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      Transmission ecology of Trypanosoma cruzi by Rhodnius prolixus (Reduviidae: Triatominae) infesting palm-tree species in the Colombian Orinoco, indicates risks to human populations

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          Abstract

          Background

          Chagas disease, affecting approximately eight million individuals in tropical regions, is primarily transmitted by vectors. Rhodnius prolixus, a triatomine vector, commonly inhabits in ecotopes with diverse palm tree species, creating optimal conditions for vector proliferation. This study aims to explore the transmission ecology of Trypanosoma cruzi, the causative parasite of Chagas disease, by investigating the feeding patterns and natural infection rates of R. prolixus specimens collected from various wild palm species in the Colombian Orinoco region.

          Materials and methods

          To achieve this objective, we sampled 35 individuals from three palm species ( Attalea butyracea, Acrocomia aculeata, and Mauritia flexuosa) in a riparian forest in the Casanare department of eastern Colombia, totaling 105 sampled palm trees. DNA was extracted and analyzed from 115 R. prolixus specimens at different developmental stages using quantitative PCR (qPCR) for T. cruzi detection and identification of discrete typing units. Feeding preferences were determined by sequencing the 12S rRNA gene amplicon through next-generation sequencing.

          Results

          A total of 676 R. prolixus specimens were collected from the sampled palms. The study revealed variation in population densities and developmental stages of R. prolixus among palm tree species, with higher densities observed in A. butyracea and lower densities in M. flexuosa. TcI was the exclusive T. cruzi discrete typing unit (DTU) found, with infection frequency positively correlated with R. prolixus abundance. Insects captured in A. butyracea exhibited higher abundance and infection rates than those from other palm species. The feeding sources comprised 13 mammal species, showing no significant differences between palm species in terms of blood sources. However, Didelphis marsupialis and Homo sapiens were present in all examined R. prolixus, and Dasypus novemcinctus was found in 89.47% of the insects.

          Conclusion

          This study highlights the significance of wild palms, particularly A. butyracea, as a substantial risk factor for T. cruzi transmission to humans in these environments. High population densities and infection rates of R. prolixus were observed in each examined palm tree species.

          Author summary

          Previous studies on Chagas disease in the Orinoco region primarily focused on domestic and peri-domestic areas of rural residences. However, to fully grasp the dynamics of T. cruzi transmission from natural, preserved areas to humans, it is crucial to comprehend the habitats and food resources that kissing bugs encounter in their natural distribution zones. In this study, we delved into both the habitat conditions and the food sources available on wild palms in the eastern plains region of Colombia, with the aim of understanding the establishment of the Chagas disease vector. Notably, our findings revealed that the studied kissing bugs fed on both wild and domestic animals, as well as humans, across all stages of their development. Furthermore, this research identified differences in the structural physiognomy of wild palms directly linked to the establishment of bug colonies. This knowledge enhances our understanding of the role of wild habitats in the dynamics of T. cruzi transmission in endemic areas.

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          Most cited references66

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          RCircos: an R package for Circos 2D track plots

          Background Circos is a Perl language based software package for visualizing similarities and differences of genome structure and positional relationships between genomic intervals. Running Circos requires extra data processing procedures to prepare plot data files and configure files from datasets, which limits its capability of integrating directly with other software tools such as R. Recently published R Bioconductor package ggbio provides a function to display genomic data in circular layout based on multiple other packages, which increases its complexity of usage and decreased the flexibility in integrating with other R pipelines. Results We implemented an R package, RCircos, using only R packages that come with R base installation. The package supports Circos 2D data track plots such as scatter, line, histogram, heatmap, tile, connectors, links, and text labels. Each plot is implemented with a specific function and input data for all functions are data frames which can be objects read from text files or generated with other R pipelines. Conclusion RCircos package provides a simple and flexible way to make Circos 2D track plots with R and could be easily integrated into other R data processing and graphic manipulation pipelines for presenting large-scale multi-sample genomic research data. It can also serve as a base tool to generate complex Circos images.
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            DNA markers define two major phylogenetic lineages of Trypanosoma cruzi.

            R. Souto (1996)
            Parasitic protozoa within the taxon Trypanosoma cruzi are considered to be derived from multiple clonal lineages, and show broad genetic diversity as a result of propagation with little or no genetic exchange. We have analyzed a wide sample of T. cruzi isolates from vertebrate and invertebrate hosts by PCR amplification of a ribosomal RNA gene sequence, a mini-exon gene sequence and random amplified polymorphic DNA (RAPD). Amplification of the distinct rDNA and mini-exon gene sequences indicated a dimorphism within both of the tandemly-repeated genes: 125 or 110 bp products for rDNA and 300 or 350 bp products for the mini-exon. Within individual isolates, one of three associations was observed: the 125 bp rDNA product with the 300 bp mini-exon product (defined as group 1), the 110 bp rDNA product with the 350 bp mini-exon product (defined as group 2) and the presence of both rDNA amplification products with the mini-exon group 1 product (group 1/2). The RAPD analysis showed variability between individual isolates, however, tree analysis clearly indicated the presence of two major branches. Interestingly, the rDNA/mini-exon group 2 isolates correlated precisely with one branch of the RAPD-derived tree; group 1 and group 1/2 isolates correlated with the other branch. Our studies show a clear division of T. cruzi into two major lineages presenting a high phylogenetic divergence. Hypotheses are discussed to explain the origin of the two lineages as well as isolates that are hybrid for group 1 and 2 rDNA markers.
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              Classification, evolution, and species groups within the Triatominae.

              Classification of the Triatominae has become a complex balance between traditional approaches and a wide variety of evolutionary interpretations. On the one hand is the need for a stable classification of practical use for those involved in vector surveillance and control. On the other is the desire to adequately reflect evolutionary theory derived from a range of molecular, cytogenetic and morphometric comparisons, with additional complications raised by current interpretations of the subfamily as a recently derived polyphyletic assemblage. Here we review key aspects of triatomine systematics and evolution, to derive a pragmatic classification that seeks to build on traditional morphological concepts within the context of current evolutionary theories.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                PLOS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                20 February 2024
                February 2024
                : 18
                : 2
                : e0011981
                Affiliations
                [1 ] Centro de Investigaciones en Microbiología y Parasitología Tropical (CIMPAT), Departamento de Ciencias Biológicas, Universidad de los Andes, Bogotá, Colombia
                [2 ] Grupo de Investigaciones Biológicas de la Orinoquia, Universidad Internacional del Trópico Americano (Unitrópico), Yopal, Colombia
                [3 ] Centro de Investigaciones en Microbiología y Biotecnología-UR (CIMBIUR), Facultad de Ciencias Naturales, Universidad del Rosario, Bogotá, Colombia
                [4 ] Molecular Microbiology Laboratory, Department of Pathology, Molecular and Cell-Based Medicine, Icahn School of Medicine at Mount Sinai, New York City, New York, United States of America
                [5 ] Centro de Tecnología en Salud (CETESA), Innovaseq SAS, Bogotá, Colombia
                [6 ] Departamento de Ecología Humana, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), Mérida, Yucatán, México
                Universidade Federal de Minas Gerais, BRAZIL
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0002-1344-9312
                Article
                PNTD-D-23-00601
                10.1371/journal.pntd.0011981
                10906903
                38377140
                2c4f8c36-f35a-4754-bbbc-ad70afb2a74d
                © 2024 Urbano et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 16 May 2023
                : 8 February 2024
                Page count
                Figures: 5, Tables: 1, Pages: 19
                Funding
                Funded by: Universidad del Rosario
                Award ID: Internal funds
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100017703, Fundación CeiBA;
                Award ID: PhD scholarship
                Award Recipient :
                We thank the Direccion de Investigacion e Innovación from Universidad del Rosario (JDR) for funding the study. We thank the CEIBA foundation for funding the PhD studies of PU. The funder had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Protozoans
                Parasitic Protozoans
                Trypanosoma
                Trypanosoma Cruzi
                Biology and Life Sciences
                Zoology
                Entomology
                Insects
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Zoology
                Animals
                Invertebrates
                Arthropoda
                Insects
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Nymphs
                Medicine and Health Sciences
                Epidemiology
                Medical Risk Factors
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Population Density
                Medicine and Health Sciences
                Medical Conditions
                Parasitic Diseases
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Biology and Life Sciences
                Zoology
                Animals
                Vertebrates
                Medicine and Health Sciences
                Medical Conditions
                Infectious Diseases
                Disease Vectors
                Insect Vectors
                Biology and Life Sciences
                Species Interactions
                Disease Vectors
                Insect Vectors
                Custom metadata
                vor-update-to-uncorrected-proof
                2024-03-01
                All the data is available in the manuscript and the supplementary files.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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