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

International audienceChagas 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. Chagas disease is a major public health problem in the Americas, where it affects seven-eight million people (WHO 2014). The pathogenic agent is a protozoan parasite, Trypanosoma cruzi, mainly transmitted to humans and other mammals through the contaminated faeces of blood-sucking insects called triatomines (Hemiptera: Redu-viidae), also known as " kissing bugs ". Control of Chagas disease relies on the treatment of infected patients and prevention of transmission is based mainly on vector control. Currently, more than 140 species of triatomines are recognised. Over half of them have been shown to be naturally or experimentally infected with T. cruzi, but all are suspected to be able to transmit the parasite (or " serve as vectors ") (Bargues et al. 2010). Nevertheless, not all the triatomine species are considered important vectors of T. cruzi. Vector competence varies considerably between the different species/populations of triatomines and depends on multiple criterions. Among these, the level of domiciliation, which is understood as the level of adaptation to human and its domestic environment, is one of the most important, as it defines the level of human-vector contacts (Dujardin et al. 2002). Indeed, species highly adapted to and able to colonise human dwellings are more likely to actively contribute to the transmission of T. cruzi to humans than species that are only found in sylvatic environment. While the domiciliation of triatomine spe-cies/populations is clearly a gradual evolutionary process (Schofield et al. 1999), it has important implications for the design and efficacy of vector control interventions. To date, vector control is mainly achieved through indoor residual insecticide spraying, initially designed to target triatomine species living inside human dwellings and highly adapted to the domestic environment (i.e. domicil-iated or domesticated). However, it is becoming increasingly clear that triatomine species presenting lower levels of domiciliation are also playing an important role in T. cruzi transmission to humans and thus need to be taken into account by vector control programs in many regions. The efficacy of conventional insecticide spraying may indeed be directly affected by the level of domiciliation of triatomines and alternative control strategies thus need to be considered against nondomiciliated species/popula-tions. These populations are a potential source of continuous house infestation and post-spraying re-infestation, making the control by insecticide spraying unsustainable, even in areas where transmission is primarily due to highly domiciliated vectors. The level of domiciliation/intru-sion of triatomine species thus needs to be clearly defined in operative terms to allow for its precise evaluation and the design of effective vector control interventions. In this review, we examine how the domiciliation/ intrusion level of different triatomine species/popula-tions 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