Dynamics of Triatoma infestans populations in the Paraguayan Chaco: Population genetic analysis of household reinfestation following vector control

Abstract

Background: Although domestic infestations by Triatoma infestans have been successfully controlled across Latin America, in areas of the Gran Chaco region, recurrent post-spraying house colonization continues to be a significant challenge, jeopardizing Chagas disease vector control and maintaining active Trypanosoma cruzi transmission.

Methodology/principal findings: To investigate the dynamics of triatomine reinfestation in a rural area of the Paraguayan Chaco, genetic characterization (based on 10 microsatellite loci and cytochrome B sequence polymorphisms) was performed on baseline and reinfestant T. infestans (n = 138) from four indigenous communities and adjacent sylvatic sites. House quality and basic economic activities were assessed across the four communities. Significant genetic differentiation was detected among all baseline triatomine populations. Faster reinfestation was observed in the communities with higher infestation rates pre-spraying. Baseline and reinfestant populations from the same communities were not genetically different, but two potentially distinct processes of reinfestation were evident. In Campo Largo, the reinfestant population was likely founded by domestic survivor foci, with reduced genetic diversity relative to the baseline population. However, in 12 de Junio, reinfestant bugs were likely derived from different sources, including survivors from the pre-spraying population and sympatric sylvatic bugs, indicative of gene-flow between these habitats, likely driven by high human mobility and economic activities in adjacent sylvatic areas.

Conclusions/significance: Our results demonstrate that sylvatic T. infestans threatens vector control strategies, either as a reinfestation source or by providing a temporary refuge during insecticide spraying. Passive anthropogenic importation of T. infestans and active human interactions with neighboring forested areas also played a role in recolonization. Optimization of spraying, integrated community development and close monitoring of sylvatic areas should be considered when implementing vector control activities in the Gran Chaco.

Fig 1. Map of the study area indicating positions of the four communities: Campo Alegre (Mariscal Estigarribia, Boquerón Department) and Campo Largo, 10 Leguas and 12 de Junio (Benjamín Aceval, Presidente Hayes Department).

Yellow and orange dots indicate triatomine capture sites inside houses or from the sylvatic environment [26], respectively. Note: multiple bugs were collected per capture site. Map was made using ESRI 2016. "World Imagery" [basemap]. Scale Not Given. "World Imagery Map". October 13, 2021. https://www.arcgis.com/home/item.html?id=10df2279f9684e4a9f6a7f08febac2a9. (Oct 26, 2021). QGIS Development Team, 2021. QGIS Version 3.20.3. Geographic Information System. Open Source Geospatial Foundation. Data source: DGEEC 2012. https://www.ine.gov.py/microdatos/microdatos.php. Detailed World Polygons (LSIB), South America, 2013. http://purl.stanford.edu/vc965bq8111.

Fig 2

Examples of typical houses, constructed with local materials in Campo Alegre (A), Campo Largo (B), 10 Leguas (C) and 12 de Junio (D).

Fig 3. Quality of housing construction materials used in dwellings in the four study communities (CA, CL, 12J and 10L).

CALMAT I: The dwelling contains durable resistant materials and solids for all parameters (floors, walls, ceilings) and incorporates all elements of insulation and plastering. CALMAT II: The dwelling presents durable materials and solids in all components, but it lacks elements of insulation or plastering in at least one of its components (floors, walls, and ceilings). CALMAT III: The dwelling presents durable materials and solids in all parameters, but it lacks elements of insulation or plastering in all its components, or either has sheet metal or fiber cement roofs or no ceiling; or walls of sheet metal or fiber cement. CALMAT IV: The dwelling presents materials not durable or solid in at least one of the components, but not in all of them. CALMAT V: The dwelling has no resistant or solid materials in any components [39].

Fig 4. NJ tree based on Da pairwise distance values (estimated in POPTREEW) based on MLGs of 10 microsatellite loci.

Fig 5. Bayesian cluster analysis results of T. infestans populations from domestic and sylvatic areas from four communities from Paraguay.

5A) Mean of estimated Ln likelihood of the probability data adjust to the model with K clusters (Ln(P)), versus K number of genetic clusters considered [58]. 5B) Graphic representation of Delta K = mean ((|L″(K)|)/SD(L(K)) [59], to evaluate the rate of change in the Ln(P) versus the number of genetic clusters considered (K = 1–10). 5C) Bar plot representing the a priori assignment probability of each multilocus genotype (MLG) to be assigned to a specific genetic cluster (represented by colors). Upper: graphic representation of the population relative composition to each genetic cluster (K = 3). Lower: each vertical bar represents an individual and the different colors are the probability with which each individual resulted assigned to each of three genetic clusters.

Fig 6

A: Haplotype network based on a median-joining model, constructed from sequences identified in this study (shown in red) and 71 additional T. infestans CytB haplotypes available in Genebank from Argentina and Bolivia [–74]. Sequences were classified as ‘Andean’ or ‘Non-Andean’ based on geographical origin (S2 File). The distance among haplotypes is represented by the number of mutational steps between them. Note: that several haplotypes converged into a few centrally located haplotypes as the original sequence length was shortened for this analysis, causing some variable sites to be lost. B: Cytochrome B haplotype distribution among study communities. Numbers indicate individuals with that haplotype detected per community. Hybrid haplotypes are heteroplasmid individuals.