The genomic basis of domestic colonisation and dispersal in Chagas disease vectors

The biology of vector adaptation to the human habitat remains poorly understood for many arthropod-borne diseases but underpins effective and sustainable disease control. We adopted a landscape genomics approach to investigate gene flow, signatures of local adaptation, and drivers of population structure among multiple linked wild and domestic population pairs in Rhodnius ecuadoriensis, an important vector of Chagas Disease. Evidence of high triatomine gene flow (FST) between wild and domestic ecotopes at sites throughout the study area indicate insecticide-based control will be hindered by constant re-infestation of houses. Genome scans revealed genetic loci with strong signal of local adaptation to the domestic setting, which we mapped to annotated regions in the Rhodnius prolixus genome. Our landscape genomic mixed effects models showed Rhodnius ecuadoriensis population structure and connectivity is driven by landscape elevation at a regional scale. Our ecologically- and spatially-explicit vector dispersal model enables targeted vector control and recommends spatially discrete, periodic interventions to local authorities as more efficacious than current, haphazard approaches. In tandem, evidence for parallel genomic adaptation to colonisation of the domestic environment at multiple sites sheds new light on the evolutionary basis of adaptation to the human host in arthropod vectors.

Triatomine Feeding Profiles and Trypanosoma cruzi Infection, Implications in Domestic and Sylvatic Transmission Cycles in Ecuador

Understanding the blood meal patterns of insects that are vectors of diseases is fundamental in unveiling transmission dynamics and developing strategies to impede or decrease human–vector contact. Chagas disease has a complex transmission cycle that implies interactions between vectors, parasites and vertebrate hosts. In Ecuador, limited data on human infection are available; however, the presence of active transmission in endemic areas has been demonstrated. The aim of this study was to determine the diversity of hosts that serve as sources of blood for triatomines in domestic, peridomestic and sylvatic transmission cycles, in two endemic areas of Ecuador (central coastal and southern highland regions). Using conserved primers and DNA extracted from 507 intestinal content samples from five species of triatomines (60 Panstrongylus chinai, 17 Panstrongylus howardi, 1 Panstrongylus rufotuberculatus, 427 Rhodnius ecuadoriensis and 2 Triatoma carrioni) collected from 2006 to 2013, we amplified fragments of the cytb mitochondrial gene. After sequencing, blood meal sources were identified in 416 individuals (146 from central coastal and 270 from southern highland regions), achieving ≥ 95% identity with GenBank sequences (NCBI-BLAST tool). The results showed that humans are the main source of food for triatomines, indicating that human–vector contact is more frequent than previously thought. Although other groups of mammals, such as rodents, are also an available source of blood, birds (particularly chickens) might have a predominant role in the maintenance of triatomines in these areas. However, the diversity of sources of blood found might indicate a preference driven by triatomine species. Moreover, the presence of more than one source of blood in triatomines collected in the same place indicated that dispersal of vectors occurs regardless the availability of food. Dispersal capacity of triatomines needs to be evaluated to propose an effective strategy that limits human–vector contact and, in consequence, to decrease the risk of T. cruzi transmission.

Under pressure: phenotypic divergence and convergence associated with microhabitat adaptations in Triatominae

BackgroundTriatomine bugs, the vectors of Chagas disease, associate with vertebrate hosts in highly diverse ecotopes. When these blood-sucking bugs adapt to new microhabitats, their phenotypes may change. Although understanding phenotypic variation is key to the study of adaptive evolution and central to phenotype-based taxonomy, the drivers of phenotypic change and diversity in triatomines remain poorly understood.Methods/FindingsWe combined a detailed phenotypic appraisal (including morphology and morphometrics) with mitochondrial cytb and nuclear ITS2 DNA-sequence analyses to study Rhodnius ecuadoriensis populations from across the species’ range. We found three major, naked-eye phenotypic variants. Southern-Andean bugs (SW Ecuador/NW Peru) from house and vertebrate-nest microhabitats are typical, light-colored, small bugs with short heads/wings. Northern-Andean bugs (W Ecuador wet-forest palms) are dark, large bugs with long heads/wings. Finally, northern-lowland bugs (coastal Ecuador dry-forest palms) are light-colored and medium-sized. Wing and (size-free) head shapes are similar across Ecuadorian populations, regardless of habitat or naked-eye phenotype, but distinct in Peruvian bugs. Bayesian phylogenetic and multispecies-coalescent DNA-sequence analyses strongly suggest that Ecuadorian and Peruvian populations are two independently-evolving lineages, with little within-lineage structuring/differentiation.ConclusionsWe report sharp naked-eye phenotypic divergence of genetically similar Ecuadorian R. ecuadoriensis (house/nest southern-Andean vs. palm-dwelling northern bugs; and palm-dwelling Andean vs. lowland); and sharp naked-eye phenotypic similarity of typical, yet genetically distinct, southern-Andean bugs from house and nest (but not palm) microhabitats (SW Ecuador vs. NW Peru). This remarkable phenotypic diversity within a single nominal species likely stems from microhabitat adaptations possibly involving predator-driven selective pressure (yielding substrate-matching camouflage coloration) and a shift from palm-crown to vertebrate-nest microhabitats (yielding smaller bodies and shorter heads and wings). These findings shed new light on the origins of phenotypic diversity in triatomines, warn against excess reliance on phenotype-based triatomine-bug taxonomy, and confirm the Triatominae as an informative model-system for the study of phenotypic change under ecological pressure.Author summaryTriatomine bugs feed on the blood of vertebrates including humans and transmit the parasite that causes Chagas disease. The bugs, of which 150+ species are known, are highly diverse in size, shape, and color. Some species look so similar that they are commonly confused, whereas a few same-species populations look so different that they were thought to be separate species. Despite the crucial role of naked-eye phenotypes in triatomine-bug identification and classification (which are essential for vector control-surveillance), the origins of this variation remain unclear. Here, we describe a striking case of phenotypic divergence, with genetically similar bugs looking very different from one another, and phenotypic convergence, with bugs from two genetically distinct populations (likely on their way to speciation) looking very similar – and all within a single nominal species, Rhodnius ecuadoriensis. Phenotypically divergent populations occupy different ecological regions (wet vs. dry) and microhabitats (palm-crowns vs. vertebrate nests), whereas convergent populations occupy man-made and nest (but not palm) microhabitats. These findings suggest that triatomines can ‘respond’ to ecological novelty by changing their external, naked-eye phenotypes as they adapt to new microhabitats. We therefore warn that phenotypic traits such as overall size or color may confound triatomine-bug species identification and classification.

Rhodnius pallescens microsatellite markers for population genetic analysis in Rhodnius ecuadoriensis: preliminary assessment

Rhodnius ecuadoriensis Lent & León (Hemiptera: Reduviidae) es el prinicipal vector de la enfermedad de Chagas en Ecuador, donde la estructura genética de sus poblaciones es poco conocida. Nosotros probamos seis Repeticiones Cortas en Tamdem (RCT) de R. pallescens Barber en poblaciones selváticas y domésticas de R. ecuadoriensis. Dos microsatelites fueron monomórficos, dos dieron resultados ambiguos y dos fueron polimórficos (16 y 19 alelos) y fueron utilizados para análisis. Los resultados de las frecuencias alélicas, AMOVA y los pruebas Bayesianas para genética favorecen la teorí­a de la existencia de una sola población. Estos resultados preliminares sugieren que las poblaciones selváticas y domésticas d R. ecuadoriensis intercambian frecuentemente migrantes. Por consiguiente el control de la Enfermedad de Chagas requiere vigilancia entomológica continua en la costa del Ecuador.

Rhodnius pallescens microsatellite markers for population genetic analysis in Rhodnius ecuadoriensis: preliminary assessment

Rhodnius ecuadoriensis Lent & León (Hemiptera: Reduviidae) es el prinicipal vector de la enfermedad de Chagas en Ecuador, donde la estructura genética de sus poblaciones es poco conocida. Nosotros probamos seis Repeticiones Cortas en Tamdem (RCT) de R. pallescens Barber en poblaciones selváticas y domésticas de R. ecuadoriensis. Dos microsatelites fueron monomórficos, dos dieron resultados ambiguos y dos fueron polimórficos (16 y 19 alelos) y fueron utilizados para análisis. Los resultados de las frecuencias alélicas, AMOVA y los pruebas Bayesianas para genética favorecen la teorí­a de la existencia de una sola población. Estos resultados preliminares sugieren que las poblaciones selváticas y domésticas d R. ecuadoriensis intercambian frecuentemente migrantes. Por consiguiente el control de la Enfermedad de Chagas requiere vigilancia entomológica continua en la costa del Ecuador.

Uso de microsatélites en Rhodnius ecuadoriensis para determinar estructura poblacional y patrones de migración en el Ecuador.

El entender el comportamiento migratorio de triatominos entre los ambientes silvestres hacia zonas habitadas es crucial para la lucha contra la Enfermedad de Chagas. Los marcadores basados en ADN muestran ventaja para desarrollar dicho fenómeno específicamente la plasticidad en microsatélites, que en un principio fueron desarrollados para estudiar a Rhodnius pallescens y que posteriormente mostraron ser efectivos en Rhodnius ecuadoriensis. En donde no solamente su análisis es congruente con el origen evolutivo de la clina pallescens-colombiensis-ecuadoriensis, sino que además permite observar patrones de migración en R. ecuadoriensis dentro de las provincias del Ecuador. La migración humana está relacionada directamente con la de los insectos, dicho movimiento se puede constatar en la homogeneidad que existe entre los triatominos encontrados en Loja con aquellos ubicados en Manabí.