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Regional Disparity in the Axial Skeleton of Saurichthyidae and Implications for Axial Regionalization in Non‐Teleostean Actinopterygians

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Regional Disparity in the Axial Skeleton of Saurichthyidae and Implications for Axial Regionalization in Non‐Teleostean Actinopterygians Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2021 Regional disparity in the axial skeleton of Saurichthyidae and implications for axial regionalization in non‐teleostean actinopterygians Maxwell, E E ; Romano, C ; Wu, F ‐X Abstract: The postcranial axial skeleton of actinopterygian fishes is typically divided into three regions: (1) an anterior abdominal region, (2) a posterior caudal region and (3) those vertebrae supporting the caudal fin. However, in some actinopterygians, the axial skeleton is more finely subdivided, withup to six morphologically distinctsub-regions recognized. Phylogenetic continuity and homology of struc- tures across these sub-regions have not been investigated in detail, either between or among groups. We examine variation in axial regionalization in saurichthyid fishes, a clade of extinct non-teleostean actinopterygians with highly variable axial skeletal morphology but an otherwise conservative body plan, and compare these findings to other non-teleostean actinopterygians to assess conservation of a regional- ized axial skeleton within bony fishes. We document up to eight distinct regions in the vertebral column of Triassic Saurichthys: (1) a postoccipital region, (2) an anterior and (3) a posterior abdominal region, (4) a transitional region spanning the abdominal– caudal boundary, (5) an anterior and (6) a posterior caudal region and (7) preural and (8) ural regions. Based on taphonomical and morphological evidence, the transitional region appears to function in axial stiffening in the area of the median fins, whereas the abdominal region is highly flexible. The degree to which these axial regions are osteologically dif- ferentiated is highly variable across Saurichthyidae, implying iterative evolution of differentiation and de-differentiation over relatively short geological timescales. Such variably expressed regionalization was also identified in the outgroup non-teleostean actinopterygians Birgeria and Australosomus. Despite variation in morphological disparity, the regions identified in saurichthyids correlate well with those doc- umented in some teleosts and Paleozoic actinopterygians, suggesting potential deep patterning homology but independent evolution of specific regionalized axial morphologies in response to changing functional demands. DOI: https://doi.org/10.1111/jzo.12878 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-201272 Journal Article Published Version The following work is licensed under a Creative Commons: Attribution-NonCommercial 4.0 International (CC BY-NC 4.0) License. Originally published at: Maxwell, E E; Romano, C; Wu, F ‐X (2021). Regional disparity in the axial skeleton of Saurichthyidae and implications for axial regionalization in non‐teleostean actinopterygians. Journal of Zoology:jzo.12878. DOI: https://doi.org/10.1111/jzo.12878 2 Journal of Zoology. Print ISSN 0952-8369 Regional disparity in the axial skeleton of Saurichthyidae and implications for axial regionalization in non-teleostean actinopterygians E. E. Maxwell1 , C. Romano2 & F.-X. Wu3,4 1Staatliches Museum fur€ Naturkunde Stuttgart, Stuttgart, Germany 2Palaontologisches€ Institut und Museum, Universitat€ Zurich,€ Zurich,€ Switzerland 3Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China 4Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Beijing, China Keywords Abstract Saurichthyidae; Birgeria; Actinopterygii; vertebral column; morphology; evolution; axial skeleton; The postcranial axial skeleton of actinopterygian fishes is typically divided into Triassic. three regions: (1) an anterior abdominal region, (2) a posterior caudal region and (3) those vertebrae supporting the caudal fin. However, in some actinopterygians, Correspondence the axial skeleton is more finely subdivided, with up to six morphologically distinct Erin Maxwell, Staatliches Museum fur€ sub-regions recognized. Phylogenetic continuity and homology of structures across Naturkunde Stuttgart, Rosenstein 1, 70191 these sub-regions have not been investigated in detail, either between or among Stuttgart, Germany. groups. We examine variation in axial regionalization in saurichthyid fishes, a clade Email: [email protected] of extinct non-teleostean actinopterygians with highly variable axial skeletal mor- phology but an otherwise conservative body plan, and compare these findings to Editor: Andrew Kitchener other non-teleostean actinopterygians to assess conservation of a regionalized axial Associate Editor: Christine Bohmer€ skeleton within bony fishes. We document up to eight distinct regions in the verte- bral column of Triassic Saurichthys: (1) a postoccipital region, (2) an anterior and Funding information (3) a posterior abdominal region, (4) a transitional region spanning the abdominal– Open Access funding enabled and organized by caudal boundary, (5) an anterior and (6) a posterior caudal region and (7) preural Projekt DEAL. WOA Institution: STAATLICHES and (8) ural regions. Based on taphonomical and morphological evidence, the tran- MUSEUM FUR NATURKUNDE STUTTGART. sitional region appears to function in axial stiffening in the area of the median fins, Blended DEAL: Projekt DEAL. whereas the abdominal region is highly flexible. The degree to which these axial regions are osteologically differentiated is highly variable across Saurichthyidae, Received 25 April 2020; revised 12 January implying iterative evolution of differentiation and de-differentiation over relatively 2021; accepted 28 January 2021 short geological timescales. Such variably expressed regionalization was also identi- fied in the outgroup non-teleostean actinopterygians Birgeria and Australosomus. doi:10.1111/jzo.12878 Despite variation in morphological disparity, the regions identified in saurichthyids correlate well with those documented in some teleosts and Paleozoic actinoptery- gians, suggesting potential deep patterning homology but independent evolution of specific regionalized axial morphologies in response to changing functional demands. Introduction areas: an abdominal and a caudal region, distinguished by the presence of haemal spines in the latter (e.g. Bird & Mabee, A highly regionalized axial skeleton consisting of cervical, tho- 2003). Some actinopterygians show more complex patterns of racic, lumbar, sacral and caudal regions has historically been axial regionalization (e.g. the Weberian vertebrae of ostario- viewed as a typical feature of tetrapods (Sallan, 2012). physans in the anterior column; the ural skeleton of teleosts: Although best-developed in mammals, these regions can be Bird and Mabee, 2003), but historically these have been inter- morphometrically recovered even within groups showing more preted as isolated specializations of specific lineages of highly subtle variation along the vertebral column (e.g. snakes: Head derived teleosteans, external to a conserved framework of axial & Polly, 2015; odontocete cetaceans: Buchholtz & Gee, 2017); patterning. However, detailed examination of the axial skeleton this is referred to as ‘regionalized but de-differentiated’ (Buch- in the Paleozoic (Carboniferous) basal actinopterygian Tarra- holtz and Gee, 2017). In contrast, the vertebral column of sius indicates five clearly differentiated regions within the pre- actinopterygian fishes has been divided into only two general caudal axial skeleton (Sallan, 2012), and more recently five Journal of Zoology (2021) – ª 2021 The Authors. Journal of Zoology published by John Wiley & Sons Ltd on behalf of Zoological Society of London 1 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. Axial regionalization in Saurichthyidae E. E. Maxwell et al. distinct axial regions have been recognized in salmonids (De characterized by an unconstricted notochord; ossified centra are Clercq et al., 2017), which have a generalized body plan. absent (aspondylous vertebrae: Arratia, Schultze & Casciotta, These reports raise intriguing questions as to the prevalence of 2001). Within one axial segment, ossified components dorsal axial regionalization in actinopterygians and structural variabil- to the notochord include neural arches with medially unfused ity within morphologically disparate regions. neural spines; the neural arches articulate with adjacent arcual In vertebrates, precaudal axial regionalization is patterned by elements via zygapophyses (Stensio,€ 1925). Posterior to the spatially and temporally collinear expression of Hox genes true neural arch of each segment, Saurichthys possesses a sec- within the somitic mesoderm during embryonic development ond neural arch-like element, convergent in morphology to the (Burke et al., 1995). Gene expression in zebrafish, the best- first but homologous to an expanded interdorsal element (Max- known actinopterygian developmental model system, suggests well, Furrer & Sanchez-Villagra, 2013). Supraneurals are anteriorly shifted, overlapping patterns of Hox expression dur- absent, as are ossified ribs and intermuscular elements. Ossifi- ing embryonic development (Prince et al., 1998; Morin-Ken- cations ventral to the notochord are more variable, but when sicki,
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