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Spiny chondrichthyan from the lower Silurian of South China

Abstract

Modern representatives of chondrichthyans (cartilaginous fishes) and osteichthyans (bony fishes and tetrapods) have contrasting skeletal anatomies and developmental trajectories1,2,3,4 that underscore the distant evolutionary split5,6,7 of the two clades. Recent work on upper Silurian and Devonian jawed vertebrates7,8,9,10 has revealed similar skeletal conditions that blur the conventional distinctions between osteichthyans, chondrichthyans and their jawed gnathostome ancestors. Here we describe the remains (dermal plates, scales and fin spines) of a chondrichthyan, Fanjingshania renovata gen. et sp. nov., from the lower Silurian of China that pre-date the earliest articulated fossils of jawed vertebrates10,11,12. Fanjingshania possesses dermal shoulder girdle plates and a complement of fin spines that have a striking anatomical similarity to those recorded in a subset of stem chondrichthyans5,7,13 (climatiid ‘acanthodians’14). Uniquely among chondrichthyans, however, it demonstrates osteichthyan-like resorptive shedding of scale odontodes (dermal teeth) and an absence of odontogenic tissues in its spines. Our results identify independent acquisition of these conditions in the chondrichthyan stem group, adding Fanjingshania to an increasing number of taxa7,15 nested within conventionally defined acanthodians16. The discovery of Fanjingshania provides the strongest support yet for a proposed7 early Silurian radiation of jawed vertebrates before their widespread appearance5 in the fossil record in the Lower Devonian series.

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Fig. 1: Dermoskeletal elements of Fanjingshania renovata.
Fig. 2: Histological and developmental features of the pectoral shoulder girdle and trunk scales of F.renovata.
Fig. 3: Phylogenetic placement of F.renovata within early jawed vertebrates.

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Data availability

Supplementary data for this study provided as tomography slices (.bmp), volume renderings (.ply) and phylogenetic analyses files (.tnt, .nex, .tre, .rtf, .log, .ckp, .mcmc, .parts, .t, .tprobs, .tstat and .vstat) are available at Figshare (https://doi.org/10.6084/m9.figshare.20366838.v1). The ZooBank LSID code for this publication is urn:lsid:zoobank.org:pub:09B4CB7A-9640-4685-B9C1-97A7B682F45B. The ZooBank LSID code for the new genus Fanjingshania is urn:lsid:zoobank.org:act:71E5E18E-FE0A-41F0-B928-A1019EF92E28. The ZooBank LSID code for the new species Fanjingshania renovata is urn:lsid:zoobank.org:act:E4ED8B95-866A-4D1B-961A-695373908692. Fanjingshania specimens with assigned accession numbers (IVPP V27433.1–V27443.1) are available upon request from the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences.

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Acknowledgements

We thank Y.-M. Hou for the acquisition of the micro-CT X-ray data, Y. Hwu and Y.-T. Weng for performing and assisting with the synchrotron X-ray analyses, and Y. Z. Hu for her comments and advice during the volumetric reconstructions of the specimens. This research was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA19050102 and XDB26000000), the National Natural Science Foundation of China (41530102), the Key Research Program of Frontier Sciences, CAS (QYZDJ-SSW-DQC002), an Open Project Grant of the Key Laboratory of Vertebrate Evolution and Human Origins, IVPP, CAS (LVEHO19001), MOST 108-2116-M-213-001 (Taiwan), Chinese Postdoctoral Science Foundation grant (2019M663440) and the National Synchrotron Radiation Research Center, Taiwan (beamtime project numbers 2019-3-083-1 and 2019-3-185-1).

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Authors

Contributions

Research design: M.Z., P.S.A. and I.J.S.; fieldwork and sample collection: M.Z., W.Z., Q.L., J.W., L.J., T.Q. and L.P.; data processing: Q.L., P.S.A., L.P., J.W. and M.Z.; synchrotron X‐ray tomography analyses: P.S.A. and C.-C.W.; manuscript text and figure preparation: P.S.A., I.J.S., Q.L., J.W. and M.Z.

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Correspondence to Min Zhu.

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Extended data figures and tables

Extended Data Fig. 1 The Shiqian-Tunping section at Leijiatun (Shiqian County, Guizhou Province, China).

Diagram revealing the relationship of the Rongxi to the other Silurian lithostratigraphic units (color coded) exposed at Shiqian-Tunping and the location of the Fanjingshania-bearing beds (depicted in grey, sample 35SQTP) within the sequence.

Extended Data Fig. 2 Head and trunk dermoskeletal elements of Fanjingshania renovata.

Volume renderings based on X-ray microcomputed tomography data (a–c, e, f, h, i), scanning electron micrographs (d, g, j, k) and optical micrographs (l, m). Fused tectal tesserae (V27438.4) in a, crown and b, basal views. c, Broad asymmetrical trunk scale in crown view (V27435.23). d, Asymmetrical trunk scale (V27435.6) in crown view. Incomplete symmetrical trunk scale (V27435.7) in e, crown and f, base views. g, Crown view of an asymmetrical trunk scale (V27435.12). h, Crown view of a symmetrical trunk scale (V27435.24) with a large anterior tubercle. i, Basal view of V27435.24. j, Crown view of a trunk scale (V27435.11) with an anterior replacement odontode. k, Incomplete trunk scale (V27435.9) with an anteriorly excavated crown. l, Section through two fused tectal tesserae (V27438.5). m, Longitudinal section through a trunk scale (V27435.8). Arrowheads point to anterior. ad, atubular dentine; cb, cellular bone; po, primary odontodes; ro, replacement odontode; sb, scale base; sc, scale crown; so, secondary odontodes, tt, tectal tesserae. Scale bars, 1 mm.

Extended Data Fig. 3 Fin spines of Fanjingshania renovata.

Volume renderings based on X-ray microcomputed tomography data (a–t) and optical micrographs (u–x). Incomplete pectoral fin spine (V27437.9) in a, lateral and b, apical lateral view. Incomplete pectoral spine (V27437.10) in (c, d) lateral and e, posterior lateral views. Pelvic fin spine (V27437.11) in f, lateral and g, posterior views. Partial anterior dorsal fin spine (V27437.12) in (h, j) and i, posterior views. Incomplete posterior dorsal fin spine (V27437.13) in k, lateral and l, posterior views. Incomplete anal fin spine (V27437.14) in m, lateral and n, posterior views. (o, p) Incomplete prepelvic fin spine (V27441.4) in lateral views. Prepelvic fin spine (V27441.5) in q, lateral and r, basal lateral views. (s, t) Incomplete prepelvic fin spine (V27441.6) in lateral apical views. u, Transversely sectioned fin spine fragment (V27437.2) shown in part. v, Transversely sectioned apical fragment of a fin spine (V27437.1). w, Enlarged anterior of v, showing detail of the spine’s tissue structure. Portion of a longitudinally sectioned pectoral fin spine (V27437.14). cc, calcified cartilage; cb, cellular bone; lz, lamellar zone; vz, vascular zone. Scale bars, 1 mm (a–t), 0.5 mm (v), 0.25 mm (u), 0.2 mm (x) and 0.05 mm.

Extended Data Fig. 4 Elements of the dermal shoulder girdle of Fanjingshania renovata.

Optical micrographs (a, d, i), scanning electron micrograph (b) and volume renderings based on synchrotron (e–h) and microcomputed (j–l) X-ray tomography data. a, Section through a fragment of a pectoral fin spine wall fused to a partial pinnal plate (V27433.3). b, Fragment of a pectoral fin spine wall fused to a partial pinnal plate (V27433.5) in external view. c, Horizontal virtual section through a partial pinnal plate fused to a pectoral fin spine fragment (V27433.1, holotype). d, Detail of a pectoral fin spine wall (from a sectioned pectoral fin spine fragment fused to a partial pinnal plate, V27433.6). e, Lateral view of an admedian fin spine fused to a pinnal plate fragment (V27434.3). f, Transverse virtual slice through V27434.3 shown in anterior view. g, Lateral view of an incomplete admedian fin spine fused to a fragment of pinnal plate (V27434.1). h, Virtual transverse section through V27434.1 in posterior view. i, Portion of basal wall of an admedian fin spine (V27434.4) sectioned along its long axis, apical to the left. j, Lateral view of two prepectoral spines fused to a partial pinnal plate (V27436.1). k, Vertical virtual slice through V27436.1 in ventral view. l, Lateral view of V27436.1 showing ventral pinnal plate lamina (downturned due to a post-mortem fracture). l, Horizontal virtual slice through the prepectoral spines of V27436.1. Arrowheads point to anterior. admfs, admedian fin spine; al, ascending lamina; bp, basal plate; cb, cellular bone; pfs, pectoral fin spine; pi, pinnal plate; pps, prepectoral spines; s1–4, scales 1–4; sc, scale crown; vl, ventral lamina. Scale bars, 1 mm (a–c, e–h, j–l), 0.5 mm (d) and 0.2 mm (i).

Extended Data Fig. 5 Resorption features in the dermal skeleton of Fanjingshania renovata.

Volume renderings based on synchrotron X-ray tomography data (a–d, f–i), optical micrograph (e) and scanning electron micrograph (i). a, Trunk scale (V27435.10) with an anterior replacement odontode and ‘exploded view’ of the same specimen revealing the resorption surfaces in the scale crown and base. b, Basal view of an asymmetrical trunk scale (V27435.1) and the crown and base of the same specimen in crown aspect demonstrating absence of resorption surfaces in contrast to V27435.10. c, Transverse virtual slice through V27435.10 at the level of the replacement odontode. d, Transverse virtual slice through V27435.1 at the level of the primordial odontode. e, Longitudinally sectioned trunk scale (V27435.4) with an anterior resorption surface. f, A partially resorbed pinnal plate scale highlighted in a dermal shoulder girdle fragment (V27433.1, partial admedian fin spine fused to a fragment of a pinnal plate) shown in external (ventral) view. g, Horizontal virtual slice through the pinnal plate and fin spine wall of V27433.1. h, Vertical virtual slice through the pinnal plate and fin spine wall of V27433.1. i, Partially resorbed pinnal plate scale shown in (f–h) superimposed onto an isolated trunk scale (V27435. 27). Image of resorbed scale reflected and magnified 1.5x the scale in (i). ad, atubular dentine; admfs, admedian fin spine; bp, basal plate; cb, cellular bone; pi, pinnal plate; po, primary odontodes; ro, replacement odontode; rs, resorption surface; sb, scale base; sc, scale crown; so, secondary odontodes. Scale bars, 1 mm (a–d, f–i) and 0.5 mm (e).

Extended Data Fig. 6 Phylogenetic reconstructions of early gnathostomes based on a data matrix of 105 taxa and 292 characters.

a, 50 percent majority-rule and b, strict consensus trees from an analysis performed under parsimony optimality criteria (numbers in (a) and (b) represent 50 percent and above bootstrap support for internal nodes). c, 50 percent majority-rule consensus tree from a Bayesian phylogenetic analysis (numbers represent posterior probability values).

Extended Data Fig. 7 Life reconstruction of Fanjingshania renovata.

Original artwork by Fu Boyuan and Fu Baozhong published with their permission.

Extended Data Table 1 Relative abundance of Fanjingshania dermoskeletal elements

Supplementary information

Supplementary Information

Details regarding horizon and locality; specimen descriptions; remarks on the dermoskeletal characters of Fanjingshania; a list of characters; Supplementary Table 1 and Supplementary References. It also contains descriptions for Supplementary Data 1–8, which are available at Figshare (https://doi.org/10.6084/m9.figshare.20366838.v1).

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Andreev, P.S., Sansom, I.J., Li, Q. et al. Spiny chondrichthyan from the lower Silurian of South China. Nature 609, 969–974 (2022). https://doi.org/10.1038/s41586-022-05233-8

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