Abstract
Much progress has been achieved in disentangling evolutionary relationships among species in the tree of life, but some taxonomic groups remain difficult to resolve despite increasing availability of genome-scale data sets. Here we present a practical approach to studying ancient divergences in the face of high levels of conflict, based on explicit gene genealogy interrogation (GGI). We show its efficacy in resolving the controversial relationships within the largest freshwater fish radiation (Otophysi) based on newly generated DNA sequences for 1,051 loci from 225 species. Initial results using a suite of standard methodologies revealed conflicting phylogenetic signal, which supports ten alternative evolutionary histories among early otophysan lineages. By contrast, GGI revealed that the vast majority of gene genealogies supports a single tree topology grounded on morphology that was not obtained by previous molecular studies. We also reanalysed published data sets for exemplary groups with recalcitrant resolution to assess the power of this approach. GGI supports the notion that ctenophores are the earliest-branching animal lineage, and adds insight into relationships within clades of yeasts, birds and mammals. GGI opens up a promising avenue to account for incompatible signals in large data sets and to discern between estimation error and actual biological conflict explaining gene tree discordance.
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References
Rokas, A., Williams, B. L., King, N. & Carroll, S. B. Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature 425, 798– 804 (2003).
Betancur-R., R., Naylor, G. & Orti, G. Conserved genes, sampling error, and phylogenomic inference. Syst. Biol. 63, 257– 262 (2014).
Simmons, M. P., Sloan, D. B. & Gatesy, J. The effects of subsampling gene trees on coalescent methods applied to ancient divergences. Mol. Phylogenet. Evol. 97, 76– 89 (2016).
Salichos, L. & Rokas, A. Inferring ancient divergences requires genes with strong phylogenetic signals. Nature 497, 327– 331 (2013).
Chen, M. Y., Liang, D. & Zhang, P. Selecting question-specific genes to reduce incongruence in phylogenomics: a case study of jawed vertebrate backbone phylogeny. Syst. Biol. 64, 1104– 1120 (2015).
Jeffroy, O., Brinkmann, H., Delsuc, F. & Philippe, H. Phylogenomics: the beginning of incongruence? Trends Genet. 22, 225– 231 (2006).
Kubatko, L. S. & Degnan, J. H. Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst. Biol. 56, 17– 24 (2007).
Degnan, J. H. & Rosenberg, N. A. Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol. Evol. 24, 332– 340 (2009).
Sen, S., Liu, L., Edwards, S. V. & Wu, S. Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model. Proc. Natl Acad. Sci. USA 109, 14942–14947 (2012).
Edwards, S. V., Liu, L. & Pearl, D. K. High-resolution species trees without concatenation. Proc. Natl Acad. Sci. USA 104, 5936– 5941 (2007).
Roch, S. & Steel, M. Likelihood-based tree reconstruction on a concatenation of aligned sequence data sets can be statistically inconsistent. Theor. Popul. Biol. 100C, 56– 62 (2014).
Heled, J. & Drummond, A. J. Bayesian inference of species trees from multilocus data. Mol. Biol. Evol. 27, 570– 580 (2010).
Chou, J. et al. A comparative study of SVDquartets and other coalescent-based species tree estimation methods. BMC Genomics 16, S2 (2015).
Gatesy, J. & Springer, M. S. Phylogenetic analysis at deep timescales: unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum. Mol. Phylogenet. Evol. 80, 231–266 (2014).
Roch, S. & Warnow, T. On the robustness to gene tree estimation error (or lack thereof) of coalescent-based species tree methods. Syst. Biol. 64, 663–676 (2015).
Mirarab, S., Bayzid, M. S., Boussau, B. & Warnow, T. Statistical binning enables an accurate coalescent-based estimation of the avian tree. Science 346, 1250463 (2014).
Bayzid, M. S., Mirarab, S., Boussau, B. & Warnow, T. Weighted statistical binning: enabling statistically consistent genome-scale phylogenetic analyses. PLoS ONE 10, e0129183 (2015).
Shen, X. X., Salichos, L. & Rokas, A. A genome-scale investigation of how sequence-, function-, and tree-based gene properties influence phylogenetic inference. Genome Biol. Evol. 8, 2565–2580 (2016).
Liu, L. & Edwards, S. V. Comment on “Statistical binning enables an accurate coalescent-based estimation of the avian tree”. Science 350, 171 (2015).
Springer, M. S. & Gatesy, J. The gene tree delusion. Mol. Phylogenet. Evol. 94, 1–33 (2016).
Edwards, S. V. et al. Implementing and testing the multispecies coalescent model: a valuable paradigm for phylogenomics. Mol. Phylogenet. Evol. 94, 447–462 (2016).
Chifman, J. & Kubatko, L. Quartet inference from SNP data under the coalescent model. Bioinformatics 30, 3317–3324 (2014).
Mirarab, S., Bayzid, M. S., Boussau, B. & Warnow, T. Response to Comment on “Statistical binning enables an accurate coalescent-based estimation of the avian tree”. Science 350, 171 (2015).
Posada, D. Phylogenomics for systematic biology. Syst. Biol. 65, 353–356 (2016).
Wu, Y. C., Rasmussen, M. D., Bansal, M. S. & Kellis, M. TreeFix: statistically informed gene tree error correction using species trees. Syst. Biol. 62, 110–120 (2013).
Alfaro, M. E. et al. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proc. Natl Acad. Sci. USA 106, 13410–13414 (2009).
Fink, S. V. & Fink, W. L. Interrelationships of the ostariophysan fishes (Teleostei). Zool. J. Linnean Soc. 72, 297–353 (1981).
Saitoh, K., Miya, M., Inoue, J. G., Ishiguro, N. B. & Nishida, M. Mitochondrial genomics of ostariophysan fishes: perspectives on phylogeny and biogeography. J. Mol. Evol. 56, 464–472 (2003).
Nakatani, M., Miya, M., Mabuchi, K., Saitoh, K. & Nishida, M. Evolutionary history of Otophysi (Teleostei), a major clade of the modern freshwater fishes: Pangaean origin and Mesozoic radiation. BMC Evol. Biol. 11, 177 (2011).
Chen, W. J., Lavoue, S. & Mayden, R. L. Evolutionary origin and early biogeography of otophysan fishes (Ostariophysi: Teleostei). Evolution 67, 2218–2239 (2013).
Chakrabarty, P., McMahan, C., Fink, W., Stiassny, M. L. & Alfaro, M. in ASIH – American Society of Ichthyologists and Herpetologists (eds Crump, M. L. & Donnelly, M. A.) (2013).
Hillis, D. M., Heath, T. A. & St. John, K. Analysis and visualization of tree space. Syst. Biol. 54, 471–482 (2005).
Betancur-R., R., Li, C., Munroe, T. A., Ballesteros, J. A. & Orti, G. Addressing gene-tree discordance and non-stationarity to resolve a multi-locus phylogeny of the flatfishes (Teleostei: Pleuronectiformes). Syst. Biol. 62, 763–785 (2013).
Romiguier, J., Ranwez, V., Delsuc, F., Galtier, N. & Douzery, E. J. Less is more in mammalian phylogenomics: AT-rich genes minimize tree conflicts and unravel the root of placental mammals. Mol. Biol. Evol. 30, 2134–2144 (2013).
Shimodaira, H. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492–508 (2002).
Allman, E. S., Degnan, J. H. & Rhodes, J. A. Identifying the rooted species tree from the distribution of unrooted gene trees under the coalescent. J. Math. Biol. 62, 833–862 (2010).
Degnan, J. H. Anomalous unrooted gene trees. Syst. Biol. 62, 574–590 (2013).
Maddison, W. P. Gene trees in species trees. Syst. Biol. 46, 523–536 (1997).
Pisani, D. et al. Genomic data do not support comb jellies as the sister group to all other animals. Proc. Natl Acad. Sci. USA 112, 15402–15407 (2015).
Whelan, N. V., Kocot, K. M., Moroz, L. L. & Halanych, K. M. Error, signal, and the placement of Ctenophora sister to all other animals. Proc. Natl Acad. Sci. USA 112, 5773–5778 (2015).
Dunn, C. W., Giribet, G., Edgecombe, G. D. & Hejnol, A. Animal phylogeny and its evolutionary implications. Annu. Rev. Ecol. Evol. Syst. 45, 371– 395 (2014).
Ryan, J. F. et al. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342, 1242592 (2013).
Prum, R. O. et al. A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526, 569–573 (2015).
Suh, A., Smeds, L. & Ellegren, H. The dynamics of incomplete lineage sorting across the ancient adaptive radiation of neoavian birds. PLoS Biol. 13, e1002224 (2015).
Jarvis, E. D. et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346, 1320–1331 (2014).
Song, S., Liu, L., Edwards, S. V. & Wub, S. Correction for Song et al., Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model. Proc. Natl Acad. Sci. USA 112, E6079 (2015).
Hahn, M. W. & Nakhleh, L. Irrational exuberance for resolved species trees. Evolution 70, 7–17 (2016).
Mamanova, L. et al. Target-enrichment strategies for next-generation sequencing. Nat. Methods 7, 111–118 (2010).
Li, C., Hofreiter, M., Straube, N., Corrigan, S. & Naylor, G. J. Capturing protein-coding genes across highly divergent species. BioTechniques 54, 321–326 (2013).
Dimmick, W. W. & Larson, A. A molecular and morphological perspective on the phylogenetic relationships of the otophysan fishes. Mol. Phylog. Evol. 6, 120–133 (1996).
Alves-Gomes, J. A. in Gonorynchiformes and Ostariophysan Relationships (eds Grande, T., Potayo-Ariza, F. J. & Diogo, R.) (Science Publishers, 2010) 517–565.
Near, T. J. et al. Resolution of ray-finned fish phylogeny and timing of diversification. Proc. Natl Acad. Sci. USA 109, 13698–13703 (2012).
Lavoue, S. et al. Molecular systematics of the gonorynchiform fishes (Teleostei) based on whole mitogenome sequences: Implications for higher-level relationships within the Otocephala. Mol. Phylog. Evol. 37, 165–177 (2005).
Betancur-R., R. et al. The tree of life and a new classificaion of bony fishes. PLoS Curr. Tree of Life http://dx.doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288 (2013).
Shimodaira, H. & Hasegawa, M. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246–1247 (2001).
Li, C., Orti, G., Zhang, G. & Lu, G. A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol. Biol. 7, 44 (2007).
Dettai, A. & Lecointre, G. New insights into the organization and evolution of vertebrate IRBP genes and utility of IRBP gene sequences for the phylogenetic study of the Acanthomorpha (Actinopterygii: Teleostei). Mol. Phylog. Evol. 48, 258–269 (2008).
Li, C., Riethoven, J. J. & Naylor, G. J. P. EvolMarkers: a database for mining exon and intron markers for evolution, ecology and conservation studies. Mol. Ecol. Resour. 12, 967–971 (2012).
Abascal, F., Zardoya, R. & Telford, M. J. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 38, 7–13 (2010).
Sharma, P. P. et al. Phylogenomic interrogation of arachnida reveals systemic conflicts in phylogenetic signal. Mol. Biol. Evol. 31, 2963–2984 (2014).
Inoue, J., Sato, Y., Sinclair, R., Tsukamoto, K. & Nishida, M. Rapid genome reshaping by multiple-gene loss after whole-genome duplication in teleost fish suggested by mathematical modeling. Proc. Natl Acad. Sci. USA 112, 14918–14923 (2015).
Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).
R Development Core Team, R: A Language and Environment for Statistical Computing . (R Foundation for Statistical Computing, 2011); http://www.R-project.org/
Kumar, S., Stecher, G., Peterson, D. & Tamura, K. MEGA-CC: computing core of molecular evolutionary genetics analysis program for automated and iterative data analysis. Bioinformatics 28, 2685–2686 (2012).
Murray, K., Mìller, S. & Turlach, B. A. Revisiting fitting monotone polynomials to data. Comp. Stat. 28, 1989–2005 (2013).
Maddison, W. & Maddision, D. Mesquite: a modular system for evolutionary analysis, version 2.6. (2009).
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree: computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix. Mol. Biol. Evol. 26, 1641–1650 (2009).
Aberer, A. J., Kobert, K. & Stamatakis, A. ExaBayes: massively parallel bayesian tree inference for the whole-genome era. Mol. Biol. Evol. 31, 2553–2556 (2014).
Tracer v1.6 (2014); http://beast.bio.ed.ac.uk/Tracer
Goloboff, P. A., Farris, J. S. & Nixon, K. C. TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786 (2008).
Liu, L., Yu, L., Pearl, D. K. & Edwards, S. V. Estimating species phylogenies using coalescence times among sequences. Syst. Biol. 58, 468–477 (2009).
Liu, L. & Yu, L. Estimating species trees from unrooted gene trees. Syst. Biol. 60, 661–667 (2011).
Shaw, T. I., Ruan, Z., Glenn, T. C. & Liu, L. STRAW: Species TRee Analysis Web server. Nucleic Acids Res. 41, 238–241 (2013).
Philippe, H. et al. Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol. 9, e1000602 (2011).
Song, S., Liu, L., Edwards, S. V. & Wu, S. Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent modeL. Proc. Natl Acad. Sci. USA 2012 (2012).
Acknowledgements
We dedicate this contribution in honour and memory of our friend and valued colleague Richard Vari whose untimely death has left a huge lacuna in the world of otophysan systematics. We thank D. Maddison, for helping with the MDS analyses in Mesquite, and R. Rivero, for helping with illustrations. We also thank S. Edwards and T. Warnow for providing extensive comments on earlier versions of the paper. J. P. Sullivan kindly provided a photograph for Citharinoidei. This work was supported by National Science Foundation (NSF) grants (DEB-147184, DEB-1541491) to R.B.R., (DEB-1457426 and DEB-1541554) to G.O., (DEB-0315963 and DEB-1023403) to J.W.A., and (DEB-1350474) to L.J.R. This project was also funded by the Opportunity Research Program between George Washington University and the Natural History Museum (Smithsonian) to G.O. and R.V and the Smithsonian Peter Buck fellowship to R.B.R.
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D.A., R.B.R., R.V. and G.O. planned the project; R.B.R., K.K and G.O. conducted the pilot experiment; D.A. and R.B.R. carried out the experiments and collected the data; D.A., R.B.R., L.J.R., and G.O. conceived the GGI method; D.A. and R.B.R. analysed data; J.W.A., J.L., M.L.J.S., and M.H.S. collected, identified and curated the fish specimens examined; R.B.R., D.A. and G.O. wrote the paper and all other authors contributed to the writing.
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Arcila, D., Ortí, G., Vari, R. et al. Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life. Nat Ecol Evol 1, 0020 (2017). https://doi.org/10.1038/s41559-016-0020
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DOI: https://doi.org/10.1038/s41559-016-0020
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