Galeaspid anatomy and the origin of vertebrate paired appendages (original) (raw)

Data availability

All data analysed in this paper are available in the Article, Extended Data Figs. 1–7 and Supplementary Data 1–5. The nomenclatural acts in this publication have been registered at ZooBank (LSID: urn:lsid:zoobank.org:pub: BD7A6929-33DE-4DDD-ADE2-51A67A489E1B).

Code availability

The R script used for the analyses is available as Supplementary Data 5.

References

  1. Larouche, O., Zelditch, M. L. & Cloutier, R. Fin modules: an evolutionary perspective on appendage disparity in basal vertebrates. BMC Biol. 15, 32 (2017).
    Article PubMed PubMed Central Google Scholar
  2. Tulenko, F. J. et al. Body wall development in lamprey and a new perspective on the origin of vertebrate paired fins. Proc. Natl Acad. Sci. USA 110, 11899–11904 (2013).
    Article ADS CAS PubMed PubMed Central Google Scholar
  3. Donoghue, P. C. J. & Keating, J. N. Early vertebrate evolution. Palaeontology 57, 879–893 (2014).
    Article Google Scholar
  4. Wilson, M. V. H., Hanke, G. F. & Märss, T. in Major Transitions in Vertebrate Evolution (eds Anderson, J. S. & Sues, H.-D.) 122–149 (Indiana Univ. Press, 2007).
  5. Coates, M. I. The origin of vertebrate limbs. Development 1994, 169–180 (1994).
    Article Google Scholar
  6. Mivart, S. G. Notes on the fins of elasmobranchs, with considerations on the nature and homologues of vertebrate limbs. Trans. Zool. Soc. Lond. 10, 439–484 (1879).
    Article Google Scholar
  7. Thacher, J. K. Median and Paired Fins: A Contribution to the History of Vertebrate Limbs Vol. 3 (Connecticut Academy of Arts and Sciences, 1877).
  8. Balfour, F. M. On the development of the skeleton of the paired fins of Elasmobranchii, considered in relation to its bearings on the nature of the limbs of the vertebrata. Proc. Zool. Soc. Lond. 49, 656–670 (1881).
    Article Google Scholar
  9. Goodrich, E. S. Notes on the development, structure, and origin of the median and paired fins of fish. Q. J. Microsc. Sci. 50, 333–376 (1906).
    Google Scholar
  10. Westoll, T. S. (ed.) in Studies on Fossil Vertebrates 180–211 (Athlone, 1958).
  11. Gai, Z. K., Donoghue, P. C. J., Zhu, M., Janvier, P. & Stampanoni, M. Fossil jawless fish from China foreshadows early jawed vertebrate anatomy. Nature 476, 324–327 (2011).
    Article ADS CAS PubMed Google Scholar
  12. Liu, Y. H. Lower Devonian agnathans of Yunnan and Sichuan. Vert. Palasiat. 13, 202–216 (1975).
    Google Scholar
  13. Pan, J. New Galeapsids (Agnatha) from the Silurian and Devonian of China (Geological Publishing House, 1992).
  14. Pan, J. & Chen, L. Z. Geraspididae, a new family of Polybranchiaspidida (Agnatha) from Silurian of northern Anhui. Vert. Palasiat. 31, 225–230 (1993).
    Google Scholar
  15. Stensiö, E. A. A new anaspid from the Upper Devonian of Scaumenac Bay in Canada, with remarks on other anaspids. K. Svenska Vet. Akad. Handl. 18, 1–25 (1939).
    Google Scholar
  16. Ritchie, A. New light on the morphology of the Norwegian Anaspida. Skr. Norske Vidensk. Akad. Oslo 14, 1–35 (1964).
    Google Scholar
  17. Sansom, R. S., Freedman, K., Gabbott, S. E., Aldridge, R. J. & Purnell, M. A. Taphonomy and affinity of an enigmatic Silurian vertebrate, Jamoytius kerwoodi White. Palaeontology 53, 1393–1409 (2010).
    Article Google Scholar
  18. Sansom, R. S., Gabbott, S. E. & Purnell, M. A. Unusual anal fin in a Devonian jawless vertebrate reveals complex origins of paired appendages. Biol. Lett. 9, 20130002 (2013).
    Article PubMed PubMed Central Google Scholar
  19. Stensiö, E. A. The Cephalaspids of Great Britain (British Museum, 1932).
  20. Heintz, A. Cephalaspida from Downtonian of Norway. Skr. Norske Vidensk. Akad. Oslo 1939, 1–119 (1939).
    Google Scholar
  21. Ritchie, A. Ateleaspis tessellata Traquair, a non‐cornuate cephalaspid from the Upper Silurian of Scotland. Zool. J. Linn. Soc. 47, 69–81 (1967).
    Article Google Scholar
  22. Coates, M. I. in Developmental Patterning of the Vertebrate Limb (eds Hinchliffe, J. et al.) 325–337 (Plenum, 1991).
  23. Larouche, O., Zelditch, M. L. & Cloutier, R. A critical appraisal of appendage disparity and homology in fishes. Fish Fish. 20, 1138–1175 (2019).
    Article Google Scholar
  24. Keating, J. N. & Donoghue, P. C. J. Histology and affinity of anaspids, and the early evolution of the vertebrate dermal skeleton. Proc. R. Soc. B 283, 20152917 (2016).
    Article PubMed PubMed Central Google Scholar
  25. Miyashita, T., Gess, R. W., Tietjen, K. & Coates, M. I. Non-ammocoete larvae of Palaeozoic stem lampreys. Nature 591, 408–412 (2021).
    Article ADS CAS PubMed Google Scholar
  26. Gans, C. & Northcutt, R. G. Neural crest and the origin of the vertebrates: a new head. Science 220, 268–274 (1983).
    Article ADS CAS PubMed Google Scholar
  27. Northcutt, R. G. & Gans, C. The genesis of neural crest and epidermal placodes: a reinterpretation of vertebrate origins. Q. Rev. Biol. 58, 1–28 (1983).
    Article CAS PubMed Google Scholar
  28. Coates, M. Hox genes, fin folds and symmetry. Nature 364, 195–196 (1993).
    Article ADS Google Scholar
  29. Coates, M. I. The evolution of paired fins. Theory Biosci. 122, 266–287 (2003).
    Article Google Scholar
  30. Shubin, N., Tabin, C. & Carroll, S. Fossils, genes and the evolution of animal limbs. Nature 388, 639–648 (1997).
    Article ADS CAS PubMed Google Scholar
  31. Pieretti, J. et al. Organogenesis in deep time: a problem in genomics, development, and paleontology. Proc. Natl Acad. Sci. USA 112, 4871–4876 (2015).
    Article ADS CAS PubMed PubMed Central Google Scholar
  32. Yonei‐Tamura, S. et al. Competent stripes for diverse positions of limbs/fins in gnathostome embryos. Evol. Dev. 10, 737–745 (2008).
    Article PubMed Google Scholar
  33. Romer, A. S. Vertebrate evolution. Copeia 1962, 223–227 (1962).
    Article Google Scholar
  34. Johanson, Z. Evolution of paired fins and the lateral somitic frontier. J. Exp. Zool. 314B, 347–352 (2010).
    Article Google Scholar
  35. Sordino, P., van der Hoeven, F. & Duboule, D. Hox gene expression in teleost fins and the origin of vertebrate digits. Nature 375, 678–681 (1995).
    Article ADS CAS PubMed Google Scholar
  36. Neumann, C. J., Grandel, H., Gaffield, W., Schulte-Merker, S. & Nüsslein-Volhard, C. Transient establishment of anteroposterior polarity in the zebrafish pectoral fin bud in the absence of sonic hedgehog activity. Development 126, 4817–4826 (1999).
    Article CAS PubMed Google Scholar
  37. Ahn, D. G., Kourakis, M. J., Rohde, L. A., Silver, L. M. & Ho, R. K. T-box gene tbx5 is essential for formation of the pectoral limb bud. Nature 417, 754–758 (2002).
    Article ADS CAS PubMed Google Scholar
  38. Freitas, R., Zhang, G. J. & Cohn, M. J. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442, 1033–1037 (2006).
    Article ADS CAS PubMed Google Scholar
  39. Dahn, R. D., Davis, M. C., Pappano, W. N. & Shubin, N. H. Sonic hedgehog function in chondrichthyan fins and the evolution of appendage patterning. Nature 445, 311–314 (2007).
    Article ADS CAS PubMed Google Scholar
  40. Letelier, J. et al. A conserved Shh _cis_-regulatory module highlights a common developmental origin of unpaired and paired fins. Nat. Genet. 50, 504–509 (2018).
    Article CAS PubMed PubMed Central Google Scholar
  41. Abe, G. & Ota, K. G. Evolutionary developmental transition from median to paired morphology of vertebrate fins: perspectives from twin-tail goldfish. Dev. Biol. 427, 251–257 (2017).
    Article CAS PubMed Google Scholar
  42. Freitas, R., Gomez-Skarmeta, J. L. & Rodrigues, P. N. New frontiers in the evolution of fin development. J. Exp. Zool. 322, 540–552 (2014).
    Article Google Scholar
  43. Rong, J. et al. Silurian integrative stratigraphy and timescale of China. Sci. China Earth Sci. 62, 89–111 (2019).
    Article ADS CAS Google Scholar
  44. Wang, Y. et al. On the late Silurian stratigraphy of the Zhangjiajie area, Hunan province, with a discussion on age of the Xiaoxi Formation. J. Strat. 34, 113–126 (2010).
    Google Scholar
  45. Wang, Y. et al. Discovery of the late Silurian Xiaoxi Formation in the Xiushan area, Chongqing city, China, and the revision of the Huixingshao Formation. J. Strat. 35, 113–121 (2011).
    Google Scholar
  46. Zhao, W.-J. & Zhu, M. Siluro-Devonian vertebrate biostratigraphy and biogeography of China. Palaeoworld 19, 4–26 (2010).
    Article Google Scholar
  47. Zhao, W. et al. A review of Silurian fishes from north-western Hunan, China and related biostratigraphy. Acta Geol. Pol. 68, 475–486 (2018).
    Google Scholar
  48. Rahman, I. A. & Lautenschlager, S. Applications of three-dimensional box modeling to paleontological functional analysis. Palaeontol. Soc. Pap. 22, 119–132 (2016).
    Article Google Scholar
  49. Videler, J. J. Fish Swimming (Springer Science & Business Media, 2012).
  50. Lowndes, A. G. XXXII.—Density of fishes: some notes on the swimming of fish to be correlated with density, sinking factor and load carried. Ann. Mag. Nat. Hist. 8, 241–256 (1955).
    Article Google Scholar
  51. Botella, H. Microictiolitos del Devónico Inferior de Nigüella (Cordillera Ibérica); Consideraciones Paleobiológicas e Hidrodinámicas de Condrictios y Agnatos Primitivos (Univ. València, 2005).
  52. Randle, E. & Sansom, R. S. Phylogenetic relationships of the ‘higher heterostracans’ (Heterostraci: Pteraspidiformes and Cyathaspididae), extinct jawless vertebrates. Zool. J. Linn. Soc. 181, 910–926 (2017).
    Article Google Scholar
  53. Wilson, M. V. H. & Märss, T. Thelodont phylogeny revisited, with inclusion of key scale-based taxa. Est. J. Earth Sci. 58, 297–310 (2009).
    Article Google Scholar
  54. Sansom, R. S. Phylogeny, classification and character polarity of the Osteostraci (Vertebrata). J. Syst. Palaeontol. 7, 95–115 (2009).
    Article Google Scholar
  55. Lu, J., Giles, S., Friedman, M., den Blaauwen, J. L. & Zhu, M. The oldest actinopterygian highlights the cryptic early history of the hyperdiverse ray-finned fishes. Curr. Biol. 26, 1602–1608 (2016).
    Article CAS PubMed Google Scholar
  56. Dornburg, A., Townsend, J. P., Friedman, M. & Near, T. J. Phylogenetic informativeness reconciles ray-finned fish molecular divergence times. BMC Evol. Biol. 14, 169 (2014).
    Article PubMed PubMed Central Google Scholar
  57. Delsuc, F. et al. A phylogenomic framework and timescale for comparative studies of tunicates. BMC Biol. 16, 39 (2018).
    Article PubMed PubMed Central Google Scholar
  58. Bapst, D. W. paleotree: an R package for paleontological and phylogenetic analyses of evolution. Methods Ecol. Evol. 3, 803–807 (2012).
    Article Google Scholar
  59. Louca, S. & Doebeli, M. Efficient comparative phylogenetics on large trees. Bioinformatics 34, 1053–1055 (2018).
    Article CAS PubMed Google Scholar
  60. Bell, M. A. & Lloyd, G. T. strap: an R package for plotting phylogenies against stratigraphy and assessing their stratigraphic congruence. Paleontology 58, 379–389 (2015).
  61. Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
    Article Google Scholar

Download references

Acknowledgements

We thank R. Freitas for helpful discussion on mechanisms of fin development, R. Zhao, X. Shan, X. Lin, L. Peng, L. Jia, Q. Wang, Q. Wen, Q. Rao, Y. Zhao, Q. Xue, Z. Xian, X. Meng, Y. Luo, Y. Yan, H. Wang, Q. Deng, J. Xiong, C. H. Xiong, C. Y. Xiong, J. Zhang, Y. Chen, Z. Zhou and L. Nie for the fieldwork assistance, J. Xiong for the specimen preparation, J. Rong and Y. Wang for discussion on stratrigraphy, A. Shi for drawing the interpretive illustrations, Q. Zheng for drawing the artistic life restoration, D. Yang for generating the 3D reconstruction, L. Peng and L. Jia for photographing the fossil and X. Jin for scanning electron microscopy imaging. This work was supported by the National Natural Science Foundation of China (42130209, 41972006, 42072026), the Key Research Program of Frontier Sciences, CAS (QYZDB-SSW-DQC040), the Strategic Priority Research Program of CAS (XDA19050102, XDB26000000), the National Program for support of Topnotch Young Professionals and Mee-mann Chang Academician Workstation of Yunnan province. P.C.J.D. was funded by the Natural Environment Research Council (NE/G016623/1, NE/P013678/1), the Biotechnology and Biological Sciences Research Council (BB/T012773/1) and the Leverhulme Trust (RF-2022-167). H.G.F. was funded by the European Commission through a Marie Skłodowska-Curie Research Fellowship (H2020-MSCA-IF-2018-839636). J.N.K was funded by ERC grant no. 788203 (INNOVATION).

Author information

Authors and Affiliations

  1. Key CAS Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences (CAS), Beijing, China
    Zhikun Gai, Qiang Li, Junqing Wang & Min Zhu
  2. CAS Center for Excellence in Life and Paleoenvironment, Beijing, China
    Zhikun Gai & Min Zhu
  3. University of Chinese Academy of Sciences, Beijing, China
    Zhikun Gai & Min Zhu
  4. Research Center of Natural History and Culture, Qujing Normal University, Qujing, China
    Qiang Li
  5. Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK
    Humberto G. Ferrón, Joseph N. Keating & Philip C. J. Donoghue
  6. Instituto Cavanilles de Biodiversidad i Biología Evolutiva, Universitat de València, Valencia, Spain
    Humberto G. Ferrón

Authors

  1. Zhikun Gai
    You can also search for this author inPubMed Google Scholar
  2. Qiang Li
    You can also search for this author inPubMed Google Scholar
  3. Humberto G. Ferrón
    You can also search for this author inPubMed Google Scholar
  4. Joseph N. Keating
    You can also search for this author inPubMed Google Scholar
  5. Junqing Wang
    You can also search for this author inPubMed Google Scholar
  6. Philip C. J. Donoghue
    You can also search for this author inPubMed Google Scholar
  7. Min Zhu
    You can also search for this author inPubMed Google Scholar

Contributions

M.Z. and P.C.J.D. conceived the project. M.Z., J.W., Z.G. and Q.L. conducted the fieldwork, fossil preparation and fossil curation. Z.G., P.C.J.D., M.Z. and H.G.F. contributed to fossil interpretation and wrote the manuscript. H.G.F. and P.C.J.D. conducted computational fluid-dynamics analyses. J.N.K. undertook the ancestral-state reconstruction analyses. All authors edited and approved the manuscript.

Corresponding authors

Correspondence toPhilip C. J. Donoghue or Min Zhu.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature thanks John Dabiri, Matt Friedman and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Geological setting of Tujiaaspis vividus.

a, Maps of the two fossil localities in Xiangxi and Xiushan Tujia and Miao Autonomous Prefecture (County). b, Horizon of the fish-bearing Huixingshao Formation.

Extended Data Fig. 2 The postcranial anatomy of Tujiaaspis vividus.

uncoated counterpart (b) with an interpretative drawing (c), the paratype, IVPP V27410 (right, in dorsal view) and V27411 (left, in ventral view). d, Close-up of the tail magnified from the box region of (b), in lateral view. e, Close-up of the tail of the holotype, IVPP V26668, in lateral view. Abbreviations as in Figs. 1, 2.

Extended Data Fig. 3 The postcranial anatomy of another new form of Eugaleaspidiformes from the same locality and horizon with the holotype of Tujiaaspis vividus.

a, b. Photographs of specimen IVPP V26669 uncoated (a) and coated (b) by a layer of ammonium chloride sublimate, respectively, in ventral view, Abbreviations as in Figs. 1, 2.

Extended Data Fig. 5 3D virtual restoration of Tujiaaspis vividus.

a, In dorsal view. b, In ventral view. c, Close-up of the anterior two dorsal fins. d, Close-up of the tail, (c,d), in lateral view.

Extended Data Fig. 6 Computed Fluid Dynamics analysis of Tujiaaspis vividus.

a, 3D model including ventrolateral ridges in dorsal (dr), ventral (vn), lateral (lt) and frontal (fr) views. b, c, d, Computational domain (b), mesh overlying the models without (upper) and with (lower) ventrolateral fins in dorsal (dr) and ventral (vn) views, and general mesh (c) employed in the CFD analysis noting the different boundary conditions (in, inlet; ou, outlet; ns, non-slip; ss, slip symmetry), refinement volume (rf) and inflation layers (if).

Extended Data Fig. 7 The artistic life restoration of Tujiaaspis vividus (Picture credit Qiuyang Zheng).

The ventral side of the body in Tujiaaspis vividus manifests a pair of continuous pectoral-pelvic lateral fins which our Computed Fluid Dynamic experiments demonstrate passively generate lift to escape from predators such as sea scorpions to escape from predators such as sea scorpions.

Supplementary information

Reporting Summary

Supplementary Data 1

Results of all CFD simulations performed with the models of Tujiaaspis with and without ventrolateral ridges (VL), including details about the mesh and the calculations of the Reynolds number, apparent weight, drag and lift coefficients and lift-to-drag ratios.

Supplementary Data 2

Results of independence tests for mesh size, domain size and refinement volume.

Supplementary Data 3

Character data and stratigraphic data used in the ancestral state estimation analyses.

Supplementary Data 4

Results of the ancestral state estimation analyses.

Supplementary Data 5

R script used in the ancestral state estimation analyses.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Cite this article

Gai, Z., Li, Q., Ferrón, H.G. et al. Galeaspid anatomy and the origin of vertebrate paired appendages.Nature 609, 959–963 (2022). https://doi.org/10.1038/s41586-022-04897-6

Download citation