To tackle incongruence, the topological conflict between different gene trees, phylogenomic studies couple concatenation with practices such as rogue taxon removal or the use of slowly evolving genes. Phylogenomic analysis of 1,070 orthologues from 23 yeast genomes identified 1,070 distinct gene trees, which were all incongruent with the phylogeny inferred from concatenation. Incongruence severity increased for shorter internodes located deeper in the phylogeny. Notably, whereas most practices had little or negative impact on the yeast phylogeny, the use of genes or internodes with high average internode support significantly improved the robustness of inference. We obtained similar results in analyses of vertebrate and metazoan phylogenomic data sets. These results question the exclusive reliance on concatenation and associated practices, and argue that selecting genes with strong phylogenetic signals and demonstrating the absence of significant incongruence are essential for accurately reconstructing ancient divergences.
At a glance
- Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749 (2008) et al.
- Animal evolution and the molecular signature of radiations compressed in time. Science 310, 1933–1938 (2005) , &
- Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706–712 (2009) et al.
- Concatenated analysis sheds light on early metazoan evolution and fuels a modern “urmetazoon” hypothesis. PLoS Biol. 7, e20 (2009) et al.
- Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463, 1079–1083 (2010) et al.
- Genome-scale phylogeny and the detection of systematic biases. Mol. Biol. Evol. 21, 1455–1458 (2004) , &
- Addressing inter-gene heterogeneity in maximum likelihood phylogenomic analysis: yeasts revisited. PLoS ONE 6, e22783 (2011) &
- Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332–340 (2009) &
- Bushes in the tree of life. PLoS Biol. 4, e352 (2006) &
- Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 9, e1000602 (2011) et al.
- Phylogenomics reveals deep molluscan relationships. Nature 477, 452–456 (2011) et al.
- Resolving the evolutionary relationships of molluscs with phylogenomic tools. Nature 480, 364–367 (2011) et al.
- Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida. Nature 444, 85–88 (2006) et al.
- Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–968 (2006) , , &
- Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267 (2006) &
- Resolving arthropod phylogeny: exploring phylogenetic signal within 41 kb of protein-coding nuclear gene sequence. Syst. Biol. 57, 920–938 (2008) et al.
- Sources of signal in 62 protein-coding nuclear genes for higher-level phylogenetics of arthropods. PLoS ONE 6, e23408 (2011) &
- Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56, 564–577 (2007) &
- Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798–804 (2003) , , &
- The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 15, 1456–1461 (2005) &
- Analysis of gene evolution and metabolic pathways using the Candida Gene Order Browser. BMC Genomics 11, 290 (2010) , , &
- Multiple rounds of speciation associated with reciprocal gene loss in polyploid yeasts. Nature 440, 341–345 (2006) , , , &
- Evaluating ortholog prediction algorithms in a yeast model clade. PLoS ONE 6, e18755 (2011) &
- Multiple GAL pathway gene clusters evolved independently and by different mechanisms in fungi. Proc. Natl Acad. Sci. USA 107, 10136–10141 (2010) &
- A phase transition for a random cluster model on phylogenetic trees. Math. Biosci. 187, 189–203 (2004) &
- Phylogenetic signal and noise: predicting the power of a data set to resolve phylogeny. Syst. Biol. 61, 835–849 (2012) , &
- The awesome power of yeast evolutionary genetics: new genome sequences and strain resources for the Saccharomyces sensu stricto genus. G3 1, 11–25 (2011) et al.
- Comparison of phylogenetic trees. Math. Biosci. 53, 131–147 (1981) &
- Testing significance of incongruence. Cladistics 10, 315–319 (1995) , , &
- Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and apes. Evolution 37, 221–244 (1983)
- Multiple sources of character information and the phylogeny of Hawaiian drosophilids. Syst. Biol. 46, 654–673 (1997) &
- A randomisation test of the null hypothesis that two cladograms are sample estimates of a parametric phylogenetic tree. N. Z. J. Bot. 31, 257–268 (1993) , , &
- The probability of a gene tree topology within a phylogenetic network with applications to hybridization detection. PLoS Genet. 8, e1002660 (2012) , &
- Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc. Natl Acad. Sci. USA 101, 14144–14149 (2004) , &
- More genes or more taxa? The relative contribution of gene number and taxon number to phylogenetic accuracy. Mol. Biol. Evol. 22, 1337–1344 (2005) &
- Phylogenomics: the beginning of incongruence? Trends Genet. 22, 225–231 (2006) , , &
- A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol. 6, 99 (2006) , , &
- Estimating species phylogenies using coalescence times among sequences. Syst. Biol. 58, 468–477 (2009) , , &
- Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791 (1985)
- Leveraging skewed transcript abundance by RNA-seq to increase the genomic depth of the tree of life. Proc. Natl Acad. Sci. USA 107, 1476–1481 (2010) , , &
- Statistics and truth in phylogenomics. Mol. Biol. Evol. 29, 457–472 (2012) , , , &
- Can three incongruence tests predict when data should be combined? Mol. Biol. Evol. 14, 733–740 (1997)
- Recent developments in the MAFFT multiple sequence alignment program. Brief. Bioinform. 9, 286–298 (2008) &
- Prottest: selection of best-fit models of protein evolution. Bioinformatics 21, 2104–2105 (2005) , &
- RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690 (2006)
- Yeast evolutionary genomics. Nature Rev. Genet. 11, 512–524 (2010)
- Yeast genome evolution-the origin of the species. Yeast 24, 929–942 (2007) , &
- Contribution of horizontal gene transfer to the evolution of Saccharomyces cerevisiae. Eukaryot. Cell 4, 1102–1115 (2005) , &
- The ASP3 locus in Saccharomyces cerevisiae originated by horizontal gene transfer from Wickerhamomyces. FEMS Yeast Res. 12, 859–863 (2012) , &
- Eukaryote-to-eukaryote gene transfer events revealed by the genome sequence of the wine yeast Saccharomyces cerevisiae EC1118. Proc. Natl Acad. Sci. USA 106, 16333–16338 (2009) et al.
- Gene ontology: tool for the unification of biology. Nature Genet. 25, 25–29 (2000) et al.
- GOstat: find statistically overrepresented Gene Ontologies within a group of genes. Bioinformatics 20, 1464–1465 (2004) &
- A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18, 691–699 (2001) &
- Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets under the Maximum Likelihood Criterion. Ph.D. thesis, Univ. Texas at Austin. (2006)
- MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003) &
- 163–184 (American Mathematical Society and DIMACS, 2003) in Bioconsensus (eds et al.)
- 2003) Inferring Phylogenies. (Sinauer,
- T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucleic Acids Res. 40, W573–W579 (2012) , &
- A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol. Biol. Evol. 11, 459–468 (1994) &
- Using consensus networks to visualize contradictory evidence for species phylogeny. Mol. Biol. Evol. 21, 1459–1461 (2004) , , &
- A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423 (1948)
- Ecdysozoan clade rejected by genome-wide analysis of rare amino acid replacements. Mol. Biol. Evol. 24, 1080–1090 (2007) , , &
- Large-scale parsimony analysis of metazoan indels in protein-coding genes. Mol. Biol. Evol. 27, 441–451 (2010) , &
- Supplementary Information (1 MB)
This file contains Supplementary Tables 1-2 and Supplementary Figures 1-17.