Devonian arthrodire embryos and the origin of internal fertilization in vertebrates

Devonian arthrodire embryos and the origin of internal fertilization in vertebrates

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ABSTRACT Evidence of reproductive biology is extremely rare in the fossil record. Recently the first known embryos were discovered within the Placodermi1, an extinct class of armoured fish,


indicating a viviparous mode of reproduction in a vertebrate group outside the crown-group Gnathostomata (Chondrichthyes and Osteichthyes). These embryos were found in ptyctodontids, a small


group of placoderms phylogenetically basal to the largest group, the Arthrodira2,3. Here we report the discovery of embryos in the Arthrodira inside specimens of _Incisoscutum ritchiei_


from the Upper Devonian Gogo Formation of Western Australia4 (approximately 380 million years ago), providing the first evidence, to our knowledge, for reproduction using internal


fertilization in this diverse group. We show that _Incisoscutum_ and some phyllolepid arthrodires possessed pelvic girdles with long basipterygia that articulated distally with an additional


cartilaginous element or series, as in chondrichthyans, indicating that the pelvic fin was used in copulation. As homology between similar pelvic girdle skeletal structures in


ptyctodontids, arthrodires and chondrichthyans is difficult to reconcile in the light of current phylogenies of lower gnathostomes2,3,5, we explain these similarities as being most likely


due to convergence (homoplasy). These new finds confirm that reproduction by internal fertilization and viviparity was much more widespread in the earliest gnathostomes than had been


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SPAWNING WITH GAMETE RELEASE FROM BODY RUPTURES DURING REPRODUCTION OF _XENOTURBELLA BOCKI_ Article Open access 17 February 2023 REFERENCES * Long, J. A., Trinajstic, K., Young, G. C. &


Senden, T. Live birth in the Devonian period. _Nature_ 453, 650–652 (2008) Article  ADS  CAS  Google Scholar  * Goujet, D. & Young, G. C. in _Recent Advances in the Origin and Early


Radiation of Vertebrates_ (eds Arratia, G., Wilson, M. V. H. & Cloutier, R.) 109–126 (Dr Freiderich Pfeil, 2004) Google Scholar  * Brazeau, M. D. The braincase and jaws of a Devonian


‘acanthodian’ and modern gnathostome origins. _Nature_ 457, 305–308 (2009) Article  ADS  CAS  Google Scholar  * Dennis, K. & Miles, R. S. A pachyosteomorph arthrodire from Gogo, Western


Australia. _Zool. J. Linn. Soc._ 73, 213–258 (1981) Article  Google Scholar  * Janvier, P. in _Major Events in Early Vertebrate Evolution_ (ed. Ahlberg, P. E.) 172–186 (Taylor & Francis,


2001) Google Scholar  * Wourms, J. Viviparity: The maternal-fetal relationship in fishes. _Am. Zool._ 21, 473–515 (1981) Article  Google Scholar  * Blackburn, D. in _Viviparous Fishes_ (eds


Grier, H. & Uribe, M.) 287–301 (New Life Publications, 2005) Google Scholar  * López, J. A., Ryburn, J. A., Fedrigo, O. & Naylor, G. J. P. Phylogeny of sharks of the family


Triakidae (Carcharhiniformes) and its implications for the evolution of carcharhiniform placental viviparity. _Mol. Phyl. Evol._ 40, 50–60 (2006) Article  Google Scholar  * Mank, J. E. &


Avise, J. C. Supertree analyses of the roles of viviparity and habitat in the atherinomorph fishes. _Eur. Soc. Evol. Biol_ 19, 734–740 (2006) Article  CAS  Google Scholar  * Webb, S. et al.


Molecular phylogeny of the livebearing Goodeidae (Cyprinidontiformes). _Mol. Phyl. Evol._ 30, 527–544 (2004) Article  CAS  Google Scholar  * Lee, M. Y. S. & Shine, R. Reanalysis of the


evolution of viviparity and egg-guarding in squamate reptiles. _Herpetologica_ 55, 538–549 (1998) Google Scholar  * Davidson, R. & Trewin, N. Unusual preservation of the internal organs


of acanthodian and actinopterygian fish in the Middle Devonian of Scotland. _Scot. J. Geol._ 41, 129–134 (2005) Article  Google Scholar  * Long, J. A. _Swimming in Stone—The Amazing Gogo


Fossils of the Kimberley_ 320 (Fremantle Arts Centre Press, 2006) Google Scholar  * Trewin, N. H. Palaeoecology and sedimentology of the Achanarras fish bed of the Middle Old Red Sandstone,


Scotland. _Trans. R. Soc. Edinb. Earth Sci._ 77, 21–46 (1986) Article  Google Scholar  * Maxwell, E. E. & Caldwell, M. W. First record of live birth in Cretaceous ichthyosaurs: closing


an 80 million year gap. _Proc. R. Soc. Lond. B_ 270 (suppl.). S104–S107 (2003) Article  Google Scholar  * Chiappe, L. M., Cordorniu, L., Greller-Tinner, G. & Rivarola, D. Argentinian


unhatched pterosaur fossil. _Nature_ 432, 571–572 (2004) Article  ADS  CAS  Google Scholar  * Young, G. C. Antiarchs (placoderm fishes) from the Devonian Aztec Siltstone, southern Victoria


Land, Antarctica. _Palaeontographica_ A202, 1–125 (1988) Google Scholar  * Upeniece, I. The unique fossil assemblage from the Lode Quarry (Upper Devonian, Latvia). _Mitt. Mus. Natkd. Berl.


Geowiss_ 4, 101–119 (2001) Google Scholar  * Long, J. A. New phyllolepid placoderms from the Late Devonian of Victoria, Australia and the relationships of the group. _Proc. Linn. Soc. NSW_


107, 263–308 (1984) Google Scholar  * Ritchie, A. _Cowralepis_, a new genus of phyllolepid fish (Pisces, Placodermi) from the Late Middle Devonian of New South Wales, Australia. _Proc. Linn.


Soc. NSW_ 126, 215–259 (2005) Google Scholar  * Sewertzoff, A. N. Development of the pelvic fins of _Acipenser ruthenus_. New data for the theory of the paired fins of fishes. _J. Morph.


Physiol._ 41, 547–579 (1926) Article  Google Scholar  * Bürgin, T. Reproduction in the Middle Triassic actinopterygians; complex fin structures and evidence of viviparity in fossil fishes.


_Zool. J. Linn. Soc._ 100, 379–391 (1990) Article  Google Scholar  * Schultze, H.-P. Early growth stages in coelacanth fishes. _Nat. New Biol._ 236, 90–91 (1972) Article  CAS  Google Scholar


  * Lund, R. Viviparity and interuterine feeding in a new holocephalan fish from the Lower Carboniferous of Montana. _Science_ 209, 697–699 (1980) Article  ADS  CAS  Google Scholar  * Miles,


R. S. Observations on the ptyctodont fish, _Rhamphodopsis_ Watson. _Zool. J. Linn. Soc._ 47, 99–120 (1967) Article  Google Scholar  * Young, G. C. The relationships of placoderm fishes.


_Zool. J. Linn. Soc._ 88, 1–57 (1986) Article  MathSciNet  Google Scholar  * Stensiö, E. A. Anatomical Studies on the Arthrodiran Head. _Kungl. Svenska Vetensk. Akad. Handl._ 4 (9) 2, 1–419


(1963) Download references ACKNOWLEDGEMENTS We thank M. Brazeau for access to his manuscript before publication, A. Ritchie for discussions, and G. Young and G. Edgecombe for reviewing the


manuscript. We also thank K. Bifield for the photograph of WAM 04.10.02, and the Centre for Microscopy, Characterisation and Analysis, UWA, for microscopy assistance. J.A.L. and K.T. are


supported by Australian Research Council Discovery grants. AUTHOR CONTRIBUTIONS All three authors contributed equally to the description of the new embryos and arthrodire pelvic structures,


and to the general discussion; J.A.L. provided new data on Victorian phyllolepids. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Museum Victoria, PO Box 666, Melbourne 3001, Victoria,


Australia , John A. Long * Research School of Earth Sciences, The Australian National University, Canberra 2600, Australian Capital Territory, Australia , John A. Long * School of


Geosciences, Monash University, Clayton 3800, Victoria, Australia , John A. Long * School of Earth and Geographical Sciences, The University of Western Australia, Perth 6009, Western


Australia, Australia , Kate Trinajstic * Natural History Museum, Cromwell Road, London SW7 5BD, UK , Zerina Johanson Authors * John A. Long View author publications You can also search for


this author inPubMed Google Scholar * Kate Trinajstic View author publications You can also search for this author inPubMed Google Scholar * Zerina Johanson View author publications You can


also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to John A. Long. SUPPLEMENTARY INFORMATION SUPPLEMENTARY INFORMATION This file contains Supplementary


Notes, Supplementary References and Supplementary Figures 1-3 with Legends (PDF 3355 kb) POWERPOINT SLIDES POWERPOINT SLIDE FOR FIG. 1 POWERPOINT SLIDE FOR FIG. 2 POWERPOINT SLIDE FOR FIG. 3


RIGHTS AND PERMISSIONS Reprints and permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Long, J., Trinajstic, K. & Johanson, Z. Devonian arthrodire embryos and the origin of internal


fertilization in vertebrates. _Nature_ 457, 1124–1127 (2009). https://doi.org/10.1038/nature07732 Download citation * Received: 12 November 2008 * Accepted: 17 December 2008 * Issue Date: 26


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