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Journal of Systematic Palaeontology Egg This article was downloaded by: [American Museum of Natural History] On: 08 November 2013, At: 12:43 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Systematic Palaeontology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tjsp20 Egg capsule morphology provides new information about the interrelationships of chondrichthyan fishes Jan Fischer a , Martin Licht a , Jürgen Kriwet b , Jörg W. Schneider a , Michael Buchwitz c & Peter Bartsch d a TU Bergakademie Freiberg, Geological Institute, Department of Palaeontology , Bernhard- von-Cotta Strasse 2 , 09599 Freiberg , Germany b Department of Palaeontology, Geozentrum , University of Vienna, Althanstrasse 14 , 1090 Vienna , Austria c Museum für Naturkunde Magdeburg , Otto-von-Guericke Strasse 68-73 , 39104 Magdeburg , Germany d Museum für Naturkunde Berlin , Invalidenstrasse 43 , 10115 Berlin , Germany Published online: 16 Apr 2013. To cite this article: Jan Fischer , Martin Licht , Jürgen Kriwet , Jörg W. Schneider , Michael Buchwitz & Peter Bartsch , Journal of Systematic Palaeontology (2013): Egg capsule morphology provides new information about the interrelationships of chondrichthyan fishes, Journal of Systematic Palaeontology, DOI: 10.1080/14772019.2012.762061 To link to this article: http://dx.doi.org/10.1080/14772019.2012.762061 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http:// www.tandfonline.com/page/terms-and-conditions Journal of Systematic Palaeontology, 2013 http://dx.doi.org/10.1080/14772019.2012.762061 Egg capsule morphology provides new information about the interrelationships of chondrichthyan fishes Jan Fischera∗, Martin Lichta,Jurgen¨ Kriwetb,Jorg¨ W. Schneidera, Michael Buchwitzc and Peter Bartschd aTU Bergakademie Freiberg, Geological Institute, Department of Palaeontology, Bernhard-von-Cotta Strasse 2, 09599 Freiberg, Germany; bDepartment of Palaeontology, Geozentrum, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria; cMuseum fur¨ Naturkunde Magdeburg, Otto-von-Guericke Strasse 68-73, 39104 Magdeburg, Germany; dMuseum fur¨ Naturkunde Berlin, Invalidenstrasse 43, 10115 Berlin, Germany (Received 5 July 2012; accepted 25 October 2012) Chondrichthyan egg capsules have been well known since the nineteenth century, although their systematic affinities have been controversial for much of this time. Currently, 10 chondrichthyan egg capsule morphotypes are distinguished but their phylogenetic signal and evolutionary traits have not yet been analysed. Here, we present an analysis of all extant and currently known fossil chondrichthyan egg capsule types, and use a purported placoderm egg capsule as an outgroup for character coding. The phylogenetic hypothesis based on discrete morphological characters indicates that the enigmatic Carboniferous egg capsule morphotypes Crookallia and Vetacapsula form a monophyletic group together with the egg capsule morphotype of chimaerid holocephalans. The elasmobranch egg capsule morphotypes are sister to the holocephalan types. Based on these results we conclude that the ancestral chondrichthyan egg capsule morphotype combined features of those found in callorhinchid holocephalans and placoderms. From this ancestral type, two lineages of chondrichthyan egg capsule morphotypes diverged leading towards the major modern egg capsule morphotypes. Keywords: Elasmobranchii; Holocephali; Placodermi; Vetacapsula; Crookallia; Orectolobiformes; oviparity Introduction reproduction in extant elasmobranchs, with four out of five orders of batomorphs and the majority of sharks display- Cartilaginous fishes, which are commonly placed in the ing this trait, whereas oviparity occurs in 43% of all living monophyletic group Chondrichthyes, are the oldest living chondrichthyan species including all skates (Rajiformes), group of jawed vertebrates with a fossil record consisting all bullhead sharks (Heterodontiformes), some nurse sharks of isolated ‘shark-like’ scales extending back to the Middle (Orectolobiformes), most catsharks (Carcharhiniformes) Ordovician some 465 million years ago (e.g. Sansom et al. (e.g. Compagno 1990; Dulvy & Reynolds 1997; Musick & 2012), whereas the oldest osteichthyan remains are from Ellis 2005; Wyffels 2009), and all Holocephali (Chimaeri- the Late Silurian, about 422 million years ago (Davis et al. formes) with the probable exception of a single Palaeozoic 2012). The oldest chondrichthyan teeth and skeletal remains taxon (Lund 1980; Grogan & Lund 2011). Oviparity are from the Early Devonian (e.g. Miller et al. 2003; Botella represents a yolk-based embryonic feeding (lecithotrophy) et al. 2009; Ginter et al. 2010). Thus, chondrichthyans are (Hamlett et al. 2005), in which the fertilized eggs are important for inferring evolutionary traits in basal gnathos- enclosed in large leathery, structurally complex capsules tomes. They exhibit an impressive diversity of reproductive composed of multilamellar collagen (e.g. Knupp & Squire Downloaded by [American Museum of Natural History] at 12:43 08 November 2013 modes within an ontogenetic system of direct development 1998; Hamlett et al. 2005). These capsules are eventu- and high maternal investment, and might be considered ally laid and deposited, either attached or unattached to an experimental system in which key transitions in early bottom structures. There, in the absence of maternal care, vertebrate evolution are illustrated. The oldest fossil holo- the capsules remain several months to more than a year cephalan record from the Early to Middle Devonian (e.g. until hatching of the juveniles (e.g. Dean 1906; Compagno Ginter & Piechota 2004; Darras et al. 2008) suggests an 1990). early divergence of chondrichthyans into two groups, Holo- Although oviparity is the less widespread reproductive cephali and Elasmobranchii, in the Palaeozoic. Fertilization mode in extant chondrichthyans, it is most likely the is internal with modified pelvic fins in all living and, as far as ancestral condition for cartilaginous fishes (Compagno can be ascertained, fossil chondrichthyans (Grogan & Lund 1990; Wourms & Lombardi 1992; Dulvy & Reynolds 1997; 2004), and reproduction is either oviparous (egg-laying) or Carrier et al. 2004). Accordingly, viviparity represents viviparous (live-bearing). Viviparity is the dominant type of the derived state, and is assumed to have evolved several ∗Corresponding author. Email: j.fi[email protected] C 2013 Natural History Museum 2 J. Fischer et al. times independently within elasmobranchs (e.g. Dulvy & Reynolds 1997; Carrier et al. 2004). Notwithstanding possi- ble ambiguities in fossil forms (e.g. Kohring 1995; Grogan & Lund 2004; Musick & Ellis 2005; Grogan & Lund 2011), the known stratigraphical record of oviparity indicated by different egg capsule morphotypes and pronounced spawning grounds in chondrichthyans extends further back (Late Devonian–Middle Mississippian: Stainier 1894; Schneider et al. 2005; Schneider & Fischer 2011) than recorded viviparity (Late Mississippian: Grogan & Lund 2011). Apart from the earlier occurrence of oviparity in the fossil record of chondrichthyans, it is the only known mode of reproduction in stem-group elasmobranchs (‘non-neoselachian elasmobranchs’), and has also been observed in placoderms and holocephalans (Stahl 1999; Ritchie 2005; Carr 2010a, b), whereas viviparity has only been registered twice in Palaeozoic basal gnathostomes (in placoderms: Long et al. 2008; and in holocephalans: Grogan & Lund 2011). Thus, from a phylogenetic perspec- tive, we consider it unlikely that ‘viviparity’ represents the state of reproduction in the common gnathosthomate ancestor. The fossil record of chondrichthyan egg capsules mirrors that of teeth and skeletal remains and extends back into the Late Devonian (Stainier 1894). Most fossil chondrichthyan egg capsules are from Palaeozoic strata. Their systematic Figure 1. Descriptive terminology of the egg capsule morphology affinities were long a source of controversy after the first after Crookall (1928), Didier (1995), Ebert et al. (2006), Caruso & discoveries in the nineteenth century. Early findings were Bor (2007), Wyffels (2009), Fischer et al. (2011) and Mabragana˜ often misinterpreted as plant organs such as inflorescences
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