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Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved April 13, 2018 (received for review November 7, 2017)
Significance
Ray-finned fishes form the largest and most diverse group of vertebrates. Establishing their phylogenetic relationships is a critical step to explaining their diversity. We compiled the largest comparative genomic database of fishes that provides genome-scale support for previous phylogenetic results and used it to resolve further some contentious relationships in fish phylogeny. A vetted set of exon markers identified in this study is a promising resource for current sequencing approaches to significantly increase genetic and taxonomic coverage to resolve the tree of life for all fishes. Our time-calibrated analysis suggests that most lineages of living fishes were already established in the Mesozoic Period, more than 65 million years ago.
Abstract
Our understanding of phylogenetic relationships among bony fishes has been transformed by analysis of a small number of genes, but uncertainty remains around critical nodes. Genome-scale inferences so far have sampled a limited number of taxa and genes. Here we leveraged 144 genomes and 159 transcriptomes to investigate fish evolution with an unparalleled scale of data: >0.5 Mb from 1,105 orthologous exon sequences from 303 species, representing 66 out of 72 ray-finned fish orders. We apply phylogenetic tests designed to trace the effect of whole-genome duplication events on gene trees and find paralogy-free loci using a bioinformatics approach. Genome-wide data support the structure of the fish phylogeny, and hypothesis-testing procedures appropriate for phylogenomic datasets using explicit gene genealogy interrogation settle some long-standing uncertainties, such as the branching order at the base of the teleosts and among early euteleosts, and the sister lineage to the acanthomorph and percomorph radiations. Comprehensive fossil calibrations date the origin of all major fish lineages before the end of the Cretaceous.
Footnotes
↵1L.C.H., G.O., Y.H., and Y.S. contributed equally to this work.
- ↵2To whom correspondence may be addressed. Email: lilychughes{at}gwu.edu, gorti{at}gwu.edu, mcbbv{at}imcb.a-star.edu.sg, or shiqiong{at}genomics.cn.
Author contributions: L.C.H., G.O., Y.H., Y.S., C.C.B., R.B.-R., B.V., and Q.S. designed research; L.C.H., G.O., Y.H., A.W.T., D.A., R.B.-R., L.B., N.B., X.Z., X.L., M.W., C.F., B.X., and Q.S. performed research; L.C.H., G.O., Y.H., C.C.B., A.W.T., D.A., R.B.-R., Z.Z., H.H., S.C., B.V., and Q.S. contributed new reagents/analytic tools; L.C.H., G.O., Y.H., A.W.T., D.A., R.B.-R., C.L., L.B., N.B., X.Z., X.L., M.W., C.F., and B.X. analyzed data; and L.C.H., G.O., Y.H., D.A., R.B.-R., B.V., and Q.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The accession numbers reported in this paper are listed in SI Appendix, Table S1, and have been deposited to the National Center for Biotechnology Information (NCBI) BioProject (https://www.ncbi.nlm.nih.gov/bioproject/398732). Additional analysis files have been deposited to the Dryad Digital Repository (https://doi.org/10.5061/dryad.5b85783).
See Commentary on page 6107.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1719358115/-/DCSupplemental.
Published under the PNAS license.
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Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data
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