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      Phylogeny and Niche Conservatism in North and Central American Triatomine Bugs (Hemiptera: Reduviidae: Triatominae), Vectors of Chagas' Disease

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          Abstract

          The niche conservatism hypothesis states that related species diverge in niche characteristics at lower rates than expected, given their lineage divergence. Here we analyze whether niche conservatism is a common pattern among vector species (Hemiptera: Reduviidae: Triatominae) of Trypanosoma cruzi that inhabit North and Central America, a highly heterogeneous landmass in terms of environmental gradients. Mitochondrial and nuclear loci were used in a multi-locus phylogenetic framework to reconstruct phylogenetic relationships among species and estimate time of divergence of selected clades to draw biogeographic inferences. Then, we estimated similarity between the ecological niche of sister species and tested the niche conservatism hypothesis using our best estimate of phylogeny. Triatoma is not monophyletic. A primary clade with all North and Central American (NCA) triatomine species from the genera Triatoma, Dipetalogaster, and Panstrongylus, was consistently recovered. Nearctic species within the NCA clade ( T. p. protracta, T. r. rubida) diverged during the Pliocene, whereas the Neotropical species ( T. phyllosoma, T. longipennis, T. dimidiata complex) are estimated to have diverged more recently, during the Pleistocene. The hypothesis of niche conservatism could not be rejected for any of six sister species pairs. Niche similarity between sister species best fits a retention model. While this framework is used here to infer niche evolution, it has a direct impact on spatial vector dynamics driven by human population movements, expansion of transportation networks and climate change scenarios.

          Author Summary

          Knowledge regarding the evolutionary history of insect vectors of pathogens is essential to design precise and appropriately integrated control strategies, since species' dispersal and invasive capacity are key components to prevent human-vector interaction. Given several well-known invasive or dispersal events of Triatominae, and their adaptive capacity to colonize modified habitats, the question arises whether niche conservatism (i.e. the limited capacity for niche differentiation within clades) across sister species could influence distribution patterns. Niche conservatism is herein analyzed across the highly heterogeneous landmass of North and Central America where most species complexes of the Triatominae are vectors of Trypanosoma cruzi. Since phylogenetic relationships among and within triatomine species complexes are still ill-defined, we first used a multi-locus phylogenetic analysis using mitochondrial and nuclear loci to validate relationships between species. Similarity of the ecological niche between six sister species' pairs was used to test the niche conservatism hypothesis. The results provide robust evidence of monophyly for North and Central America triatomine species. The hypothesis of niche conservatism was not rejected for any sister species pair, independently of niche width, distribution range, biogeographic affinity, or environmental heterogeneity; niche similarity correlated inversely with taxa divergence and according to a retention model.

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          Most cited references 57

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          MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.

          Comparative analysis of molecular sequence data is essential for reconstructing the evolutionary histories of species and inferring the nature and extent of selective forces shaping the evolution of genes and species. Here, we announce the release of Molecular Evolutionary Genetics Analysis version 5 (MEGA5), which is a user-friendly software for mining online databases, building sequence alignments and phylogenetic trees, and using methods of evolutionary bioinformatics in basic biology, biomedicine, and evolution. The newest addition in MEGA5 is a collection of maximum likelihood (ML) analyses for inferring evolutionary trees, selecting best-fit substitution models (nucleotide or amino acid), inferring ancestral states and sequences (along with probabilities), and estimating evolutionary rates site-by-site. In computer simulation analyses, ML tree inference algorithms in MEGA5 compared favorably with other software packages in terms of computational efficiency and the accuracy of the estimates of phylogenetic trees, substitution parameters, and rate variation among sites. The MEGA user interface has now been enhanced to be activity driven to make it easier for the use of both beginners and experienced scientists. This version of MEGA is intended for the Windows platform, and it has been configured for effective use on Mac OS X and Linux desktops. It is available free of charge from http://www.megasoftware.net.
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            MrBayes 3: Bayesian phylogenetic inference under mixed models.

            MrBayes 3 performs Bayesian phylogenetic analysis combining information from different data partitions or subsets evolving under different stochastic evolutionary models. This allows the user to analyze heterogeneous data sets consisting of different data types-e.g. morphological, nucleotide, and protein-and to explore a wide variety of structured models mixing partition-unique and shared parameters. The program employs MPI to parallelize Metropolis coupling on Macintosh or UNIX clusters.
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              Bayesian Phylogenetics with BEAUti and the BEAST 1.7

              Computational evolutionary biology, statistical phylogenetics and coalescent-based population genetics are becoming increasingly central to the analysis and understanding of molecular sequence data. We present the Bayesian Evolutionary Analysis by Sampling Trees (BEAST) software package version 1.7, which implements a family of Markov chain Monte Carlo (MCMC) algorithms for Bayesian phylogenetic inference, divergence time dating, coalescent analysis, phylogeography and related molecular evolutionary analyses. This package includes an enhanced graphical user interface program called Bayesian Evolutionary Analysis Utility (BEAUti) that enables access to advanced models for molecular sequence and phenotypic trait evolution that were previously available to developers only. The package also provides new tools for visualizing and summarizing multispecies coalescent and phylogeographic analyses. BEAUti and BEAST 1.7 are open source under the GNU lesser general public license and available at http://beast-mcmc.googlecode.com and http://beast.bio.ed.ac.uk
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                1935-2727
                1935-2735
                October 2014
                30 October 2014
                : 8
                : 10
                Affiliations
                [1 ]Departamento de Ecología Humana, Centro de Investigación y de Estudios Avanzados del IPN (Cinvestav), Unidad Mérida, Mérida, Yucatán, México
                [2 ]Departamento de Zoología, Instituto de Biología, UNAM, México DF, México
                [3 ]Biodiversity Institute, University of Kansas, Lawrence, Kansas, United States of America
                [4 ]Centro Regional de Investigaciones en Salud Pública (CRISP), Instituto Nacional de Salud Pública (INSP), Tapachula, México
                Universidad Autónoma de Yucatán, Mexico
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: CNIC AZR ATP VSC JMR. Performed the experiments: CNIC AZR. Analyzed the data: CNIC AZR. Contributed reagents/materials/analysis tools: VSC JMR. Wrote the paper: CNIC AZR JMR ATP VSC.

                Article
                PNTD-D-13-01554
                10.1371/journal.pntd.0003266
                4214621
                25356550

                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.

                Page count
                Pages: 11
                Funding
                CNIC was funded with a graduate scholarship from CONACYT (Consejo Nacional de Ciencia y Tecnologia) for his PhD studies in the Biomedical Sciences Program of the UNAM (Universidad Nacional Autonoma de Mexico), fulfilled in part by this study. Studies on vector bionomics and ecology were funded by CONACYT Fomix Morelos MOR-2004-C02-012 and CONACYT FONSEC 69997 and 161405 to JMR. This work was partially supported by DGAPA-UNAM (PAPIIT 487 IN225408, IN202711) and the CONACYT-CB-2009/132811 to VSC, and PAPIIT 2013488 and CONACYT-511 to AZR. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Ecology
                Spatial and Landscape Ecology
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Evolutionary Systematics
                Phylogenetics
                Animal Phylogenetics
                Zoology
                Entomology
                Ecology and Environmental Sciences
                Terrestrial Environments
                Medicine and Health Sciences
                Epidemiology
                Disease Vectors
                Triatoma
                Infectious Diseases
                Parasitic Diseases
                Protozoan Infections
                Chagas Disease
                Tropical Diseases
                Neglected Tropical Diseases

                Infectious disease & Microbiology

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