Assessing the risk of West Nile Virus seasonal outbreaks and its vector control in an urbanizing bird community: An integrative R0-modelling study in the city of Merida, Mexico.

Urbanization is a global trend associated with key socio-economic issues, one of them being to control the transmission of infectious diseases to a urban fraction of the world's population that shall reach 68% in 2050. While urban growth has been shown to favor mosquito species responsible for the transmission of the West Nile Virus (WNV), a major human arbovirosis, the effects of concomitant changes in the host bird communities remain hard to anticipate albeit essential to quantify disease risk and to plan control initiatives. We developed a R0 modelling of WNV transmission in a urban bird community to assess the risk of outbreak in Merida, one of the cities with the highest growth rate in Mexico. The model was parameterized using ecological and epidemiological data collected over the past 15-years on the local vector, Culex quinquefasciatus, and avian community. We identified a 3-weeks summer period during which the vector population strongly amplifies the WNV enzootic transmission and lead to a significant risk of outbreaks in humans. Extensive sensitivity analyses showed that urbanization induced changes in the bird community could lead to an up-to 6-fold increase in the duration of the risk period, while the daily risk could rise by 40%. Interestingly, the increase in Quiscalus mexicanus abundance had 4-5 times larger impact than any other change in the bird community. In such a context, annihilating the current and future risk of WNV outbreaks in Merida requires reducing the mosquito population by 13% and up to 56%, respectively. This study provides an integrative assessment of the current and future risks of WNV outbreak in the fast urbanizing city of Merida, and points toward the implementation of epidemiological monitoring combined with preemptive measures targeting both C. quinquefasciatus and Q. mexicanus populations, as they are expected to have synergistic effects.

Ecology, evolution, and epidemiology of zoonotic and vector-borne infectious diseases in French Guiana: Transdisciplinarity does matter to tackle new emerging threats.

French Guiana is a European ultraperipheric region located on the northern Atlantic coast of South America. It constitutes an important forested region for biological conservation in the Neotropics. Although very sparsely populated, with its inhabitants mainly concentrated on the Atlantic coastal strip and along the two main rivers, it is marked by the presence and development of old and new epidemic disease outbreaks, both research and health priorities. In this review paper, we synthetize 15 years of multidisciplinary and integrative research at the interface between wildlife, ecosystem modification, human activities and sociodemographic development, and human health. This study reveals a complex epidemiological landscape marked by important transitional changes, facilitated by increased interconnections between wildlife, land-use change and human occupation and activity, human and trade transportation, demography with substantial immigration, and identified vector and parasite pharmacological resistance. Among other French Guianese characteristics, we demonstrate herein the existence of more complex multi-host disease life cycles than previously described for several disease systems in Central and South America, which clearly indicates that today the greater promiscuity between wildlife and humans due to demographic and economic pressures may offer novel settings for microbes and their hosts to circulate and spread. French Guiana is a microcosm that crystallizes all the current global environmental, demographic and socioeconomic change conditions, which may favor the development of ancient and future infectious diseases.

The ecology of the genome and the dynamics of the biological dark matter.

Transposable elements (TEs) are essential components of the eukaryotic genomes. While mostly deleterious, evidence is mounting that TEs provide the host with beneficial adaptations. How 'selfish' or 'parasitic' DNA persists until it helps species evolution is emerging as a major evolutionary puzzle, especially in asexual taxa where the lack of sex strongly impede the spread of TEs. Since occasional but unchecked TE proliferations would ultimately drive host lineages toward extinction, asexual genomes are typically predicted to be free of TEs, which contrasts with their persistence in asexual taxa. We designed innovative 'Eco-genomic' models that account for both host demography and within-host molecular mechanisms of transposition and silencing to analyze their impact on TE dynamics in asexual genome populations. We unraveled that the spread of TEs can be limited to a stable level by density-dependent purifying selection when TE copies are over-dispersed among lineages and the host demographic turn-over is fast. We also showed that TE silencing can protect host populations in two ways; by preventing TEs with weak effects to accumulate or by favoring the elimination of TEs with large effects. Our predictions may explain TE persistence in known asexual taxa that typically show fast demography and where TE copy number variation between lineages is expected. Such TE persistence in asexual taxa potentially has important implications for their evolvability and the preservation of sexual reproduction.

Virus-host coexistence in phytoplankton through the genomic lens.

Virus-microbe interactions in the ocean are commonly described by "boom and bust" dynamics, whereby a numerically dominant microorganism is lysed and replaced by a virus-resistant one. Here, we isolated a microalga strain and its infective dsDNA virus whose dynamics are characterized instead by parallel growth of both the microalga and the virus. Experimental evolution of clonal lines revealed that this viral production originates from the lysis of a minority of virus-susceptible cells, which are regenerated from resistant cells. Whole-genome sequencing demonstrated that this resistant-susceptible switch involved a large deletion on one chromosome. Mathematical modeling explained how the switch maintains stable microalga-virus population dynamics consistent with their observed growth pattern. Comparative genomics confirmed an ancient origin of this "accordion" chromosome despite a lack of sequence conservation. Together, our results show how dynamic genomic rearrangements may account for a previously overlooked coexistence mechanism in microalgae-virus interactions.

Trypanosoma cruzi transmission dynamics in a synanthropic and domesticated host community.

Trypanosoma cruzi is the causative agent of Chagas disease, a Neglected Tropical Disease affecting 8 million people in the Americas. Triatomine hematophagous vectors feed on a high diversity of vertebrate species that can be reservoirs or dead-end hosts, such as avian species refractory to T. cruzi. To understand its transmission dynamics in synanthropic and domesticated species living within villages is essential to quantify disease risk and assess the potential of zooprophylaxis. We developed a SI model of T. cruzi transmission in a multi-host community where vector reproduction and parasite transmission depend on a triatomine blood-feeding rate accounting for vector host preferences and interference while feeding. The model was parameterized to describe T. cruzi transmission in villages of the Yucatan peninsula, Mexico, using the information about Triatoma dimidiata vectors and host populations accumulated over the past 15 years. Extensive analyses of the model showed that dogs are key reservoirs and contributors to human infection, as compared to synanthropic rodents and cats, while chickens or other domesticated avian hosts dilute T. cruzi transmission despite increasing vector abundance. In this context, reducing the number of dogs or increasing avian hosts abundance decreases incidence in humans by up to 56% and 39%, respectively, while combining such changes reduces incidence by 71%. Although such effects are only reached over >10-years periods, they represent important considerations to be included in the design of cost-effective Integrated Vector Management. The concomitant reduction in T. cruzi vector prevalence estimated by simulating these zooprophylactic interventions could indeed complement the removal of colonies from the peridomiciles or the use of insect screens that lower vector indoor abundance by ~60% and ~80%. These new findings reinforce the idea that education and community empowerment to reduce basic risk factors is a cornerstone to reach and sustain the key objective of interrupting Chagas disease intra-domiciliary transmission.

Non-randomized controlled trial of the long-term efficacy of an Ecohealth intervention against Chagas disease in Yucatan, Mexico.

Non-domiciliated intrusive triatomine vectors are responsible for a low but significant transmission of Trypanosoma cruzi to humans. Their control is a challenge as insecticide spraying is of limited usefulness, and alternative strategies need to be developed for a sustainable control. We performed a non-randomized controlled trial of an Ecohealth intervention based on window insect screens and community participation to reduce house infestation by Triatoma dimidiata in two rural villages in Yucatan, Mexico. Efficacy of the intervention was measured over a three years follow-up period and entomological indicators showed that the proportion of triatomines found inside houses was significantly reduced in houses with insect screens, which effectively kept more bugs on the outside of houses. Using a previously developed model linking entomological data to the prevalence of infection in human, we predicted that the intervention would lead to a 32% reduction in yearly incidence and in the prevalence of T. cruzi infection. The cost for the coverage of all the windows of a house was of comparable magnitude to what families currently spend on various domestic insecticide, and most screens were still in good conditions after three years. In conclusion, the Ecohealth approach proposed here is effective for the long-term and sustainable control of intrusive T. dimidiata vectors in the Yucatan peninsula, Mexico. This strategy may also be easily adapted to other intrusive triatomine species as well as other regions/countries with comparable eco-epidemiological settings, and would be an excellent component of a larger integrated program for the control of a variety of other vector-borne diseases, bringing additional benefits to the communities. Our results should encourage a further scaling-up of our implementation strategy in additional villages in the region.

Evolutionary ecology of Chagas disease; what do we know and what do we need?

The aetiological agent of Chagas disease, Trypanosoma cruzi, is a key human pathogen afflicting most populations of Latin America. This vectorborne parasite is transmitted by haematophageous triatomines, whose control by large-scale insecticide spraying has been the main strategy to limit the impact of the disease for over 25 years. While those international initiatives have been successful in highly endemic areas, this systematic approach is now challenged by the emergence of insecticide resistance and by its low efficacy in controlling species that are only partially adapted to human habitat. In this contribution, we review evidences that Chagas disease control shall now be entering a second stage that will rely on a better understanding of triatomines adaptive potential, which requires promoting microevolutionary studies and -omic approaches. Concomitantly, we show that our knowledge of the determinants of the evolution of T. cruzi high diversity and low virulence remains too limiting to design evolution-proof strategies, while such attributes may be part of the future of Chagas disease control after the 2020 WHO's target of regional elimination of intradomiciliary transmission has been reached. We should then aim at developing a theory of T. cruzi virulence evolution that we anticipate to provide an interesting enrichment of the general theory according to the specificities of transmission of this very generalist stercorarian trypanosome. We stress that many ecological data required to better understand selective pressures acting on vector and parasite populations are already available as they have been meticulously accumulated in the last century of field research. Although more specific information will surely be needed, an effective research strategy would be to integrate data into the conceptual and theoretical framework of evolutionary ecology and life-history evolution that provide the quantitative backgrounds necessary to understand and possibly anticipate adaptive responses to public health interventions.

Detailed ecological associations of triatomines revealed by metabarcoding and next-generation sequencing: implications for triatomine behavior and Trypanosoma cruzi transmission cycles.

Trypanosoma cruzi is the agent of Chagas disease, transmitted by hematophagous triatomine vectors. Establishing transmission cycles is key to understand the epidemiology of the disease, but integrative assessments of ecological interactions shaping parasite transmission are still limited. Current approaches also lack sensitivity to assess the full extent of this ecological diversity. Here we developed a metabarcoding approach based on next-generation sequencing to identify triatomine gut microbiome, vertebrate feeding hosts, and parasite diversity and their potential interactions. We detected a dynamic microbiome in Triatoma dimidiata, including 23 bacterial orders, which differed according to blood sources. Fourteen vertebrate species served as blood sources, corresponding to domestic, synantropic and sylvatic species, although four (human, dog, cow and mice) accounted for over 50% of blood sources. Importantly, bugs fed on multiple hosts, with up to 11 hosts identified per bug, indicating very frequent host-switching. A high clonal diversity of T. cruzi was detected, with up to 20 haplotypes per bug. This analysis provided much greater sensitivity to detect multiple blood meals and multiclonal infections with T. cruzi, which should be taken into account to develop transmission networks, and characterize the risk for human infection, eventually leading to a better control of disease transmission.

Epidemiological modeling of Trypanosoma cruzi: Low stercorarian transmission and failure of host adaptive immunity explain the frequency of mixed infections in humans.

People living in areas with active vector-borne transmission of Chagas disease have multiple contacts with its causative agent, Trypanosoma cruzi. Reinfections by T. cruzi are possible at least in animal models leading to lower or even hardly detectable parasitaemia. In humans, although reinfections are thought to have major public health implications by increasing the risk of chronic manifestations of the disease, there is little quantitative knowledge about their frequency and the timing of parasite re-inoculation in the course of the disease. Here, we implemented stochastic agent-based models i) to estimate the rate of re-inoculation in humans and ii) to assess how frequent are reinfections during the acute and chronic stages of the disease according to alternative hypotheses on the adaptive immune response following a primary infection. By using a hybrid genetic algorithm, the models were fitted to epidemiological data of Argentinean rural villages where mixed infections by different genotypes of T. cruzi reach 56% in humans. To explain this percentage, the best model predicted 0.032 (0.008-0.042) annual reinfections per individual with 98.4% of them occurring in the chronic phase. In addition, the parasite escapes to the adaptive immune response mounted after the primary infection in at least 20% of the events of re-inoculation. With these low annual rates, the risks of reinfection during the typically long chronic stage of the disease stand around 14% (4%-18%) and 60% (21%-70%) after 5 and 30 years, with most individuals being re-infected 1-3 times overall. These low rates are better explained by the weak efficiency of the stercorarian mode of transmission than a highly efficient adaptive immune response. Those estimates are of particular interest for vaccine development and for our understanding of the higher risk of chronic disease manifestations suffered by infected people living in endemic areas.

Amazonian Triatomine Biodiversity and the Transmission of Chagas Disease in French Guiana: In Medio Stat Sanitas.

The effects of biodiversity on the transmission of infectious diseases now stand as a cornerstone of many public health policies. The upper Amazonia and Guyana shield are hot-spots of biodiversity that offer genuine opportunities to explore the relationship between the risk of transmission of Chagas disease and the diversity of its triatomine vectors. Over 730 triatomines were light-trapped in four geomorphological landscapes shaping French-Guiana, and we determined their taxonomic status and infection by Trypanosoma cruzi. We used a model selection approach to unravel the spatial and temporal variations in species abundance, diversity and infection. The vector community in French-Guiana is typically made of one key species (Panstrongylus geniculatus) that is more abundant than three secondary species combined (Rhodnius pictipes, Panstrongylus lignarius and Eratyrus mucronatus), and four other species that complete the assemblage. Although the overall abundance of adult triatomines does not vary across French-Guiana, their diversity increases along a coastal-inland gradient. These variations unravelled a non-monotonic relationship between vector biodiversity and the risk of transmission of Chagas disease, so that intermediate biodiversity levels are associated with the lowest risks. We also observed biannual variations in triatomine abundance, representing the first report of a biannual pattern in the risk of Chagas disease transmission. Those variations were highly and negatively correlated with the average monthly rainfall. We discuss the implications of these patterns for the transmission of T. cruzi by assemblages of triatomine species, and for the dual challenge of controlling Amazonian vector communities that are made of both highly diverse and mostly intrusive species.

Invasion speeds of Triatoma dimidiata, vector of Chagas disease: An application of orthogonal polynomials method.

Demographic processes and spatial dispersal of Triatoma dimidiata, a triatomine species vector of Chagas disease, are modeled by integrodifference equations to estimate invasion capacity of this species under different ecological conditions. The application of the theory of orthogonal polynomials and the steepest descent method applied to these equations, allow a good approximation of the abundance of the adult female population and the invasion speed. We show that: (1) under the same mean conditions of demography and dispersal, periodic spatial dispersal results in an invasion speed 2.5 times larger than the invasion speed when spatial dispersal is continuous; (2) when the invasion speed of periodic spatial dispersal is correlated to adverse demographic conditions, it is 34.7% higher as compared to a periodic dispersal that is correlated to good demographic conditions. From our results we conclude, in terms of triatomine population control, that the invasive success of T. dimidiata may be most sensitive to the probability of transition from juvenile to adult stage. We discuss our main theoretical predictions in the light of observed data in different triatomines species found in the literature.

Intrusive versus domiciliated triatomines and the challenge of adapting vector control practices against Chagas disease.

Chagas disease prevention remains mostly based on triatomine vector control to reduce or eliminate house infestation with these bugs. The level of adaptation of triatomines to human housing is a key part of vector competence and needs to be precisely evaluated to allow for the design of effective vector control strategies. In this review, we examine how the domiciliation/intrusion level of different triatomine species/populations has been defined and measured and discuss how these concepts may be improved for a better understanding of their ecology and evolution, as well as for the design of more effective control strategies against a large variety of triatomine species. We suggest that a major limitation of current criteria for classifying triatomines into sylvatic, intrusive, domiciliary and domestic species is that these are essentially qualitative and do not rely on quantitative variables measuring population sustainability and fitness in their different habitats. However, such assessments may be derived from further analysis and modelling of field data. Such approaches can shed new light on the domiciliation process of triatomines and may represent a key tool for decision-making and the design of vector control interventions.

Intrusive versus domiciliated triatomines and the challenge of adapting vector control practices against Chagas disease

Chagas disease prevention remains mostly based on triatomine vector control to reduce or eliminate house infestation with these bugs. The level of adaptation of triatomines to human housing is a key part of vector competence and needs to be precisely evaluated to allow for the design of effective vector control strategies. In this review, we examine how the domiciliation/intrusion level of different triatomine species/populations has been defined and measured and discuss how these concepts may be improved for a better understanding of their ecology and evolution, as well as for the design of more effective control strategies against a large variety of triatomine species. We suggest that a major limitation of current criteria for classifying triatomines into sylvatic, intrusive, domiciliary and domestic species is that these are essentially qualitative and do not rely on quantitative variables measuring population sustainability and fitness in their different habitats. However, such assessments may be derived from further analysis and modelling of field data. Such approaches can shed new light on the domiciliation process of triatomines and may represent a key tool for decision-making and the design of vector control interventions.

Ecology, evolution and control of Chagas disease: a century of neglected modelling and a promising future.

More than 100 years after its formal description, Chagas disease remains a major public health concern in Latin America with a yearly burden of 430,000 Disability-Adjusted Life Years (DALYs). The aetiological agent, a protozoan named Trypanosoma cruzi, is mainly transmitted to mammalian hosts by triatomine vectors. Multiple species of mammals and triatomines can harbour and transmit the parasite, and the feeding range of triatomine species typically includes many noncompetent hosts. Furthermore, the transmission of the pathogen can occur via several routes including the typical vector's faeces, but also oral, congenital and blood transfusion routes. These ecological and epidemiological complexities of the disease have hindered many control initiatives. In such a context, mathematical models provide invaluable tools to explore and understand the dynamics of T. cruzi transmission, and to design, optimize and monitor the efficacy of control interventions. We intend here to provide the first review of the mathematical models of Chagas disease, focussing on how they have contributed to our understanding of (1) the population dynamics and control of triatomine vectors, and (2) the epidemiology of T. cruzi infections. We also aim at suggesting promising lines of modelling that could further improve our understanding of the ecology, evolution, and control of the disease.

Fundamental factors determining the nature of parasite aggregation in hosts.

The distribution of parasites in hosts is typically aggregated: a few hosts harbour many parasites, while the remainder of hosts are virtually parasite free. The origin of this almost universal pattern is central to our understanding of host-parasite interactions; it affects many facets of their ecology and evolution. Despite this, the standard statistical framework used to characterize parasite aggregation does not describe the processes generating such a pattern. In this work, we have developed a mathematical framework for the distribution of parasites in hosts, starting from a simple statistical description in terms of two fundamental processes: the exposure of hosts to parasites and the infection success of parasites. This description allows the level of aggregation of parasites in hosts to be related to the random variation in these two processes and to true host heterogeneity. We show that random variation can generate an aggregated distribution and that the common view, that encounters and success are two equivalent filters, applies to the average parasite burden under neutral assumptions but it does not apply to the variance of the parasite burden, and it is not true when heterogeneity between hosts is incorporated in the model. We find that aggregation decreases linearly with the number of encounters, but it depends non-linearly on parasite success. We also find additional terms in the variance of the parasite burden which contribute to the actual level of aggregation in specific biological systems. We have derived the formal expressions of these contributions, and these provide new opportunities to analyse empirical data and tackle the complexity of the origin of aggregation in various host-parasite associations.

An innovative ecohealth intervention for Chagas disease vector control in Yucatan, Mexico.

BACKGROUND: Non-domiciliated (intrusive) triatomine vectors remain a challenge for the sustainability of Chagas disease vector control as these triatomines are able to transiently (re-)infest houses. One of the best-characterized examples is Triatoma dimidiata from the Yucatan peninsula, Mexico, where adult insects seasonally infest houses between March and July. METHODS: We focused our study on three rural villages in the state of Yucatan, Mexico, in which we performed a situation analysis as a first step before the implementation of an ecohealth (ecosystem approach to health) vector control intervention. RESULTS: The identification of the key determinants affecting the transient invasion of human dwellings by T. dimidiata was performed by exploring associations between bug presence and qualitative and quantitative variables describing the ecological, biological and social context of the communities. We then used a participatory action research approach for implementation and evaluation of a control strategy based on window insect screens to reduce house infestation by T. dimidiata. CONCLUSIONS: This ecohealth approach may represent a valuable alternative to vertically-organized insecticide spraying. Further evaluation may confirm that it is sustainable and provides effective control (in the sense of limiting infestation of human dwellings and vector/human contacts) of intrusive triatomines in the region.

Competition, virulence, host body mass and the diversification of macro-parasites.

Adaptive speciation has been much debated in recent years, with a strong emphasis on how competition can lead to the diversification of ecological and sexual traits. Surprisingly, little attention has been paid to this evolutionary process to explain intrahost diversification of parasites. We expanded the theory of competitive speciation to look at the effect of key features of the parasite lifestyle, namely fragmentation, aggregation and virulence, on the conditions and rate of sympatric speciation under the standard 'pleiotropic scenario'. The conditions for competitive speciation were found similar to those for non-parasite species, but not the rate of diversification. Adaptive evolution proceeds faster in highly fragmented parasite populations and for weakly aggregated and virulent parasites. Combining these theoretical results with standard empirical allometric relationships, we showed that parasite diversification can be faster in host species of intermediate body mass. The increase in parasite load with body mass, indeed, fuels evolution by increasing mutants production, but because of the deleterious effect of virulence, it simultaneously weakens selection for resource specialization. Those two antagonistic effects lead to optimal parasite burden and host body mass for diversification. Data on the diversity of fishes' gills parasites were found consistent with the existence of such optimum.

The improbable transmission of Trypanosoma cruzi to human: the missing link in the dynamics and control of Chagas disease.

Chagas disease has a major impact on human health in Latin America and is becoming of global concern due to international migrations. Trypanosoma cruzi, the etiological agent of the disease, is one of the rare human parasites transmitted by the feces of its vector, as it is unable to reach the salivary gland of the insect. This stercorarian transmission is notoriously poorly understood, despite its crucial role in the ecology and evolution of the pathogen and the disease. The objective of this study was to quantify the probability of T. cruzi vectorial transmission to humans, and to use such an estimate to predict human prevalence from entomological data. We developed several models of T. cruzi transmission to estimate the probability of transmission from vector to host. Using datasets from the literature, we estimated the probability of transmission per contact with an infected triatomine to be 5.8 × 10(-4) (95%CI: [2.6 ; 11.0] × 10(-4)). This estimate was consistent across triatomine species, robust to variations in other parameters, and corresponded to 900-4,000 contacts per case. Our models subsequently allowed predicting human prevalence from vector abundance and infection rate in 7/10 independent datasets covering various triatomine species and epidemiological situations. This low probability of T. cruzi transmission reflected well the complex and unlikely mechanism of transmission via insect feces, and allowed predicting human prevalence from basic entomological data. Although a proof of principle study would now be valuable to validate our models' predictive ability in an even broader range of entomological and ecological settings, our quantitative estimate could allow switching the evaluation of disease risk and vector control program from purely entomological indexes to parasitological measures, as commonly done for other major vector borne diseases. This might lead to different quantitative perspectives as these indexes are well known not to be proportional one to another.

Eco-bio-social determinants for house infestation by non-domiciliated Triatoma dimidiata in the Yucatan Peninsula, Mexico.

BACKGROUND: Chagas disease is a vector-borne disease of major importance in the Americas. Disease prevention is mostly limited to vector control. Integrated interventions targeting ecological, biological and social determinants of vector-borne diseases are increasingly used for improved control. METHODOLOGY/PRINCIPAL FINDINGS: We investigated key factors associated with transient house infestation by T. dimidiata in rural villages in Yucatan, Mexico, using a mixed modeling approach based on initial null-hypothesis testing followed by multimodel inference and averaging on data from 308 houses from three villages. We found that the presence of dogs, chickens and potential refuges, such as rock piles, in the peridomicile as well as the proximity of houses to vegetation at the periphery of the village and to public light sources are major risk factors for infestation. These factors explain most of the intra-village variations in infestation. CONCLUSIONS/SIGNIFICANCE: These results underline a process of infestation distinct from that of domiciliated triatomines and may be used for risk stratification of houses for both vector surveillance and control. Combined integrated vector interventions, informed by an Ecohealth perspective, should aim at targeting several of these factors to effectively reduce infestation and provide sustainable vector control.

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.