Implementing and testing the multispecies coalescent model: A valuable paradigm for phylogenomics

In recent articles published in Molecular Phylogenetics and Evolution, Mark Springer and John Gatesy (S&G) present numerous criticisms of recent implementations and testing of the multispecies coalescent (MSC) model in phylogenomics, popularly known as “species tree” methods. After pointing out...

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Published inMolecular phylogenetics and evolution Vol. 94; no. Pt A; pp. 447 - 462
Main Authors Edwards, Scott V., Xi, Zhenxiang, Janke, Axel, Faircloth, Brant C., McCormack, John E., Glenn, Travis C., Zhong, Bojian, Wu, Shaoyuan, Lemmon, Emily Moriarty, Lemmon, Alan R., Leaché, Adam D., Liu, Liang, Davis, Charles C.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.01.2016
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Abstract In recent articles published in Molecular Phylogenetics and Evolution, Mark Springer and John Gatesy (S&G) present numerous criticisms of recent implementations and testing of the multispecies coalescent (MSC) model in phylogenomics, popularly known as “species tree” methods. After pointing out errors in alignments and gene tree rooting in recent phylogenomic data sets, particularly in Song et al. (2012) on mammals and Xi et al. (2014) on plants, they suggest that these errors seriously compromise the conclusions of these studies. Additionally, S&G enumerate numerous perceived violated assumptions and deficiencies in the application of the MSC model in phylogenomics, such as its assumption of neutrality and in particular the use of transcriptomes, which are deemed inappropriate for the MSC because the constituent exons often subtend large regions of chromosomes within which recombination is substantial. We acknowledge these previously reported errors in recent phylogenomic data sets, but disapprove of S&G’s excessively combative and taunting tone. We show that these errors, as well as two nucleotide sorting methods used in the analysis of Amborella, have little impact on the conclusions of those papers. Moreover, several concepts introduced by S&G and an appeal to “first principles” of phylogenetics in an attempt to discredit MSC models are invalid and reveal numerous misunderstandings of the MSC. Contrary to the claims of S&G we show that recent computer simulations used to test the robustness of MSC models are not circular and do not unfairly favor MSC models over concatenation. In fact, although both concatenation and MSC models clearly perform well in regions of tree space with long branches and little incomplete lineage sorting (ILS), simulations reveal the erratic behavior of concatenation when subjected to data subsampling and its tendency to produce spuriously confident yet conflicting results in regions of parameter space where MSC models still perform well. S&G’s claims that MSC models explain little or none (0–15%) of the observed gene tree heterogeneity observed in a mammal data set and that MSC models assume ILS as the only source of gene tree variation are flawed. Overall many of their criticisms of MSC models are invalidated when concatenation is appropriately viewed as a special case of the MSC, which in turn is a special case of emerging network models in phylogenomics. We reiterate that there is enormous promise and value in recent implementations and tests of the MSC and look forward to its increased use and refinement in phylogenomics.
AbstractList In recent articles published in Molecular Phylogenetics and Evolution, Mark Springer and John Gatesy (S&G) present numerous criticisms of recent implementations and testing of the multispecies coalescent (MSC) model in phylogenomics, popularly known as “species tree” methods. After pointing out errors in alignments and gene tree rooting in recent phylogenomic data sets, particularly in Song et al. (2012) on mammals and Xi et al. (2014) on plants, they suggest that these errors seriously compromise the conclusions of these studies. Additionally, S&G enumerate numerous perceived violated assumptions and deficiencies in the application of the MSC model in phylogenomics, such as its assumption of neutrality and in particular the use of transcriptomes, which are deemed inappropriate for the MSC because the constituent exons often subtend large regions of chromosomes within which recombination is substantial. We acknowledge these previously reported errors in recent phylogenomic data sets, but disapprove of S&G’s excessively combative and taunting tone. We show that these errors, as well as two nucleotide sorting methods used in the analysis of Amborella, have little impact on the conclusions of those papers. Moreover, several concepts introduced by S&G and an appeal to “first principles” of phylogenetics in an attempt to discredit MSC models are invalid and reveal numerous misunderstandings of the MSC. Contrary to the claims of S&G we show that recent computer simulations used to test the robustness of MSC models are not circular and do not unfairly favor MSC models over concatenation. In fact, although both concatenation and MSC models clearly perform well in regions of tree space with long branches and little incomplete lineage sorting (ILS), simulations reveal the erratic behavior of concatenation when subjected to data subsampling and its tendency to produce spuriously confident yet conflicting results in regions of parameter space where MSC models still perform well. S&G’s claims that MSC models explain little or none (0–15%) of the observed gene tree heterogeneity observed in a mammal data set and that MSC models assume ILS as the only source of gene tree variation are flawed. Overall many of their criticisms of MSC models are invalidated when concatenation is appropriately viewed as a special case of the MSC, which in turn is a special case of emerging network models in phylogenomics. We reiterate that there is enormous promise and value in recent implementations and tests of the MSC and look forward to its increased use and refinement in phylogenomics.
In recent articles published in Molecular Phylogenetics and Evolution, Mark Springer and John Gatesy (S&G) present numerous criticisms of recent implementations and testing of the multispecies coalescent (MSC) model in phylogenomics, popularly known as "species tree" methods. After pointing out errors in alignments and gene tree rooting in recent phylogenomic data sets, particularly in Song et al. (2012) on mammals and Xi et al. (2014) on plants, they suggest that these errors seriously compromise the conclusions of these studies. Additionally, S&G enumerate numerous perceived violated assumptions and deficiencies in the application of the MSC model in phylogenomics, such as its assumption of neutrality and in particular the use of transcriptomes, which are deemed inappropriate for the MSC because the constituent exons often subtend large regions of chromosomes within which recombination is substantial. We acknowledge these previously reported errors in recent phylogenomic data sets, but disapprove of S&G's excessively combative and taunting tone. We show that these errors, as well as two nucleotide sorting methods used in the analysis of Amborella, have little impact on the conclusions of those papers. Moreover, several concepts introduced by S&G and an appeal to "first principles" of phylogenetics in an attempt to discredit MSC models are invalid and reveal numerous misunderstandings of the MSC. Contrary to the claims of S&G we show that recent computer simulations used to test the robustness of MSC models are not circular and do not unfairly favor MSC models over concatenation. In fact, although both concatenation and MSC models clearly perform well in regions of tree space with long branches and little incomplete lineage sorting (ILS), simulations reveal the erratic behavior of concatenation when subjected to data subsampling and its tendency to produce spuriously confident yet conflicting results in regions of parameter space where MSC models still perform well. S&G's claims that MSC models explain little or none (0-15%) of the observed gene tree heterogeneity observed in a mammal data set and that MSC models assume ILS as the only source of gene tree variation are flawed. Overall many of their criticisms of MSC models are invalidated when concatenation is appropriately viewed as a special case of the MSC, which in turn is a special case of emerging network models in phylogenomics. We reiterate that there is enormous promise and value in recent implementations and tests of the MSC and look forward to its increased use and refinement in phylogenomics.In recent articles published in Molecular Phylogenetics and Evolution, Mark Springer and John Gatesy (S&G) present numerous criticisms of recent implementations and testing of the multispecies coalescent (MSC) model in phylogenomics, popularly known as "species tree" methods. After pointing out errors in alignments and gene tree rooting in recent phylogenomic data sets, particularly in Song et al. (2012) on mammals and Xi et al. (2014) on plants, they suggest that these errors seriously compromise the conclusions of these studies. Additionally, S&G enumerate numerous perceived violated assumptions and deficiencies in the application of the MSC model in phylogenomics, such as its assumption of neutrality and in particular the use of transcriptomes, which are deemed inappropriate for the MSC because the constituent exons often subtend large regions of chromosomes within which recombination is substantial. We acknowledge these previously reported errors in recent phylogenomic data sets, but disapprove of S&G's excessively combative and taunting tone. We show that these errors, as well as two nucleotide sorting methods used in the analysis of Amborella, have little impact on the conclusions of those papers. Moreover, several concepts introduced by S&G and an appeal to "first principles" of phylogenetics in an attempt to discredit MSC models are invalid and reveal numerous misunderstandings of the MSC. Contrary to the claims of S&G we show that recent computer simulations used to test the robustness of MSC models are not circular and do not unfairly favor MSC models over concatenation. In fact, although both concatenation and MSC models clearly perform well in regions of tree space with long branches and little incomplete lineage sorting (ILS), simulations reveal the erratic behavior of concatenation when subjected to data subsampling and its tendency to produce spuriously confident yet conflicting results in regions of parameter space where MSC models still perform well. S&G's claims that MSC models explain little or none (0-15%) of the observed gene tree heterogeneity observed in a mammal data set and that MSC models assume ILS as the only source of gene tree variation are flawed. Overall many of their criticisms of MSC models are invalidated when concatenation is appropriately viewed as a special case of the MSC, which in turn is a special case of emerging network models in phylogenomics. We reiterate that there is enormous promise and value in recent implementations and tests of the MSC and look forward to its increased use and refinement in phylogenomics.
Author Janke, Axel
Zhong, Bojian
Lemmon, Alan R.
Leaché, Adam D.
Liu, Liang
Wu, Shaoyuan
Glenn, Travis C.
Xi, Zhenxiang
McCormack, John E.
Faircloth, Brant C.
Davis, Charles C.
Lemmon, Emily Moriarty
Edwards, Scott V.
Author_xml – sequence: 1
  givenname: Scott V.
  surname: Edwards
  fullname: Edwards, Scott V.
  email: sedwards@fas.harvard.edu
  organization: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
– sequence: 2
  givenname: Zhenxiang
  surname: Xi
  fullname: Xi, Zhenxiang
  organization: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
– sequence: 3
  givenname: Axel
  surname: Janke
  fullname: Janke, Axel
  organization: Senckenberg Biodiversity and Climate Research Centre, Senckenberg Gesellschaft für Naturforschung, Senckenberganlage 25, D-60325 Frankfurt am Main, Germany
– sequence: 4
  givenname: Brant C.
  surname: Faircloth
  fullname: Faircloth, Brant C.
  organization: Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803, USA
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  givenname: John E.
  surname: McCormack
  fullname: McCormack, John E.
  organization: Moore Laboratory of Zoology, Occidental College, Los Angeles, CA 90041, USA
– sequence: 6
  givenname: Travis C.
  surname: Glenn
  fullname: Glenn, Travis C.
  organization: Department of Environmental Health Science, University of Georgia, Athens, GA 30602, USA
– sequence: 7
  givenname: Bojian
  surname: Zhong
  fullname: Zhong, Bojian
  organization: College of Life Sciences, Nanjing Normal University, Nanjing 210023, China
– sequence: 8
  givenname: Shaoyuan
  surname: Wu
  fullname: Wu, Shaoyuan
  organization: Department of Biochemistry and Molecular Biology & Tianjin Key Laboratory of Medical Epigenetics, School of Basic Medical Sciences, Tianjin Medical University, Tianjin 300070, China
– sequence: 9
  givenname: Emily Moriarty
  surname: Lemmon
  fullname: Lemmon, Emily Moriarty
  organization: Department of Biological Science, Florida State University, Tallahassee, FL 32306, USA
– sequence: 10
  givenname: Alan R.
  surname: Lemmon
  fullname: Lemmon, Alan R.
  organization: Department of Scientific Computing, Florida State University, Tallahassee, FL 32306, USA
– sequence: 11
  givenname: Adam D.
  surname: Leaché
  fullname: Leaché, Adam D.
  organization: Department of Biology & Burke Museum of Natural History and Culture, University of Washington, Seattle, WA 98195, USA
– sequence: 12
  givenname: Liang
  surname: Liu
  fullname: Liu, Liang
  organization: Department of Statistics and Institute of Bioinformatics, University of Georgia, Athens, GA 30602, USA
– sequence: 13
  givenname: Charles C.
  surname: Davis
  fullname: Davis, Charles C.
  organization: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/26518740$$D View this record in MEDLINE/PubMed
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Snippet In recent articles published in Molecular Phylogenetics and Evolution, Mark Springer and John Gatesy (S&G) present numerous criticisms of recent...
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SubjectTerms Amborella
Animals
chromosomes
Computer Simulation
data collection
Evolution, Molecular
exons
Genetic Speciation
Genomics - methods
Magnoliopsida - classification
Magnoliopsida - genetics
mammals
Mammals - classification
Mammals - genetics
Models, Genetic
Phylogeny
Recombination, Genetic
rooting
transcriptome
Title Implementing and testing the multispecies coalescent model: A valuable paradigm for phylogenomics
URI https://dx.doi.org/10.1016/j.ympev.2015.10.027
https://www.ncbi.nlm.nih.gov/pubmed/26518740
https://www.proquest.com/docview/1735333734
https://www.proquest.com/docview/1825426459
Volume 94
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