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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

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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 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 display- Cartilaginous fishes, which are commonly placed in the ing this trait, whereas oviparity occurs in 43% of all living monophyletic group , are the oldest living chondrichthyan including all skates (Rajiformes), group of jawed vertebrates with a fossil record consisting all bullhead sharks (Heterodontiformes), some nurse sharks of isolated ‘-like’ scales extending back to the Middle (Orectolobiformes), most catsharks (Carcharhiniformes) 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 , 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 (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 et al. (2011). or fructifications, stems of algae, or sometimes even as coprolites (e.g. Hollick 1893; Crookall 1932; Fischer & chondrichthyan egg capsules have been distinguished, Kogan 2008). This state of misinterpretation lasted until the presenting a range of species-specific morphological traits. end of the nineteenth century when the accurate taxonomic Eight egg capsule morphotypes are known from the identity of several fossil egg capsules types belonging to fossil record, with five types exclusively represented by cartilaginous fishes was established (Renault & Zeiller fossil finds. The very incompletely known Pennsylvanian 1888). Nevertheless it took decades before this attribu- Scapellites Pruvost, 1922 does not provide information tion was widely accepted (Fischer & Kogan 2008), and for the majority of the coded morphological traits here knowledge of the morphological and taphonomic variety, and subsequently was removed from the analysis. Conse- and geographical and stratigraphical distributions of chon- quently, nine morphotypes were included in our analysis drichthyan egg capsules and their potential producers has (Fig. 2). increased significantly since then. However, whether the

Downloaded by [American Museum of Natural History] at 12:43 08 November 2013 morphology of egg capsules of chondrichthyans and basal 1. Palaeoxyris Brongniart, 1828 (also known by its gnathostomes yields phylogenetic signals has not yet been synonym Spirangium) has a three-fold division. It scrutinized. Here, we present an analysis of the phylogenetic consists of a fusiform body tapering gradually at the signals conserved in both recent and fossil egg capsules of posterior end into a pointed beak and at the ante- chondrichthyans, with comments on the possible placoderm rior end into a long and slender pedicle. Its features egg capsule from the Devonian presented by Chaloner et al. are ≥3 spirally twisted membranous collarettes (1980) and an evolutionary scenario of chondrichthyan egg (= flanges; spirally twisted on the pedicles in pre- capsule development. specimens, and with parallel arrangement in Mesozoic ones) with smooth surfaces, and equipped with coiled tendrils at the apex of the beak (Fig. 2A; Egg capsule morphotypes Fischer et al. 2011). Twenty-six valid species of Middle Mississippian to Late age were The nomenclature used for egg capsule morphology is described from predominantly freshwater to brackish provided in Figure 1. To date, 10 distinct morphotypes of deposits of Europe, Russia, Asia, Australia and the Egg capsule morphology in chondrichthyan fishes 3 Downloaded by [American Museum of Natural History] at 12:43 08 November 2013

Figure 2. Schematic drawings of egg capsule morphotypes. A, Palaeoxyris, Palaeozoic type left, Mesozoic type right; B, Vetacapsula; C, Crookallia; D, Fayolia; E, Callorhinchidae; F, Rhinochimaeridae; G, Chimaeridae; H, putative Placodermi (according to Chaloner et al. 1980); I, Rajoidae; J, Scyliorhinidae; K, Orectolobidae; L, Heterodontidae. Figures not to scale, and arranged with the posterior end upwards. 4 J. Fischer et al.

USA. Hybodontiform sharks are considered to be the 2005) and the USA (Bock 1949) has been repeat- most probable producers (Crookall 1932; Zidek 1976; edly questioned (Obruchev 1967; Stahl 1999); such Muller¨ 1978; Fischer et al. 2010, 2011). specimens probably should be assigned to pteropods 2. Vetacapsula Mackie, 1867 shows a three-fold divi- (Chaloner et al. 1980). sion similar to Palaeoxyris but is more bulb-shaped 6. Extant batoid capsules are characterized by a with a large number of longitudinal ribs on the surface dorsoventrally flattened, rectangular body outline, and a prominent middle ridge (Fig. 2B; Pruvost 1919; two smooth, small, lateral collarettes, and inwardly Crookall 1930). The presence of collarettes has not oriented pairs of horns at the anterior and poste- yet been documented. Twelve species were described rior ends with tendril-like tips and aprons between from Pennsylvanian (Bashkirian) paralic strata of (Fig. 2I). The anterior horns are shorter than the poste- Europe and the USA. The producer remains ambigu- rior ones (Concha et al. 2009). Attachment tendrils ous (Fischer & Kogan 2008). exist in a few forms (Mabragana˜ et al. 2011). Fossil 3. Crookallia Chabakov, 1949 contains specimens batoid egg capsules of three well-known and one formerly assigned to Vetacapsula and which were later unnamed species combined in the Rajitheca morpho- separated due to the lack of a median ridge, presence type by Steininger (1966) range from Late to of only few longitudinal ribs, and a less bulb-shaped Miocene within shallow marine deposits of Central body (Moysey 1913; Crookall 1930; Chabakov 1949). Europe (Fischer-Oster 1867; Peyer 1928; Kubacska One specimen (Stainier 1938) exhibits two moder- 1932; Steininger 1966). ate lateral collarettes (Fig. 2C) comparable to the 7. Scyliorhinid (catshark) egg capsules are dorsoven- collarettes in capsules of extant chimaeras (Fig. 2G), trally flattened and have a vase-shaped fusiform body except for the smooth surface. Five species are known with a slightly constricted waist, two smooth, reduced from Pennsylvanian (Bashkirian) paralic strata of lateral collarettes, possible aprons at both ends, as well Belgium, the Netherlands and Ukraine. The producer as anterior and posterior pairs of horns. The poste- of this egg capsule morphotype is also ambiguous, as rior horns are strongly curved in an inward direction for Vetacapsula (Fischer & Kogan 2008). However, and cross each other (Fig. 2J). The horns merge into Stainier (1938) briefly mentioned one find of Ve t a - coiled tendrils (Ebert et al. 2006; Concha et al. 2010). capsula close to a cochliodont tooth remain, a puta- Several specimens display straight longitudinal stria- tive representative of the extinct holocephalan family tions (Mabragana˜ et al. 2011). Fossil remains of the Helodontidae (Patterson 1965). type Scyliorhinotheca (Kiel et al. 2013) are reported 4. Fayolia Renault & Zeiller, 1884 is spirally twisted from Late Eocene deep marine sediments of the USA like Palaeoxyris and displays tendrils on the beak. (Treude et al. 2011). However, it differs from Palaeoxyris in its shape, 8. Capsules of Orectolobiformes (carpetsharks) exhibit which is more cylindrical and ‘screw-like’ due to a bulbous body with two smooth, small lateral two smooth collarettes, in the reduced shaping of collarettes along the edges, aprons at both ends, and pedicle and beak, and its collarette-parallel scar-lines two curved and twisted horns with tendrils at each (Fig. 2D; Crookall 1928; Fischer et al. 2011). The end. One horn is elongated, while the other one is fossil record of the 16 species ranges from Late Devo- shorter or even largely reduced (Fig. 2K). The attach- nian to Middle in predominantly freshwater ment tendrils form a mass extending from the lateral successions of Europe, Asia and the USA. Xenacan- edges (Caruso & Bor 2007). To date no fossil remains thiform sharks are considered the most likely produc- of this capsule type are known although orectolobid ers (Renault & Zeiller 1888; Pruvost 1919; Schneider sharks date back to the (Underwood

Downloaded by [American Museum of Natural History] at 12:43 08 November 2013 & Reichel 1989). 2006; Kriwet & Klug 2008; Kriwet et al. 2009). 5. Extant holocephalan egg capsules of callorhinchids, 9. Heterodontid egg capsules are characterized by a rhinochimaerids and chimaerids show a bulbous bulky body with possible slightly constricted waist central fusiform body accompanied by two ribbed and narrow and broad ends. The body is surrounded lateral collarettes of different size that taper towards by two large, spirally twisted collarettes with smooth each end with the anterior end forming an elongate tail surfaces that may merge into coiled tendrils at the (Fig. 2E–G; Didier 1995). Eleven fossil species have narrow end (Fig. 2L; Smith 1942; Rodda & Seymour been recorded from shallow marine strata of Germany, 2008). In one species, the collarettes merge into horn- Russia, USA and Canada. They date back to the like structures at both ends (Compagno et al. 2005). Late Triassic (Obruchev 1967; Stahl 1999), except for Heterodontiform sharks are known back to the Early one doubtful record from the Pennsylvanian (Brown Jurassic (Underwood 2006; Kriwet 2008), whereas 1950). A holocephalan affinity of Lower Triassic the characteristic ‘screw-like’ eggs have not yet been small butterfly-like remains from Iran (Dashtban found in the fossil record. Egg capsule morphology in chondrichthyan fishes 5

Cladistic analysis >3.5 and display a tripartition into a short posterior section (beak), a central body and a tapered and pointed anterior A parsimony analysis was performed with Winclada version portion (pedicle/tail). The length ratio of the latter to the 1.00.08 (Nixon 1999) and analysed with NONA version 2.0 central body is >1, and the length ratio of the beak to the (Goloboff 1999). All characters were treated as unordered central body is ≤1. The ribbed lateral collarette is broad and unweighted. A heuristic tree search was conducted and more-or-less parallel to the body axis. The surface of using 10,000 replicates. Bootstrap and jackknife analyses the egg capsule is ribbed without any defined middle ridge. were conducted with 10,000 replicates each (holding 10 Next to Callorhinchidae and Rhinochimaeridae, two trees per replicate) to evaluate node supports. The dataset monophyletic groupings are recognized. The first group additionally was analysed with TNT version 1.1 (Goloboff consists of the crookallian, vetacapsulan and chimaerid et al. 2008) (1000 replicates, holding 10 trees per replicate) capsule types. This topology is present in all analyses, to confirm the results of the first bootstrap analysis. All providing strong support for the arrangement. These egg analyses are based on the dataset given in Online Supple- capsule types are characterized by the lack of a broad lateral mentary Material Appendices 1 and 2. collarette. Crookallia is resolved with moderate support as sister taxon of Chimaeridae and Vetacapsula. Chimaeridae displays the closest morphological similarities to Vetacap- Results sula, with a support of 64% and 61%, respectively. Both egg capsule types share a median ridge on the body. The phylogenetic analysis resulted in a single most parsi- The second group encompasses the elasmobranch egg monious hypothesis of egg capsule relationships based on capsule types. This arrangement is supported by 60% and morphological traits. According to this analysis, the egg 59%, respectively, in our analyses. Within this group, the capsule morphotypes of two of the three extant holocepha- fossil capsule types of Palaeoxyris and Fayolia cluster next lan lineages, Callorhinchidae and Rhinochimaeridae, clus- to all neoselachian types (living sharks, rays and skates) ter at the base of all other egg capsules (Fig. 3). These (Fig. 3). This sister-group relationship, however, is not two families are separated from the other morphotypes by strongly supported (1% for all analyses). more than 50% of both analysed values. The callorhinchid The neoselachian clade is very well supported by both and rhinochimaerid egg capsule types share an aspect ratio values of more than 80%. All neoselachian egg capsules (length/maximum diameter without collarette and horns) of have an aspect ratio (length/maximum diameter without collarette and horns) of ≤3.5 and show no tripartition. Within Neoselachii, the egg capsule type of Heterodon- tus exemplifies the basal egg type morphology (Fig. 3). The sister grouping of orectolobiform and batomorph egg capsules is supported by bootstrap as well as jackknife values of more than 60% (Fig. 3). Both types have aprons at their anterior and posterior edges. The capsule morphology of cat sharks, Scyliorhinidae, forms the basal sister group of the latter arrangement. This is supported by values of more than 80%. Scyliorhinids are the only neoselachians with egg capsules displaying ribbed surfaces.

Downloaded by [American Museum of Natural History] at 12:43 08 November 2013 Discussion

Assignment of fossil egg capsule morphotypes to potential producers has been controversial ever since their origin was initially proposed (e.g. Renault & Zeiller 1888; Moysey 1910; Pruvost 1919; Schneider & Reichel 1989). This is mainly due to the rare co-occurrences of egg Figure 3. Strict consensus interrelationships of fossil and recent capsules and skeletal remains, as well as the complete egg capsule type morphologies. Single most parsimonious heuris- lack of capsules containing embryos, or capsules preserved tic tree (length 23, CI 82, RI 88) obtained in a cladistic analysis of 15 characters for 11 taxa. Filled circles represent autapomor- within body fossils of gravid female chondrichthyans phies and unfilled convergent apomorphies. Support values are (Fischer & Kogan 2008). Consequently, taxonomic shown beneath the branches (bootstrap values followed by jack- identification is mainly based on coincidences in strati- knife values) and the character numbers above. graphical ranges of certain fossil chondrichthyan groups 6 J. Fischer et al.

and capsule types, as well as rare co-occurrences of to chimaeroid capsules but with spirally twisted collarettes capsules and their likely producers within the same rock and posterior attachment fibres like those of the recent basal unit (Crookall 1932; Zidek 1976; Fischer et al. 2010, 2011). neoselachian Heterodontus (Daber 1969; Bottcher¨ McGhee (1982) tried to establish closer links between fossil 2010). It appears that twisted collarettes and elongated and recent egg capsules using their allometric properties. attachment structures are basal characteristics for elas- In our study, the egg morphotypes of Crookallia and Ve t a - mobranch egg capsule morphotypes (Fig. 5). However, capsula cluster together with those of Chimaeridae in one the eggs of neoselachians display additional differentia- branch. This arrangement has been previously proposed tion into varied morphotypes. The capsules of all extant by some authors (Moysey 1910; Chabakov 1949; Daber representatives have attachment fibres and/or anterior and 1969), whereas others rejected any chimaeroid affiliation posterior horns as well as aprons. Moreover, in most for these fossil egg capsules (Pruvost 1919; Crookall 1932; species of derived neoselachians the collarette is extremely McGhee 1982). However, both assumptions were based reduced into delicate, lateral seams. Accordingly, the bull- on superficial comparisons rather than employing robust head shark, Heterodontus, displaying a broad and twisted methodological approaches like those used in this study. collarette, represents the most basal type within neoselachi- Our results show that the two fossil types share ribbed ans (Fig. 5). The origin and timing of the development capsule surfaces and reduced lateral collarettes, as found of unique neoselachian egg capsule characters at present in living chimaerids. The branch comprising this group- remains ambiguous. It also remains unclear whether the egg ing is not well supported, whereas closer morphologi- capsule morphotype of heterodontids represents an ancient, cal relationships between chimaerid and Vetacapsula egg ctencanthiform or hybodontiform character, or whether it is capsules is indicated by the presence of a middle ridge on a ‘reinvented’ apomorphic trait of neoselachians. Interest- their surface. This relationship is supported by a bootstrap ingly, orectolobiforms and batoids share similar egg capsule value of more than 60%. Interestingly, the egg capsules morphotypes although both belong to two distinct super- of Crookallia and Vetacapsula are about 200 million years orders, Batomorphii and Galeomorphii, respectively. The older than the oldest known fossil chimaerid egg, which significance of this remains ambiguous for the moment comes from the (Albian) (Stahl 1999). and probably can only be solved when egg capsules of Although our results suggest closer relationships between stem group neoselachians, such as the Synechodontiformes, these, a common ancestral morphotype characterized by which is sister to all living neoselachians (Klug 2009), are a reduced lateral collarette is not supported by the known recognized. fossil record, resulting in a rather long ghost lineage (Fig. 4). The sister relationships between the egg capsule morpho- types of Crookallia plus Vetacapsula with those of the holo- The ancestral gnathostome egg capsule type cephalans indicate that the lateral collarette was seemingly reduced several times independently during holocephalan The egg capsule morphotypes of the two extant holocepha- evolution. This is supported by Callorhinchidae being the lan families, Callorhinchidae and Rhinochimaeridae, share basal sister taxon of Chimaeridae and Rhinochimaeridae a broad, lateral, ribbed collarette, which closely encircles based on morphological and genetic features of extant the egg body, and both types cluster basally to all other chon- forms (e.g. Maisey 1986; Didier 1995; Stahl 1999; Inoue drichthyan egg capsule types. This is supported by bootstrap et al. 2010; Licht et al. 2012). and jackknife values of more than 50%. The callorhinchid Indirect evidence of the holocephalan nature of the Ve t a - egg capsule type is seemingly the basal sister morphotype capsula capsule type is provided by a single capsule found of Rhinochimaeridae. closely associated with the teeth of a putative member of the Remarkably, the presumed placoderm egg morphotype

Downloaded by [American Museum of Natural History] at 12:43 08 November 2013 extinct holocephalan family Helodontidae, which is closely from the Devonian of South Africa, which is used as related to Chimaeridae (Stainier 1938). Any final conclu- outgroup in this study, resembles that of callorhinchids to sion about their relationships and frequency of collarette some extent (Fig. 2H; Chaloner et al. 1980). Although holo- reduction within Holocephali is rendered impossible as long cephalans are known as fossils in the Early to Middle Devo- as there is no direct evidence of their producers. Neverthe- nian (Stahl 1999; Coates & Sequira 2001; Ginter & Piechota less, our results are the first indication that crookalian and 2004; Darras et al. 2008), and molecular clock analyses of vetacapsulan morphotypes might have closer relationships extant specimens dates them back to the Early Devonian with holocephalans rather than with elasmobranchs. This (Licht et al. 2012), they are completely absent from the egg assumption is also supported by the fact that egg capsule capsule-bearing strata of the Bokkeveld Series of South morphotypes for which the producers are known are all Africa. Arthrodire remains, however, are very common elasmobranchs and form a distinct monophyletic group. and are found closely associated with egg capsules. There- The stratigraphically older elasmobranch egg capsule fore, Chaloner et al. (1980) stated that the eggs may be lineage consisting of Fayolia and Palaeoxyris (Fig. 4) is those of a placoderm. Accordingly, we hypothesize that the characterized by spindle-shaped egg capsule bodies similar putative arthrodiran/placoderm egg capsule morphology Egg capsule morphology in chondrichthyan fishes 7 Downloaded by [American Museum of Natural History] at 12:43 08 November 2013

Figure 4. Stratigraphical distribution of egg capsule morphotypes and their potential producers. The chronostratigraphical scale is adopted from the International Chronostratigraphic Chart 2012 (www.stratigraphy.org). The grey column represents the known stratigraphical occurrence of the chondrichthyan producer groups; the black bar indicates the first occurrence of the egg capsule morphotype in the fossil record. Stratigraphical ranges of possible producers are based on Duffin (2001), Delsate & Candoni (2002), Underwood (2006), Darras et al. (2008), Rees (2008) and Turner & Burrow (2011). 8 J. Fischer et al. Downloaded by [American Museum of Natural History] at 12:43 08 November 2013

Figure 5. Summary of chondrichthyan egg capsule phylogeny based on the cladistic analysis and stratigraphical ranges. Egg capsule morphotypes: A, callorhinchid or placoderm; B, Rhinochimaeridae; C, Chimaeridae, Vetacapsula, Crookallia; D, Fayolia; E, Palaeoxyris; F, Heterodontidae; G, extant sharks and rays. Figures not to scale. Egg capsule morphology in chondrichthyan fishes 9

closely resembled the callorhinchid and probably rhinochi- References maerid morphotypes. A broad, lateral, ribbed collarette seems to be a plesiomorphic character of gnathostome egg Ahlberg, P., Trinajstic, K., Johanson, Z. & Long, J. 2009. Pelvic capsules (Fig. 5). Dean (1912) already assumed that the claspers confirm chondrichthyan-like internal fertilization in ancestral egg capsule morphology in chimeroids was char- arthrodires. Nature, 460, 888–889. Bock, W. 1949. Triassic chimaeroid egg capsules from the acterized by a broad, lateral collarette. Conneticut Valley. Journal of Paleontology, 23, 515–517. A ‘horny’ egg capsule was used as strong evidence Botella, H., Valenzuela-R´ıos, J. I. & Mart´ınez-Perez,´ C. 2009. for a close relationship between Holocephali and Elasmo- Tooth replacement rates in early chondrichthyans: a qualita- branchii (e.g. Dean 1906). Reproductive mode includes tive approach. 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C. 2009. Egg capsules produced by F. Spindler (Freiberg) under the supervision of of the raspthorn sandskate, Psammobatis scobina (Philippi, the authors. We appreciate the constructive comments and 1857) (Rajiformes, Rajidae). Revista de Biolog´ıa Marina y critical evaluation of R. K. Carr (River Forest), R. Bottcher¨ Oceanograf´ıa, 44(1), 253–256. (Stuttgart) and Associate Editor Z. Johanson (London), as Coates, M. I. & Sequeira, S. E. K. 2001. Early sharks and primitive gnathostome interrelationships. Pp. 223–240 in P. well as the linguistic assistance of A. J. Lerner (Albu- E. Ahlberg (ed.) Major Events in Early Vertebrate Evolution. querque). This research was financed by a German Science Palaeontology, phylogeny, genetics and development.Taylor Foundation grant to JF (DFG-SCHN 408/14–1). & Francis, London. Crookall, R. 1928. The genus Fayolia. The Naturalist, 1928, 325–332. Supplementary material Crookall, R. 1930. 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