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A Late Devonian actinopterygian suggests high lineage survivorship across the end-Devonian mass extinction

Nature Ecology & Evolution volume 7, pages 10–19 (2023)Cite this article

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Abstract

Many accounts of the early history of actinopterygians (ray-finned fishes) posit that the end-Devonian mass extinction had a major influence on their evolution. Existing phylogenies suggest this episode could have acted as a bottleneck, paring the early diversity of the group to a handful of survivors. This picture, coupled with increases in taxonomic and morphological diversity in the Carboniferous, contributes to a model of explosive post-extinction radiation. However, most actinopterygians from within a roughly 20-million year (Myr) window surrounding the extinction are poorly known, contributing to uncertainty about the meaning of these patterns. Here, we report an exceptionally preserved fossil from 7 Myr before the extinction that reveals unexpected anatomical features. Palaeoneiros clackorum gen. et sp. nov. nests within a clade of post-Devonian species and, in an expanded phylogenetic analysis, draws multiple lineages of Carboniferous actinopterygians into the Devonian. This suggests cryptic but extensive lineage diversification in the latest Devonian, followed by more conspicuous feeding and locomotor structure diversification in the Carboniferous. Our revised model matches more complex patterns of divergence, survival and diversification around the Devonian/Carboniferous boundary in other vertebrate clades. It also fundamentally recalibrates the onset of diversification early in the history of this major radiation.

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Fig. 1: Anatomy of Palaeoneiros clackorum MCZ VPF-5114.
Fig. 2: Internal and external anatomy of Palaeoneiros clackorum MCZ VPF-5114.
Fig. 3: Comparative anatomy of Palaeoneiros clackorum with Devonian and Carboniferous actinopterygians.
Fig. 4: Hypotheses of early actinopterygian diversification and timescaled phylogenetic tree.
Fig. 5: Patterns in early ray-finned fish size around the Devonian/Carboniferous boundary.

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Data availability

The specimen described in this study is deposited in the collections of the Harvard Museum of Comparative Zoology. CT data and derivatives are available on Morphosource (projection series: https://doi.org/10.17602/M2/M417031; TIFF stack: https://doi.org/10.17602/M2/M420055; OBJ file of all segmented three-dimensional objects https://doi.org/10.17602/M2/M420865; PLY file of all segemented three-dimensional objects: https://doi.org/10.17602/M2/M420629). The Mimics file can be downloaded by contacting the Department of Vertebrate Paleontology at the Museum of Comparative Zoology, Harvard University. All other data associated with this paper are included in the Supplementary Data. This work and associated nomenclatural acts are registered in ZooBank. ZooBank LSIDs are accessible at the URL generated by appending the LSID to http://zoobank.org.

Code availability

The code needed to perform the trait analyses is included in the Supplementary Data.

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Acknowledgements

We thank the Museum of Comparative Zoology, Harvard University for specimen access and especially J. Cundiff for organizing the loan of material that formed the basis of this study. We also thank E. Bernard, D. Gelsthorpe, Z. Johanson, L. Loughtman, P. Shephard and S. Walsh for facilitating access to comparative collections; G. Lloyd for helpful discussions; and C. Byrd for assistance with data archiving. S.G. was supported by a Royal Society Dorothy Hodgkin Research Fellowship (no. DH160098). This research was also supported by funding from the National Science Foundation (NSF) to M.F. (NSF-GEO 2219007) and S.E.P. (NSF-GEO 2219069). This study includes data produced in the CTEES facility at University of Michigan, supported by the Department of Earth and Environmental Sciences and College of Literature, Science, and the Arts.

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Authors and Affiliations

  1. School of Geography, Earth and Environmental Sciences, University of Birmingham, Birmingham, UK

    Sam Giles

  2. Natural History Museum, London, UK

    Sam Giles & Matt Friedman

  3. Museum of Paleontology, University of Michigan, Ann Arbor, MI, USA

    Kara Feilich & Matt Friedman

  4. GeoZentrum Nordbayern, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany

    Rachel C. M. Warnock

  5. Museum of Comparative Zoology and Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    Stephanie E. Pierce

  6. Department of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI, USA

    Matt Friedman

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Contributions

M.F. and S.E.P. designed the research. S.G., M.F., K.F. and R.W. performed the research and analysed the data. S.G. and M.F. wrote the paper and designed figures. All authors edited the manuscript.

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Correspondence to Sam Giles.

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Extended data

Extended Data Fig. 1 Geological context of Palaeoneiros clackorum MCZ VPF-5114.

(A) Map of Pennsylvania showing location; inset shows geological map for the area of Warren County (based on (36)) and simplified geological column (based on (68)). City of Warren indicated by solid bounding lines. (B) External photograph of Palaeoneiros clackorum showing right lateral flank. Colors in stratigraphic column relate to geological map: latest Devonian and post-Devonian strata condensed into one color. Scale bar in (A): 10 km, in (B): 10 mm. Credit: Museum of Comparative Zoology, Harvard University; © President and Fellows of Harvard College.

Extended Data Fig. 2 External photographs of Palaeoneiros clackorum MCZ VPF-5114.

Right lateral flank in (A) part and (B) counterpart. (C) Ventral view showing entire specimen, and (D) closeup of skull and pectoral region. (E) Right anal fin. (F) Scales from right lateral flank. Scale bar in (A)-(C): 10 mm, in (D)-(F): 5 mm. Photos copyright President and Fellows of Harvard College. Abbreviations: an, anal fin; br, branchiostegal; chy, ceratohyal; clth, cleithrum; dent, dentary; dors, dorsal fin; frf, fringing fulcra; lep, lepidotrichia; mx, maxilla; pect, pectoral fin; pelv, pelvic fin; sc, scale. Credit: Museum of Comparative Zoology, Harvard University; © President and Fellows of Harvard College.

Extended Data Fig. 3 Anatomy of Palaeoneiros clackorum MCZ VPF-5114.

Interpretive drawing of (A) right lateral view of specimen; (B) medial view of right upper and lower jaws; (C) medial view of left shoulder girdle and fin, and (D) left lateral view of gill skeleton, hyoid arch and braincase. Scale bar in (A): 10 mm, in (B)-(D): 5 mm. Abbreviations: ang, angular; art, articular; asp, ascending process of parasphenoid; av, accessory vomer; br, branchiostegal; cb, ceratobranchial; chy, ceratohyal; clav, clavicle; clth, cleithrum; dent, dentary; dmpt, dermatopterygoid; dsph, dermosphenotic; ecpt, ectopterygoid and dermopalatines; eb, epibranchial; enpt, entopteryygoid; exo, exoccipital; hmd, hyomandibula;?ic, possible intercalar; icl, interclavicle; ioc, infraorbital canal; it, intertemporal; jug, jugal; jugc, jugal canal; lep, lepidotrichia; ll, lateral line; mc, mandibular canal; mx, maxilla; op, operculum; part, prearticular and coronoid; popc, preopercular canal; popl, preopercular pit lines;?pmx, possible premaxilla; psp, parasphenoid; qu, quadrate; rad, radials; sc, scale; scl, sclerotic ossicle; scpc, scapulocoracoid; sop, suboperculum; sorb, suborbitals; sph, sphenotic ossification; st, supratemporal; t, teeth; tp, toothplate; unc, uncinate process.

Extended Data Fig. 4 External anatomy of Palaeoneiros clackorum MCZ VPF-5114.

Renders of specimen in (A) right lateral, (B) left lateral, (C) dorsal, (D) anterior, and (E) ventral view; and an isolated scale (F). Colour coding of skeleton: blue, cheek and jaw; purple, skull roof and sclerotic ossicle; pink, braincase; dark green, hyomandibula; light green, operculogular system; turquoise, shoulder girdle; yellow, gill skeleton. Scale bar in (A)-(C),(E): 5 mm, in (D): 2 mm, in(F):1 mm. Abbreviations: ang, angular; antd, anterodorsal process; art, articular; asc, ascending process of the parasphenoid; av, accessory vomer; br, branchiostegal; cb, ceratobranchial; chy, ceratohyal; clav, clavicle; clth, cleithrum; dent, dentary; dsph, dermosphenotic; eb, epibranchial; ecpt, ectopterygoid and dermopalatines; enpt, entopterygoid; exsc, extrascapular; fr, frontal; fu, fused lepidotrichia; hb, hypobranchial; hmd, hyomandibula;?ic, possible intercalar; icl, interclavicle; ioc, infraorbital canal; it, intertemporal; jgl, jugal canal; jug, jugal; lac, lacrimal; lep, lepidotrichia; ll, lateral line; mc, mandibular canal; mpl, middle pit line; mx, maxilla; op, operculum; pa, parietal; part, prearticular and coronoids; peg, scale peg; pi, pineal foramen;?pmx, possible premaxilla; pop, preoperculum; popl, preopercular pit line; ppl, posterior pit line; pscl, presupracleithrum; psp, parasphenoid; pt, posttemporal; qu, quadrate; rad, radial; sc, scale; scl, sclerotic ossicle; sclth, supracleithrum; soc, supraorbital canal; sop, suboperculum; sorb, suborbital; sph, sphenotic ossification; st, supratemporal; unc, uncinate process. Renders copyright President and Fellows of Harvard College.

Extended Data Fig. 5 Renders of Palaeoneiros clackorum MCZ VPF-5114.

(A) Skull roofing bones in visceral view. (B) Possible premaxilla. (C) Right maxilla, dentary and postdentary in medial view. (D) Right lower jaw in dorsal view. (E) Left lower jaw in medial view. Scale bar in all: 2 mm. Abbreviations: add, adductor fossa; ang, angular; art, articular; dent, dentary; exsc, extrascapular; fr, frontal; ll, lateral line; mc, mandibular canal; mx, maxilla; na, nasal; ov, maxilla overlap of dentary;?pmx, premaxilla; part, prearticular plus coronoids; pi, pineal foramen; pt, posttemporal; qu, quadrate; ri, ridge; pa, parietal; sh, maxillary shelf; soc, supraorbital canal; t, tooth; tp, toothplate. Credit: Museum of Comparative Zoology, Harvard University; © President and Fellows of Harvard College.

Extended Data Fig. 6 Renders of gill skeleton of Palaeoneiros clackorum MCZ VPF-5114.

(A) Gill skeleton in dorsal view. (B) Gill skeleton in ventral view. Scale bar: 5 mm. Abbreviations: bb, basibranchial; cb, ceratobranchial; eb, epibranchial; hb, hyobranchial; pb, pharyngobranchial. Credit: Museum of Comparative Zoology, Harvard University; © President and Fellows of Harvard College.

Extended Data Fig. 7 Renders of shoulder and fin of Palaeoneiros clackorum MCZ VPF-5114.

(A) Shoulder girdle and pectoral fin in left lateral view, and (B) closeup with dermal girdle removed. (C) Shoulder girdle and pectoral fin in medial view, and (D) with radials and lepidotrichia removed. (E) Shoulder girdle and pectoral fin in posterior view, and (F) with radials and lepidotrichia removed. Radials in (G) dorsal and (H) ventral view. Scale bar in (A)-(F): 2 mm, in (G)-(H): 1 mm. Abbreviations: clav, clavicle; clth, cleithrum; fu, fused lepidotrichia; gl, glenoid fossa; icl, interclavicle; lep, lepidotrichia; mptg, metapterygium; pr.rad, preaxial radial; ptg, propterygium; ptg.ca, propterygial canal; rad, radial; scpc.hz, horizontal plate of scapulocoracoid; scpc.pl, scapulocoracoid plates. Credit: Museum of Comparative Zoology, Harvard University; © President and Fellows of Harvard College.

Extended Data Fig. 8 Results of parsimony analysis.

(A) Strict consensus of the 20,000 trees (1616 steps) for 121 taxa and 292 equally weighted characters. Digits above nodes indicate Bremer decay indices above 1. (B) Agreement subtree. New taxon indicated in bold.

Extended Data Fig. 9 Results of Bayesian analysis.

50% majority rule tree for 121 taxa and 292 equally weighted characters. Digits at nodes indicate posterior probability support. New taxon indicated in bold.

Extended Data Fig. 10 Results of fossil birth-death analysis.

Blue bars associated with nodes indicate 95% highest posterior density for age estimates. New taxon indicated in bold.

Supplementary information

Supplementary Information

Supplementary Text, Table and References.

Reporting Summary

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Supplementary Data 1

Zip file containing the files needed to perform the parsimony analysis in TNT (morphological data matrix, TNT script, constraint tree) and a consensus tree file.

Supplementary Data 2

Zip file containing the morphological data matrix formatted for the Bayesian analysis and a consensus tree file.

Supplementary Data 3

Zip file containing the code required to perform the trait analyses and the Excel file containing the data for the timescaling and lower-jaw analyses. Sheet 1 contains taxon list, data source, standard length, jaw length, age data, locality and stratigraphy. NA indicates that lower-jaw length or taxon was not included in our analysis. Red, inapplicable; orange, measured from literature; green, measured from the specimen. Sheet 2 contains the taxonomic notes. Sheet 3 contains the average jaw and standard lengths for taxa in which both can be measured.

Supplementary Data 4

Zip file containing the MrBayes script for the fossil birth–death analysis and consensus file.

Supplementary Data 5

Large-format PDF of a single most parsimonious tree showing all character optimizations.

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Giles, S., Feilich, K., Warnock, R.C.M. et al. A Late Devonian actinopterygian suggests high lineage survivorship across the end-Devonian mass extinction. Nat Ecol Evol 7, 10–19 (2023). https://doi.org/10.1038/s41559-022-01919-4

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