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      Geological Changes of the Americas and their Influence on the Diversification of the Neotropical Kissing Bugs (Hemiptera: Reduviidae: Triatominae)

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          Abstract

          Background

          The family Reduviidae (Hemiptera: Heteroptera), or assassin bugs, is among the most diverse families of the true bugs, with more than 6,000 species. The subfamily Triatominae (kissing bugs) is noteworthy not simply because it is the only subfamily of the Reduviidae whose members feed on vertebrate blood but particularly because all 147 known members of the subfamily are potential Chagas disease vectors. Due to the epidemiological relevance of these species and the lack of an efficient treatment and vaccine for Chagas disease, it is more common to find evolutionary studies focusing on the most relevant vectors than it is to find studies aiming to understand the evolution of the group as a whole. We present the first comprehensive phylogenetic study aiming to understand the events that led to the diversification of the Triatominae.

          Methodology/Principal Findings

          We gathered the most diverse samples of Reduviidae and Triatominae (a total of 229 Reduviidae samples, including 70 Triatominae species) and reconstructed a robust dated phylogeny with several fossil (Reduviidae and Triatominae) calibrations. Based on this information, the possible role of geological events in several of the major cladogenetic events within Triatominae was tested for the first time. We were able to not only correlate the geological changes in the Neotropics with Triatominae evolution but also add to an old discussion: Triatominae monophyly vs. paraphyly.

          Conclusions/Significance

          We found that most of the diversification events observed within the Rhodniini and Triatomini tribes are closely linked to the climatic and geological changes caused by the Andean uplift in South America and that variations in sea levels in North America also played a role in the diversification of the species of Triatoma in that region.

          Author Summary

          We present the first comprehensive phylogenetic study aiming to understand the geological events that led to Triatominae diversification. We gathered the most diverse sampling of Reduviidae and Triatominae to construct a robust and accurate phylogeny and to be able to use more than the two Triatominae fossils as calibration points for our time estimates. The possible role of geological events in several of the major cladogenetic events within Triatominae is tested for the first time in the present study. We were able not only to correlate the geological changes in the Neotropics with Triatominae evolution but also to add to an old discussion: Triatominae monophyly vs. paraphyly.

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          Most cited references18

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          An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks.

          A unified understanding of >390 Myr of insect evolution requires insight into their origin. Molecular clocks are widely applied for evolutionary dating, but clocks for the class Insecta have remained elusive. We now define a robust nucleotide and amino acid mitochondrial molecular clock encompassing five insect orders, including the Blattaria (cockroaches), Orthoptera (crickets and locusts), Hemiptera (true bugs), Diptera, and Lepidoptera (butterflies and moths). Calibration of the clock using one of the earliest, most extensive fossil records for insects (the early ancestors of extant Blattaria) was congruent with all available insect fossils, with biogeographic history, with the Cambrian explosion, and with independent dating estimates from Lepidopteran families. In addition, dates obtained from both nucleotide and amino acid clocks were congruent with each other. Of particular interest to vector biology is the early date of the emergence of triatomine bugs (99.8-93.5 MYA), coincident with the formation of the South American continent during the breakup of Gondwanaland. More generally, we reveal the insects arising from a common ancestor with the Anostraca (fairy shrimps) at around the Silurian-Ordovician boundary (434.2-421.1 MYA) coinciding with the earliest plant megafossil. We explore Tilyard's theory proposing that the terrestrial transition of the aquatic arthropod ancestor to the insects is associated with a particular plant group (early vascular plants). The major output of the study is a comprehensive series of dates for deep-branching points within insect evolution that can act as calibration points for further dating studies within insect families and genera.
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            Is sparse taxon sampling a problem for phylogenetic inference?

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              Is it better to add taxa or characters to a difficult phylogenetic problem?

              A Graybeal (1998)
              The effects on phylogenetic accuracy of adding characters and/or taxa were explored using data generated by computer simulation. The conditions of this study were constrained but allowed for systematic investigation of certain parameters. The starting point for the study was a four-taxon tree in the "Felsenstein zone," representing a difficult phylogenetic problem with an extreme situation of long branch attraction. Taxa were added sequentially to this tree in a manner specifically designed to break up the long branches, and for each tree data matrices of different sizes were simulated. Phylogenetic trees were reconstructed from these data using the criteria of parsimony and maximum likelihood. Phylogenetic accuracy was measured in three ways: (1) proportion of trees that are completely correct, (2) proportion of correctly reconstructed branches in all trees, and (3) proportion of trees in which the original four-taxon statement is correctly reconstructed. Accuracy improved dramatically with the addition of taxa and much more slowly with the addition of characters. If taxa can be added to break up long branches, it is much more preferable to add taxa than characters.
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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, CA USA )
                1935-2727
                1935-2735
                8 April 2016
                April 2016
                : 10
                : 4
                : e0004527
                Affiliations
                [1 ]Departamento de Genética, Universidade Federal do Rio de Janeiro, Brazil
                [2 ]Laboratório Nacional e Internacional de Referência em Taxonomia de Triatomíneos, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil
                Temple University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: SAJ CG CGS. Performed the experiments: SAJ CGS. Analyzed the data: SAJ CGS. Contributed reagents/materials/analysis tools: SAJ CG CGS. Wrote the paper: SAJ CGS.

                [¤]

                Current address: Department of Biology, University of Vermont, Burlington, Vermont, United States of America

                Article
                PNTD-D-15-01595
                10.1371/journal.pntd.0004527
                4825970
                27058599
                372d742c-11a0-4f1a-a17e-b606e6f8fef5
                © 2016 Justi 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
                : 13 October 2015
                : 18 February 2016
                Page count
                Figures: 4, Tables: 3, Pages: 22
                Funding
                CGS was funded by CNPq grant 310974/2015-1. SAJ was a funded PostDoctoral Fellow by the Brazilian National Research Council (CNPq) and is now funded by by NSF grant BCS-1216193 as part of the joint NSF-NIH-USDA Ecology and Evolution of Infectious Diseases program. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Infectious disease & Microbiology

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