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

Abstract

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.

triatomine; domiciliation; intrusion; vector control; ecohealth; integrated vector management


Chagas disease is a major public health problem in the Americas, where it affects seven-eight million people (WHO 2014WHO - World Health Organization 2014. Chagas disease (American trypanosomiasis). Available from: http://who.int/mediacentre/factsheets/fs340/en/.
http://who.int/mediacentre/factsheets/fs...
). 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: Reduviidae), 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. 2010Bargues MD, Schofield CJ, Dujardin JP 2010. Classification and phylogeny of the Triatominae. In J Telleria, M Tibayrenc (eds.),American trypanosomiasis Chagas disease - One hundred years of research, Elsevier, Burlington, p. 117-147.). 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. 2002Dujardin JP, Schofield CJ, Panzera F 2002. Los vectores de la enfermedad de Chagas, Académie Royale des Sciences d’Outre-Mer, Bruxelles, 189 pp.). 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 species/populations is clearly a gradual evolutionary process (Schofield et al. 1999Schofield CJ, Diotaiuti L, Dujardin JP 1999. The process of domestication in Triatominae. Mem Inst Oswaldo Cruz 94 (Suppl. I): 375-378.), 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. domiciliated or domesticated). However, it is becoming increasingly clear that triatomine species presenting lower levels of domiciliation are also playing an important role inT. 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/populations. 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/intrusion 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/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.

Level of domiciliation of triatomine species

Triatomine species have for a long time been classified according to their adaptation to human dwellings. According to Lent and Wygodzinsky (1979)Lent H, Wygodzinsky P 1979. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist Nat 163: 123-520., the habits of the various species of triatomines allow to divide them into sylvatic and domestic species, with an intermediate category of peridomestic species, which are occasionally attracted into houses, but do not effectively colonise them, and which thus feed on man only occasionally.Dujardin et al. (2002)Dujardin JP, Schofield CJ, Panzera F 2002. Los vectores de la enfermedad de Chagas, Académie Royale des Sciences d’Outre-Mer, Bruxelles, 189 pp. and Noireau and Dujardin (2010)Noireau F, Dujardin JP 2010. Biology of Triatominae. In J Telleria, M Tibayrenc (eds.), American trypanosomiasis: Chagas disease one hundred years of research, Elsevier, Burlington, 870 pp. later refined these definitions and proposed four different categories: sylvatic, intrusive, domiciliary and domestic species (Table I). These definitions have been the most widely accepted and used in the literature for the classification of many triatomine species. In Table II, we summarise how some triatomine species have been classified and the type of data and observations that helped defining their potential association with human habitat. These species/populations were selected based on their epidemiological significance and contribution to T. cruzitransmission to human. As can be observed in Table II, their level of domiciliation appears highly variable depending on the type of data collected by the authors, their own interpretation and the study area. Field collections by manual searches and/or community participation are the most common type of studies, allowing to establish conventional entomological indexes including infestation index (percentage of houses with triatomines), colonisation index (percentage of infested houses with evidence of reproductive cycle: presence of nymphs, but also eggs and/or exuviae), density index (number of triatomines per house) and dispersion index (percentage of localities infested) as the most commonly used (WHO 1991WHO - World Health Organization 1991. Control of Chagas disease: report of a WHO expert committee. Available from: http://whqlibdoc.who.int/trs/WHO_TRS_811.pdf.
http://whqlibdoc.who.int/trs/WHO_TRS_811...
). Infestation and density index have often been considered as indicators of the level of intrusion of a species into the domestic habitat, while the colonisation index can be viewed as a measure of its domiciliation/domestication. More recently, a visitation index has been proposed (percentage of houses visited exclusively by adult triatomines) to evaluate intrusion by adult bugs (Zeledón 2003Zeledón R 2003. A new entomological indicator useful in epidemiological studies and in control campaigns against Chagas disease.Entomol Vect 10: 269-276.). As indicated in Table I, the peridomicile is considered as part of the domicile by Dujardin et al. (2002)Dujardin JP, Schofield CJ, Panzera F 2002. Los vectores de la enfermedad de Chagas, Académie Royale des Sciences d’Outre-Mer, Bruxelles, 189 pp. and Noireau and Dujardin (2010)Noireau F, Dujardin JP 2010. Biology of Triatominae. In J Telleria, M Tibayrenc (eds.), American trypanosomiasis: Chagas disease one hundred years of research, Elsevier, Burlington, 870 pp., so that species adapted to peridomestic areas, but not found inside houses, are considered domiciliated/domesticated. However, some of these species have also been classified as peridomestic (e.g.,Tritoma sordida) or synanthropic by other authors to differentiate them from those that are also extensively found inside houses.

TABLE I
Classification of triatomine species according to their relationship with human housing

TABLE II
Main triatomine species and their level of domiciliation

Population genetics studies based on morphometric and molecular markers are also commonly used. Phylogeographic studies have been used to understand the general distribution of species over wide geographic areas and finer scale studies have focused on evaluating the relationships among populations from different habitats (Gourbière et al. 2012Gourbière S, Dorn P, Tripet F, Dumonteil E 2012. Genetics and evolution of triatomines: from phylogeny to vector control. Heredity 108: 190-202.). A high gene flow between populations found inside dwellings and sylvatic environment (and the concomitant lack of population genetic structure - i.e., panmixia) is indicative of an elevated dispersal of bugs between habitats, hence a strongly intrusive behaviour. Conversely, a low gene flow resulting in the genetic differentiation of domestic and sylvatic populations suggests a significant domiciliation/domestication of a population. These approaches have been extensively used to assess the population genetic structure of several species (Table II).

Interestingly, based on the observation of a reduced sexual dimorphism in domesticated populations compared to sylvatic ones, Dujardin et al. (1999)Dujardin JP, Steindel M, Chavez T, Machane M, Schofield CJ 1999. Changes in the sexual dimorphism of triatominae in the transition from natural to artificial habitats. Mem Inst Oswaldo Cruz 94: 565-569. proposed that morphometry may be used as an indicator of the level of adaptation of a species to domestic habitat. However, these observations were not associated with a clear measure of adaptation or fitness of the populations to the domestic habitat.

The data presented in Table II indicate that the classification of triatomine association with human habitat according to current definitions (Table I) is sometimes subjective, depending on the type of data available to establish the nature of the infestation process and this may have important implications for an effective vector control. Indeed, while very few species have been able to reach domestication [estimated at less than 5% of all species following Noireau and Dujardin (2010)Noireau F, Dujardin JP 2010. Biology of Triatominae. In J Telleria, M Tibayrenc (eds.), American trypanosomiasis: Chagas disease one hundred years of research, Elsevier, Burlington, 870 pp.], most show very variable capability to invade human housing. It is clear that more objective (and quantitative) criteria are needed to describe this process. We next focus on three triatomine species that have been extensively studied to evaluate additional criteria which may be helpful for a better understanding of infestation.

Case studies

Triatoma dimidiata - T. dimidiata is one of the most important vector of T. cruzi, distributed from central Mexico throughout Central America, to Colombia, Venezuela, Ecuador and Peru (Dorn et al. 2007Dorn PL, Monroy C, Curtis A 2007. Triatoma dimidiata (Latreille, 1811): a review of its diversity across its geographic range and the relationship among populations. Infect Genet Evol 7: 343-352.) (Figure). It is actually a species complex, although the exact number of taxonomic groups to be considered is still debated (Bargues et al. 2008Bargues MD, Klisiowicz DR, Gonzalez-Candelas F, Ramsey J, Monroy C, Ponce C, Salazar-Schettino PM, Panzera F, Abad F, Sousa OE, Schofield C, Dujardin JP, Guhl F, Mas-Coma S 2008. Phylogeography and genetic variations ofTriatoma dimidiata, the main Chagas disease vector in Central America and its position within the genus Triatoma.PLoS Negl Trop Dis 2: e233., Dorn et al. 2009, Herrera-Aguilar et al. 2009Herrera-Aguilar M, Be-Barragán LA, Ramirez-Sierra MJ, Tripet F, Dorn P, Dumonteil E 2009. Identification of a large hybrid zone between sympatric sibling species of Triatoma dimidiata in the Yucatan Peninsula, Mexico, and its epidemiological importance. Infect Genet Evol 9: 1345-1351., Monteiro et al. 2013Monteiro FA, Peretolchina T, Lazoski C, Harris K, Dotson EM, Abad-Franch F, Tamayo E, Pennington PM, Monroy C, Cordon-Rosales C, Salazar-Schettino PM, Gomez-Palacio A, Grijalva MJ, Beard CB, Marcet PL 2013. Phylogeographic pattern and extensive mitochondrial DNA divergence disclose a species complex within the Chagas disease vector Triatoma dimidiata. PLoS ONE 8: e70974.). This species complex presents highly variable levels of adaptation to humans housing, depending of the geographic region, but possibly also depending on the taxonomic group.

In Guatemala, populations are well domesticated as evidenced by bug collections throughout the country showing high infestation and colonisation indexes (Monroy et al. 2003aMonroy C, Rodas A, Mejía M, Rosales R, Tabaru Y 2003a. Epidemiology of Chagas disease in Guatemala: infection rate of Triatoma dimidiata, Triatoma nitida and Rhodnius prolixus (Hemiptera, Reduviidae) with Trypanosoma cruzi and Trypanosoma rangeli (Kinetoplastida, Trypanosomatidae). Mem Inst Oswaldo Cruz 98: 305-310., bMonroy MC, Bustamante DM, Rodas AG, Enriquez ME, Rosales RG 2003b. Habitats, dispersion and invasion of sylvatic Triatoma dimidiata (Hemiptera: Reduviidae: Triatominae) in Peten, Guatemala.J Med Entomol 40: 800-806., Nakagawa et al. 2005Nakagawa J, Juarez J, Nakatsuji K, Akiyama T, Hernandez G, Macal R, Flores C, Ortiz M, Marroquin L, Bamba T, Wakai S 2005. Geographical characterization of the triatomine infestations in north-central Guatemala.Ann Trop Med Parasitol 99: 307-315.). Housing quality and type are key factors affecting domestic colonisation/infestation and in particular poor wall plastering, which may offer a favourable habitat for bugs (Bustamante et al. 2009Bustamante DM, Monroy C, Pineda S, Rodas A, Castro X, Ayala V, Quinones J, Moguel B, Trampe R 2009. Risk factors for intradomiciliary infestation by the Chagas disease vector Triatoma dimidiata in Jutiapa, Guatemala. Cad Saude Publica 25 (Suppl. 1): 83-92.). Population genetics studies showed some conflicting results, with limited gene flow in agreement with domestication in some cases, but also significant gene flow between sylvatic and domestic populations, suggesting dispersal (Calderon et al. 2004Calderon CI, Dorn PL, Melgar S, Chavez JJ, Rodas A, Rosales R, Monroy CM 2004. A preliminary assessment of genetic differentiation ofTriatoma dimidiata (Hemiptera: Reduviidae) in Guatemala by random amplification of polymorphic DNA-polymerase chain reaction. J Med Entomol 41: 882-887.). The analysis of the genetic structure of the population in a single house further showed a great genetic heterogeneity suggesting polyandry and/or high levels of migration of the vector (Melgar et al. 2007Melgar S, Chávez JJ, Landaverde P, Herrera F, Rodas A, Enríquez E, Dorn P, Monroy C 2007. The number of families of Triatoma dimidiata in a Guatemalan house. Mem Inst Oswaldo Cruz 102: 221-223.).

Vector control with insecticide spraying has been relatively effective in Guatemala, although some re-infestation has been occurring (Nakagawa et al. 2003bNakagawa J, Hashimoto K, Cordón-Rosales C, Juarez JA, Trampe R, Marroquin LM 2003b. The impact of vector control on Triatoma dimidiata in the Guatemalan department of Jutiapa. Ann Trop Med Parasitol 97: 288-297., Hashimoto et al. 2006Hashimoto K, Cordón-Rosales C, Trampe R, Kawabata M 2006. Impact of single and multiple residual sprayings of pyrethroid insecticides againstTriatoma dimidiata (Reduviiade; Triatominae), the principal vector of Chagas disease in Jutiapa, Guatemala. Am J Trop Med Hyg 75: 226-230.). Dispersing sylvatic bugs may contribute to re-infestation (Monroy et al. 2003b), as well as to the seasonal variations in infestation that have been observed, but the importance of sylvatic populations in domestic infestation is still unclear. More recent studies suggest that integrated and community-based interventions may provide a better and more sustainable control of T. dimidiata in this region (Monroy et al. 2012Monroy C, Castro X, Bustamante DM, Pineda SS, Rodas A, Moguel B, Ayala V, Quiñonez J 2012. An ecosystem approach for the prevention of Chagas disease in rural Guatemala. In DF Charron (ed.), Ecohealth research in practice. Innovative applications of an ecosystem approach to health, Springer, New York, p. 153-162., Pellecer et al. 2013Pellecer MJ, Dorn PL, Bustamante DM, Rodas A, Monroy MC 2013. Vector blood meals are an early indicator of the effectiveness of the ecohealth approach in halting Chagas transmission in Guatemala. Am J Trop Med Hyg 88: 638-644., Bustamante et al. 2014Bustamante DM, de Urioste-Stone SM, Juarez JG, Pennington PM 2014. Ecological, social and biological risk factors for continued Trypanosoma cruzi transmission by Triatoma dimidiata in Guatemala. PLoS ONE 9: e104599., de Urioste-Stone et al. 2015de Urioste-Stone SM, Pennington PM, Pellecer E, Aguilar TM, Samayoa G, Perdomo HD, Enríquez H, Juárez JG 2015. Development of a community-based intervention for the control of Chagas disease based on peridomestic animal management: an eco-bio-social perspective. Trans R Soc Trop Med Hyg 109: 159-167.).

On the other hand, in the Yucatan Peninsula, Mexico, T. dimidiatapopulations are one of the best-characterised examples of a nondomiciliated but intrusive vector. Initial observations indicated that adult T. dimidiata transiently infests houses on a seasonal basis during the months of March-July (Dumonteil et al. 2002Dumonteil E, Gourbière S, Barrera-Perez M, Rodriguez-Felix E, Ruiz-Piña H, Baños-Lopez O, Ramirez-Sierra MJ, Menu F, Rabinovich JE 2002. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruzi in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 67: 176-183.,2009Dumonteil E, Ferral J, Euan-García M, Chavez-Nuñez L, Ramirez-Sierra MJ 2009. Usefullness of community participation for the fine-scale monitoring of non-domiciliated triatomines. J Parasitol 95: 469-471., Guzman-Tapia et al. 2007Guzman-Tapia Y, Ramirez-Sierra MJ, Dumonteil E 2007. Urban infestation by Triatoma dimidiata in the city of Mérida, Yucatan, Mexico. Vector Borne Zoonotic Dis 7: 597-606., Payet et al. 2009Payet V, Ramirez-Sierra MJ, Rabinovich J, Menu F, Dumonteil E 2009. Variations in sex-ratio, feeding and fecundity of Triatoma dimidiata between habitats in the Yucatan Peninsula, Mexico.Vector Borne Zoonotic Dis 9: 243-251.). This infestation is responsible for a seroprevalence of T. cruzi infection in humans of about 1-5% (Guzman-Bracho et al. 1998Guzman-Bracho C, Garcia-Garcia L, Floriani-Verdugo J, Guerrero-Martinez S, Torres-Cosme M, Ramirez-Melgar C, Velasco-Castrejon O 1998. Riesgo de transmisión de Trypanosoma cruzi por transfusión de sangre en México. Rev Panam Salud Publica 4: 94-99., Sosa-Estani et al. 2008Sosa-Estani S, Gamboa-Leon MR, Del Cid-Lemus J, Althabe F, Alger J, Almendares O, Cafferata ML, Chippaux JP, Dumonteil E, Gibbons L, Padilla-Raygoza N, Schneider D, Belizan JM, Buekens P 2008. Use of a rapid test on umbilical cord blood to screen for Trypanosoma cruzi infection in pregnant women in Argentina, Bolivia, Honduras and Mexico. Am J Trop Med Hyg 79: 755-759., Gamboa-León et al. 2014Gamboa-León R, Ramirez-Gonzalez C, Pacheco-Tucuch F, O’Shea M, Rosecrans K, Pippitt J, Dumonteil E, Buekens P 2014. Chagas disease among mothers and children in rural Mayan communities. Am J Trop Med Hyg 91: 348-353.). Population genetics and mathematical models describing the population stage-structure as well as the dispersal of T. dimidiataindicate that house infestation is caused by the seasonal dispersal of bugs from peridomestic and sylvatic habitats surrounding the villages, while triatomine reproduction in the domestic habitat (i.e., domiciliation) plays a negligible role (Dumonteil et al. 2007Dumonteil E, Tripet F, Ramirez-Sierra MJ, Payet V, Lanzaro G, Menu F 2007. Assessment of Triatoma dimidiata dispersal in the Yucatan Peninsula of Mexico using morphometry and microsatellite markers. Am J Trop Med Hyg 76: 930-937., Gourbière et al. 2008Gourbière S, Dumonteil E, Rabinovich J, Minkoue R, Menu F 2008. Demographic and dispersal constraints for domestic infestation by non-domiciliated Chagas disease vectors in the Yucatan Peninsula, Mexico.Am J Trop Med Hyg 78: 133-139., Barbu et al. 2009Barbu C, Dumonteil E, Gourbière S 2009. Optimization of control strategies for non-domiciliated Triatoma dimidiata, Chagas disease vector in the Yucatan Peninsula, Mexico. PLoS Negl Trop Dis 3: e416.). Indeed, while nymphs may occasionally be found in houses (Dumonteil et al. 2002Dumonteil E, Gourbière S, Barrera-Perez M, Rodriguez-Felix E, Ruiz-Piña H, Baños-Lopez O, Ramirez-Sierra MJ, Menu F, Rabinovich JE 2002. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruzi in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 67: 176-183.), the low colonisation index (< 20%) rather suggests unsuccessful attempts at colonising the domestic habitat by intruding bugs, possibly because of insufficient feeding (Payet et al. 2009Payet V, Ramirez-Sierra MJ, Rabinovich J, Menu F, Dumonteil E 2009. Variations in sex-ratio, feeding and fecundity of Triatoma dimidiata between habitats in the Yucatan Peninsula, Mexico.Vector Borne Zoonotic Dis 9: 243-251.). Such poor feeding in the domestic habitat may be associated with sleeping habits in the region, as hammocks were found to complicate bug access to a host and particularly for nymphs (E Waleckx et al., unpublished observations).

Further modelling and field investigations of the spatiotemporal infestation patterns indicated that houses located in the periphery of the villages are significantly more infested than those located in the village centre (Slimi et al. 2009Slimi R, El Yacoubi S, Dumonteil E, Gourbière S 2009. A cellular automata model for Chagas disease. Applied Math Modelling 33: 1072-1085., Barbu et al. 2010Barbu C, Dumonteil E, Gourbière S 2010. Characterization of the dispersal of non-domiciliated Triatoma dimidiata through the selection of spatially explicit models. PLoS Negl Trop Dis 4: e777., 2011Barbu C, Dumonteil E, Gourbière S 2011. Evaluation of spatially targeted strategies to control non-domiciliated Triatoma dimidiata vector of Chagas disease. PLoS Negl Trop Dis 5: e1045., Ramirez-Sierra et al. 2010Ramirez-Sierra MJ, Herrera-Aguilar M, Gourbière S, Dumonteil E 2010. Patterns of house infestation dynamics by non-domiciliated Triatoma dimidiata reveal a spatial gradient of infestation in rural villages and potential insect manipulation by Trypanosoma cruzi. Trop Med Int Health 15: 77-86.). Attraction by public lights also contributes significantly to transient infestation (Pacheco-Tucuch et al. 2012Pacheco-Tucuch FS, Ramirez-Sierra MJ, Gourbière S, Dumonteil E 2012. Public street lights increase house infestation by the Chagas disease vectorTriatoma dimidiata. PLoS ONE 7: e36207.), together with the presence of domestic animals such as dogs and chickens, while housing type and quality or socioeconomic level do not play a significant role (Dumonteil et al. 2013Dumonteil E, Nouvellet P, Rosecrans K, Ramirez-Sierra MJ, Gamboa-León R, Cruz-Chan V, Rosado-Vallado M, Gourbière S 2013. Eco-bio-social determinants for house infestation by non-domiciliated Triatoma dimidiata in the Yucatan Peninsula, Mexico. PLoS Negl Trop Dis 7: e2466.). Inhabitants are rather familiar with this seasonal invasive behaviour of T. dimidiata (Rosecrans et al. 2014Rosecrans K, Cruz-Martin G, King A, Dumonteil E 2014. Opportunities for improved Chagas disease vector control based on knowledge, attitudes and practices of communities in the Yucatan Peninsula, Mexico. PLoS Negl Trop Dis 8: e2763.).

In this situation, effective insecticide spraying would require yearly applications within a narrow time window of less than two months, which would be difficult to implement and clearly unsustainable, while insect screens may offer a sustainable and effective alternative (Dumonteil et al. 2004Dumonteil E, Ruiz-Piña H, Rodriguez-Félix E, Barrera-Pérez M, Ramirez-Sierra MJ, Rabinovich JE, Menu F 2004. Re-infestation of houses by Triatoma dimidiata after intra-domicile insecticide application in the Yucatán Peninsula, Mexico. Mem Inst Oswaldo Cruz 99: 253-256., Barbu et al. 2009Barbu C, Dumonteil E, Gourbière S 2009. Optimization of control strategies for non-domiciliated Triatoma dimidiata, Chagas disease vector in the Yucatan Peninsula, Mexico. PLoS Negl Trop Dis 3: e416., 2011Barbu C, Dumonteil E, Gourbière S 2011. Evaluation of spatially targeted strategies to control non-domiciliated Triatoma dimidiata vector of Chagas disease. PLoS Negl Trop Dis 5: e1045., Ferral et al. 2010Ferral J, Chavez-Nuñez L, Euan-Garcia M, Ramirez-Sierra MJ, Najera-Vasquez MR, Dumonteil E 2010. Comparative field trial of alternative vector control strategies for non-domiciliated Triatoma dimidiata in the Yucatan Peninsula, Mexico. Am J Trop Med Hyg 82: 60-66.). Environmental management of the peridomiciles, i.e., the elimination of peridomestic colonies by cleaning and insecticide spraying, was found to partially but durably reduce house infestation and may thus be an important component of vector control interventions (Ferral et al. 2010Ferral J, Chavez-Nuñez L, Euan-Garcia M, Ramirez-Sierra MJ, Najera-Vasquez MR, Dumonteil E 2010. Comparative field trial of alternative vector control strategies for non-domiciliated Triatoma dimidiata in the Yucatan Peninsula, Mexico. Am J Trop Med Hyg 82: 60-66.). Spatially targeted interventions may allow for further optimisation of vector control (Barbu et al. 2011Barbu C, Dumonteil E, Gourbière S 2011. Evaluation of spatially targeted strategies to control non-domiciliated Triatoma dimidiata vector of Chagas disease. PLoS Negl Trop Dis 5: e1045.). Based on this, an ecohealth approach has recently been tested at a small scale, based on a community-based installation of window insect screens in bedrooms, with or without education for improved peridomestic animal management (Waleckx et al. 2015Waleckx E, Camara-Mejia J, Ramirez-Sierra MJ, Cruz-Chan V, Rosado-Vallado M, Vazquez-Narvaez S, Najera-Vazquez R, Gourbière S, Dumonteil E 2015. An innovative ecohealth intervention for Chagas disease vector control in Yucatan, Mexico. Trans R Soc Trop Med Hyg 109: 143-149.). Such integrated control strategy seems very promising for the sustainable control of this intrusive vector in the Yucatan Peninsula.

Analysis of the genetic structure of T. dimidiata in Boyaca, Colombia, also indicated a low level of genetic differentiation and a high level of exchanges of bugs among domestic, peridomestic and sylvatic habitats (Ramirez et al. 2005Ramirez CJ, Jaramillo CA, Delgado MP, Pinto NA, Aguilera G, Guhl F 2005. Genetic structure of sylvatic, peridomestic and domestic populations ofTriatoma dimidiata (Hemiptera: Reduviidae) from an endemic zone of Boyaca, Colombia. Acta Trop 93: 23-29.), suggesting that the situation observed in the Yucatan Peninsula and Belize (Polonio et al. 2009Polonio R, Ramirez-Sierra MJ, Dumonteil E 2009. Dynamics and distribution of house infestation by Triatoma dimidiata in central and southern Belize. Vector Borne Zoonotic Dis 9: 19-24.) may also be occurring in parts of Colombia.

Panstrongylus geniculatus - P. geniculatus is one of the most widely distributed species of triatomine in South and Central America (Leite et al. 2007Leite GR, dos Santos CB, Falqueto A 2007. Insecta, Hemiptera, Reduviidae, Panstrongylus geniculatus: geographic distribution map. Check List 3: 147-152.) (Figure). It is commonly considered as a sylvatic species frequently flying to human habitations, probably attracted by light (Lent & Wygodzinsky 1979Lent H, Wygodzinsky P 1979. Revision of the Triatominae (Hemiptera, Reduviidae) and their significance as vectors of Chagas disease. Bull Am Mus Nat Hist Nat 163: 123-520.). The intrusion of adult bugs is well documented and collections of only adult specimens inside dwellings have been reported in different areas (particularly in the Amazon Basin, but not only) in Venezuela (Serrano et al. 2008Serrano O, Mendoza F, Suarez B, Soto A 2008. Seroepidemiology of Chagas disease in two rural populations in the municipality of Costa de Oro, at Aragua state, northern Venezuela. Biomedica 28: 108-115., Reyes-Lugo 2009)Reyes-Lugo M 2009. Panstrongylus geniculatusLatreille 1811 (Hemiptera: Reduviidae: Triatominae), vector de la enfermedad de Chagas en el ambiente domiciliario del centro-norte de Venezuela. Rev Biomed 20: 180-205., Colombia (Angulo et al. 2012)Angulo VM, Esteban L, Luna KP 2012. Attalea butyracea palms adjacent to housing as a source of infestation byRhodnius prolixus (Hemiptera: Reduviidae).Biomedica 32: 277-285., Brazil (Naiff et al. 1998Naiff MF, Naiff RD, Barett TV 1998. Vetores selváticos de doença de Chagas na área urbana de Manaus (AM): atividade de vôo nas estações secas e chuvosas. Rev Soc Bras Med Trop 31: 103-105., Fe et al. 2009Fe NF, Magalhães LK, Fe FA, Arakian SK, Monteiro WM, Barbosa MD 2009. Occurrences of triatomines in wild and domestic environments in the municipality of Manaus, state of Amazonas. Rev Soc Bras Med Trop 42: 642-646., Maeda et al. 2012)Maeda MH, Knox MB, Gurgel-Gonçalves R 2012. Occurrence of synanthropic triatomines (Hemiptera: Reduviidae) in the Federal District of Brazil. Rev Soc Bras Med Trop 45: 71-76., Peru (Cáceres et al. 2002Cáceres AG, Troyes L, Gonzáles-Pérez A, Llontop E, Bonilla C, Murias E, Heredia N, Velásquez C, Yáñez C 2002. Enfermedad de Chagas en la región nororiental del Perú. I. Triatominos (Hemiptera, Reduviidae) presentes en Cajamarca y Amazonas. Rev Peru Med Exp Salud Publica 19: 17-23.,Torres & Cabrera 2010)Torres DB, Cabrera R 2010. Geographical distribution and intra-domiciliary capture of sylvatic triatomines in La Convención province, Cusco, Peru. Rev Inst Med Trop Sao Paulo 52: 157-160., Bolivia (Depickère et al. 2011, 2012)Depickère S, Durán P, López R, Chávez T 2011. Presence of intra- domicile colonies of the triatomine bug Panstrongylus rufotuberculatus in Muñecas, La Paz, Bolivia. Acta Trop 117: 97-100., 2012Depickère S, Duran P, Lopez R, Martinez E, Chavez T 2012. After five years of chemical control: colonies of the triatomine Eratyrus mucronatus are still present in Bolivia. Acta Trop 123: 234-238.) and Argentina (Damborsky et al. 2001)Damborsky MP, Bar ME, Oscherov EB 2001. Detección de triatominos (Hemiptera: Reduviidae) en ambientes domésticos y extradomésticos, Corrientes, Argentina. Cad Saude Publica 17: 843-849.. The main factors that cause P. geniculatus to increasingly invade human dwellings seem to be the devastation of the primary forests (for example for the construction of human dwellings), overhunting and burning of forests, all of which destroying the triatomines’ natural habitat and causing them to seek alternative shelter and hosts (Valente 1999)Valente VC 1999. Potential for domestication ofPanstrongylus geni- culatus (Latreille, 1811) (Hemiptera, Reduviidae, Triatominae) in the municipality of Muaná, Marajó Island, Pará state, Brazil. Rev Soc Bras Med Trop 32: 595-597.. Although the intrusion of adult bugs and the absence of colonisation seem to be the most common behaviours of this species, some events of domicile colonisation have also been reported. Indeed, there are some reports of nymphal stages and colonies of P. geni- culatus found in peridomiciles and/or inside dwellings in Venezuela (Reyes-Lugo & Rodriguez-Acosta 2000Reyes-Lugo M, Rodriguez-Acosta A 2000. Domiciliation of the sylvatic Chagas disease vector Panstrongylus geniculatus Latreille, 1811 (Triatominae: Reduviidae) in Venezuela. Trans R Soc Trop Med Hyg 94: 508.,Feliciangeli et al. 2004Feliciangeli MD, Carrasco H, Patterson JS, Suarez B, Martinez C, Medina M 2004. Mixed domestic infestation by Rhodnius prolixusStål, 1859 and Panstrongylus geniculatus Latreille, 1811, vector incrimination and seroprevalence for Trypanosoma cruziamong inhabitants in El Guamito, Lara state, Venezuela. Am J Trop Med Hyg 71: 501-505., Rodríguez-Bonfante et al. 2007)Rodríguez-Bonfante C, Amaro A, García M, Wohlert LEM, Guillen P, García RA, Álvarez N, Díaz M, Cárdenas E, Castillo S, Bonfante-Garrido R, Bonfante-Cabarcas R 2007. Epidemiology of Chagas disease in Andres Eloy Blanco, Lara, Venezuela: triatomine infestation and human seroprevalence. Cad Saude Publica 23: 1133-1140., Brazil (Valente et al. 1998)Valente VC, Valente SAS, Noireau F, Carrasco HJ, Miles MA 1998. Chagas disease in the Amazon Basin: association of Panstrongylus geniculatus (Hemiptera: Reduviidae) with domestic pigs. J Med Entomol 35: 99-103., Ecuador (Chico et al. 1997)Chico HM, Sandoval C, Guevara EA, Calvopiña HM, Cooper PJ, Reed SG, Guderian RH 1997. Chagas disease in Ecuador: evidence for disease transmission in an indigenous population in the Amazon Region. Mem Inst Oswaldo Cruz 92: 317-320., Bolivia (Depickère et al. 2011)Depickère S, Durán P, López R, Chávez T 2011. Presence of intra- domicile colonies of the triatomine bug Panstrongylus rufotuberculatus in Muñecas, La Paz, Bolivia. Acta Trop 117: 97-100. and Colombia (Maestre-Serrano & Eyes-Escalante 2012)Maestre-Serrano R, Eyes-Escalante M 2012. Current state of the presence and distribution of triatomine in the department of Atlantico-Colombia: 2003-2010. Bol Mal Salud Amb 52: 125-128.. Consequently, the species is now increasingly considered as a species in the process of domiciliation/domestication.


Geographic distribution of T. dimidiata, P. geniculatus and R. ecuadoriensis.

Interestingly, Aldana et al. (2011)Aldana E, Heredia-Coronado E, Avendano-Rangel F, Lizano E, Concepcion JL, Bonfante-Cabarcas R, Rodríguez-Bonfante C, Pulido MM 2011. Morphometric analysis of Panstrongylus geniculatus(Heteroptera: Reduviidae) from Caracas city, Venezuela. Biomedica 31: 108-117. found that the sexual dimorphism of the isometric size of adults of P. geniculatus was reduced in bugs collected in domestic environment compared to bugs collected in sylvatic environments in Venezuela. In this study, the authors considered that this may be an indicator of domiciliation, as proposed byDujardin et al. (1999)Dujardin JP, Steindel M, Chavez T, Machane M, Schofield CJ 1999. Changes in the sexual dimorphism of triatominae in the transition from natural to artificial habitats. Mem Inst Oswaldo Cruz 94: 565-569..

Additionally, there are reports of people being attacked by this bug species inside their homes (Valente et al. 1998Valente VC, Valente SAS, Noireau F, Carrasco HJ, Miles MA 1998. Chagas disease in the Amazon Basin: association of Panstrongylus geniculatus (Hemiptera: Reduviidae) with domestic pigs. J Med Entomol 35: 99-103., Reyes-Lugo & Rodriguez-Acosta 2000Reyes-Lugo M, Rodriguez-Acosta A 2000. Domiciliation of the sylvatic Chagas disease vector Panstrongylus geniculatus Latreille, 1811 (Triatominae: Reduviidae) in Venezuela. Trans R Soc Trop Med Hyg 94: 508., Carrasco et al. 2005Carrasco HJ, Torrellas A, Garcia C, Segovia M, Feliciangeli MD 2005. Risk of Trypanosoma cruzi I (Kinetoplastida: Trypanosomatidae) transmission by Panstrongylus geniculatus (Hemiptera: Reduviidae) in Caracas (metropolitan district) and neighboring states, Venezuela. Int J Parasitol 35: 1379-1384., Reyes-Lugo 2009)Reyes-Lugo M 2009. Panstrongylus geniculatusLatreille 1811 (Hemiptera: Reduviidae: Triatominae), vector de la enfermedad de Chagas en el ambiente domiciliario del centro-norte de Venezuela. Rev Biomed 20: 180-205., which has been confirmed by blood meal analyses (Feliciangeli et al. 2004Feliciangeli MD, Carrasco H, Patterson JS, Suarez B, Martinez C, Medina M 2004. Mixed domestic infestation by Rhodnius prolixusStål, 1859 and Panstrongylus geniculatus Latreille, 1811, vector incrimination and seroprevalence for Trypanosoma cruziamong inhabitants in El Guamito, Lara state, Venezuela. Am J Trop Med Hyg 71: 501-505., Carrasco et al. 2005)Carrasco HJ, Torrellas A, Garcia C, Segovia M, Feliciangeli MD 2005. Risk of Trypanosoma cruzi I (Kinetoplastida: Trypanosomatidae) transmission by Panstrongylus geniculatus (Hemiptera: Reduviidae) in Caracas (metropolitan district) and neighboring states, Venezuela. Int J Parasitol 35: 1379-1384.. P. geniculatus has also been increasingly identified as the likely responsible vector in some acute cases of Chagas disease (Vega et al. 2006Vega S, Mendoza A, Cabrera R, Cáceres AG, Campos E, Ancca J, Pinto J, Torres S, Cabrera D, Yale G, Cevallos R, Náquira C 2006. Primer caso de enfermedad de Chagas aguda en la Selva Central del Perú: investigación de colaterales, vectores y reservorios. Rev Peru Med Exp Salud Publica 23: 288-292., Valente et al. 2009Valente SAS, Valente VC, Pinto AYN, César MJB, dos Santos MP, Miranda COS, Cuervo P, Fernandes O 2009. Analysis of an acute Chagas disease outbreak in the Brazilian Amazon: human cases, triatomines, reservoir mammals and parasites. Trans R Soc Trop Med Hyg 103: 291-297., Cabrera et al. 2010Cabrera R, Vega S, Caceres AG, Ramal AC, Alvarez C, Ladera P, Pinedo R, Chuquipiondo G 2010. Epidemiological investigation of an acute case of Chagas disease in an area of active transmission in Peruvian Amazon Region. Rev Inst Med Trop Sao Paulo 52: 269-272.,Rios et al. 2011)Rios JF, Arboleda M, Montoya AN, Alarcon EP, Parra-Henao GJ 2011. Probable outbreak of oral transmission of Chagas disease in Turbo, Antioquia.Biomedica 31: 185-195. in South America. Consequently, it is given more consideration as a major vector of Chagas disease by vector control programs, but no strategy has been specifically defined against this vector and current data indicate that a more precise evaluation of its level of intrusion inside houses and of its potential for domiciliation/domestication is clearly needed so that these aspects may be taken into account for the design of effective and sustainable vector control interventions against P. geniculatus.

Rhodnius ecuadoriensisR. ecuadoriensis is distributed from southern Colombia throughout eastern Ecuador and in northern Peru, where it is considered an important vector of T. cruzi (Figure). However, studies on its ecology and vectorial role have been limited and report somewhat conflicting results. The species was initially described infesting and colonising domiciles in Peru and Ecuador and this was quickly extended to the peridomestic habitat and R. ecuadoriensis was labelled as a synanthropic species (Abad-Franch et al. 2002Abad-Franch F, Aguilar VHM, Paucar CA, Lorosa ES, Noireau F 2002. Observations on the domestic ecology of Rhodnius ecuadoriensis(Triatominae). Mem Inst Oswaldo Cruz 97: 199-202., Cuba Cuba et al. 2002Cuba Cuba CA, Abad-Franch F, Rodríguez JR, Vásquez FV, Velásquez LP, Miles MA 2002. The triatomines of northern Peru with emphasis on the ecology and infection by trypanosomes of Rhodnius ecuadoriensis(Triatominae). Mem Inst Oswaldo Cruz 97: 175-183., 2003Cuba Cuba CA, Vargas F, Roldan J, Ampuero C 2003. DomesticRhodnius ecuadoriensis (Hemiptera, Reduviidae) infestation in northern Peru: a comparative trial of detection methods during a six-month follow-up. Rev Inst Med Trop Sao Paulo 45: 85-90., Grijalva et al. 2005Grijalva MJ, Palomeque-Rodriguez FS, Costales JA, Davila S, Arcos-Teran L 2005. High household infestation rates by synanthropic vectors of Chagas disease in southern Ecuador. J Med Entomol 42: 68-74.), in the sense that it was domiciliated/domesticated. Frequent blood feeding on humans from these bug populations was also reported (Abad-Franch et al. 2002Abad-Franch F, Aguilar VHM, Paucar CA, Lorosa ES, Noireau F 2002. Observations on the domestic ecology of Rhodnius ecuadoriensis(Triatominae). Mem Inst Oswaldo Cruz 97: 199-202.). However, further studies showed thatR. ecuadoriensis was also abundant in sylvatic habitats, principally associated with palm trees, as most Rhodnius species (Abad-Franch et al. 2000Abad-Franch F, Noireau F, Paucar A, Aguilar HM, Carpio C, Racines J 2000. The use of live-bait traps for the study of sylvatic Rhod- nius populations (Hemiptera: Reduviidae) in palm trees. Trans R Soc Trop Med Hyg 94: 629-630., 2005Abad-Franch F, Palomeque FS, Aguilar HM, Miles MA 2005. Field ecology of sylvatic Rhodnius populations (Heteroptera, Triatominae): risk factors for palm tree infestation in western Ecuador.Trop Med Int Health 10: 1258-1266., Grijalva & Villacis 2009Grijalva MJ, Villacis AG 2009. Presence of Rhodnius ecuadoriensis in sylvatic habitats in the southern highlands (Loja province) of Ecuador. J Med Entomol 46: 708-711., Suarez-Davalos et al. 2010Suarez-Davalos V, Dangles O, Villacis AG, Grijalva MJ 2010. Microdistribution of sylvatic triatomine populations in central-coastal Ecuador.J Med Entomol 47: 80-88., Grijalva et al. 2012)Grijalva MJ, Suarez-Davalos V, Villacis AG, Ocana-Mayorga S, Dangles O 2012. Ecological factors related to the widespread distribution of sylvaticRhodnius ecuadoriensis populations in southern Ecuador.Parasit Vectors 5: 17., raising the question of the relationship between its sylvatic and domestic/peridomestic populations. The initial hypothesis was that synanthropic populations were relatively isolated from sylvatic ones, at least in southern Ecuador and northern Peru, raising the possibility that synanthropic populations may be eliminated by insecticide spraying interventions (Abad-Franch et al. 2001Abad-Franch F, Paucar CA, Carpio CC, Cuba Cuba CA, Aguilar VHM, Miles MA 2001. Biogeography of Triatominae (Hemiptera: Reduviidae) in Ecuador: implications for the design of control strategies. Mem Inst Oswaldo Cruz 96: 611-620., Cuba Cuba et al. 2002)Cuba Cuba CA, Abad-Franch F, Rodríguez JR, Vásquez FV, Velásquez LP, Miles MA 2002. The triatomines of northern Peru with emphasis on the ecology and infection by trypanosomes of Rhodnius ecuadoriensis(Triatominae). Mem Inst Oswaldo Cruz 97: 175-183.. However, such interventions were met with limited success, as a significant re-infestation was observed following spraying (Grijalva et al. 2011)Grijalva MJ, Villacis AG, Ocana-Mayorga S, Yumiseva CA, Baus EG 2011. Limitations of selective deltamethrin application for triatomine control in central coastal Ecuador. Parasit Vectors 4: 20., indicating that vector control may result much more challenging.

Morphometric analysis of wing size and shape supported the presence of extensive exchanges of bugs among habitats in coastal Ecuador, but conversely suggested a significant population structuring in southern Ecuador, with a low dispersal and exchange of bugs among habitats (Villacis et al. 2010Villacis AG, Grijalva MJ, Catala SS 2010. Phenotypic variability ofRhodnius ecuadoriensis populations at the Ecuadorian central and southern Andean region. J Med Entomol 47: 1034-1043.). Such variability may be due to ecological differences in these regions, but may also reflect intrinsic differences in behaviour linked to genetic differences within the species. Indeed, two phylogenetic clades have been described in R. ecuadoriensis based on the cytochrome B mitochondrial marker (Abad-Franch & Monteiro 2005Abad-Franch F, Monteiro FA 2005. Molecular research and the control of Chagas disease vectors. An Acad Bras Cienc 77: 437-454.) and significant morphometric differences have been observed as well (Villacis et al. 2010)Villacis AG, Grijalva MJ, Catala SS 2010. Phenotypic variability ofRhodnius ecuadoriensis populations at the Ecuadorian central and southern Andean region. J Med Entomol 47: 1034-1043.. The level of domiciliation of R. ecuadoriensis may thus be variable, being more domiciliated in southern Ecuador and northern Peru and more sylvatic and intrusive in eastern Ecuador, although the factors underlying these differences remain unclear.

As evidenced by the difficulties in controlling this vector with indoor insecticide spraying (Grijalva et al. 2011Grijalva MJ, Villacis AG, Ocana-Mayorga S, Yumiseva CA, Baus EG 2011. Limitations of selective deltamethrin application for triatomine control in central coastal Ecuador. Parasit Vectors 4: 20.), defining the exact level of domiciliation/intrusion of the different populations of R. ecuadoriensis is still needed to define effective vector control interventions in the different regions where this species is present.

Revisiting the domiciliation process: toward operational definitions for vector control

The classification of triatomine species/populations into sylvatic, intrusive, domiciliary and domestic proposed earlier (Noireau & Dujardin 2010Noireau F, Dujardin JP 2010. Biology of Triatominae. In J Telleria, M Tibayrenc (eds.), American trypanosomiasis: Chagas disease one hundred years of research, Elsevier, Burlington, 870 pp.) is useful from a general evolutionary perspective. However, as evidenced in Table II and the examples detailed above, these theoretical concepts may be challenged by the realities of vector control.

A major limitation of current criteria defining the association of triatomine with human habitat is that these are essentially qualitative (Table I) and do not rely on quantitative variables, leaving much to the subjective interpretation of the data. This and the apparent regional variability of domiciliation level of the different populations of a same species may be the main reasons why some species/populations are classified differently by authors as shown in Table II. For most species, a quantification of the ability of species/population to reproduce and adapt in human habitat is needed for effective vector control. Indeed, indoor residual insecticide spraying has been very effective in only two settings: domesticTriatoma infestans in most of the Southern Cone countries and domestic R. prolixus in Central America. Thus, several Southern Cone countries and regions have been certified (or are in the process) as free ofT. infestans vectorial transmission and similarly in Central America with R. prolixus (Schofield et al. 2006Schofield CJ, Jannin J, Salvatella R 2006. The future of Chagas disease control. Trends Parasitol 22: 583-588.). This success is largely due to the fact that these T. infestans and R. prolixus populations were exclusively domesticated and introduced in these countries (i.e., with no sylvatic populations), which considerably limited the possibilities for re-infestation following spraying. On the other hand, the control of most other triatomine species/populations has been more challenging, mostly because domestic populations remain connected to sylvatic populations, which can then contribute to re-infestation. The same fact mostly explains why, in areas where T. infestans sylvatic foci exist, the elimination of house infestation is jeopardised. Indeed, while T. infestans has been described as one of the most domesticated triatomine species, the persistence and re-infestation of houses by this species in the Andean region can be attributed, at least in part, to the dispersal of bugs from sylvatic populations (Noireau et al. 2005Noireau F, Cortez MGR, Monteiro FA, Jansen AM, Torrico F 2005. Can wild Triatoma infestans foci in Bolivia jeopardize Chagas disease control efforts? Trends Parasitol 21: 7-10., Ceballos et al. 2011Ceballos LA, Piccinali RV, Marcet PL, Vazquez-Prokopec GM, Cardinal MV, Schachter-Broide J, Dujardin JP, Dotson EM, Kitron U, Gurtler RE 2011. Hidden sylvatic foci of the main vector of Chagas disease Triatoma infestans: threats to the vector elimination campaign? PLoS Negl Trop Dis 5: e1365., Brenière et al. 2013Brenière SF, Salas R, Buitrago R, Bremond P, Sosa V, Bosseno MF, Waleckx E, Depickère S, Barnabé C 2013. Wild populations of Triatoma infestans are highly connected to intra-peridomestic conspecific populations in the Bolivian Andes. PLoS ONE 8: e80786.). In the Andes, these have been found to be well established in sylvatic habitats over an extensive region (Buitrago et al. 2010Buitrago R, Waleckx E, Bosseno MF, Zoveda F, Vidaurre P, Salas R, Mamani E, Noireau F, Brenière SF 2010. First report of widespread wild populations of Triatoma infestans (Reduviidae, Triatominae) in the valleys of La Paz, Bolivia. Am J Trop Med Hyg 82: 574-579., Waleckx et al. 2011Waleckx E, Salas R, Huamán N, Buitrago R, Bosseno MF, Aliaga C, Barnabé C, Rodriguez R, Zoveda F, Monje M, Baune M, Quisberth S, Villena E, Kengne P, Noireau F, Brenière SF 2011. New insights on the Chagas disease main vector Triatoma infestans (Reduviidae, Triatominae) brought by the genetic analysis of Bolivian sylvatic populations. Infect Genet Evol 11: 1045-1057., Bremond et al. 2014Bremond P, Salas R, Waleckx E, Buitrago R, Aliaga C, Barnabé C, Depickère S, Dangles O, Brenière SF 2014. Variations in time and space of an Andean wild population of T. infestans at a microgeographic scale. Parasit Vectors 7: 164.) and to feed on humans relatively frequently (Buitrago et al. 2013Buitrago R, Bosseno MF, Waleckx E, Bremond P, Vidaurre P, Zoveda F, Brenière SF 2013. Risk of transmission of Trypanosoma cruzi by wild Triatoma infestans (Hemiptera: Reduviidae) in Bolivia supported by the detection of human blood meals. Infect Genet Evol 19: 141-144.). Dispersal of these sylvatic bugs towards houses for re-infestation will thus need to be taken into account for an effective control, even in the case of this emblematic highly domesticated species.

From the perspective of vector control, it is thus of major importance to determine precisely three aspects of the relationship of triatomines with humans: (i) the presence of sylvatic populations of triatomines, (ii) the level of intrusion of these sylvatic populations in peridomiciles and inside domiciles and (iii) the level of domiciliation or domestication in peridomiciles and inside houses. Indeed, this information should guide vector control program in their decision-making over the design of evidence-based interventions to ensure their effectiveness. A significant domiciliation or domestication inside dwellings would suggest that indoor insecticide spraying and/or housing-improvement interventions aimed at reducing the suitability of the domestic habitat would be effective in reducing/eliminating house infestation as was the case with T. infestans (Schofield et al. 2006Schofield CJ, Jannin J, Salvatella R 2006. The future of Chagas disease control. Trends Parasitol 22: 583-588.). On the other hand, a high level of intrusion inside dwellings would rule out indoor insecticide spraying as a key component of vector control, which would rather need to focus on limiting triatomine entry inside houses. Interventions based on window insect screens or insecticide-impregnated curtains (Herber & Kroeger 2003Herber O, Kroeger A 2003. Pyrethroid-impregnated curtains for Chagas disease control in Venezuela. Acta Trop 88: 33-38., Barbu et al. 2009, 20Barbu C, Dumonteil E, Gourbière S 2009. Optimization of control strategies for non-domiciliated Triatoma dimidiata, Chagas disease vector in the Yucatan Peninsula, Mexico. PLoS Negl Trop Dis 3: e416., 2011Barbu C, Dumonteil E, Gourbière S 2011. Evaluation of spatially targeted strategies to control non-domiciliated Triatoma dimidiata vector of Chagas disease. PLoS Negl Trop Dis 5: e1045., Ferral et al. 2010Ferral J, Chavez-Nuñez L, Euan-Garcia M, Ramirez-Sierra MJ, Najera-Vasquez MR, Dumonteil E 2010. Comparative field trial of alternative vector control strategies for non-domiciliated Triatoma dimidiata in the Yucatan Peninsula, Mexico. Am J Trop Med Hyg 82: 60-66., Waleckx et al. 2015)Waleckx E, Camara-Mejia J, Ramirez-Sierra MJ, Cruz-Chan V, Rosado-Vallado M, Vazquez-Narvaez S, Najera-Vazquez R, Gourbière S, Dumonteil E 2015. An innovative ecohealth intervention for Chagas disease vector control in Yucatan, Mexico. Trans R Soc Trop Med Hyg 109: 143-149. would thus be recommended. In any case, community education should also be considered as part of all vector interventions to strengthen their sustainability. Importantly, long-term entomological surveillance should be implemented to detect potential changes in vector population dynamics due to the adaptation or replacement of vector species, as well as the emergence of insecticide resistance.

Analysis of Table II and of the cases studies presented provides clues to the type of empirical and theoretical data needed to appreciate the levels of intrusion and domiciliation of triatomine species. As can be seen, the primary source of evidences comes from field studies based on timed-manuals collections, traps and sensors and/or community participation to document infestation patterns in different habitats. However, such studies may be misleading if too limited in scope, geographic coverage and sample size, as seen with the initial studies of R. ecuadoriensis, which suggested that it was synanthropic. Additionally to the collections in the domestic habitat, exhaustive searches in peridomestic and sylvatic habitats are needed for a complete description of triatomine distribution. Infestation data at different geographic scales is critical, with in depth studies limited to a small number of villages providing precise data on population structure and demography, complemented with larger scale studies including many villages, to allow for generalisation over large regions. The establishment of the level of domiciliation/intrusion of triatomines in the different habitats should be properly done at the same geographic scale as that of vector control intervention, since species can present regional differences in their level of domiciliation. In addition, while most studies are based on a single time-point, longitudinal studies clearly provide a more complete description of the infestation dynamics and its potential seasonal variations (Dumonteil et al. 2002Dumonteil E, Gourbière S, Barrera-Perez M, Rodriguez-Felix E, Ruiz-Piña H, Baños-Lopez O, Ramirez-Sierra MJ, Menu F, Rabinovich JE 2002. Geographic distribution of Triatoma dimidiata and transmission dynamics of Trypanosoma cruzi in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 67: 176-183., Schettino et al. 2007Schettino PMS, Piña JSR, Wastavino GR, Bravo MC, Blanco MV, Cárdenas JL 2007. Triatoma mexicana (Hemiptera: Reduviidae) in Guanajuato, Mexico: house infestation and seasonal variation. Mem Inst Oswaldo Cruz 102: 803-807., Payet et al. 2009Payet V, Ramirez-Sierra MJ, Rabinovich J, Menu F, Dumonteil E 2009. Variations in sex-ratio, feeding and fecundity of Triatoma dimidiata between habitats in the Yucatan Peninsula, Mexico.Vector Borne Zoonotic Dis 9: 243-251.).

The definitions in Table I are rather subjective and lack clear “thresholds” between the different domiciliation levels to objectively classify the triatomine populations in any of the categories. The classical entomologic indexes mentioned above may be seen as attempts to provide a quantitative evaluation of the domiciliation status of triatomines. However, they do not provide a clear description of the level of adaptation to human habitat. For example, while the colonisation index is often taken as indicative of the domiciliation/domestication of a species/population, it actually falls short of demonstrating the occurrence of the complete reproductive cycle of the bugs, nor of its sustainability over time. Also, nymphs may reach houses by walking or may have emerged from eggs released by a visiting female. Similarly, the visitation index does not take into account seasonal intrusion or may be biased by a low detection of nymphs.

Population genetics analysis leading to the characterisation of population genetic structure, population assignment and assessment of gene flow can also shed some light on bug dispersal among habitat and on domiciliation (Gourbière et al. 2012Gourbière S, Dorn P, Tripet F, Dumonteil E 2012. Genetics and evolution of triatomines: from phylogeny to vector control. Heredity 108: 190-202.). However, these studies remain costly and technically challenging and more appropriate for basic research than for vector control programs. It is also worth noting that the genetic structure strictly depends on the molecular clock of the genetic markers used and these needs to be carefully selected to provide reliable information. Indeed, conflicting results may be obtained depending on the methods used to infer gene flow among populations, as observed for T. infestans (Brenière et al. 1998Brenière SF, Bosseno MF, Vargas F, Yaksic N, Noireau F, Noel S, Dujardin JP, Tibayrenc M 1998. Smallness of the panmictic unit ofTriatoma infestans (Hemiptera: Reduviidae). J Med Entomol 35: 911-917.). Similarly, other types of molecular studies, such as the identification of blood feeding sources and profiles are central to further evaluate and quantify the risks of transmission of T. cruzi to humans (Dumonteil et al. 2013Dumonteil E, Nouvellet P, Rosecrans K, Ramirez-Sierra MJ, Gamboa-León R, Cruz-Chan V, Rosado-Vallado M, Gourbière S 2013. Eco-bio-social determinants for house infestation by non-domiciliated Triatoma dimidiata in the Yucatan Peninsula, Mexico. PLoS Negl Trop Dis 7: e2466., Waleckx et al. 2014Waleckx E, Suarez J, Richards B, Dorn PL 2014. Triatoma sangui- suga blood meals and potential of Chagas disease transmission in Louisiana, United States. Emerg Infect Dis 20: 2141-2143.), but may be limited to a research setting. On the other hand, the analysis of infestation risk factors may be useful and can be applied to entomological data from very large number of houses from surveillance program (Campbell-Lendrum et al. 2007Campbell-Lendrum D, Angulo VM, Esteban L, Tarazona Z, Parra GJ, Restrepo M, Restrepo BN, Guhl F, Pinto N, Aguilera G, Wilkinson P, Davies CR 2007. House-level risk factors for triatomine infestation in Colombia.Int J Epidemiol 36: 866-872.), but the evidence provided is very indirect, so often insufficient to determine the level of intrusion/domiciliation.

Finally, the modelling of vector population dynamics and T. cruzitransmission provides a very powerful way of analysing field collection data, as it allows quantifying the effects of bug dispersal (i.e., intrusion) and demography (i.e., domiciliation) on the infestation process and transmission of T. cruzi, as well as anticipating the potential efficacy of control strategies when empirical approaches are difficult for practical, financial or ethical reasons. An interesting example in the field is the modelling of T. dimidiata source-sink dynamics in the Yucatan Peninsula, that provided quantitative evidences that although nymph stages were occasionally detected inside houses, such limited colonisation was not compatible with an effective domiciliation, as domestic populations were not self-sustainable, but rather strictly depended on seasonal intrusion of adult bugs (Gourbière et al. 2008Gourbière S, Dumonteil E, Rabinovich J, Minkoue R, Menu F 2008. Demographic and dispersal constraints for domestic infestation by non-domiciliated Chagas disease vectors in the Yucatan Peninsula, Mexico.Am J Trop Med Hyg 78: 133-139., Barbu et al. 2009Barbu C, Dumonteil E, Gourbière S 2009. Optimization of control strategies for non-domiciliated Triatoma dimidiata, Chagas disease vector in the Yucatan Peninsula, Mexico. PLoS Negl Trop Dis 3: e416., 2010Barbu C, Dumonteil E, Gourbière S 2010. Characterization of the dispersal of non-domiciliated Triatoma dimidiata through the selection of spatially explicit models. PLoS Negl Trop Dis 4: e777., 2011Barbu C, Dumonteil E, Gourbière S 2011. Evaluation of spatially targeted strategies to control non-domiciliated Triatoma dimidiata vector of Chagas disease. PLoS Negl Trop Dis 5: e1045.). Such models can easily be adjusted to a variety of bug collection data from field studies [see Nouvellet et al. (2015)Nouvellet P, Cucunubá ZM, Gourbière S 2015. Ecology, evolution and control of Chagas disease: a century of neglected modelling and a promising future. Adv Parasitol 87: 135-191. for a review] and sensitivity analysis can provide (theoretical) thresholds for both intrusion/domiciliation of bugs populations, as well as for the transmission of T. cruzi to humans (Rascalou et al. 2012Rascalou G, Pontier D, Menu F, Gourbière S 2012. Emergence and prevalence of human vector-borne diseases in sink vector populations.PLoS ONE 7: e36858., Nouvellet et al. 2013Nouvellet P, Dumonteil E, Gourbière S 2013. The improbable transmission of Trypanosoma cruzi to human: the missing link in the dynamics and control of Chagas disease. PLoS Negl Trop Dis 7: e2505.). Setting up more (“Leslie” or “Lefkovitch”) (Caswell 2001Caswell H 2001. Matrix population models: construction, analysis and interpretation, 2nd ed., Sinauer Associates Inc, Sunderland, 722 pp.) matrix models of triatomine’s life history and population dynamics would also lay the foundations for micro-evolutionary studies. In fisherian optimality approaches (Roff 2010Roff DA 2010. Modeling evolution: an introduction to numerical methods, Oxford University Press, Oxford, 352 pp.), this type of modelling indeed allows identifying the fitness value of a given strategy according to the complete life history it corresponds to. Direct comparisons between the fitness values of alternative strategies then provide an objective and quantitative way to predict the evolutionary “optimal” strategy. More elaborated description of the meta-population dynamics (Gourbière & Gourbière 2002Gourbière S, Gourbière F 2002. Competition between unit-restricted fungi: a metapopulation model. J Theor Biol 217: 351-368.), the nonlinear ecological (e.g., competitive) interactions and/or the genetic determinism of the strategies can be accounted in identifying evolutionary dynamics (Meszena et al. 2001Meszena G, Kisdi E, Dieckmann U, Geritz SAH, Metz JAJ 2001. Evolutionary optimisation models and matrix games in the unified perspective of adaptive dynamics. Selection 2: 193-210.,Dieckmann et al. 2002)Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K 2002. Adaptive dynamics of infectious diseases: in pursuit of virulence management, Cambridge University Press, Cambridge, 463 pp., potentially leading to more complex insect life-history evolutionary dynamics according to frequency and density-dependent fitness values (Gourbière & Menu 2009)Gourbière S, Menu F 2009. Adaptive dynamics of dormancy duration variability: evolutionary trade-off and priority effect lead to suboptimal adaptation. Evolution 63: 1879-1892.. These approaches are barely used to understand triatomine’s evolution [but see Menu et al. (2010)Menu F, Ginoux M, Rajon E, Lazzari CR, Rabinovich JE 2010. Adaptive developmental delay in Chagas disease vectors: an evolutionary ecology approach.PLoS Negl Trop Dis 4: e691. and Pelosse et al. (2013)Pelosse P, Kribs-Zaleta CM, Ginoux M, Rabinovich JE, Gourbière S, Menu F 2013. Influence of vectors’ risk-spreading strategies and environmental stochasticity on the epidemiology and evolution of vector-borne diseases: the example of Chagas disease. PLoS ONE 8: e70830.], while they could provide critical quantitative insights into the domiciliation of triatomine or their adaptive response to control interventions, two issues that are critical to our understanding of the ecology, evolution and control of Chagas disease.

Concluding remarks

While domiciliation is clearly a gradual evolutionary process, we argued here that more precise evaluations of the level of adaptation of triatomine species to human habitats are needed for the optimisation of vector control. While only a few species have been able to effectively adapt to human housing, most remain connected to sylvatic populations and show variable levels of intrusion. Such behaviour requires the design of specific vector control interventions targeting this intrusion process, rather than insecticide spraying which only targets domesticated triatomine populations. Most current approaches used to assess triatomine association with human habitat, based on field and laboratory studies, provide insufficient information on the level of domestic adaptation of triatomines. Further analysis and modelling of field data can provide quantitative estimates of population persistence and fitness, shed new light on the domiciliation process of triatomine and may represent a key tool for decision-making and the design of vector control interventions.

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  • Financial support: UNDP/World Bank/WHO-TDR/IDRC (A90276)

Publication Dates

  • Publication in this collection
    14 Mar 2015
  • Date of issue
    May 2015

History

  • Received
    31 Oct 2014
  • Accepted
    9 Mar 2015
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