Multilocus analysis uncovers the evolution of the Rhodniini tribe, vectors of Trypanosoma cruzi

Abstract

In this study, we investigate the origin and diversification of Trypanosoma cruzi vectors within the Rhodniini tribe (Triatominae subfamily) through phylogenetic analyses based on eight genes from 17 species and 497 specimens-the largest sampling of this tribe to date. Our results predominantly support the paraphyly of the genus Rhodnius, with the three Psammolestes species forming a well-supported monophyletic clade nested within it. In two reconstructions, however, Psammolestes and Rhodnius are recovered as reciprocally monophyletic, each with strong support. In Rhodnius, we find monophyletic pallescens and pictipes groups, but a paraphyletic prolixus group, with persistent phylogenetic discordances underscoring uncertainties in species placements. Divergence estimates suggest Rhodniini originated around 5.26 million years ago, notably more recent than previously thought. Evolution within the tribe appears shaped by geography, gene flow, and incomplete lineage sorting rather than traditional taxonomy. Only four species-P. arthuri, R. ecuadoriensis, R. neivai, and R. neglectus-are consistently supported across analyses, likely diversifying during Pleistocene climate changes. Other Rhodniini species may represent a panmictic population with minor structuring influenced by the Andes uplift. This study underscores the need for integrative research combining genetic, ecological, and biogeographical data to fully understand Rhodniini speciation and diversification.

Keywords: Psammolestes; Rhodnius; Chagas disease; Evolutionary history; Genetic structure; Insect vectors; Multilocus analysis; Phylogenetic analysis; Phylogenetic discordances; Pleistocene arc hypothesis; Population genetics; Rhodniini tribe; Speciation patterns; Vector-borne diseases.

Fig. 1

Geographic distribution of the species in the Rhodniini tribe. The map shows the distribution of the 17 species included in this study, with dots indicating sampling locations. Each species is color coded. The map was generated using the free and open-source QGIS software, with a base shapefile obtained from Natural Earth (https://www.naturalearthdata.com/downloads/10m-cultural-vectors/) and an elevation raster from SRTM (https://csidotinfo.wordpress.com/data/srtm-90m-digital-elevation-database-v4-1/).

Fig. 2

Maximum credibility phylogenetic reconstruction of the Rhodniini tribe. This figure shows the maximum credibility phylogenetic reconstruction of the Rhodniini tribe based on a concatenated alignment (size = 4368 bp) of the eight loci used in this study (nuclear, ribosomal, and mitochondrial). The reconstruction was performed using the Maximum Likelihood algorithm with PHYML and 1000 bootstrap repetitions. Bootstrap values are indicated by red squares, with only nodes having bootstrap values greater than 95% shown. Different genera, species, groups, and clades are represented by distinct colors The rings surrounding the phylogeny represent the groups of the genus Rhodnius and the clades of the prolixus group.

Fig. 3

Species tree and divergence time estimation based on multilocus data. (A) Species tree inferred from Bayesian analysis; posterior probabilities are shown as red squares with varying sizes. (B) Divergence time estimation; purple bars represent the 95% highest posterior density (HPD) intervals for node divergence times. Species and genera are color coded.

Fig. 4

Bayesian species delimitation. Bayesian species delimitations inferred under nine different theta (θ) and tau (τ) prior combinations. The posterior probability of each of these combinations is color-coded and indicated in 3 × 3 boxes on each node of the guide tree. The large 3 × 3 inset indicates the position of each prior combination in these boxes.

Fig. 5

Population clustering in the Rhodniini tribe as revealed by STRUCTURE. The numbers of ancestry groups (K) are between 2 and 6. (A). K = 2 (B). K = 4 and C. K = 6 and the matrix of aligned Q values from individuals included in this study obtained from CLUMPP. Each bar represents an individual, and the color of the bar represents the likelihood of that individual belonging to a population.