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      A Species-Level Phylogeny of Extant Snakes with Description of a New Colubrid Subfamily and Genus

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          Abstract

          Background

          With over 3,500 species encompassing a diverse range of morphologies and ecologies, snakes make up 36% of squamate diversity. Despite several attempts at estimating higher-level snake relationships and numerous assessments of generic- or species-level phylogenies, a large-scale species-level phylogeny solely focusing on snakes has not been completed. Here, we provide the largest-yet estimate of the snake tree of life using maximum likelihood on a supermatrix of 1745 taxa (1652 snake species + 7 outgroup taxa) and 9,523 base pairs from 10 loci (5 nuclear, 5 mitochondrial), including previously unsequenced genera (2) and species (61).

          Results

          Increased taxon sampling resulted in a phylogeny with a new higher-level topology and corroborate many lower-level relationships, strengthened by high nodal support values (> 85%) down to the species level (73.69% of nodes). Although the majority of families and subfamilies were strongly supported as monophyletic with > 88% support values, some families and numerous genera were paraphyletic, primarily due to limited taxon and loci sampling leading to a sparse supermatrix and minimal sequence overlap between some closely-related taxa. With all rogue taxa and incertae sedis species eliminated, higher-level relationships and support values remained relatively unchanged, except in five problematic clades.

          Conclusion

          Our analyses resulted in new topologies at higher- and lower-levels; resolved several previous topological issues; established novel paraphyletic affiliations; designated a new subfamily, Ahaetuliinae, for the genera Ahaetulla, Chrysopelea, Dendrelaphis, and Dryophiops; and appointed Hemerophis ( Coluber) zebrinus to a new genus, Mopanveldophis. Although we provide insight into some distinguished problematic nodes, at the deeper phylogenetic scale, resolution of these nodes may require sampling of more slowly-evolving nuclear genes.

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          Most cited references60

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          Is a new and general theory of molecular systematics emerging?

          The advent and maturation of algorithms for estimating species trees-phylogenetic trees that allow gene tree heterogeneity and whose tips represent lineages, populations and species, as opposed to genes-represent an exciting confluence of phylogenetics, phylogeography, and population genetics, and ushers in a new generation of concepts and challenges for the molecular systematist. In this essay I argue that to better deal with the large multilocus datasets brought on by phylogenomics, and to better align the fields of phylogeography and phylogenetics, we should embrace the primacy of species trees, not only as a new and useful practical tool for systematics, but also as a long-standing conceptual goal of systematics that, largely due to the lack of appropriate computational tools, has been eclipsed in the past few decades. I suggest that phylogenies as gene trees are a "local optimum" for systematics, and review recent advances that will bring us to the broader optimum inherent in species trees. In addition to adopting new methods of phylogenetic analysis (and ideally reserving the term "phylogeny" for species trees rather than gene trees), the new paradigm suggests shifts in a number of practices, such as sampling data to maximize not only the number of accumulated sites but also the number of independently segregating genes; routinely using coalescent or other models in computer simulations to allow gene tree heterogeneity; and understanding better the role of concatenation in influencing topologies and confidence in phylogenies. By building on the foundation laid by concepts of gene trees and coalescent theory, and by taking cues from recent trends in multilocus phylogeography, molecular systematics stands to be enriched. Many of the challenges and lessons learned for estimating gene trees will carry over to the challenge of estimating species trees, although adopting the species tree paradigm will clarify many issues (such as the nature of polytomies and the star tree paradox), raise conceptually new challenges, or provide new answers to old questions.
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            The Effect of Ambiguous Data on Phylogenetic Estimates Obtained by Maximum Likelihood and Bayesian Inference

            Abstract Although an increasing number of phylogenetic data sets are incomplete, the effect of ambiguous data on phylogenetic accuracy is not well understood. We use 4-taxon simulations to study the effects of ambiguous data (i.e., missing characters or gaps) in maximum likelihood (ML) and Bayesian frameworks. By introducing ambiguous data in a way that removes confounding factors, we provide the first clear understanding of 1 mechanism by which ambiguous data can mislead phylogenetic analyses. We find that in both ML and Bayesian frameworks, among-site rate variation can interact with ambiguous data to produce misleading estimates of topology and branch lengths. Furthermore, within a Bayesian framework, priors on branch lengths and rate heterogeneity parameters can exacerbate the effects of ambiguous data, resulting in strongly misleading bipartition posterior probabilities. The magnitude and direction of the ambiguous data bias are a function of the number and taxonomic distribution of ambiguous characters, the strength of topological support, and whether or not the model is correctly specified. The results of this study have major implications for all analyses that rely on accurate estimates of topology or branch lengths, including divergence time estimation, ancestral state reconstruction, tree-dependent comparative methods, rate variation analysis, phylogenetic hypothesis testing, and phylogeographic analysis.
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              Pruning Rogue Taxa Improves Phylogenetic Accuracy: An Efficient Algorithm and Webservice

              The presence of rogue taxa (rogues) in a set of trees can frequently have a negative impact on the results of a bootstrap analysis (e.g., the overall support in consensus trees). We introduce an efficient graph-based algorithm for rogue taxon identification as well as an interactive webservice implementing this algorithm. Compared with our previous method, the new algorithm is up to 4 orders of magnitude faster, while returning qualitatively identical results. Because of this significant improvement in scalability, the new algorithm can now identify substantially more complex and compute-intensive rogue taxon constellations. On a large and diverse collection of real-world data sets, we show that our method yields better supported reduced/pruned consensus trees than any competing rogue taxon identification method. Using the parallel version of our open-source code, we successfully identified rogue taxa in a set of 100 trees with 116 334 taxa each. For simulated data sets, we show that when removing/pruning rogue taxa with our method from a tree set, we consistently obtain bootstrap consensus trees as well as maximum-likelihood trees that are topologically closer to the respective true trees.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 September 2016
                2016
                : 11
                : 9
                : e0161070
                Affiliations
                [1 ]Department of Biological Sciences, University of New Orleans, New Orleans, LA, United States of America
                [2 ]Department of Biology, The Graduate School and Center, City University of New York, New York, NY, United States of America
                [3 ]Department of Biology, 6S-143, College of Staten Island, 2800 Victory Boulevard, Staten Island, NY, United States of America
                [4 ]Department of Biology, La Sierra University, 4500 Riverwalk Parkway, Riverside, CA, United States of America
                National and Kapodistrian University of Athens, GREECE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceived and designed the experiments: AF SPL ADM.

                • Performed the experiments: AF ADM.

                • Analyzed the data: AF ADM.

                • Contributed reagents/materials/analysis tools: LLG CDB.

                • Wrote the paper: AF SPL ADM.

                Author information
                http://orcid.org/0000-0002-5083-9993
                Article
                PONE-D-16-12736
                10.1371/journal.pone.0161070
                5014348
                27603205
                2ae50cd1-48b9-40a7-a992-aa523214353f
                © 2016 Figueroa 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
                : 29 March 2016
                : 28 July 2016
                Page count
                Figures: 10, Tables: 1, Pages: 31
                Funding
                This work was supported by National Science Foundation East Asia & Pacific Summer Institute (OISE-1107819); University of New Orleans College of Sciences Graduate Student Research Grant; University of New Orleans Department of Biological Science Dissertation Enhancement Award; University of New Orleans Dissertation Improvement Grant; and University of New Orleans Latin American Studies Abroad Program Award. The funders 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
                Molecular Biology
                Molecular Biology Techniques
                Molecular Biology Assays and Analysis Techniques
                Phylogenetic Analysis
                Research and Analysis Methods
                Molecular Biology Techniques
                Molecular Biology Assays and Analysis Techniques
                Phylogenetic Analysis
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Reptiles
                Squamates
                Snakes
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
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                Taxonomy
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                Biology and Life Sciences
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                Custom metadata
                GenBank accession numbers are contained within the paper. All other relevant data are within the paper and its Supporting Information files.

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