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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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Contact customer support SIMILAR CONTENT BEING VIEWED BY OTHERS FIRST REPORT OF RECURRENT PARTHENOGENESIS AS AN ADAPTIVE REPRODUCTIVE STRATEGY IN THE ENDANGERED COMMON SMOOTH-HOUND SHARK
_MUSTELUS MUSTELUS_ Article Open access 26 July 2024 DISCOVERY OF A NEW MODE OF OVIPAROUS REPRODUCTION IN SHARKS AND ITS EVOLUTIONARY IMPLICATIONS Article Open access 23 July 2020 INDUCED
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
February 2009 * DOI: https://doi.org/10.1038/nature07732 SHARE THIS ARTICLE Anyone you share the following link with will be able to read this content: Get shareable link Sorry, a shareable
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