Early members of ‘living fossil’ lineage imply later origin of modern ray-finned fishes

  • An Erratum to this article was published on 22 November 2017

Abstract

Modern ray-finned fishes (Actinopterygii) comprise half of extant vertebrate species and are widely thought to have originated before or near the end of the Middle Devonian epoch (around 385 million years ago)1,2,3,4. Polypterids (bichirs and ropefish) represent the earliest-diverging lineage of living actinopterygians, with almost all Palaeozoic taxa interpreted as more closely related to other extant actinopterygians than to polypterids5,6,7,8,9,10. By contrast, the earliest material assigned to the polypterid lineage is mid-Cretaceous in age (around 100 million years old)11, implying a quarter-of-a-billion-year palaeontological gap. Here we show that scanilepiforms, a widely distributed radiation from the Triassic period (around 252–201 million years ago), are stem polypterids. Importantly, these fossils break the long polypterid branch and expose many supposedly primitive features of extant polypterids as reversals. This shifts numerous Palaeozoic ray-fins to the actinopterygian stem, reducing the minimum age for the crown lineage by roughly 45 million years. Recalibration of molecular clocks to exclude phylogenetically reassigned Palaeozoic taxa results in estimates that the actinopterygian crown lineage is about 20–40 million years younger than was indicated by previous molecular analyses1,2,3,4. These new dates are broadly consistent with our revised palaeontological timescale and coincident with an interval of conspicuous morphological and taxonomic diversification among ray-fins centred on the Devonian–Carboniferous boundary12,13,14. A shifting timescale, combined with ambiguity in the relationships of late Palaeozoic actinopterygians, highlights this part of the fossil record as a major frontier in understanding the evolutionary assembly of modern vertebrate diversity.

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Figure 1: Comparative cranial anatomy of Fukangichthys longidorsalis (IVPP V4096.6 and IVPP V4096.13) and Erpetoichthys calabaricus (BMNH 2016.9.22.3) based on high-resolution computed tomography.
Figure 2: Phylogenetic results and implications for polypterid total group and actinopterygian crown group.
Figure 3: Measures of taxon stability.

Change history

  • 22 November 2017

    Please see accompanying Erratum (http://doi.org/10.1038/nature25004). Nine Supplementary Data files were missing from the online version of this Letter; these have been added to the HTML.

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Acknowledgements

Y.-M. Hou, D. Sykes and R. Summerfield assisted with CT scanning. C. Healy, Z. Johanson and M. M. Smith provided scans of Erpetoichthys. L. Sallan provided helpful discussion. N. Brocklehurst helped with R, and L. Parry assisted with R and MrBayes. S.G. was supported by a Junior Research Fellowship from Christ Church, Oxford, and a L’Oréal-UNESCO For Women in Science Fellowship. G.-H.X. was supported by the National Natural Science Foundation of China (41672001). T.J.N was supported by the National Science Foundation (ANT-134166) and the Bingham Oceanographic Fund from the Peabody Museum of Natural History, Yale University. M.F. was supported by a Philip Leverhulme Prize (PLP-2012-130) and Leverhulme Trust Project Grant (RPG-2012-65A).

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The project was conceived by M.F. CT scanning was carried out by S.G., G.-H.X. and M.F. S.G. segmented the CT data, conducted phylogenetic and leaf stability analyses and created the figures, with input from M.F. T.J.N. calculated divergence estimates. S.G. and M.F. wrote the manuscript, with comments from all authors.

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Correspondence to Sam Giles.

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Reviewer Information Nature thanks W. Bemis and M. Coates for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 Cranial anatomy of Fukangichthys longidorsalis based on high-resolution computed tomography.

a, Lateral view of whole skull (IVPP V4096.13). b, Lateral view of braincase, hyomandibula and lower jaw (IVPP V4096.6). c, Braincase in anterior view (IVPP V4096.6). d, Hyoid and branchial arches in dorsal view (IVPP V4096.13). e, Jaws and palate in ventral view (IVPP V4096.13). f, Left lateral view of whole skull (IVPP V4096.6). g, Right lateral view of whole skull (IVPP V4096.6). bb, basibranchial; clav, clavicle; clth, cleithrum; dsph, dermosphenotic; eb, epibranchial; hh, hypohyal; jug, jugal; la, lachrymal; l.ex, lateral extrascapular; m.ex, median extrascapular; opm, operculum; pb, pharyngobranchial; pq, palatoquadrate; prop, preoperculum; pt, posttemporal; qj, quadratojugal; sop, suboperculum; spcl, supracleithrum; sr, skull roof. Mouldic portion of lower jaw shaded. Other abbreviations and colours as in Fig. 1. Scale bars, 5 mm (a, b, dg); 2 mm (c).

Extended Data Figure 2 Photographs of Fukangichthys longidorsalis specimens examined in this study.

a, IVPP V4096.13 in left lateral view. b, IVPP V4096.13 in ventral view. c, IVPP V4096.13 in dorsal view. d, IVPP V4096.6 in left lateral view. e, IVPP V4096.6 in right lateral view. f, IVPP V4096.6 in dorsal view. Scale bar, 10 mm.

Extended Data Figure 3 Interpretive drawings of comparative cranial anatomy of Fukangichthys longidorsalis (IVPP V4096.6 and IVPP V4096.13) and Erpetoichthys calabaricus (BMNH 2016.9.22.3) based on high-resolution computed tomography.

ae, Fukangichthys longidorsalis. fj, Erpetoichthys calabaricus. a, Lateral view of whole skull (IVPP V4096.13). b, Lateral view of braincase, hyomandibula and lower jaw (IVPP V4096.6). c, Braincase in anterior view (IVPP V4096.6). d, Hyoid and branchial arches in dorsal view (IVPP V4096.13). e, Jaws and palate in ventral view (IVPP V4096.13). f, Left lateral view of whole skull (IVPP V4096.6). g, Right lateral view of whole skull (IVPP V4096.6). Scale bars, 5 mm (a, b, eg, j); 2 mm (c, d, h, i).

Extended Data Figure 4 Comparative palatal anatomy of Fukangichthys longidorsalis (IVPP V4096.6 and IVPP V4096.13) and Erpetoichthys calabaricus (BMNH 2016.9.22.3) based on high-resolution computed tomography.

ac, e, Fukangichthys longidorsalis. d, f, Erpetoichthys calabaricus. a, Medial view of left palate (IVPP V4096.13). b, Medial view of right palate (IVPP V4096.13). c, Medial view of left palate (IVPP V4096.6). d, Medial view of left palate. e, Anterolateral view of left palate (IVPP V4096.13). e, Anterolateral view of left palate. qu, quadrate. Scale bars, 5 mm.

Extended Data Figure 5 Comparative hyoid and branchial anatomy of Fukangichthys longidorsalis (IVPP V4096.6 and IVPP V4096.13) and Erpetoichthys calabaricus (BMNH 2016.9.22.3) based on high-resolution computed tomography.

a, d, g, j, Erpetoichthys calabaricus. b, c, e, f, h, i, km, Fukangichthys longidorsalis. a, Braincase, palate, mandibular arch, hyoid arch and ventral portion of branchial arch in ventral view. b, Braincase, palate, mandibular arch, hyoid arch and ventral portion of branchial arch in ventral view (IVPP V4096.6). c, Braincase, palate, mandibular arch, hyoid arch and branchial arch in ventral view (IVPP V4096.13). d, Ventral portion of hyoid and branchial arches in ventral view. e, Ventral portion of hyoid and branchial arches in ventral view (IVPP V4096.6). f, Branchial arches and ventral portion of hyoid arch in ventral view (IVPP V4096.13). g, Ventral portion of hyoid and branchial arches in dorsal view. h, Ventral portion of hyoid and branchial arches in dorsal view (IVPP V4096.6). i, Branchial arches and ventral portion of hyoid arch in ventral view (IVPP V4096.13). j, Hyoid arch and ventral portion of branchial arches in lateral view. k, Hyoid arch and ventral portion of branchial arches in lateral view (IVPP V4096.6). l, Hyoid and branchial arches in lateral view (IVPP V4096.13). m, Close-up of uncinated process of epibranchial. ahy, groove for afferent hyoid artery; ih, interhyal; up, uncinate process. Colours as in Fig. 1. Scale bars 5 mm (a–l); 1 mm (m).

Extended Data Figure 6 Results of phylogenetic analyses.

a, Strict consensus of the 14,450 shortest trees (1,347 steps) for 93 taxa and 265 equally weighted characters. Digits above nodes indicate Bremer decay indices above 1. Digits below nodes indicate percentage bootstrap support above 50%. b, Adams consensus tree of the 14,450 shortest trees (1,347 steps) for 93 taxa and 265 equally weighted characters. Scanilepids and polypterids shown in bold.

Extended Data Figure 7 Results of phylogenetic analyses.

Agreement subtree of the 14,450 shortest trees (1,347 steps) for 93 taxa and 265 equally weighted characters. Scanilepids and polypterids shown in bold. 78 of 93 taxa are included, and the following taxa are pruned from the tree: Beagiascus pulcherrimus, Beishanichthys brevicaudalis, Birgeria groenlandica, Cosmoptychius striatus, Cyranorhis bergeraci, Guiyu oneiros, Howqualepis rostridens, Lawrenciella schaefferi, Mimipiscis toombsi, Onychodus jandemarrai, Platysomus superbus, Psarolepis romeri, Scanilepis dubia, Tanaocrossus kalliokoskii and Wendyichthys dicksoni.

Extended Data Figure 8 Results of Bayesian analyses.

a, Combined morphological and molecular dataset. Terminals in blue are coded for both molecular and morphological data. Scanilepids and polypterids shown in bold. b, Morphological-only dataset. Numbers at nodes represent posterior probability support; asterisks represent a posterior probability of 1.

Extended Data Figure 9 Endocast and bony labyrinth of Erpetoichthys calabaricus (BMNH 2016.9.22.3) showing vestigial lateral cranial canal.

a, Dorsal view. b, Lateral view. c, Transverse tomograph through otic region. a.amp, ampulla of the anterior semicircular canal; asc, posterior semicircular canal; cr.cav, cranial cavity; h.amp, ampulla of the horizontal semicircular canal; hsc, horizontal semicircular canal; lcc, lateral cranial canal; psc, posterior semicircular canal; sac, sacculus. Scale bars, 5 mm.

Extended Data Figure 10 Leaf stability analyses.

a, Raw leaf stability plotted against taxon age (same data as in Fig. 3a). b, Raw leaf stability plotted against taxon age. Error bars represent s.d. (same data as in Fig. 3a). c, Residuals from a linear regression of stability against taxon incompleteness, plotted against taxon age (same data as in Fig. 3b). Taxa identified in Supplementary Table 2.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Supplementary Tables 1-2, Phylogenetic analysis including anatomical character list and additional references. (PDF 2114 kb)

Supplementary Data

This file contains a large format PDF of a single most parsimonious tree showing all character optimisations. (PDF 477 kb)

Reporting Summary (PDF 70 kb)

Supplementary Data

This file contains Supplementary Data files 1-9 and a Supplementary Data guide – this file was added 22nd November 2017, see Erratum 10.1038/nature25004 for details. (ZIP 722 kb)

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Giles, S., Xu, G., Near, T. et al. Early members of ‘living fossil’ lineage imply later origin of modern ray-finned fishes. Nature 549, 265–268 (2017). https://doi.org/10.1038/nature23654

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