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Lineage Imply Later Origin of Modern Ray-Finned Fishes Giles, Sam; Xu, Guang-Hui; Near, Tom; Friedman, Matt University of Birmingham Early members of ‘living fossil’ lineage imply later origin of modern ray-finned fishes Giles, Sam; Xu, Guang-Hui; Near, Tom; Friedman, Matt DOI: 10.1038/nature23654 License: Other (please specify with Rights Statement) Document Version Peer reviewed version Citation for published version (Harvard): Giles, S, Xu, G-H, Near, T & Friedman, M 2017, 'Early members of ‘living fossil’ lineage imply later origin of modern ray-finned fishes', Nature, vol. 549, no. 7671, pp. 265–268. https://doi.org/10.1038/nature23654 Link to publication on Research at Birmingham portal Publisher Rights Statement: Checked for eligibility: 23/10/2018 This is the accepted manuscript of a paper published in its final form in Nature which can be found at: https://doi.org/10.1038/nature23654 General rights Unless a licence is specified above, all rights (including copyright and moral rights) in this document are retained by the authors and/or the copyright holders. The express permission of the copyright holder must be obtained for any use of this material other than for purposes permitted by law. •Users may freely distribute the URL that is used to identify this publication. •Users may download and/or print one copy of the publication from the University of Birmingham research portal for the purpose of private study or non-commercial research. •User may use extracts from the document in line with the concept of ‘fair dealing’ under the Copyright, Designs and Patents Act 1988 (?) •Users may not further distribute the material nor use it for the purposes of commercial gain. Where a licence is displayed above, please note the terms and conditions of the licence govern your use of this document. When citing, please reference the published version. Take down policy While the University of Birmingham exercises care and attention in making items available there are rare occasions when an item has been uploaded in error or has been deemed to be commercially or otherwise sensitive. If you believe that this is the case for this document, please contact [email protected] providing details and we will remove access to the work immediately and investigate. Download date: 29. Sep. 2021 1 Early members of ‘living fossil’ lineage imply later origin of modern ray-finned 2 fishes 3 4 Sam Giles1*, Guang-Hui Xu2, Thomas J. Near3, Matt Friedman1,4 5 6 1Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, 7 OX1 3AN, UK. 8 9 2 Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of 10 Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese 11 Academy of Sciences, Beijing 100044, China 12 3Department of Ecology & Evolutionary Biology and Peabody Museum of Natural 13 History, Yale University, 165 Prospect St, New Haven, CT 06520, USA 14 4Museum of Paleontology and Department of Earth and Environmental Sciences, 15 University of Michigan, 1109 Geddes Ave, Ann Arbor, MI 48109, USA 16 17 *Corresponding author. E-mail: [email protected] 18 19 20 Modern ray-finned fishes (Actinopterygii) comprise half of extant vertebrate 21 species and are widely thought to have originated before or near the end of the 22 Middle Devonian (~385 million years (Myr) ago)1-4. Polypterids (bichirs and 23 ropefish) represent the earliest-diverging lineage of living actinopterygians, with 24 almost all Palaeozoic taxa interpreted as more closely related to other extant 25 actinopterygians than to polypterids5-10. By contrast, the earliest material 26 assigned to the polypterid lineage is mid-Cretaceous (ca. 100 Mya) in age11, 27 implying a quarter-of-a-billion-year palaeontological gap. We show that 28 scanilepiforms, a widely distributed Triassic (ca. 252-201 Mya) radiation, are 29 stem polypterids. Significantly, these fossils break the long polypterid branch 30 and expose many supposedly primitive features of extant polypterids as 31 reversals. This shifts numerous Palaeozoic ray-fins to the actinopterygian stem, 32 reducing the minimum age for the crown lineage by roughly 45 Myr. 33 Recalibration of molecular clocks to exclude phylogenetically reassigned 34 Palaeozoic taxa results in age estimates for the actinopterygian crown lineage 35 ~20–40 million years younger than previous molecular analyses1-4. These new 36 dates are broadly consistent with our revised palaeontological timescale and 37 coincident with an interval of conspicuous morphological and taxonomic 38 diversification among ray-fins centred on the Devonian-Carboniferous 39 boundary12-14. A shifting timescale, combined with ambiguity in the relationships 40 of late Palaeozoic actinopterygians, highlights this part of the fossil record as a 41 major frontier in understanding the evolutionary assembly of modern vertebrate 42 diversity. 43 44 The roughly dozen living species of polypterids have long vexed vertebrate 45 biologists15. These freshwater, African endemics were only recognized as ray-finned 46 fishes in the early 20th century16,17, although this view was resisted by some until the 47 1970s18. Anatomical and molecular data now support placement of polypterids as the 48 living sister group of all other extant actinopterygians1-7,9,19. Morphological analyses 49 generally resolve polypterids as one of the earliest diverging ray-finned lineages, with 50 only the Middle-Late Devonian Cheirolepis consistently falling on the 51 actinopterygian stem5-7,9,20. Despite apparently ancient evolutionary origins and 52 perceived status as ‘living fossils’15, polypterids have a meagre palaeontological 53 record consisting largely of fragments10,11. The oldest polypterids are mid-Cretaceous 54 in age21, postdating the predicted origin of the lineage by at least 285 Myr, and show 55 few differences from modern species17,22,23, which originated in the Miocene (ca. 20 56 Myr15). The lack of specializations found in early representatives of other living ray- 57 fin groups suggests an ancient origin for polypterids, but several of these absences 58 concern distinctive aspects of polypterid morphology that do not closely resemble the 59 anatomy of the oldest ray-finned fishes10,15. Fossils have played an important role in 60 establishing relationships among living actinopterygian lineages16,19, so the lack of 61 early polypterids leaves an outstanding gap in our understanding of the evolutionary 62 history of this group and of vertebrates more generally. 63 64 Scanilepiformes is a widespread group of Triassic ‘palaeoniscoid’ fishes known from 65 continental or marginal marine deposits in Sweden, Russia, China, Kyrgyzstan and 66 the United States. Links between scanilepiforms and polypterids have been made 67 based on morphological similarity, referencing a mix of ancestral (e.g., large gular 68 plates) and derived, but homoplastic (e.g., long-based dorsal fin), characters24-25. 69 However, past cladistic analyses resolve scanilepiforms as actinopterans, specifically 70 stem-group neopterygians9,26, rejecting a close phylogenetic relationship with 71 polypterids. 72 73 Most scanilepiform fossils are heavily compressed, limiting investigations to external 74 anatomy. The Middle Triassic Fukangichthys represents an important exception (Fig. 75 1, Extended Data Figures 1–3). High-resolution micro-computed tomography (µCT) 76 of three-dimensionally preserved skulls illuminates internal cranial anatomy of 77 scanilepiforms. The trough-shaped interorbital walls, which do not contact at the 78 midline (Fig. 1c and Extended Data Figure 1c), are separated from the weakly ossified 79 otic and occipital regions of the neurocranium (Extended Data Figure 1a). The optic 80 foramen is ventrally positioned, and the parasphenoid contributes to its lower margin 81 (Fig. 1b,c and Extended Data Figure 1b,c). The parasphenoid has long but simple 82 ascending processes, a triangular corpus pierced by a hypophysial canal, and no 83 posterior stalk (Fig. 1b,e and Extended Data Figure 1b,e). A small median vomer lies 84 anterior to the parasphenoid (Fig. 1e and Extended Data Figure 1e). Dermal bones on 85 the inner surface of the palate include the accessory vomer, dermetapterygoid, three 86 dermopalatines, entopterygoid, and an ectopterygoid bearing a lateral process that 87 articulates with the inner face of the maxilla (Fig. 1e and Extended Data Figures 1e, 88 4). Like the maxilla and premaxilla, the dentary bears a single row of peg-like teeth. 89 The hook-shaped coronoid process is composed exclusively of the prearticular (Fig. 90 1b and Extended Data Figures 1a, 4e). A modest opercular process extends from the 91 ‘L’-shaped hyomandibula, which is imperforate and unfused to the dermohyal (Fig. 92 1b and Extended Data Figure 1b). Plate-like ceratohyals, which bear a groove for the 93 afferent hyoid artery, flank the four pairs of ceratobranchials and hypobranchials (Fig. 94 1d and Extended Data Figures 1d, 5). Epibranchials bear uncinate processes, and 95 multiple basibranchial ossifications may be present (Fig. 1d and Extended Data 96 Figures 1d, 5). 97 98 We conducted a revised analysis of actinopterygian interrelationships based on an 99 expanded morphological dataset27 (93 taxa, 265 characters), and an analysis of this 100 morphological dataset combined with DNA sequences of 12 nuclear genes. 101 Phylogenies were inferred using both parsimony (Fig. 2 and Extended Data Figures 6, 102 7) and Bayesian methods (Extended Data Figure 8). In contrast to some, but not all28- 103 29, previous studies, we have rooted our analyses on a set of non-actinopterygian 104 outgroups,
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