Phylogeography and genetic variation of Triatoma dimidiata, the main Chagas disease vector in Central America, and its position within the genus Triatoma

Abstract

Background: Among Chagas disease triatomine vectors, the largest genus, Triatoma, includes species of high public health interest. Triatoma dimidiata, the main vector throughout Central America and up to Ecuador, presents extensive phenotypic, genotypic, and behavioral diversity in sylvatic, peridomestic and domestic habitats, and non-domiciliated populations acting as reinfestation sources. DNA sequence analyses, phylogenetic reconstruction methods, and genetic variation approaches are combined to investigate the haplotype profiling, genetic polymorphism, phylogeography, and evolutionary trends of T. dimidiata and its closest relatives within Triatoma. This is the largest interpopulational analysis performed on a triatomine species so far.

Methodology and findings: Triatomines from Mexico, Guatemala, Honduras, Nicaragua, Panama, Cuba, Colombia, Ecuador, and Brazil were used. Triatoma dimidiata populations follow different evolutionary divergences in which geographical isolation appears to have had an important influence. A southern Mexican-northern Guatemalan ancestral form gave rise to two main clades. One clade remained confined to the Yucatan peninsula and northern parts of Chiapas State, Guatemala, and Honduras, with extant descendants deserving specific status. Within the second clade, extant subspecies diversity was shaped by adaptive radiation derived from Guatemalan ancestral populations. Central American populations correspond to subspecies T. d. dimidiata. A southern spread into Panama and Colombia gave the T. d. capitata forms, and a northwestern spread rising from Guatemala into Mexico gave the T. d. maculipennis forms. Triatoma hegneri appears as a subspecific insular form.

Conclusions: The comparison with very numerous Triatoma species allows us to reach highly supported conclusions not only about T. dimidiata, but also on different, important Triatoma species groupings and their evolution. The very large intraspecific genetic variability found in T. dimidiata sensu lato has never been detected in a triatomine species before. The distinction between the five different taxa furnishes a new frame for future analyses of the different vector transmission capacities and epidemiological characteristics of Chagas disease. Results indicate that T. dimidiata will offer problems for control, although dwelling insecticide spraying might be successful against introduced populations in Ecuador.

Figure 1. Geographical distribution of the sampling sites furnishing the triatomine materials.

Numbers correspond to sampling sites listed in Table 1. • = Triatoma dimidiata; ▴ = other Triatoma species studied.

Figure 2. Interhaplotype sequence differences found in the rDNA ITS-2 of the Triatoma dimidiata populations analyzed.

Numbers (to be read in vertical) refer to positions obtained in the alignments made with CLUSTAL-W 1.8 and MEGA 3.3. . = identical; * = singelton sites (7); • = parsimony informative positions (24); − = insertion/deletion. Rectangled area = microsatellite region. Horizontal lines separate the four major T. dimidiata haplotype groupings according to sequence analyses.

Figure 3. Median network for Triatoma dimidiata haplotypes based on rDNA ITS-2 sequences.

The area of each haplotype is proportional to the total sample. Small black-filled circles represent haplotypes not present in the sample. Mutational steps between haplotypes are represented by a line. More than one mutational step is represented by numbers. H = haplotype. Blue: Colombia; orange: Panama; yellow: Mexico; red: Honduras; lilac: Ecuador; ocher: Nicaragua; green: Guatemala.

Figure 4. Phylogenetic ML tree of Triatoma species and haplotypes within the Phyllosoma, Rubrofasciata and Infestans groups.

The scale bar indicates the number of substitutions per sequence position. Support for nodes a/b/c: a: bootstrap with ML reconstruction using PhyML with 1000 replicates; values larger than 70%; b: bootstrap with NJ reconstruction using PAUP with ML distance and 1000 replicates; values larger than 70%; c: Bayesian posterior probability with ML model using MrBayes; values larger than 90%.

Figure 5. Phylogeography of Triatoma dimidiata sensu lato.

Distribution and spreading routes of T. d. dimidiata, T. d. capitata, T. d. maculipennis, T. d. hegneri and Triatoma sp. aff. dimidiata in Mesoamerica, Central America and the northwestern part of South America are represented according to network analyses and genetic variation studies based on rDNA ITS-2 sequences.