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The origin of the internal nostril of tetrapods
Naturevolume 432, pages94–97 (2004)Cite this article
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Abstract
The choana, a unique ‘internal nostril’ opening from the nasal sac into the roof of the mouth, is a key part of the tetrapod (land vertebrate) respiratory system. It was the first component of the tetrapod body plan to evolve, well before the origin of limbs, and is therefore crucial to our understanding of the beginning of the fish–tetrapod transition. However, there is no consensus on the origin of the choana despite decades of heated debate1,2,3,4,5,6,7,8,9; some have claimed that it represents a palatally displaced external nostril4,6, but others have argued that this is implausible because it implies breaking and rejoining the maxillary–premaxillary dental arcade and the maxillary branch of nerve V2,6. The fossil record has not resolved the dispute, because the choana is fully developed in known tetrapod stem-group members8,10,11. Here we present new material ofKenichthys, a 395-million-year-old fossil fish from China12,13,14, that provides direct evidence for the origin of the choana and establishes its homology: it is indeed a displaced posterior external nostril that, during a brief transitional stage illustrated byKenichthys, separated the maxilla from the premaxilla.
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References
Jarvik, E. On the structure of the snout of crossopterygians and lower gnathostomes in general.Zool. Bidrag Uppsala21, 235–675 (1942)
Panchen, A. L. The nostrils of choanate fishes and early tetrapods.Biol. Rev.42, 374–420 (1967)
Jarvik, E.Basic Structure and Evolution of VertebratesVol. 1 (Academic, London, 1980)
Rosen, D. E. et al. Lungfishes, tetrapods, paleontology, and plesiomorphy.Bull. Am. Mus. Nat. Hist.167, 157–276 (1981)
Maisey, J. G. Heads and tails: a chordate phylogeny.Cladistics2, 201–256 (1986)
Panchen, A. L. & Smithson, T. R. Character diagnosis, fossils and the origin of tetrapods.Biol. Rev.62, 341–438 (1987)
Forey, P. L. inThe Biology and Evolution of Lungfishes (eds Bemis, W. E., Burggren, W. W. & Kemp, N.) 39–74 (Alan R. Liss, New York, 1987)
Schultze, H.-P. inOrigins of the Higher Groups of Tetrapods: Controversy and Consensus (eds Schultze, H.-P. & Trueb, L.) 29–67 (Cornell Univ. Press, Ithaca, 1991)
Ahlberg, P. E. A re-examination of sarcopterygian interrelationships, with special reference to the Porolepiformes.Zool. J. Linn. Soc.103, 241–287 (1991)
Long, J. A., Campbell, K. S. W. & Barwick, R. E. Osteology and functional morphology of the osteolepiform fishGogonasus andrewsae Long, 1985, from the Upper Devonian Gogo Formation, Western Australia.Rec. W. Aust. Mus. Suppl.53, 1–89 (1997)
Ahlberg, P. E. & Johanson, Z. Osteolepiforms and the ancestry of tetrapods.Nature395, 792–794 (1998)
Chang, M. M. & Zhu, M. A new Middle Devonian osteolepidid from Qujing, Yunnan.Mem. Assoc. Australas. Palaeontol.15, 183–198 (1993)
Zhu, M. & Wang, J.-Q. On the Early–Middle Devonian boundary in Qujing, Yunnan.Acta Stratigr. Sin.20, 58–63 (1996)
Chang, M. M. & Yu, X. B. Reexamination of the relationship of Middle Devonian osteolepids—fossil characters and their interpretations.Am. Mus. Novitat.3189, 1–20 (1997)
Lebedev, O. A. Morphology of a new osteolepidid fish from Russia.Bull. Mus. Natl Hist. Nat. Paris17, 287–341 (1995)
Chang, M. M. .The Braincase of Youngolepis, a Lower Devonian Crossopterygian from Yunnan, South-western China Thesis, Stockholm Univ. (1982)
Tong-Dzuy, T. & Janvier, P. Les Vertébrés du Dévonien inférieur du Bac Bo oriental (provinces de Bac Thaï et Lang Son, Viêt Nam).Bull. Mus. Natl Hist. Nat. Paris12, 143–223 (1990)
Johanson, Z. & Ahlberg, P. E. A complete primitive rhizodont from Australia.Nature394, 569–572 (1998)
Long, J. A. A new rhizodontiform fish from the Early Carboniferous of Victoria, Australia, with remarks on the phylogenetic position of the group.J. Vert. Paleontol.9, 1–17 (1989)
Clement, G. Evidence for lack of choanae in the Porolepiformes.J. Vert. Paleontol.21, 795–802 (2001)
Ahlberg, P. E., Clack, J. A. & Lukťevičs, E. Rapid braincase evolution betweenPanderichthys and the earliest tetrapods.Nature381, 61–64 (1996)
Chang, M. M. & Yu, X. B. Structure and phylogenetic significance ofDiabolichthys speratus gen. et sp. nov., a new dipnoan-like form from the early Devonian of southeastern Yunnan, China.Proc. Linn. Soc. N.S.W.107, 171–184 (1984)
Zhu, M., Yu, X. B. & Ahlberg, P. E. A primitive sarcopterygian fish with an eyestalk.Nature410, 81–84 (2001)
Bemis, W. E. & Grande, L. Early development of the actinopterygian head. I. External development and staging of the paddlefishPolyodon spathula.J. Morphol.213, 47–83 (1992)
Ashique, A. M., Fu, K. & Richman, J. M. Endogenous bone morphogenetic proteins regulate outgrowth and epithelial survival during avian lip fusion.Development129, 4647–4660 (2002)
Hu, D. & Helms, J. The role ofsonic hedgehog in normal and abnormal craniofacial morphogenesis.Development126, 4873–4884 (1999)
Zhang, Z. et al. Rescue of cleft palate inMsx1-deficient mice by transgenicBmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis.Development129, 4135–4146 (2002)
Acknowledgements
We thank M. M. Chang for advice and discussions, M. Yang for artwork, and X. Lu for specimen preparation. This work was supported by the Special Funds for Major State Basic Research Projects of China and the Chinese Foundation of Natural Sciences. P.E.A. thanks the Royal Society and Chinese Academy of Sciences for supporting his visit to Beijing in 2002 through their exchange programme.
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Authors and Affiliations
Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, P.O. Box 643, Beijing, 100044, China
Min Zhu
Department of Evolutionary Organismal Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18A, SE-752 36, Uppsala, Sweden
Per E. Ahlberg
- Min Zhu
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- Per E. Ahlberg
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Correspondence toMin Zhu.
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Supplementary information
Supplementary Methods
Summary of the phylogenetic analysis. The character list. The data matrix. The consensus tree of 18 most parsimonious trees. The analysis based on a new expanded character suite confirms thatKenichthys is the most basal member of the tetrapod stem group. (DOC 709 kb)
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Zhu, M., Ahlberg, P. The origin of the internal nostril of tetrapods.Nature432, 94–97 (2004). https://doi.org/10.1038/nature02843
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