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. 2013 Apr 18:5:ecurrents.tol.53ba26640df0ccaee75bb165c8c26288.
doi: 10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288.

The tree of life and a new classification of bony fishes

Ricardo Betancur-R  1 , Richard E Broughton, Edward O Wiley, Kent Carpenter, J Andrés López, Chenhong Li, Nancy I Holcroft, Dahiana Arcila, Millicent Sanciangco, James C Cureton Ii, Feifei Zhang, Thaddaeus Buser, Matthew A Campbell, Jesus A Ballesteros, Adela Roa-Varon, Stuart Willis, W Calvin Borden, Thaine Rowley, Paulette C Reneau, Daniel J Hough, Guoqing Lu, Terry Grande, Gloria Arratia, Guillermo Ortí
Affiliations

The tree of life and a new classification of bony fishes

Ricardo Betancur-R et al. PLoS Curr. .

Abstract

The tree of life of fishes is in a state of flux because we still lack a comprehensive phylogeny that includes all major groups. The situation is most critical for a large clade of spiny-finned fishes, traditionally referred to as percomorphs, whose uncertain relationships have plagued ichthyologists for over a century. Most of what we know about the higher-level relationships among fish lineages has been based on morphology, but rapid influx of molecular studies is changing many established systematic concepts. We report a comprehensive molecular phylogeny for bony fishes that includes representatives of all major lineages. DNA sequence data for 21 molecular markers (one mitochondrial and 20 nuclear genes) were collected for 1410 bony fish taxa, plus four tetrapod species and two chondrichthyan outgroups (total 1416 terminals). Bony fish diversity is represented by 1093 genera, 369 families, and all traditionally recognized orders. The maximum likelihood tree provides unprecedented resolution and high bootstrap support for most backbone nodes, defining for the first time a global phylogeny of fishes. The general structure of the tree is in agreement with expectations from previous morphological and molecular studies, but significant new clades arise. Most interestingly, the high degree of uncertainty among percomorphs is now resolved into nine well-supported supraordinal groups. The order Perciformes, considered by many a polyphyletic taxonomic waste basket, is defined for the first time as a monophyletic group in the global phylogeny. A new classification that reflects our phylogenetic hypothesis is proposed to facilitate communication about the newly found structure of the tree of life of fishes. Finally, the molecular phylogeny is calibrated using 60 fossil constraints to produce a comprehensive time tree. The new time-calibrated phylogeny will provide the basis for and stimulate new comparative studies to better understand the evolution of the amazing diversity of fishes.

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Figures

Main phylogenetic hypothesis of bony fish groups collapsed to depict higher-level clades.
Main phylogenetic hypothesis of bony fish groups collapsed to depict higher-level clades.
The phylogenetic tree was estimated in RAxML using the 3+ dataset (1416 taxa) and 24 partitions with divergence times estimated under PL using 126 fixed secondary calibrations from the BEAST analysis (see Fig. 11). Terminal clades are either orders or supraordinal taxa with multiple orders included. Values in parentheses indicate number of families examined. See also Figs. 3-10 for relationship details on selected percomorph clades. The complete phylogeny with bootstrap support values and names for supraordinal taxa is in Fig. S1).
Sensitivity analyses for selected clades obtained in this study (shown in Figs. 1, 3-10) and for selected alternative hypotheses.
Sensitivity analyses for selected clades obtained in this study (shown in Figs. 1, 3-10) and for selected alternative hypotheses.
For each case, we assess support from individual gene trees (indicating whether the group was obtained) or from the concatenated data sets (indicating whether the group was obtained and showing boostrap support). For some gene trees, monophyletic groups ignore a few rogue taxa falling outside. N/A: insufficient taxonomic sampling to test hypothesis. 1Excluding Gymnotiformes (e.g., Saitoh et al.77); 2Stomiatii; 3Stiassny and Moore; 4Nelson and Wiley and Johnson; 5Shan and Gras; 6Patterson and Rosen; 7Arratia; 8Fink and Fink; 9Nelson; 10Olney et al.; 11Johnson and Patterson; 12Miya et al.; 13Johnson; 14Kaufman and Liem; 15Gill; 16Acanthuriformes sensu Tyler et al. (i.e., Acanthuriformes sensu stricto plus Scatophagidae and Siganidae); 17Jordan
Detailed relationships among orders and families of Gobiomorpharia (see also Fig. 1).
Detailed relationships among orders and families of Gobiomorpharia (see also Fig. 1).
Values in parentheses indicate number of genera examined.
Detailed relationships among families of Syngnathiformes (see also Fig. 1).
Detailed relationships among families of Syngnathiformes (see also Fig. 1).
Values in parentheses indicate number of genera examined
Detailed relationships among families of Scombriformes (see also Fig. 1).
Detailed relationships among families of Scombriformes (see also Fig. 1).
Values in parentheses indicate number of genera examined.
Detailed relationships among orders and families of Anabantomorphariae (see also Fig. 1).
Detailed relationships among orders and families of Anabantomorphariae (see also Fig. 1).
Values in parentheses indicate number of genera examined.
Detailed relationships among orders and families of Carangimorphariae (see also Fig. 1).
Detailed relationships among orders and families of Carangimorphariae (see also Fig. 1).
Values in parentheses indicate number of genera examined (see also Betancur-R. et al.28).
Detailed relationships among orders and families of Ovalentariae (see also Fig. 1).
Detailed relationships among orders and families of Ovalentariae (see also Fig. 1).
Values in parentheses indicate number of genera examined (see also Wainwright et al. 31). Many clades lacking taxonomic annotations on nodes are incertae sedis taxa (for details, see classification).
Detailed relationships among orders and families of Percomorpharia (the new bush at the top; see also Fig. 1).
Detailed relationships among orders and families of Percomorpharia (the new bush at the top; see also Fig. 1).
Values in parentheses indicate number of genera examined in each terminal family or number of families and genera, respectively, in each terminal order. See also Fig. 10 for expanded relationships on perciform groups. Many clades lacking taxonomic annotations on nodes are incertae sedis taxa (for details, see classification).
Detailed relationships among families of Perciformes (see also Figs. 1 and 9).
Detailed relationships among families of Perciformes (see also Figs. 1 and 9).
Values in parentheses indicate number of genera examined. *Nototheniidae sensu lato, including the families Nototheniidae sensu stricto, Artedidraconidae, Harpagiferidae, Bathydraconidae, and Channichthyidae.
Time-calibrated BEAST phylogeny based on a subset of 202 taxa, indicating the placement for the 59 calibrations used.
Time-calibrated BEAST phylogeny based on a subset of 202 taxa, indicating the placement for the 59 calibrations used.
Bars represent the 95% highest posterior credibility intervals of divergence times. Calibration (60) was not included for this analysis (see Appendix 1).
Comparison of mean (triangle) and 95% highest posterior credibility intervals (horizontal bars) of divergence dates for selected clades (see also Figs 1, 11).
Comparison of mean (triangle) and 95% highest posterior credibility intervals (horizontal bars) of divergence dates for selected clades (see also Figs 1, 11).
Black lines and mean dates are from this study, blue are from Near et al. and green are from Broughton et al. Absent lines imply that the particular date estimation was not performed in the corresponding study.
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References

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Grants and funding

This work was supported by NSF awards DEB-0732988 (to REB), DEB-0732838, DEB-1019308 (to GO and CL), DEB-0732819 (EOW), DEB 0732589 (TG), DEB-0732894 (KC), DEB 0963767 (JAL), and DEB-0732969 (GL); GWU Selective Excellence in Diversity of Life program (to RBR); Leading Academic Discipline Project of Shanghai Municipal Education Commission, project number S30701 (CL). The Biodiversity Institute, University of Kansas, provided financial support for the collection used in this study.