Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life

D. Arcila, G. Ortí, R. Vari, J.W. Armbruster, M.L.J. Stiassny, K.D. Ko, M.H. Sabaj, J. Lundberg, L.J. Revell, R.R. Betancur

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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. © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Original languageEnglish (US)
JournalNature Ecology and Evolution
Volume1
Issue number2
DOIs
StatePublished - 2017

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Genealogy and Heraldry
Genome
Genes
Ctenophora
Fresh Water
Birds
Mammals
Fishes
Yeasts
Radiation
Datasets

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Arcila, D., Ortí, G., Vari, R., Armbruster, J. W., Stiassny, M. L. J., Ko, K. D., ... Betancur, R. R. (2017). Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life. Nature Ecology and Evolution, 1(2). https://doi.org/10.1038/s41559-016-0020
Arcila, D. ; Ortí, G. ; Vari, R. ; Armbruster, J.W. ; Stiassny, M.L.J. ; Ko, K.D. ; Sabaj, M.H. ; Lundberg, J. ; Revell, L.J. ; Betancur, R.R. / Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life. In: Nature Ecology and Evolution. 2017 ; Vol. 1, No. 2.
@article{c1d5e4a318d74d21a5f1ee331898ac64,
title = "Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life",
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. {\circledC} 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.",
author = "D. Arcila and G. Ort{\'i} and R. Vari and J.W. Armbruster and M.L.J. Stiassny and K.D. Ko and M.H. Sabaj and J. Lundberg and L.J. Revell and R.R. Betancur",
note = "Cited By :19 Export Date: 17 April 2018 References: Rokas, A., Williams, B.L., King, N., Carroll, S.B., Genome-scale approaches to resolving incongruence in molecular phylogenies (2003) Nature, 425, pp. 798-804; Betancur, R.-R., Naylor, G., Orti, G., Conserved genes, sampling error, and phylogenomic inference (2014) Syst. Biol., 63, pp. 257-262; Simmons, M.P., Sloan, D.B., Gatesy, J., The effects of subsampling gene trees on coalescent methods applied to ancient divergences (2016) Mol. Phylogenet. Evol., 97, pp. 76-89; Salichos, L., Rokas, A., Inferring ancient divergences requires genes with strong phylogenetic signals (2013) Nature, 497, pp. 327-331; Chen, M.Y., Liang, D., Zhang, P., Selecting question-specific genes to reduce incongruence in phylogenomics: A case study of jawed vertebrate backbone phylogeny (2015) Syst. Biol., 64, pp. 1104-1120; Jeffroy, O., Brinkmann, H., Delsuc, F., Philippe, H., Phylogenomics: The beginning of incongruence (2006) Trends Genet, 22, pp. 225-231; Kubatko, L.S., Degnan, J.H., Inconsistency of phylogenetic estimates from concatenated data under coalescence (2007) Syst. Biol., 56, pp. 17-24; Degnan, J.H., Rosenberg, N.A., Gene tree discordance, phylogenetic inference and the multispecies coalescent (2009) Trends Ecol. Evol., 24, pp. 332-340; Sen, S., Liu, L., Edwards, S.V., Wu, S., Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model (2012) Proc. Natl Acad. Sci. USA, 109, pp. 14942-14947; Edwards, S.V., Liu, L., Pearl, D.K., High-resolution species trees without concatenation (2007) Proc. Natl Acad. Sci. USA, 104, pp. 5936-5941; Roch, S., Steel, M., Likelihood-based tree reconstruction on a concatenation of aligned sequence data sets can be statistically inconsistent (2014) Theor. Popul. Biol., 100 C, pp. 56-62; Heled, J., Drummond, A.J., Bayesian inference of species trees from multilocus data (2010) Mol. Biol. Evol., 27, pp. 570-580; Chou, J., A comparative study of SVDquartets and other coalescent-based species tree estimation methods (2015) BMC Genomics, 16, p. S2; Gatesy, J., Springer, M.S., Phylogenetic analysis at deep timescales: Unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum (2014) Mol. Phylogenet. Evol., 80, pp. 231-266; Roch, S., Warnow, T., On the robustness to gene tree estimation error (or lack thereof) of coalescent-based species tree methods (2015) Syst. Biol., 64, pp. 663-676; Mirarab, S., Bayzid, M.S., Boussau, B., Warnow, T., Statistical binning enables an accurate coalescent-based estimation of the avian tree (2014) Science, 346, p. 1250463; Bayzid, M.S., Mirarab, S., Boussau, B., Warnow, T., Weighted statistical binning: Enabling statistically consistent genome-scale phylogenetic analyses (2015) PLoS ONE, 10, p. e0129183; Shen, X.X., Salichos, L., Rokas, A., A genome-scale investigation of how sequence-, function-, and tree-based gene properties influence phylogenetic inference (2016) Genome Biol. Evol., 8, pp. 2565-2580; Liu, L., Edwards, S.V., Comment on {"}Statistical binning enables an accurate coalescent-based estimation of the avian tree{"} (2015) Science, 350, p. 171; Springer, M.S., Gatesy, J., The gene tree delusion (2016) Mol. Phylogenet. Evol., 94, pp. 1-33; Edwards, S.V., Implementing and testing the multispecies coalescent model: A valuable paradigm for phylogenomics (2016) Mol. Phylogenet. Evol., 94, pp. 447-462; Chifman, J., Kubatko, L., Quartet inference from SNP data under the coalescent model (2014) Bioinformatics, 30, pp. 3317-3324; 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{"} (2015) Science, 350, p. 171; Posada, D., Phylogenomics for systematic biology (2016) Syst. Biol., 65, pp. 353-356; Wu, Y.C., Rasmussen, M.D., Bansal, M.S., Kellis, M., TreeFix: Statistically informed gene tree error correction using species trees (2013) Syst. Biol., 62, pp. 110-120; Alfaro, M.E., Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates (2009) Proc. Natl Acad. Sci. USA, 106, pp. 13410-13414; Fink, S.V., Fink, W.L., Interrelationships of the ostariophysan fishes (Teleostei) (1981) Zool. J. Linnean Soc., 72, pp. 297-353; Saitoh, K., Miya, M., Inoue, J.G., Ishiguro, N.B., Nishida, M., Mitochondrial genomics of ostariophysan fishes: Perspectives on phylogeny and biogeography (2003) J. Mol. Evol., 56, pp. 464-472; 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 (2011) BMC Evol. Biol., 11, p. 177; Chen, W.J., Lavoue, S., Mayden, R.L., Evolutionary origin and early biogeography of otophysan fishes (Ostariophysi: Teleostei) (2013) Evolution, 67, pp. 2218-2239; Chakrabarty, P., McMahan, C., Fink, W., Stiassny, M.L., Alfaro, M., (2013) ASIH-American Society of Ichthyologists and Herpetologists, , (eds Crump, M. L. & Donnelly, M. A.); Hillis, D.M., Heath, T.A., St. John, K., Analysis and visualization of tree space (2005) Syst. Biol., 54, pp. 471-482; 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) (2013) Syst. Biol., 62, pp. 763-785; 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 (2013) Mol. Biol. Evol., 30, pp. 2134-2144; Shimodaira, H., An approximately unbiased test of phylogenetic tree selection (2002) Syst. Biol., 51, pp. 492-508; Allman, E.S., Degnan, J.H., Rhodes, J.A., Identifying the rooted species tree from the distribution of unrooted gene trees under the coalescent (2010) J. Math. Biol., 62, pp. 833-862; Degnan, J.H., Anomalous unrooted gene trees (2013) Syst. Biol., 62, pp. 574-590; Maddison, W.P., Gene trees in species trees (1997) Syst. Biol., 46, pp. 523-536; Pisani, D., Genomic data do not support comb jellies as the sister group to all other animals (2015) Proc. Natl Acad. Sci. USA, 112, pp. 15402-15407; Whelan, N.V., Kocot, K.M., Moroz, L.L., Halanych, K.M., Error, signal, and the placement of Ctenophora sister to all other animals (2015) Proc. Natl Acad. Sci. USA, 112, pp. 5773-5778; Dunn, C.W., Giribet, G., Edgecombe, G.D., Hejnol, A., Animal phylogeny and its evolutionary implications (2014) Annu. Rev. Ecol. Evol. Syst., 45, pp. 371-395; Ryan, J.F., The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution (2013) Science, 342, p. 1242592; Prum, R.O., A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing (2015) Nature, 526, pp. 569-573; Suh, A., Smeds, L., Ellegren, H., The dynamics of incomplete lineage sorting across the ancient adaptive radiation of neoavian birds (2015) PLoS Biol., 13, p. e1002224; Jarvis, E.D., Whole-genome analyses resolve early branches in the tree of life of modern birds (2014) Science, 346, pp. 1320-1331; Song, S., Liu, L., Edwards, S.V., Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model (2015) Proc. Natl Acad. Sci. USA, 112, p. E6079. , Correction for Song; Hahn, M.W., Nakhleh, L., Irrational exuberance for resolved species trees (2016) Evolution, 70, pp. 7-17; Mamanova, L., Target-enrichment strategies for next-generation sequencing (2010) Nat. Methods, 7, pp. 111-118; Li, C., Hofreiter, M., Straube, N., Corrigan, S., Naylor, G.J., Capturing protein-coding genes across highly divergent species (2013) BioTechniques, 54, pp. 321-326; Dimmick, W.W., Larson, A., A molecular and morphological perspective on the phylogenetic relationships of the otophysan fishes (1996) Mol. Phylog. Evol., 6, pp. 120-133; Alves-Gomes, J.A., (2010) Gonorynchiformes and Ostariophysan Relationships, pp. 517-565. , (eds Grande, T, Potayo-Ariza, F. J. & Diogo, R.) (Science Publishers; Near, T.J., Resolution of ray-finned fish phylogeny and timing of diversification (2012) Proc. Natl Acad. Sci. USA, 109, pp. 13698-13703; Lavoue, S., Molecular systematics of the gonorynchiform fishes (Teleostei) based on whole mitogenome sequences: Implications for higher-level relationships within the Otocephala (2005) Mol. Phylog. Evol., 37, pp. 165-177; Betancur, R.-R., The tree of life and a new classificaion of bony fishes (2013) PLoS Curr. 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Arcila, D, Ortí, G, Vari, R, Armbruster, JW, Stiassny, MLJ, Ko, KD, Sabaj, MH, Lundberg, J, Revell, LJ & Betancur, RR 2017, 'Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life', Nature Ecology and Evolution, vol. 1, no. 2. https://doi.org/10.1038/s41559-016-0020

Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life. / Arcila, D.; Ortí, G.; Vari, R.; Armbruster, J.W.; Stiassny, M.L.J.; Ko, K.D.; Sabaj, M.H.; Lundberg, J.; Revell, L.J.; Betancur, R.R.

In: Nature Ecology and Evolution, Vol. 1, No. 2, 2017.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life

AU - Arcila, D.

AU - Ortí, G.

AU - Vari, R.

AU - Armbruster, J.W.

AU - Stiassny, M.L.J.

AU - Ko, K.D.

AU - Sabaj, M.H.

AU - Lundberg, J.

AU - Revell, L.J.

AU - Betancur, R.R.

N1 - Cited By :19 Export Date: 17 April 2018 References: Rokas, A., Williams, B.L., King, N., Carroll, S.B., Genome-scale approaches to resolving incongruence in molecular phylogenies (2003) Nature, 425, pp. 798-804; Betancur, R.-R., Naylor, G., Orti, G., Conserved genes, sampling error, and phylogenomic inference (2014) Syst. Biol., 63, pp. 257-262; Simmons, M.P., Sloan, D.B., Gatesy, J., The effects of subsampling gene trees on coalescent methods applied to ancient divergences (2016) Mol. Phylogenet. Evol., 97, pp. 76-89; Salichos, L., Rokas, A., Inferring ancient divergences requires genes with strong phylogenetic signals (2013) Nature, 497, pp. 327-331; Chen, M.Y., Liang, D., Zhang, P., Selecting question-specific genes to reduce incongruence in phylogenomics: A case study of jawed vertebrate backbone phylogeny (2015) Syst. Biol., 64, pp. 1104-1120; Jeffroy, O., Brinkmann, H., Delsuc, F., Philippe, H., Phylogenomics: The beginning of incongruence (2006) Trends Genet, 22, pp. 225-231; Kubatko, L.S., Degnan, J.H., Inconsistency of phylogenetic estimates from concatenated data under coalescence (2007) Syst. Biol., 56, pp. 17-24; Degnan, J.H., Rosenberg, N.A., Gene tree discordance, phylogenetic inference and the multispecies coalescent (2009) Trends Ecol. Evol., 24, pp. 332-340; Sen, S., Liu, L., Edwards, S.V., Wu, S., Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model (2012) Proc. Natl Acad. Sci. USA, 109, pp. 14942-14947; Edwards, S.V., Liu, L., Pearl, D.K., High-resolution species trees without concatenation (2007) Proc. Natl Acad. Sci. USA, 104, pp. 5936-5941; Roch, S., Steel, M., Likelihood-based tree reconstruction on a concatenation of aligned sequence data sets can be statistically inconsistent (2014) Theor. Popul. Biol., 100 C, pp. 56-62; Heled, J., Drummond, A.J., Bayesian inference of species trees from multilocus data (2010) Mol. Biol. Evol., 27, pp. 570-580; Chou, J., A comparative study of SVDquartets and other coalescent-based species tree estimation methods (2015) BMC Genomics, 16, p. S2; Gatesy, J., Springer, M.S., Phylogenetic analysis at deep timescales: Unreliable gene trees, bypassed hidden support, and the coalescence/concatalescence conundrum (2014) Mol. Phylogenet. Evol., 80, pp. 231-266; Roch, S., Warnow, T., On the robustness to gene tree estimation error (or lack thereof) of coalescent-based species tree methods (2015) Syst. Biol., 64, pp. 663-676; Mirarab, S., Bayzid, M.S., Boussau, B., Warnow, T., Statistical binning enables an accurate coalescent-based estimation of the avian tree (2014) Science, 346, p. 1250463; Bayzid, M.S., Mirarab, S., Boussau, B., Warnow, T., Weighted statistical binning: Enabling statistically consistent genome-scale phylogenetic analyses (2015) PLoS ONE, 10, p. e0129183; Shen, X.X., Salichos, L., Rokas, A., A genome-scale investigation of how sequence-, function-, and tree-based gene properties influence phylogenetic inference (2016) Genome Biol. Evol., 8, pp. 2565-2580; Liu, L., Edwards, S.V., Comment on "Statistical binning enables an accurate coalescent-based estimation of the avian tree" (2015) Science, 350, p. 171; Springer, M.S., Gatesy, J., The gene tree delusion (2016) Mol. Phylogenet. Evol., 94, pp. 1-33; Edwards, S.V., Implementing and testing the multispecies coalescent model: A valuable paradigm for phylogenomics (2016) Mol. Phylogenet. Evol., 94, pp. 447-462; Chifman, J., Kubatko, L., Quartet inference from SNP data under the coalescent model (2014) Bioinformatics, 30, pp. 3317-3324; 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" (2015) Science, 350, p. 171; Posada, D., Phylogenomics for systematic biology (2016) Syst. Biol., 65, pp. 353-356; Wu, Y.C., Rasmussen, M.D., Bansal, M.S., Kellis, M., TreeFix: Statistically informed gene tree error correction using species trees (2013) Syst. Biol., 62, pp. 110-120; Alfaro, M.E., Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates (2009) Proc. Natl Acad. Sci. USA, 106, pp. 13410-13414; Fink, S.V., Fink, W.L., Interrelationships of the ostariophysan fishes (Teleostei) (1981) Zool. J. Linnean Soc., 72, pp. 297-353; Saitoh, K., Miya, M., Inoue, J.G., Ishiguro, N.B., Nishida, M., Mitochondrial genomics of ostariophysan fishes: Perspectives on phylogeny and biogeography (2003) J. Mol. Evol., 56, pp. 464-472; 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 (2011) BMC Evol. Biol., 11, p. 177; Chen, W.J., Lavoue, S., Mayden, R.L., Evolutionary origin and early biogeography of otophysan fishes (Ostariophysi: Teleostei) (2013) Evolution, 67, pp. 2218-2239; Chakrabarty, P., McMahan, C., Fink, W., Stiassny, M.L., Alfaro, M., (2013) ASIH-American Society of Ichthyologists and Herpetologists, , (eds Crump, M. L. & Donnelly, M. A.); Hillis, D.M., Heath, T.A., St. John, K., Analysis and visualization of tree space (2005) Syst. Biol., 54, pp. 471-482; 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) (2013) Syst. Biol., 62, pp. 763-785; 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 (2013) Mol. Biol. Evol., 30, pp. 2134-2144; Shimodaira, H., An approximately unbiased test of phylogenetic tree selection (2002) Syst. Biol., 51, pp. 492-508; Allman, E.S., Degnan, J.H., Rhodes, J.A., Identifying the rooted species tree from the distribution of unrooted gene trees under the coalescent (2010) J. Math. Biol., 62, pp. 833-862; Degnan, J.H., Anomalous unrooted gene trees (2013) Syst. Biol., 62, pp. 574-590; Maddison, W.P., Gene trees in species trees (1997) Syst. Biol., 46, pp. 523-536; Pisani, D., Genomic data do not support comb jellies as the sister group to all other animals (2015) Proc. Natl Acad. Sci. USA, 112, pp. 15402-15407; Whelan, N.V., Kocot, K.M., Moroz, L.L., Halanych, K.M., Error, signal, and the placement of Ctenophora sister to all other animals (2015) Proc. Natl Acad. Sci. USA, 112, pp. 5773-5778; Dunn, C.W., Giribet, G., Edgecombe, G.D., Hejnol, A., Animal phylogeny and its evolutionary implications (2014) Annu. Rev. Ecol. Evol. Syst., 45, pp. 371-395; Ryan, J.F., The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution (2013) Science, 342, p. 1242592; Prum, R.O., A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing (2015) Nature, 526, pp. 569-573; Suh, A., Smeds, L., Ellegren, H., The dynamics of incomplete lineage sorting across the ancient adaptive radiation of neoavian birds (2015) PLoS Biol., 13, p. e1002224; Jarvis, E.D., Whole-genome analyses resolve early branches in the tree of life of modern birds (2014) Science, 346, pp. 1320-1331; Song, S., Liu, L., Edwards, S.V., Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model (2015) Proc. Natl Acad. Sci. USA, 112, p. E6079. , Correction for Song; Hahn, M.W., Nakhleh, L., Irrational exuberance for resolved species trees (2016) Evolution, 70, pp. 7-17; Mamanova, L., Target-enrichment strategies for next-generation sequencing (2010) Nat. Methods, 7, pp. 111-118; Li, C., Hofreiter, M., Straube, N., Corrigan, S., Naylor, G.J., Capturing protein-coding genes across highly divergent species (2013) BioTechniques, 54, pp. 321-326; Dimmick, W.W., Larson, A., A molecular and morphological perspective on the phylogenetic relationships of the otophysan fishes (1996) Mol. Phylog. Evol., 6, pp. 120-133; Alves-Gomes, J.A., (2010) Gonorynchiformes and Ostariophysan Relationships, pp. 517-565. , (eds Grande, T, Potayo-Ariza, F. J. & Diogo, R.) (Science Publishers; Near, T.J., Resolution of ray-finned fish phylogeny and timing of diversification (2012) Proc. Natl Acad. Sci. USA, 109, pp. 13698-13703; Lavoue, S., Molecular systematics of the gonorynchiform fishes (Teleostei) based on whole mitogenome sequences: Implications for higher-level relationships within the Otocephala (2005) Mol. Phylog. Evol., 37, pp. 165-177; Betancur, R.-R., The tree of life and a new classificaion of bony fishes (2013) PLoS Curr. 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PY - 2017

Y1 - 2017

N2 - 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. © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.

AB - 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. © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.

U2 - 10.1038/s41559-016-0020

DO - 10.1038/s41559-016-0020

M3 - Article

C2 - 28812610

VL - 1

IS - 2

ER -

Arcila D, Ortí G, Vari R, Armbruster JW, Stiassny MLJ, Ko KD et al. Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life. Nature Ecology and Evolution. 2017;1(2). https://doi.org/10.1038/s41559-016-0020