Abstract
So far, the Palaeozoic fossil jawless vertebrates have not provided any direct evidence for the organization of the gills, apart from vague impressions—supposedly left by gill filaments—on the bony surface of the gill chamber in certain armoured forms or ‘ostracoderms’ (for example, osteostracans and heterostracans)1. The latter are currently regarded as more closely related to the living jawed vertebrates (crown gnathostomes) than to the living jawless vertebrates (hagfish and lampreys, or cyclostomes)2,3. Here we report the first direct evidence for the position of the gill filaments—possibly supported by gill rays—enclosed by gill pouches in a 370-million year (Myr)-old jawless vertebrate, Endeiolepis, from the Late Devonian fossil fish site of Miguasha, Quebec, Canada. This extinct jawless fish has much the same gill organization as living lampreys, although it possesses an unusually large number of gill pouches—a condition unlike that in any extant vertebrates and that raises questions about gill development4. Endeiolepis is currently regarded as a close relative of anaspids3, a group of 410–430-Myr-old ‘ostracoderms’. Assuming that current vertebrate phylogeny is correct, this discovery demonstrates that pouches enclosing the gills are primitive for vertebrates, but have been subsequently lost in jawed vertebrates.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Janvier, P. Early Vertebrates (Oxford Univ. Press, Oxford, 1996)
Donoghue, P. C. J., Forey, P. L. & Aldridge, R. J. Conodont affinity and chordate phylogeny. Biol. Rev. 75, 191–251 (2000)
Donoghue, P. C. J. & Smith, M. P. The anatomy of Turinia pagei (Powrie) and the phylogenetic status of the Thelodonti. Trans. R. Soc. Edinb. (Earth Sci.) 92, 15–37 (2001)
Janvier, P. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Cloutier, R. & Wilson, M. V. H.) 29–52 (Dr Friedrich Pfeil, Munich, 2004)
Arsenault, M., Desbiens, S., Janvier, P. & Kerr, J. in Recent Advances in the Origin and Early Radiation of Vertebrates (eds Arratia, G., Cloutier, R. & Wilson, M. V. H.) 439–454 (Dr Friedrich Pfeil, Munich, 2004)
Stensiö, E. A. A new anaspid from the Upper Devonian of Scaumenac Bay in Canada, with remarks on the other anaspids. K. Svenska Vetensk. Akad. Handl. 18, 1–25 (1939)
Arsenault, M. & Janvier, P. in Early Vertebrates and Related Problems of Evolutionary Biology (eds Chang, M.-M., Liu, Y.-H. & Zhang, G.-R.) 19–37 (Science Press, Beijing, 1991)
Janvier, P. in Devonian Fishes and Plants of Miguasha, Québec, Canada (eds Schultze, H. P. & Cloutier, R.) 134–140 (Dr Friedrich Pfeil, Munich, 1996)
Janvier, P. & Arsenault, M. Calcification of early vertebrate cartilage. Nature 417, 609 (2002)
Marinelli, W. & Strenger, A. Vergleichende Anatomie und Morphologie der Wirbeltiere. 1. Lampetra fluviatilis (L.) (Franz Deuticke, Vienna, 1954)
Jarvik, E. Basic Structure and Evolution of Vertebrates Vol. 1 (Academic, London, 1980)
Maisey, J. G. Visceral skeleton and musculature of a Late Devonian shark. J. Vert. Paleont. 9, 174–190 (1989)
Hou, H. G., Aldridge, R. J., Siveter, D. J., Siveter, D. J. & Feng, X.-H. New evidence on the anatomy and phylogeny of the earliest vertebrates. Proc. R. Soc. Lond. B 269, 1865–1869 (2002)
Mallatt, J. & Chen, J. Fossil sister-group of craniates: predicted and found. J. Morphol. 258, 1–31 (2003)
Watson, D. M. S. A consideration of ostracoderms. Phil. Trans. R. Soc. Lond. B 238, 1–15 (1954)
Stensiö, E. Traité de Paléontologie Vol. 4 (Masson, Paris, 1964)
Mallatt, J. Ventilation and the origin of jawed vertebrates: a new mouth. Zool. J. Linn. Soc. 117, 329–404 (1996)
Massabuau, J. C. From low arterial- to low tissue-oxygenation strategy. An evolutionary theory. Respir. Physiol. 128, 299–315 (2001)
Prichonnet, G., Di Vergilio, M. & Chidiac, Y. in Devonian Fishes and Plants of Miguasha, Québec, Canada (eds Schultze, H. P. & Cloutier, R.) 23–36 (Dr Friedrich Pfeil, Munich, 1996)
Graham, A. & Smith, A. Patterning the pharyngeal arches. Bioessays 23, 54–61 (2001)
Quinlan, R., Martin, P. & Graham, A. The role of actin cables in directing the morphogenesis of the pharyngeal pouches. Development 131, 593–599 (2004)
Donoghue, P. C. J. & Purnell, M. A. Genome duplication, extinction and vertebrate evolution. Trends Ecol. Evol. 20, 312–319 (2005)
Acknowledgements
Author Contributions J.A.W. discovered the specimen MHNM 01-154 described herein; the other authors have contributed equally to the article.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.
Supplementary information
Supplementary Notes
This file contains a discussion on synonymy, taphonomy and interpretation of the gill pouches of Euphanerops and Endeiolepis. (DOC 23 kb)
Supplementary Figure 1
This illustrates the organization and orientation of the gill pouch natural casts in Endeiolepis. (PDF 90 kb)
Supplementary Figure 2
A simplified phylogenetic tree of euchordates, showing the nodes where gill pouches and gill rays may have appeared and then disappeared. (PDF 134 kb)
Rights and permissions
About this article
Cite this article
Janvier, P., Desbiens, S., Willett, J. et al. Lamprey-like gills in a gnathostome-related Devonian jawless vertebrate. Nature 440, 1183–1185 (2006). https://doi.org/10.1038/nature04471
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature04471
This article is cited by
-
Mode of reduction in the number of pharyngeal segments within the sarcopterygians
Zoological Letters (2016)
-
Facts and fancies about early fossil chordates and vertebrates
Nature (2015)
-
A primitive fish from the Cambrian of North America
Nature (2014)
-
Diversity and Evolution of Body Size in Fishes
Evolutionary Biology (2012)
-
The Miguasha Fossil-Fish-Lagerstätte: a consequence of the Devonian land–sea interactions
Palaeobiodiversity and Palaeoenvironments (2011)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.