Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in a blink of the evolutionary eye

Harrington, Richard C.; Faircloth, Brant C.; Eytan, Ron I.; Smith, W. Leo; Near, Thomas J.; Alfaro, Michael E.; Friedman, Matt

doi:10.1186/s12862-016-0786-x

Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in a blink of the evolutionary eye

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Published: 21 October 2016

Volume 16, article number 224, (2016)
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Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in a blink of the evolutionary eye

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Richard C. Harrington^1,2,
Brant C. Faircloth³,
Ron I. Eytan⁴,
W. Leo Smith⁵,
Thomas J. Near²,
Michael E. Alfaro⁶ &
…
Matt Friedman^1,7

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Abstract

Background

Flatfish cranial asymmetry represents one of the most remarkable morphological innovations among vertebrates, and has fueled vigorous debate on the manner and rate at which strikingly divergent phenotypes evolve. A surprising result of many recent molecular phylogenetic studies is the lack of support for flatfish monophyly, where increasingly larger DNA datasets of up to 23 loci have either yielded a weakly supported flatfish clade or indicated the group is polyphyletic. Lack of resolution for flatfish relationships has been attributed to analytical limitations for dealing with processes such as nucleotide non-stationarity and incomplete lineage sorting (ILS). We tackle this phylogenetic problem using a sequence dataset comprising more than 1,000 ultraconserved DNA element (UCE) loci covering 45 carangimorphs, the broader clade containing flatfishes and several other specialized lineages such as remoras, billfishes, and archerfishes.

Results

We present a phylogeny based on UCE loci that unequivocally supports flatfish monophyly and a single origin of asymmetry. We document similar levels of discordance among UCE loci as in previous, smaller molecular datasets. However, relationships among flatfishes and carangimorphs recovered from multilocus concatenated and species tree analyses of our data are robust to the analytical framework applied and size of data matrix used. By integrating the UCE data with a rich fossil record, we find that the most distinctive carangimorph bodyplans arose rapidly during the Paleogene (66.0–23.03 Ma). Flatfish asymmetry, for example, likely evolved over an interval of no more than 2.97 million years.

Conclusions

The longstanding uncertainty in phylogenetic hypotheses for flatfishes and their carangimorph relatives highlights the limitations of smaller molecular datasets when applied to successive, rapid divergences. Here, we recovered significant support for flatfish monophyly and relationships among carangimorphs through analysis of over 1,000 UCE loci. The resulting time-calibrated phylogeny points to phenotypic divergence early within carangimorph history that broadly matches with the predictions of adaptive models of lineage diversification.

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Background

During the past decade, a series of molecular phylogenetic analyses drawing on increasingly larger samples of taxa and genetic loci have transformed our understanding of evolutionary relationships among acanthomorphs or spiny-rayed fishes [1–6], a hyperdiverse lineage that includes nearly one in three living vertebrate species. These studies support the monophyly of many clades previously recognized by morphological phylogeneticists (e.g., Tetraodontiformes, Lophiiformes), but reject the coherence of other classical groups (e.g., Scombroidei inclusive of billfishes [7], Labroidei [8]) by removing some of their core members to other, distantly related lineages [9–11]. In resolving the ‘bush’ at the top of the teleost tree of life, these molecular phylogenies have exposed striking examples of morphological, physiological, and functional convergence among acanthomorphs [11].

A well-supported radiation [1, 12, 13], variously termed Clade L [14], Carangimorpha [2, 3], or Carangimorpharia [4, 15], represents one of the most surprising features of the emerging picture of acanthomorph interrelationships. Carangimorphs include anatomically disparate lineages characterized by remarkable behavioral and anatomical novelties: eye and brain heating organs coupled with long rostra and numerous specializations for rapid swimming in **. Bayesian posterior probabilities (x 100) are indicated by the right-hand side of discs in (h)

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The recent debate regarding flatfish monophyly spotlights the difficulties faced by many phylogenetic studies, particularly in the use of molecular data for radiations characterized by short internodes deep in evolutionary time. Methodological challenges, such as accounting for base compositional bias (i.e., non-stationarity [40]) and long branch attraction [41, 42], as well as natural phenomena such as horizontal gene flow and incomplete lineage sorting (ILS) can result in inference of gene trees that do not reflect a clade’s history of speciation [43–45]. Even under certain scenarios of branch length in species trees, the most frequent gene trees do not reflect the topology of the species tree (the so-called anomaly zone [46]). The use of analytical approaches to account for non-stationarity or application of the coalescent model for ILS is important for improving accuracy of gene tree and species tree estimation, but the addition of large numbers of unlinked loci may be the most direct approach for improving phylogenetic accuracy in the face of these processes [47]. Thus far, incrementally larger DNA sequence datasets of up to 23 loci have produced inconsistent increases in support for relationships among major carangimorph lineages, particularly with regard to flatfish monophyly (Fig. 1) and the identification of a symmetrical sister group.

Using recent advances in phylogenomics and high-throughput sequencing, we assembled a dataset of ultraconserved DNA elements (UCEs) and their flanking sequences representing over 1000 loci sampled from 45 carangimorph species. Here we use this novel dataset in conjunction with the rich fossil record of Carangimorpha to: (i) establish a well-supported hypothesis of relationships among anatomically disparate carangimorph lineages; (ii) provide a statistically decisive molecular solution to the ‘pleuronectiform problem’; and (iii) estimate divergence times for carangimorphs, with an emphasis on constraining the timescale over which remarkable anatomical innovations such as flatfish asymmetry and other specialized carangimorph bodyplans likely arose.

Methods

We use a probe set developed for application to acanthomorph phylogenetics to generate sequence data for approximately 1200 UCE loci [48]. These loci vary in size and number of variable sites per locus, but average between 300 and 500 nucleotides in length. This approach has provided resolution across a range of evolutionary depths in phylogenetic studies of acanthomorphs [5]. Gilbert et al. [49] examined the phylogenetic informativeness of a subset of the probe set used in this analysis, and found that it provides greater informativeness across ages during which carangimorphs diversified than do protein-coding genes previously used in phylogenetic analysis of acanthomorphs (including carangimorphs). Information on DNA isolation, library preparation, sequencing, and data pipelining is provided in Additional file 1: Methods 1. Raw read data are archived in the NCBI Sequence Read Archive (SRA) under accession numbers SAMN05784507, SAMN05786321-SAMN05785372, SAMN05919513, SAMN05919514. Our high-throughput sequencing generated uneven coverage across taxa and loci, resulting in an incomplete data matrix for all 1200 UCE loci. While increasing the number of nucleotides and loci is desirable for phylogenetic analysis, empirical studies of the impact of missing data on resolving difficult nodes show diminishing returns at varying thresholds of incompleteness (e.g., 25 % incomplete in [50] and 50 % incomplete in [51]). In order to evaluate the role of missing data in our matrices and whether tree topology and clade support values varied with the addition of more, but sparsely sampled loci, we performed phylogenetic analyses on 75 %, 95 %, and 100 % complete alignment matrices.

Concatenated analyses of UCE data

Across all data matrices, we conducted 20 maximum-likelihood (ML) searches for the phylogenetic tree that best fit the data using the best-fitting partitioning scheme, RAxML v. 8.0.19 [52], and the GTRGAMMA model. The best-fitting partitioning scheme was obtained using the Bayesian Information Criterion and hcluster search in PartitionFinder v 1.1.1 [53, 54], applying equal weights for overall rates, base frequencies, model parameters, and the alpha parameter. We rooted the tree on the lanternfish Ceratoscopelus warmingii. Following the best tree search, we used RAxML to generate non-parametric bootstrap pseudoreplicates using the autoMRE function of RAxML, and reconciled the best fitting ML tree with the bootstrap replicates. We also performed Bayesian analyses of each concatenated data set using ExaBayes [55]. We input the concatenated supermatrix and best-fitting partitioning scheme to ExaBayes and ran four independent analyses of 5 × 10⁵ to 1 × 10⁶ iterations. We checked results for convergence by ensuring the average standard deviation of split frequencies (ASDSF) was <1 %, effective sample size (ESS) values were >200, and the potential scale reduction factor (PSRF) for estimated parameters was approximately 1.0. We also visualized parameter estimates and ESS values in Tracer v 1.6 [1 and 2. Posterior density plots for the maximum interval over which the bodyplans of b billfishes (**phioidei) and moonfishes (Menidae); c remoras (Echeneidae); and d flatfishes (Pleuronectiformes) could have arisen. Images of modern fishes from J.E. Randall, used with permission. Fossil images from M. Friedman

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There is strong support for nearly all nodes in phylogenies inferred from concatenated analyses, with Bayesian posterior probabilities (PP) of >0.99 (approximated as ‘1’ below) and bootstrap support percentages (BP) of 100 %. With the exception of the placement of Sphyraenidae, we find strong support for many of the deepest nodes within Carangimorpha, in contrast to previous studies that have inferred inconsistent and poorly supported relationships among these deeply divergent lineages [3, 4, 15, 38].

The monophyly and relationships of flatfishes

Flatfish monophyly is unambiguously supported in phylogenies resulting from all of our concatenated analyses (PP = 1, BP = 100 %), but it also receives strong support in GT-ST analyses, and flatfishes appear as a clade in both the primary concordance and population trees generated by BCA. Concordance factors calculated for the loci containing all fifteen of the subsampled taxa (557 loci contained sequence data for Psettodes and the selected representatives of pleuronectoids and each of the remaining major carangimorph lineages) show that a plurality of loci produced gene trees in which Psettodes forms a clade with the other two sampled flatfishes, to the exclusion of all other carangimorphs (Fig. 3). The genome-wide BUCKy concordance factor estimate of 0.149 [95%CI: 0.114–0.187] for the Psettodes + Pleuronectoidei clade is higher than, and non-overlap** with, concordance factors estimated for any alternative topology in which Psettodes is recovered in a clade with any non-flatfish lineage (Fig. 3). Consistent with previous morphological hypotheses [23, 26–28, 70, 71], we resolve Psettodes as the sister lineage to Pleuronectoidei, which contains all other flatfish species. The UCE-inferred phylogenies place Citharidae as the sister lineage to all remaining pleuronectoids, in agreement with previous morphological [28, 70] and molecular analyses [4]. Interrelationships among other pleuronectoid families are identical to those reported in a recent molecular phylogenetic analysis of flatfishes [15], with universally high support (PP = 1, BP > 95 %).

Carangimorph relationships

We resolve Polynemidae as the sister lineage of a monophyletic flatfish clade (Fig. 2). Although this relationship is strongly supported for some datasets (PP ≥ 0.99 across all datasets, BP = 54, 84, and 100 % for 97, 596, and 1014 locus datasets, respectively), it has not been found in any previous molecular study of carangimorphs or on the basis of morphological features (Fig. 1). The clade containing polynemids and flatfishes is the sister lineage of a well-supported (PP = 1, BP = 100 %) and diverse clade containing species from at least nine families: Toxotidae, Leptobramidae (beach salmon), Menidae, ** 95 % credible intervals. Although GT-ST analyses provide strong support for the monophyly of Carangimorpha and Pleuronectiformes, deep divergences among major carangimorph lineages are not well supported.

A timescale for the diversification of Carangimorpha

Our multiple relaxed-clock molecular dating analyses produced similar and consistent estimates of divergence dates across different subsamples of UCE loci and between both analytical frameworks in the BEAST and PAML software packages, with overlap** 95 % highest posterior density ranges for all nodes (Fig. 2, Additional file 1: Figure S4, Additional file 1: Table S3). We refer to specific branch length and divergence date estimates derived from analysis of one set of 75 UCE loci (depicted in Fig. 2); but our BEAST analyses of three other 75 UCE-loci-datasets and PAML analysis of 596 loci provide very similar node ages, branch lengths, and overlap** 95 % highest posterior densities. We infer an origin of Carangimorpha at 71.0 Ma, shortly before the end of the Late Cretaceous, although we cannot reject an earliest Paleocene (Danian) origin [95 % highest posterior density (HPD) interval: 63.44, 80.86]. Most of the strikingly anatomically divergent carangimorph lineages arose in the subsequent 15 million years, before the end of the Paleocene. This is consistent with previous molecular phylogenetic studies [3, 4] (but see Santini and Carnevale [79]) as well as the earliest fossil occurrences of specialized lineages like billfishes, jacks, flatfishes, menids, and barracudas by the end of the first stage of the Eocene [29, 80].

We estimate the pleuronectiform crown node at 61.3 Ma [95 % HPD: 54.3–69.5 Ma]. The most recent common ancestor of flatfishes and threadfins, their living symmetrical sister lineage, is 65.7 Ma [95 % HPD: 57.3–72.6 Ma]. The mean length of the flatfish stem across our posterior sample of trees is 2.97 Myr [median: 2.45 Myr; 95 % HPD: 0.47–8.35 Myr], and it provides the longest possible span over which flatfish asymmetry could have evolved. Maximum timelines for the origin of other remarkable carangimorph bodyplans are generally longer. The divergence between Menidae and ** with a monophyletic flatfish scenario (Fig. 3). Prior to this study, the largest dataset of multiple unlinked loci applied to carangimorphs [34] found weak support from concatenated analysis of 23 loci for a flatfish clade (PP = 0.65), and attributed the low nodal support to nucleotide compositional bias in protein coding genes and to a lesser extent, ILS. The proportion of loci examined by [34] that recover a flatfish clade (3 out of 23 loci, or 13 %) is within the 95 % credible interval estimated from our analyses of UCE loci (95 % CI of 11.4–18.7 %). While other phenomena (such as the non-stationarity nucleotide composition as identified by [34]) may introduce error into gene tree estimation, the short internal branches subtending successive divergences of carangimorph lineages likely resulted in substantial ILS, making their relationships difficult to recover with small datasets.

The strong support for flatfish monophyly obtained from our molecular analyses of UCE loci bolsters the morphological consensus that this remarkable innovation evolved only once. The anatomical argument for flatfish monophyly has been caricatured as reliant almost exclusively on cranial asymmetry, and thus a hypothesis formed from limited evidence. However, probable pleuronectiform synapomorphies have been identified across multiple anatomical systems, including the axial skeleton [28, 71], caudal-fin endoskeleton [28, 71], otoliths [85], patterns of epaxial muscle insertions [86], and innervations of the trunk lateral line [87]; (Fig. 4). These synapomorphies collectively represent a strong anatomical case for flatfish monophyly, independent of cranial asymmetry.

Morphological support for relationships within carangimorpha

Although our phylogeny agrees with many aspects of previous morphological classifications (e.g., the monophyly of xiphioids [7, 75], centropomids [77], pleuronectiforms [26], and echeneoids [73]), it also reveals many unanticipated but strongly supported sister-group relationships, some of which have appeared in previous molecular phylogenies. There have been limited efforts to discover morphological evidence uniting anatomically disparate carangimorph lineages, and existing studies have been hampered by ambiguities in character polarity [71] and limited taxonomic comparisons [10].

Patterns of lineage diversification within carangimorphs suggest that unambiguous morphological support for some clades may prove elusive. Our molecular clock analyses indicate many specialized carangimorph groups have independent evolutionary histories that are considerably longer than those shared uniquely with their immediate sister taxa [3, 4, 38]. As a result, there was little time over which traits providing evidence for sister-group relationships could evolve relative to the time that any synapomorphies might be overwritten by the profound morphological specializations characteristic of individual carangimorph lineages. Nevertheless, it is clear that considerable anatomical evidence for monophyly has accumulated along some of the shortest branches within the carangimorph phylogeny. This is particularly apparent for the ca. 3 Myr-long flatfish stem (discussed above).

More careful anatomical scrutiny may yield evidence for the phylogenetic relationships in the UCE-inferred trees (Fig. 2; Additional file 1: Figures S1-S3), especially because many of the sister-group pairings within Carangimorpha have never been seriously considered—and therefore investigated—from a morphological perspective. An anatomically unanticipated sister-group relationship between billfishes and the moonfish Mene is a common motif of carangimorph molecular phylogenies, and one for which we recovered strong support in the UCE-inferred trees (e.g., Fig. 2). The anatomical specializations of these groups result in strikingly different “baupläne” that may have discouraged close comparison in the past, although we note a series of derived features common to both lineages (for details of comparative materials, see Additional file 1: Table S2): considerable elongation of the second and third pelvic-fin rays (pelvic fins are lost in xiphiids), caudal hypurostegy, a consolidated hypural plate arising from the fusion of hypurals 1-4 to one another and the ural centrum (further fusion characterizes istiophorids), and posterior extensions of the gas bladder [88–90]. Similarly, the sister-group relationship between Leptobrama and toxotids was previously unpredicted on the basis of the morphology, but the two groups share a number of unusual features among carangimorphs: presence of endopterygoid teeth (uniquely), presence of ectopterygoid teeth (with Polynemidae), and presence of more anal-fin rays than dorsal-fin rays (with Polynemidae and Lactariidae [not analysed in current study]) [90, 91]. These observations are joined by sporadic reports of shared specializations in other carangimorph lineages such as similar larval colour patterns in billfishes and sphyraenids [92]; prenasal canal units in polynemids, toxotids, and carangiforms, with ossified prenasals in the latter two [72]; and a series of specializations common to Mene, Lactarius and many carangiforms [91]. A systematic anatomical survey is required to determine whether the shared morphological similarities noted in this and previous studies corroborate the novel and strongly supported relationships in the carangimorph molecular phylogeny.

The origin of flatfish asymmetry: gradual but rapid

Our time-calibrated phylogeny provides the first robust constraints for the timescale over which the flatfish transformation occurred. On average, we conclude that complete orbital migration arose in no more than 2.97 Myr, although we cannot reject the possibility that it may have taken less than 470 kyr or as long as 7.96 Myr based on our posterior sample of trees. All stem pleuronectiforms identified to date show incomplete orbital migration [28, 71]. However, the identification of extinct flatfishes showing complete asymmetry but which branch outside the crown would further reduce the length of the stem over which modern pleuronectiform cranial geometry arose, thereby increasing the rate of this evolutionary transformation. Comparisons both within and outside Carangimorpha provide context for the rapid origin of the flatfish bodyplan. Mean maximum timescales for the evolution of billfishes, moonfishes, and remoras are on the order of 5–10 Myr, two to three times longer than comparable estimates for the origin of flatfish asymmetry. Similarly, the timescale of a few million years for the origin of flatfish asymmetry compares closely with the estimated age of some cichlid radiations in African rift lakes [93], upheld as examples of explosive evolutionary diversification [94], although flatfishes are arguably a more extreme morphological departure from standard acanthomorph bodyplans than even the most peculiar modern cichlids [95]. Outside of fishes, the timescale for the evolution of pleuronectiform asymmetry is substantially shorter than those estimated for the origins of the bodyplans associated with whales (ca. 20 Myr [96]) and anatomically modern humans (ca. 7 Myr). We hypothesize that the rapid evolution of flatfish asymmetry might reflect a steep peak associated with a new adaptive zone, as classically hypothesized for other rapid divergences by Simpson [97].

Diversification of carangimorpha

Our well-supported phylogeny provides new insight for exploring the origin of the anatomically diverse lineages that comprise Carangimorpha. The earliest diverging carangimorph lineage includes what are arguably the most anatomically ‘generalized’ members of the radiation: the superficially perch-like snooks and Nile perches. Interestingly, the two lineages constituting the principal carangimorph clade, excluding centropomids and sphyraenids, are differentiated along ecological lines. The first unnamed lineage is broadly associated with benthic environments, and its two constituent clades show striking adaptations to life at or near the sediment-water interface: profound asymmetry in flatfishes and free pectoral-fin rays in polynemids that serve a tactile function [19]. By contrast, the second major lineage contains pelagic groups like jacks, billfishes, and dolphinfishes. Our discovery of broad environmental divisions within carangimorphs represents the latest example of molecular analyses revealing novel clades of percomorph teleosts that share a common habitat preference or ecology [74]. The major ecological split in carangimorph phylogeny mirrors patterns apparent at smaller spatial and temporal scales in fishes, in which initial divergences within populations often reflect partitioning between benthic and pelagic habitats and resources [98].

Our analyses suggest that anatomically modern bodyplans evolved by the early Eocene (ca. 50 Ma), following major divergences in the latest Late Cretaceous and Paleocene. The rich fossil records of many individual groups [29], combined with our well-supported time-calibrated genomic perspective on phylogenetic relationships, make carangimorphs an ideal system for studying patterns of phenotypic diversification over spatial and temporal scales not reflected by young, geographically restricted clades that are often the focus of research on adaptive radiation [94, 99, 100]. The study of ancient marine percomorph radiations like the ecologically varied carangimorphs, pelagic scombriforms [74], and Antarctic nototheneoids [101] may provide insights into the generation of biological diversity that is persistent over long evolutionary timescales not provided by model systems like sticklebacks and cichlids that have diversified in spatially limited and geologically ephemeral environments [99, 102].

Conclusion

The invariably low support for monophyly of flatfishes found in previous molecular phylogenetic analyses is emblematic of a common problem in reconstructing the evolutionary history of rapidly diverging lineages throughout the Tree of Life. Although increasingly larger gene-by-gene datasets have provided valuable discoveries regarding the relationships among acanthomorph fishes and the timing of their divergences [3, 4], these datasets may not be large enough to overcome discordance due to phenomena such as incomplete lineage sorting for nodes within rapidly branching portions of the acanthomorph phylogeny. The resolution of carangimorph relationships provided by high throughput sequencing of UCE loci serves as an improved framework on which to study the evolution and diversification of fish bodyplans, and our results suggest similar phylogenomic approaches will be necessary to resolve historically difficult nodes in the acanthomorph phylogeny, as in the case of the flatfishes.

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Acknowledgements

We thank A. Bentley and P. Chakrabarty for tissue samples, and J. Maclaine and O. Crimmen for access to preserved specimens. Portions of this research were conducted with high performance computational resources provided by Louisiana State University (http://www.hpc.lsu.edu) and the University of Oxford (http://www.arc.ox.ac.uk), and this study was also supported, in part, by resources and technical expertise from the Georgia Advanced Computing Resource Center, a partnership between the University of Georgia’s Office of the Vice President for Research and Office of the Vice President for Information Technology.

Funding

This research was supported by NERC grant no. NE/J022632/1 and a Philip Leverhulme Prize PLP-2012-130 (both to M.F.). NSF DEB-1242260 (to BCF) supported computational portions of this work and NSF ANT-0839007 (to TJN) supported portions of laboratory expenses.

Availability of data and material

Sequence data generated for this manuscript are archived as raw reads in the NCBI Sequence Repository (SRA) and assembled contigs in NCBI GenBank (accession numbers SAMN05784507, SAMN05786321-SAMN05785372). The data sets supporting the results of this article, including alignments of UCE loci and phylogenetic trees generated from our analyses of these data, are available in the Dryad Digital Repository (doi:10.5061/dryad.2fj55 [103]). Details of fossil calibrations are provided in Additional file 2.

Authors’ contributions

MF and RCH conceived the research. RCH and BCF generated sequence data. Phylogenetic analyses were performed by BCF, MA, and RCH. All authors contributed to interpretation of results and writing of the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

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Authors and Affiliations

Department of Earth Sciences, University of Oxford, Oxford, OX1 3AN, UK
Richard C. Harrington & Matt Friedman
Department of Ecology & Evolutionary Biology and Peabody Museum of Natural History, Yale University, New Haven, CT, 06520, USA
Richard C. Harrington & Thomas J. Near
Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, LA, 70803, USA
Brant C. Faircloth
Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX, 77553, USA
Ron I. Eytan
Biodiversity Institute and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, 66045, USA
W. Leo Smith
Department of Ecology and Evolutionary Biology, University of California Los Angeles, Los Angeles, CA, 90095, USA
Michael E. Alfaro
Museum of Paleontology and Department of Earth and Environmental Science, University of Michigan, 1109 Geddes Ave, Ann Arbor, MI, 48109-1079, USA
Matt Friedman

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Richard C. Harrington
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Correspondence to Richard C. Harrington.

Additional files

Additional file 1:

Extended descriptions of protocols for DNA isolation, library preparation, sequencing, and data pipelining, and Additional file 1: Figures S1-S4. (DOCX 6704 kb)

Additional file 2:

Descriptions of fossil calibrations used in divergence dating analyses, including details of age priors and the fossil data upon which they are based. (DOCX 92 kb)

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Harrington, R.C., Faircloth, B.C., Eytan, R.I. et al. Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in a blink of the evolutionary eye. BMC Evol Biol 16, 224 (2016). https://doi.org/10.1186/s12862-016-0786-x

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Received: 12 July 2016
Accepted: 30 September 2016
Published: 21 October 2016
DOI: https://doi.org/10.1186/s12862-016-0786-x

Phylogenomic analysis of carangimorph fishes reveals flatfish asymmetry arose in a blink of the evolutionary eye