Discordance of Species Trees with Their Most Likely Gene Trees

Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly, assuming that genetic lineages follow a coalescent model of within-species evolution, we find that for any species tree topology with five o...

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Published inPLoS genetics Vol. 2; no. 5; p. e68
Main Authors Degnan, James H, Rosenberg, Noah A
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.05.2006
Public Library of Science (PLoS)
Subjects
Online AccessGet full text
ISSN1553-7404
1553-7390
1553-7404
DOI10.1371/journal.pgen.0020068

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Abstract Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly, assuming that genetic lineages follow a coalescent model of within-species evolution, we find that for any species tree topology with five or more species, there exist branch lengths for which gene tree discordance is so common that the most likely gene tree topology to evolve along the branches of a species tree differs from the species phylogeny. This counterintuitive result implies that in combining data on multiple loci, the straightforward procedure of using the most frequently observed gene tree topology as an estimate of the species tree topology can be asymptotically guaranteed to produce an incorrect estimate. We conclude with suggestions that can aid in overcoming this new obstacle to accurate genomic inference of species phylogenies.
AbstractList Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly, assuming that genetic lineages follow a coalescent model of within-species evolution, we find that for any species tree topology with five or more species, there exist branch lengths for which gene tree discordance is so common that the most likely gene tree topology to evolve along the branches of a species tree differs from the species phylogeny. This counterintuitive result implies that in combining data on multiple loci, the straightforward procedure of using the most frequently observed gene tree topology as an estimate of the species tree topology can be asymptotically guaranteed to produce an incorrect estimate. We conclude with suggestions that can aid in overcoming this new obstacle to accurate genomic inference of species phylogenies.Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly, assuming that genetic lineages follow a coalescent model of within-species evolution, we find that for any species tree topology with five or more species, there exist branch lengths for which gene tree discordance is so common that the most likely gene tree topology to evolve along the branches of a species tree differs from the species phylogeny. This counterintuitive result implies that in combining data on multiple loci, the straightforward procedure of using the most frequently observed gene tree topology as an estimate of the species tree topology can be asymptotically guaranteed to produce an incorrect estimate. We conclude with suggestions that can aid in overcoming this new obstacle to accurate genomic inference of species phylogenies.
  Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly, assuming that genetic lineages follow a coalescent model of within-species evolution, we find that for any species tree topology with five or more species, there exist branch lengths for which gene tree discordance is so common that the most likely gene tree topology to evolve along the branches of a species tree differs from the species phylogeny. This counterintuitive result implies that in combining data on multiple loci, the straightforward procedure of using the most frequently observed gene tree topology as an estimate of the species tree topology can be asymptotically guaranteed to produce an incorrect estimate. We conclude with suggestions that can aid in overcoming this new obstacle to accurate genomic inference of species phylogenies.
Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly, assuming that genetic lineages follow a coalescent model of within-species evolution, we find that for any species tree topology with five or more species, there exist branch lengths for which gene tree discordance is so common that the most likely gene tree topology to evolve along the branches of a species tree differs from the species phylogeny. This counterintuitive result implies that in combining data on multiple loci, the straightforward procedure of using the most frequently observed gene tree topology as an estimate of the species tree topology can be asymptotically guaranteed to produce an incorrect estimate. We conclude with suggestions that can aid in overcoming this new obstacle to accurate genomic inference of species phylogenies.
Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly, assuming that genetic lineages follow a coalescent model of within-species evolution, we find that for any species tree topology with five or more species, there exist branch lengths for which gene tree discordance is so common that the most likely gene tree topology to evolve along the branches of a species tree differs from the species phylogeny. This counterintuitive result implies that in combining data on multiple loci, the straightforward procedure of using the most frequently observed gene tree topology as an estimate of the species tree topology can be asymptotically guaranteed to produce an incorrect estimate. We conclude with suggestions that can aid in overcoming this new obstacle to accurate genomic inference of species phylogenies. Different genomic regions evolving along the branches of a tree of species relationships can have different evolutionary histories. Consequently, estimates of species trees from genetic data may be influenced by the particular choice of genomic regions used in an analysis. Recent work has focused on circumventing this problem by combining information from multiple regions to attempt to produce accurate species tree estimates. The authors show that the use of multiple genomic regions for species tree inference is subject to a surprising new difficulty, the problem of “anomalous gene trees.” Not only can individual genes or genomic regions have genealogical histories that differ in shape, or topology, from a species tree, the gene tree topology most likely to evolve can differ from the species tree topology. As a result, the “democratic vote” procedure of using the most frequently observed gene tree topology as an estimate of the species tree topology can converge on the wrong species tree as more genes are added. As it becomes more feasible to simultaneously investigate many regions of a genome, species tree inference algorithms will need to begin taking the problem of anomalous gene trees into consideration.
Audience Academic
Author Degnan, James H
Rosenberg, Noah A
AuthorAffiliation 1 Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, United States of America
Harvard University, United States of America
2 Department of Human Genetics, Bioinformatics Program, and the Life Sciences Institute, University of Michigan, Ann Arbor, Michigan, United States of America
AuthorAffiliation_xml – name: 2 Department of Human Genetics, Bioinformatics Program, and the Life Sciences Institute, University of Michigan, Ann Arbor, Michigan, United States of America
– name: 1 Department of Biostatistics, Harvard School of Public Health, Boston, Massachusetts, United States of America
– name: Harvard University, United States of America
Author_xml – sequence: 1
  givenname: James H
  surname: Degnan
  fullname: Degnan, James H
– sequence: 2
  givenname: Noah A
  surname: Rosenberg
  fullname: Rosenberg, Noah A
BackLink https://www.ncbi.nlm.nih.gov/pubmed/16733550$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2006 Public Library of Science
2006 Degnan and Rosenberg. 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: Degnan JH, Rosenberg NA (2006) Discordance of Species Trees with Their Most Likely Gene Trees. PLoS Genet 2(5): e68. doi:10.1371/journal.pgen.0020068
2006 Degnan and Rosenberg. 2006
Copyright_xml – notice: COPYRIGHT 2006 Public Library of Science
– notice: 2006 Degnan and Rosenberg. 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: Degnan JH, Rosenberg NA (2006) Discordance of Species Trees with Their Most Likely Gene Trees. PLoS Genet 2(5): e68. doi:10.1371/journal.pgen.0020068
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Snippet Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees. Surprisingly,...
  Because of the stochastic way in which lineages sort during speciation, gene trees may differ in topology from each other and from species trees....
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SubjectTerms Algorithms
Animals
Computational Biology - methods
Evolution
Evolution, Molecular
Genes
Genetic Speciation
Genetics
Genetics, Population
Genetics/Population Genetics
Genomics
Genomics - methods
Humans
Models, Genetic
Models, Statistical
None
Origin of species
Phylogenetics
Phylogeny
Plant genetics
Species Specificity
Statistics
Stochastic Processes
Trees
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Title Discordance of Species Trees with Their Most Likely Gene Trees
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