（SI）流行病学模型，用以探究媒介的风险分散策略与环境随机性如何影响寄生虫的流行程度与演化过程。该模型基于现有锥蝽生物人口学研究成果，但其核心结论在一定程度上可推广至其他虫媒传染病。通过对比确定性与随机模型的仿真结果，我们得出结论：环境随机性、媒介的风险分散策略（尤其是发育时长的延长与变异程度提升）及其交互作用，会对媒介种群动态、疾病流行率以及寄生虫毒力的短期相对演化产生显著影响。本研究表明，随机环境及其伴随的风险分散策略，可提升虫媒传染病的流行程度，并在相对较短的演化时间尺度上，更有利于高毒力寄生虫毒株的入侵定植。在全球气候变化与栖息地破坏、媒介防控等人类活动导致环境变异愈发不可预测的背景下，本研究提出了新的科学问题与挑战。