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      Incomplete lineage sorting impacts the inference of macroevolutionary regimes from molecular phylogenies when concatenation is employed: An analysis based on Cetacea

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          Abstract

          Interest in methods that estimate speciation and extinction rates from molecular phylogenies has increased over the last decade. The application of such methods requires reliable estimates of tree topology and node ages, which are frequently obtained using standard phylogenetic inference combining concatenated loci and molecular dating. However, this practice disregards population‐level processes that generate gene tree/species tree discordance. We evaluated the impact of employing concatenation and coalescent‐based phylogeny inference in recovering the correct macroevolutionary regime using simulated data based on the well‐established diversification rate shift of delphinids in Cetacea. We found that under scenarios of strong incomplete lineage sorting, macroevolutionary analysis of phylogenies inferred by concatenating loci failed to recover the delphinid diversification shift, while the coalescent‐based tree consistently retrieved the correct rate regime. We suggest that ignoring microevolutionary processes reduces the power of methods that estimate macroevolutionary regimes from molecular data.

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          Most cited references38

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          geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees.

          Phylogenetic comparative methods are essential for addressing evolutionary hypotheses with interspecific data. The scale and scope of such data have increased dramatically in the past few years. Many existing approaches are either computationally infeasible or inappropriate for data of this size. To address both of these problems, we present geiger v2.0, a complete overhaul of the popular R package geiger. We have reimplemented existing methods with more efficient algorithms and have developed several new approaches for accomodating heterogeneous models and data types.
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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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              Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates.

              The uneven distribution of species richness is a fundamental and unexplained pattern of vertebrate biodiversity. Although species richness in groups like mammals, birds, or teleost fishes is often attributed to accelerated cladogenesis, we lack a quantitative conceptual framework for identifying and comparing the exceptional changes of tempo in vertebrate evolutionary history. We develop MEDUSA, a stepwise approach based upon the Akaike information criterion for detecting multiple shifts in birth and death rates on an incompletely resolved phylogeny. We apply MEDUSA incompletely to a diversity tree summarizing both evolutionary relationships and species richness of 44 major clades of jawed vertebrates. We identify 9 major changes in the tempo of gnathostome diversification; the most significant of these lies at the base of a clade that includes most of the coral-reef associated fishes as well as cichlids and perches. Rate increases also underlie several well recognized tetrapod radiations, including most modern birds, lizards and snakes, ostariophysan fishes, and most eutherian mammals. In addition, we find that large sections of the vertebrate tree exhibit nearly equal rates of origination and extinction, providing some of the first evidence from molecular data for the importance of faunal turnover in shaping biodiversity. Together, these results reveal living vertebrate biodiversity to be the product of volatile turnover punctuated by 6 accelerations responsible for >85% of all species as well as 3 slowdowns that have produced "living fossils." In addition, by revealing the timing of the exceptional pulses of vertebrate diversification as well as the clades that experience them, our diversity tree provides a framework for evaluating particular causal hypotheses of vertebrate radiations.
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                Author and article information

                Contributors
                carlos.schrago@gmail.com
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                11 June 2018
                July 2018
                : 8
                : 14 ( doiID: 10.1002/ece3.2018.8.issue-14 )
                : 6965-6971
                Affiliations
                [ 1 ] Department of Genetics Federal University of Rio de Janeiro Rio de Janeiro Brazil
                Author notes
                [*] [* ] Correspondence

                Carlos G. Schrago, Instituto de Biologia, Departamento de Genética, Universidade Federal do Rio de Janeiro, CCS, A2‐092, Rua Prof. Rodolpho Paulo Rocco, SN, Cidade Universitária, Rio de Janeiro, RJ, CEP: 21941‐617 Brazil.

                Email: carlos.schrago@ 123456gmail.com

                Author information
                http://orcid.org/0000-0001-6257-8906
                Article
                ECE34212
                10.1002/ece3.4212
                6065336
                196588c3-a100-40e3-bbd4-fb5fb4d45365
                © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 27 February 2018
                : 17 April 2018
                : 19 April 2018
                Page count
                Figures: 3, Tables: 1, Pages: 7, Words: 4824
                Funding
                Funded by: Brazilian Research Council (CNPq)
                Award ID: 310974/2015‐1
                Award ID: 440954/2016‐9
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece34212
                July 2018
                Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.4.4 mode:remove_FC converted:30.07.2018

                Evolutionary Biology
                concatenation,diversification,multispecies coalescent,simulation
                Evolutionary Biology
                concatenation, diversification, multispecies coalescent, simulation

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