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Exceptional fossil preservation and evolution of the ray-finned fish brain

Nature volume 614, pages 486–491 (2023)Cite this article

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Abstract

Brain anatomy provides key evidence for the relationships between ray-finned fishes1, but two major limitations obscure our understanding of neuroanatomical evolution in this major vertebrate group. First, the deepest branching living lineages are separated from the group’s common ancestor by hundreds of millions of years, with indications that aspects of their brain morphology—like other aspects of their anatomy2,3—are specialized relative to primitive conditions. Second, there are no direct constraints on brain morphology in the earliest ray-finned fishes beyond the coarse picture provided by cranial endocasts: natural or virtual infillings of void spaces within the skull4,5,6,7,8. Here we report brain and cranial nerve soft-tissue preservation in Coccocephalus wildi, an approximately 319-million-year-old ray-finned fish. This example of a well-preserved vertebrate brain provides a window into neural anatomy deep within ray-finned fish phylogeny. Coccocephalus indicates a more complicated pattern of brain evolution than suggested by living species alone, highlighting cladistian apomorphies1 and providing temporal constraints on the origin of traits uniting all extant ray-finned fishes1,9. Our findings, along with a growing set of studies in other animal groups10,11,12, point to the importance of ancient soft tissue preservation in understanding the deep evolutionary assembly of major anatomical systems outside of the narrow subset of skeletal tissues13,14,15.

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Fig. 1: The neurocranium, endocast, otoliths and preserved brain of C. wildi (MANCH: W.12451) based on micro-computed tomography.
Fig. 2: Anatomical correspondence between the preserved brain of C. wildi and those of extant fishes.
Fig. 3: Major anatomical transformations in actinopterygian brain structure illuminated by Coccocephalus.

Data availability

The fossil described in this study has been deposited in the collections of the Manchester Museum and the extant specimens in the University of Michigan Museum of Zoology. The reconstructed .tiff stack, segmented Mimics file and .ply files for C. wildi are available at Zenodo (https://doi.org/10.5281/zenodo.6560305).

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Acknowledgements

We thank D. Gelsthorpe and L. Loughtman for access to collections; R. Nagesan and R. Singer for assistance with extant material; L. Simonitis and K. Hall for providing comparative material of Squalus; A. Capobianco, J. Díaz-Cruz and C. Mauricio Peredo for providing feedback on an earlier version of this contribution; and R. Dearden for assisting with Blender. S.G. was supported by a Royal Society Dorothy Hodgkin Research Fellowship (DH160098). This study includes data produced at the CTEES facility at University of Michigan, supported by the Department of Earth and Environmental Sciences and College of Literature, Science and the Arts.

Author information

Authors and Affiliations

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

    Rodrigo T. Figueroa & Matt Friedman

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

    Rodrigo T. Figueroa, Danielle Goodvin, Matthew A. Kolmann & Matt Friedman

  3. Department of Forestry, Wildlife and Fisheries, University of Tennessee, Knoxville, TN, USA

    Danielle Goodvin

  4. Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, USA

    Michael I. Coates

  5. Committee on Evolutionary Biology, University of Chicago, Chicago, IL, USA

    Michael I. Coates & Abigail M. Caron

  6. Natural History Museum, London, UK

    Matt Friedman & Sam Giles

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

    Sam Giles

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  1. Rodrigo T. Figueroa
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Contributions

The project was conceived by M.F. and S.G. CT scanning was performed by M.F. and R.T.F., with staining of extant material by R.T.F. and M.A.K. Segmentation of CT data was performed by M.F., S.G., D.G. and R.T.F.; M.F, S.G. and R.T.F wrote the manuscript, with comments from all of the authors.

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Correspondence to Matt Friedman or Sam Giles.

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Nature thanks Hugo Dutel and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 The brain (red) and myelencephalic sheet/gland (pink) of Coccocephalus wildi and selected extant ray-finned fishes.

a, Coccocephalus wildi. b, Acipenser brevirostrum. c, Amia calva. d, Polypterus senegalus. Grey and white delimitations show margins between forebrain, midbrain and hindbrain across all taxa. Brains are shown in dorsal view and aligned at the anterior- and posteriormost points of the forebrain (olfactory bulbs, telencephalon and diencephalon) and the posteriormost point of the fourth ventricle. Scale bar = 5 mm.

Extended Data Fig. 2 Sections through the brain of Coccocephalus wildi.

a, transverse section through the anterior portion of the telencephalon. b, horizontal section through the ventral portion of the telencephalon. c, transverse section through the posterior portion of the telencephalon. d, horizontal section through the dorsal portion of the telencephalon. e, transverse section through the anterior portion of the hypothalamus inferior lobes. f, transverse section through the posterior portion of the hypothalamus inferior lobes. Inset shows where each of sections (a)-(e) intersect the brain. h.inf, inferior lobe of the hypothalamus; l.hyp.re, lateral hypothalamic recess; tel, telencephalon; tel.sept, telencephalic septum. Scale bar = 2 mm.

Extended Data Fig. 3 Transverse sections and renders of the brain of Coccocephalus wildi.

a,b, the telencephalon. c,d, the mesencephalon and hypophysis. cce, corpus cerebellum; h.inf, inferior lobe of the hypothalamus; hyp, hypophysis; tel, telencephalon; mes, mesencephalon; ms, mesencephalic sheet; v. tr?, velum transversum; 4th v, fourth ventricle; II, optic nerve; III, oculomotor nerve; IV, trochlear nerve, V, trigeminal nerve; VII, facial nerve. Dorsal portion of forebrain and velum transversum digitally removed. Scale bar in a, c = 2.5 mm; scale bar in b, d = 2 mm.

Extended Data Fig. 4 Sections through the brain of Coccocephalus wildi and Amia calva.

a, transverse section through the diencephalon and mesencephalon of Coccocephalus wildi. b, transverse section through the diencephalon and mesencephalon of Amia calva. l.hyp.re, lateral hypothalamic recess. Scale bar = 2 mm.

Extended Data Fig. 5 Sagittal sections through the neurocranium of Coccocephalus wildi showing the brain and associated structures.

cce, corpus cerebelli, cr.c; crista cerebellaris, h.inf, hypothalamus inferior lobes; hyp, hypophysis; mes, mesencephalon; ms, myelencephalic sheet; rho, rhombencephalon; sc, spinal cord; tel, telencephalon; v.tr, velum transversum; 2nd v, second ventricle; 4th v, fourth ventricle; I, olfactory nerve; II, optic nerve. Scale bar = 5 mm.

Extended Data Fig. 6 The brain of Coccocephalus wildi (red) rendered partially transparent to show brain ventricle configuration (white).

a, dorsal view. b, left lateral view. die. v, diencephalic ventricle; 2nd v, second ventricle; 4th v, fourth ventricle. Scale bar = 5 mm.

Extended Data Fig. 7 Sections through the brain of Coccocephalus wildi showing the rhombencephalic region.

a, sagittal section through the brain. b, transverse section through the anterior portion of the rhombencephalon. c, horizontal section through the mesencephalic and rhombencephalic regions of the brain. cce, corpus cerebelli, crc, crista cerebellaris, inv, invagination of the cerebellum, 4th v, fourth ventricle. Scale bar = 1 mm.

Extended Data Fig. 8 The brain of Coccocephalus wildi within the endocavity.

a, dorsal view, b, left lateral view. d.lat, dorsal lateral line nerve, hyo.VII, hyomandibular branch of the facial nerve, hyp, hypophysis, ms, mesencephalic sheet, I, olfactory nerve, II, optic nerve, IV, trochlear nerve, V, trigeminal nerve, VI, abducens nerve, VII, facial nerve, IX, glossopharyngeal nerve, X, vagus nerve. Scale bar = 5 mm.

Supplementary information

Supplementary Information

Document (PDF) including additional text detailing: phylogenetic placement of ✝Coccocephalus wildi; potential paths for the fossilization of brain tissues; CT scanning parameters for all specimens (Supplementary Table 1); and Supplementary References.

Reporting Summary

Supplementary Data

Annotated surface file (HTML) of the segmented brain of ✝Coccocephalus wildi. For visualization open file with a web browser. Produced with Blender 2.79 “Blend4Web” extension.

Supplementary Video 1

Supplementary Video (MP4) illustrating the transverse sections through the brain of ✝Coccocephalus wildi, highlighting the telencephalic septum.

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Figueroa, R.T., Goodvin, D., Kolmann, M.A. et al. Exceptional fossil preservation and evolution of the ray-finned fish brain. Nature 614, 486–491 (2023). https://doi.org/10.1038/s41586-022-05666-1

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