JOURNAL OF MORPHOLOGY 275:586–596 (2014)

Dental Patterning in the Earliest Sharks: Implications for Tooth Evolution John G. Maisey,1* Susan Turner,2 Gavin J.P. Naylor,3 and Randall F. Miller4 1

Department of Vertebrate Paleontology, American Museum of Natural History, Central Park West, New York, New York 10024-5192 2 Department of Geosciences, Queensland Museum, Hendra, Queensland 4011, Australia 3 Hollings Marine Laboratory and Department of Biology, College of Charleston, South Carolina 29412 4 Steinhammer Palaeontology Laboratory, New Brunswick Museum, Saint John, New Brunswick E2K 1E5, Canada ABSTRACT Doliodus problematicus is the oldest known fossil shark-like fish with an almost intact dentition (Emsian, Lower Devonian, c. 397Ma). We provide a detailed description of the teeth and dentition in D. problematicus, based on tomographic analysis of NBMG 10127 (New Brunswick Museum, Canada). Comparisons with modern shark dentitions suggest that Doliodus was a ram-feeding predator with a dentition adapted to seizing and disabling prey. Doliodus provides several clues about the early evolution of the “shark-like” dentition in chondrichthyans and also raises new questions about the evolution of oral teeth in jawed vertebrates. As in modern sharks, teeth in Doliodus were replaced in a linguo-labial sequence within tooth families at fixed positions along the jaws (12–14 tooth families per jaw quadrant in NBMG 10127). Doliodus teeth were replaced much more slowly than in modern sharks. Nevertheless, its tooth formation was apparently as highly organized as in modern elasmobranchs, in which future tooth positions are indicated by synchronized expression of shh at fixed loci within the dental epithelium. Comparable dental arrays are absent in osteichthyans, placoderms, and many “acanthodians”; a “shark-like” dentition, therefore, may be a synapomorphy of chondrichthyans and gnathostomes such as Ptomacanthus. The upper anterior teeth in Doliodus were not attached to the palatoquadrates, but were instead supported by the ethmoid region of the prechordal basicranium, as in some other Paleozoic taxa (e.g., Triodus, Ptomacanthus). This suggests that the chondrichthyan dental lamina was originally associated with prechordal basicranial cartilage as well as jaw cartilage, and that the modern elasmobranch condition (in which the oral dentition is confined to the jaws) is phylogenetically advanced. Thus, oral tooth development in modern elasmobranchs does not provide a complete developmental model for chondrichthyans or gnathostomes. J. Morphol. 275:586–596, 2014. VC 2013 Wiley Periodicals, Inc.

occurs prior to the “lock in” that characterizes lineages and makes them both recognizable and definable. Oral teeth of living elasmobranchs (sharks and rays) display a characteristic development pattern that was evidently “locked in” very early in the evolution of chondrichthyans (the group of jawed vertebrates to which sharks, rays, and chimaeroid fishes belong). Until now, however, information about dental patterning in the earliest chondrichthyans came mostly from disarticulated fossil teeth. Herein, we describe the almost intact battery of oral teeth from Doliodus problematicus (Fig. 1; NBMG 10127, Lower Devonian, New Brunswick, Canada, 397 Ma; Kennedy and Gibling, 2011), the oldest known tooth-bearing shark with a relatively intact oral dentition (Miller et al., 2003; Turner, 2004). Tomographic scanning and segmentation analysis (or “digital preparation,” whereby structures are extracted virtually from surrounding rock) of NBMG 10127 provided a means to investigate and reconstruct its dentition (Fig. 2). Doliodus has been resolved cladistically as a stem chondrichthyan (i.e., below the evolutionary divergence of elasmobranchs and their holocephalan sister group; Pradel et al., 2011). Prior to the discovery of NBMG 10127,

Contract grant sponsor: Herbert and Evelyn Axelrod Research Chair in Paleoichthyology (American Museum of Natural History); Contract grant sponsor: National Science Foundation [Award No. 1036488 (Collaborative Research: Jaws and Backbone: Chondrichthyan Phylogeny and a Spine for the Vertebrate Tree of Life)]; Contract grant sponsor: George Frederic Matthew Research Grants [New Brunswick Museum (to J.G.M and S.T)].

KEY WORDS: chondrichthyan; teeth; evolution; Doliodus; Devonian

*Correspondence to: John G. Maisey; Department of Vertebrate Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024-5192. E-mail: [email protected]

INTRODUCTION

Received 18 September 2013; Revised 21 October 2013; Accepted 1 November 2013.

Vertebrates exhibit a wide range of development patterns. This is a reflection of the developmental flux and evolutionary experimentation that often

Published online 18 December 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jmor.20242

C 2013 WILEY PERIODICALS, INC. V

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stem holocephalans (e.g., Helodus, Debeerius; Patterson, 1965; Grogan and Lund, 2000) but are absent in modern chimaeroids, which instead possess large tritoral toothplates. MATERIAL AND METHODS

Fig. 1. Doliodus problematicus, NBMG 10127/1a, New Brunswick Museum. Ventral surface of the head. Scale bar 5 50 mm.

Doliodus was known only from isolated diplodont (bicuspid) teeth and short tooth whorls (Woodward, 1892; Traquair, 1893). This fossil provides evidence of highly regulated oral tooth development like that found in modern sharks, implying the presence of a shark-like dental lamina (an ectodermal fold, developed during embryogenesis, in which the oral teeth are formed). The fossil also reveals that, unlike in modern elasmobranchs, not all the upper teeth were attached to the jaws. This observation has profound implications for evolutionary-developmental models about vertebrate teeth, because it suggests that part of the dental lamina in Doliodus was not constrained to the mandibular arch. Teeth in modern sharks are arranged in a highly structured way, both to optimize biomechanical efficiency and to provide a system of continuous tooth replacement over the life of an individual. These teeth are arranged in files that physically move over the jaws from the inside (lingual) margin, where they begin their development flattened against the dental lamina. They then continue to develop while moving over the jaw toward the outside (labial) margin where they become erect and functional. This movement over the jaw from the inside to the outside continues until the teeth are no longer functional and are eventually shed. The teeth within each of these tooth files have a characteristic shape and size which differs incrementally (discretely in some species) from those in adjacent files. Herein, we refer to the set of distinct teeth in one of these characteristic tooth file trajectories as a “tooth family.” We also use the term “tooth whorl” to describe a tooth family in which successive teeth are fused together at their base (as in Doliodus). All modern elasmobranchs have their teeth arranged in families, but none possesses tooth whorls. Tooth families are also present in extinct

NBMG 10127/1a, New Brunswick Museum, Saint John, N.B., Canada, articulated head and trunk region of a complete individual in several blocks of matrix, “Atholville” beds, Campbellton Formation, Emsian, late Lower Devonian, Campbellton, N.B. (Fig. 1). Scanned 2007 at the University of Texas HighResolution X-ray computed tomography (CT) Facility, Austin, Texas, Scan parameters: 16 bit: 1024 3 1024 16-bit TIFF images. II, 200 kV, 0.13 mA, no filter, empty container wedge, no offset, slice thickness one line (5 0.0817 mm), Source-Object Detector Distance (S.O.D.) 235 mm, 2,200 views, two samples per view, interslice spacing one line (5 0.0817 mm), field of reconstruction 75 mm (maximum field of view 77.91953 mm), reconstruction offset 5,000, reconstruction scale 4,000. Image acquisition; 31 slices/ rotation, 25 slices/set. Raw sinogram data corrected using protocols “RK_SinoDeStreak” (default parameters) and “RK_SinoRingProcSimul” (parameters set: binwidth 5 21, best of 5 5 11). Reconstructed with beam hardening coefficients (0, 0.75, 0.1, and 0.05) 1,190 final slices. Scan analysis and segmentation protocols: Mimics 3 64 Version 14 (Materialize, Technologielaan 15, 3000 Leuven, Belgium); teeth were segmented individually and objects were saved as stereolithography (STL) files. Tooth images were screen-captured using Snagit software (TIFF 3 400%) and subsequently aligned using Photoshop. The holotype of Triodus sessilis Jordan, 1849 (MB f 1419.4, Museum fur Naturkunde, Berlin) from Lebach, Germany, was also examined as part of this investigation. The tooth terminology applied here is straightforward (uppers, lowers, left, and right). The unpaired upper teeth are termed mesial rather than symphyseal because they are not associated with any jaw symphysis.

Fig. 2. Doliodus problematicus, (A), (B), segmented upper and lower teeth in occlusion; (A) dorsal view, (B) ventral view. (C) oral view of separated upper and lower teeth. Ant, anterior; mes, mesial unpaired tooth family. Scale bars 5 10 mm.

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DESCRIPTION Initial tomographic analysis of NBMG 10127/1a revealed the teeth preserved in almost natural positions, with upper and lower teeth locked together (Figs. 1 and 2). It also confirmed that the dentition consists entirely of tooth whorls rather than separate teeth (Turner, 2004), each whorl corresponding to a single tooth row (5 tooth family) in a modern shark (Fig. 2A,B). An almost complete battery of lower teeth is present, but the upper dentition is less complete, with some whorls missing and others slightly displaced from their original position. As preserved, the teeth on one side of the head are crowded together, while those on the other are separated, suggesting there has been postmortem disturbance. This may account for the missing upper teeth (which could be preserved in adjacent pieces of matrix that were not scanned). The first paired upper teeth occlude with corresponding lower ones, but only the upper dentition has a mesial tooth row. The preliminary analysis revealed 12–14 tooth rows in each lower jaw quadrant and approximately the same number (allowing for missing teeth) of upper rows (Fig. 2C). The number of tooth families in Doliodus was presumably as consistent as in modern elasmobranchs, but this can only be confirmed when additional articulated specimens become available. This analysis also revealed that the palatoquadrates in NBMG 10127 are widely separated by the ethmoid region anteriorly and lack a median symphysis. However, the dentition forms a continuous buccal arcade, so that the upper mesial and first paired tooth families are located directly below the basicranium instead of on jaw cartilage (Maisey et al., 2009). A comparable arrangement is reported here in the Permian xenacanth Triodus sessilis (e.g., MB f 1419.4; Fig. 8C). A similar arrangement also occurs in the early Devonian (Lochkovian, c. 410Ma) shark-like “acanthodian” Ptomacanthus (Brazeau, 2009). At least part of the upper oral dentition in all these forms is, therefore, associated with cartilage presumed to belong to the prechordal part of the basicranium, rather than with the mandibular arch. Furthermore, the upper mesial and first paired tooth families in NBMG 10127 lie within a shallow transverse recess in the ethmoid region. This recess closely resembles the toothbearing oral groove of the palatoquadrates. Although the dental lamina is not preserved in the specimen, a thin, dark mineralized layer is present immediately beneath the teeth (Miller et al., 2003). This corresponds topographically to the basement membrane of modern elasmobranchs, to which the teeth are attached. The tooth-bearing recesses of the jaw cartilages and ethmoid region, thus, presumably all contained parts of the dental lamina. A more refined segmentation analysis was subsequently conducted, whereby each tooth whorl Journal of Morphology

was rendered individually. This permitted a detailed examination and comparison of each whorl and also allowed the entire preserved dentition to be reconstituted in lingual, labial, and other views (Figs. 3–5). These views illustrate the range of morphological variation found within the dentition, allowing comparison with modern elasmobranchs. Doliodus teeth differ in shape and size around the jaw, with a general diminution in size toward the back of the mouth. Anterior teeth have larger, more upright principal cusps and are wider than those farther posteriorly. The overall arrangement of teeth is, thus, very reminiscent of a modern shark dentition, with the obvious caveat that no modern elasmobranch has diplodont (bicuspid) teeth. In addition to this expected variation related to tooth position, other differences in tooth shape, size, and inclination of the main tooth cusps (heterodonty) were noted (summarized in Fig. 6); the upper and lower tooth morphology in Doliodus differs according to position along the jaw ramus (monognathic heterodonty), and between corresponding upper and lower teeth (dignathic heterodonty). Monognathic heterodonty in Doliodus includes variation in tooth size and shape. As shown in Figure 6, anterior lower teeth are much narrower than the lateral ones; for example, the widest lower tooth depicted here (LR8) is more than double the width of the first (LR1). Tooth width diminishes rapidly from position 9 posteriorly (especially after position 11). The diplodont principal cusps of the anterior teeth also diverge at a more acute angle than those farther posteriorly, mainly because of increased inclination of the posterior cusp (cf. UR1, UR8, UR10). Dignathic heterodonty in NBMG 10127 includes disparity in the width and robustness of corresponding upper and lower teeth (Fig. 6). For example, upper anterior teeth (e.g., UM, UR1) are 20–25% narrower than corresponding lower ones (LR1), whereas upper teeth farther posteriorly are 15–20% wider and considerably more robust than the lowers (e.g., UR5 and 8 versus LR5 and 8). Additionally, the posterior cusp in UR5–8 is inclined more posteriorly than in the corresponding lower teeth.

DISCUSSION Heterodonty in Early Shark-like Gnathostomes Although many of the teeth revealed by tomographic analysis of NBMG 10127 are complete, only the largest cusplets were revealed by the scan. It was unfortunately not possible to determine number of smaller cusplets accurately, although this could probably be accomplished at higher scan resolutions. The distribution of the largest cusplets nevertheless corroborates Turner’s

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Fig. 3. Doliodus problematicus teeth segmented from CT scan of NBMG 10127/1a in lingual view, with uppers and lowers digitally realigned into their approximate life positions. LL, lower left; LR, lower right; UL, upper left; UM, upper mesial (unpaired); UR, upper right. Paired tooth families are numbered sequentially from front to back. Scale bar 5 5 mm.

(2004) evidence for monognathic heterodonty in cusplet organization in Doliodus. Although no modern shark has diplodont teeth, the heterodonty seen in the dentition of Doliodus seems closest to that of modern sharks with “tearing-type” dentitions (e.g., the sand tiger shark, Carcharias taurus), suggesting that this ancient (397Ma) Devonian shark was an active predator, possibly analogous to modern ramfeeding sharks which typically accelerate and overtake their prey. A similar feeding strategy has also been postulated in the late Devonian Cladoselache (Williams, 2001). By contrast, Ptomacanthus has many more tooth families than Doliodus (its upper dentition has over 60; Brazeau, 2009), but these display virtually no heterodonty apart from a slight enlargement of the upper teeth in the ethmoid region (a “clutching-type” dentition, analogous to that of the modern suction-feeding bamboo shark, Chiloscyllium). Thus, a wide spectrum of functionally divergent feeding patterns is recognizable among the earliest gnathostomes with shark-like dentitions. Besides providing a means to establish the original position of isolated Doliodus tooth whorls in the jaw, the heterodonty revealed by NBMG 10127

is potentially useful for estimating the oral positions of isolated Devonian shark teeth (e.g., Leonodus, Portalodus, Aztecodus, Anareodus, Mamberodus; Mader, 1986; Long and Young, 1995; Hairapetian et al., 2008; Botella et al., 2009). For example, teeth from the Aztec Siltstone (Middle/ Upper Devonian, Givetian-Frasnian boundary) of Antarctica described by Long and Young (1995) include strongly asymmetrical forms (e.g., Aztecodus harmsenae and Anareodus statei) which could represent teeth from the distal part of the dentition, as well as larger, more symmetrical forms (e.g., Portalodus bradshawae) that could represent lateral teeth. Small intermediate cusplets are present between the main cusps in Doliodus (Traquair, 1893; Turner, 2004; Ginter et al., 2010), although these were not resolved clearly by the tomographic analysis. Based on an investigation of isolated Doliodus teeth, Turner (2004) found a correlation between tooth size and the number of cusplets, and suggested that smaller teeth (often with a single intermediate cusplet) pertained to the distal portion of the tooth series and that larger ones (usually with three or more cusplets) came from the main (lateral) part of the dentition. The Journal of Morphology

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Fig. 4. Doliodus problematicus teeth digitally realigned, in labial view. LL, lower left; LR, lower right; UL, upper left; UM, upper mesial (unpaired); UR, upper right. Paired tooth families are numbered sequentially from front to back. Scale bar 5 5 mm.

exposed teeth in NBMG 10127 generally corroborate that interpretation, but because many of them are broken it is not possible to provide quantitative data about cusplet variation. It is unclear whether tooth whorls are phylogenetically ancestral for gnathostomes, although similar oral tooth whorls are also present in some acanthodians and early osteichthyans (Reif, 1982; Janvier, 1996; Brazeau, 2009; Blais et al., 2011) and occasionally in Leonodus. Doliodus has been classified as an omalodontid (Ginter et al., 2010), but most omalodontids have separate rather than fused teeth. The oldest known chondrichthyan teeth (Leonodus carlsi Mader, 1986; Lower Devonian, Lockhovian-Pragian) are typically separate, but one pathological example was described by Botella (2006) of two teeth fused together at their base. Tooth Replacement in Doliodus The highly organized arrangement of oral teeth observed in Doliodus could only result from highly regulated developmental patterning. In modern elasmobranchs, successive teeth are added to the lingual (buccal) end of each tooth family (Tomes, 1876), while postfunctional teeth are typically shed from the labial end of each series (Breder, Journal of Morphology

1942). Studies of tooth development in modern fishes reveal that multirowed dentitions result from sequential iterative tooth initiation along well-defined mesial-to-distal and labial-to-lingual pathways (Smith, 2003; Huysseune and Witten, 2006; Fraser et al., 2006; Fraser et al., 2008). It has been suggested that diversity in vertebrate dentition patterns may have arisen at least in part through evolutionary changes in antagonistic interactions regulating these pathways across the tooth morphogenetic field (Zhang et al., 2009). Sonic hedgehog (shh) has been identified as a key regulator of tooth induction in the modern catshark, Scyliorhinus canicula (Smith et al., 2009), as well as in scale development (e.g., in zebrafish; Sire and Akimenko, 2004). The developmental expression of shh within catshark dental epithelium is confined to loci coincident with teeth at alternating iterative jaw positions, so that each locus establishes the precise sequential timing for development of successive replacement teeth within each tooth family. Nevertheless, alternating tooth succession in the catshark is but one of many replacement patterns recognized in modern elasmobranchs (Strasburg, 1963), at one extreme including the simultaneous replacement of teeth in every family (e.g., the cookiecutter shark, Isistius).

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Fig. 5. Doliodus problematicus teeth digitally realigned, in side view. LL, lower left; LR, lower right; UL, upper left; UM, upper mesial (unpaired); UR, upper right. Paired tooth families are numbered sequentially from front to back. Scale bar 5 5 mm.

In NBMG 10127, the largest and most lingually positioned tooth in each family often has an incomplete base and is only weakly attached to the lingual process of the preceding tooth. Moreover, this tooth is often misaligned with those in front (Fig. 7). The lingually positioned teeth are located deep within the dental recess of each jaw cartilage (Fig. 7E); that is, in a corresponding position to the dental lamina in modern elasmobranchs. These poorly attached, lingually positioned teeth are thus interpreted as the ontogenetically newest ones that were being added, in shark-like fashion, to the lingual end of each family. This interpretation is consistent with the presence of a tooth-forming dental lamina possessing odontogenic properties similar to that of modern elasmobranchs. Additionally, misaligned lingual teeth are present in many families (e.g., LL1, 3, 5, 6, 8; LR1, 3, 5, 11; UM, UR1, 5, 6; Figs. 3–5). If new teeth were being added to many whorls simultaneously in Doliodus, its tooth succession may have been regulated across adjacent tooth families and was perhaps even synchronized around the entire dental arcade. Tooth replacement in Doliodus was, therefore, apparently con-

strained by developmental expression patterns identical to those found in modern elasmobranchs, probably including synchronized developmental expression of shh at many loci within its dental epithelium. It is still unclear what regulates the position of tooth families within the dental lamina of living gnathostomes; field theories hypothesize the existence of morphogens traveling over the jaw and initiating teeth at successive loci at particular times, implying general control of the whole dentition; clone theories posit the existence of inhibition zones around individual teeth, implying that new teeth can form only when cells are released from inhibition (Huysseune and Witten, 2006). Whatever the case, Doliodus demonstrates that the evolution of “shark-like” tooth development occurred 400 Ma or even earlier. Successive teeth in NBMG 10127 show a marked increase in size labio-lingually, the largest teeth in each family being three or four times taller than the smallest (Figs. 5 and 7). Tooth width also increases labio-lingually along each family. In modern adult elasmobranchs, teeth are replaced rapidly (usually over a few weeks or months; Moss, 1972; Luer et al., 1990; Overstrom, Journal of Morphology

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Fig. 6. Doliodus problematicus, selected teeth from right side of mouth in NBMG 10127/1a, to illustrate monognathic and dignathic heterodonty. Scale bar 5 5 mm. UL, upper left; UM, upper mesial; UR, upper right. Monognathic heterodonty: (A) tooth width increases (files 1–8), then decreases posteriorly; (B) divergence angle of main cusps increases posteriorly, with progressively greater inclination of posterior cusp (anterior cusp remains relatively upright); and (C) height of posterior cusp increases relative to anterior cusp (files 1–9). Dignathic heterodonty: (A) upper anterior teeth are smaller than the corresponding lower teeth (at least to file 2; upper files 3 and 4 are unknown) and (B) some upper anterolateral teeth (files 5–8) are larger than the corresponding lower teeth.

1991) and successive teeth in adults are closely matched in shape and size. However, in juveniles, the ontogenetically earliest teeth may show a considerable discrepancy in size if body growth initially outpaces tooth replacement. For example, in the bull shark Carcharhinus leucas, regression analysis of tooth size against replacement number plotted against total body length (TL) in 41 individuals revealed strong initial increases in relative tooth size up to 6 mm (corresponding to 70–75 cm TL), then a sharp transition to steady, more linear size increase (G.N., unpublished data). It is unlikely that NBMG 10127 represents a rapidly growing juvenile, because of its rather large size (approximately 1 m estimated total length), its extensive endoskeletal mineralization, teeth approaching the maximum known size for Doliodus, large fin spines and a continuous shagreen of dermal denticles covering the head and body (Miller et al., 2003). Instead, tooth replacement may have been far slower in Doliodus than in modern adult elasmobranchs, with perhaps fewer than 10 teeth produced per family over its entire lifespan. Slow rates of tooth replacement Journal of Morphology

have also been suggested in other Paleozoic chondrichthyans (e.g., Cladoselache, Ctenacanthus; Williams, 2001). As in Doliodus, the smallest teeth

Fig. 7. First lower right tooth whorl (LR1 in Figs. 3–6), illustrating variation in successive tooth size and shape. Successive cusps are numbered 1–5. As in modern elasmobranchs, Cusp 1 formed earlier and is positioned labially. Cusp 5 was the last to form and is positioned lingually, within the dental groove of the lower jaw (seen in cross section below the tooth whorl). The base of Cusp 5 has not completely formed and the cusp is misaligned, showing that it was poorly attached to the rest of the whorl. Scale bar 5 1 mm.

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in those forms occupy a postfunctional position on the jaw surface (although each tooth is separate, rather than forming a tooth whorl). The arrangement of teeth in NBMG 10127 suggests that iso-

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lated tooth whorls recovered from the same locality may indicate mortalities rather than shed teeth, because they seem to include functional as well as postfunctional teeth. It is nevertheless uncertain whether Doliodus retained or shed the very earliest teeth within each family; these could have been lost if they did not become fused to form a whorl. Teeth Without Jaws? In modern elasmobranchs, the left and right palatoquadrates meet at a symphysis below the ethmoid region of the braincase. Consequently, all the upper teeth are directly supported by jaw cartilage, apart from mesial (symphyseal) teeth overlying connective tissue that strengthens the palatoquadrate symphysis. In adult living chimaeroids, the extent of the palatoquadrates is obscured by their holostylic fusion with the braincase, but in earlier ontogenetic stages, they appear to be separated from each other by the olfactory capsules and nasal septum (De Beer, 1937, Pl. 21). As mentioned above, carbonized remains of the basement membrane in NBMG 10127 are continuous around the tooth-bearing parts of the jaws. However, the significance of this is unclear, since the lamina in the living frilled shark Chlamydoselachus is discontinuous in adults, each tooth family being isolated from the next (Reif, 1982) although the basement membrane apparently extends between adjacent families. Doliodus could therefore have possessed separate ethmoidal and palatoquadrate dental laminae, or each tooth family could have been associated with its own lamina, as in adult Chlamydoselachus. In Doliodus, Triodus and Ptomacanthus, the teeth borne by the ethmoid region are morphologically similar to the jaw teeth, suggesting that tooth initiation and growth was probably regulated in identical fashion whether tooth families were located on the ethmoid region or the jaws (Fig. 8). A symphyseal connection between the palatoquadrates (e.g., in modern elasmobranchs and hybodonts such as Tribodus, (Maisey et al 2009 on Doliodus; Brazeau 2009 on Ptomacanthus)) probably represents a derived condition for chondrichthyans (Maisey, 1980; Maisey et al., 2009; Lane and Maisey, 2012) rather than a primitive one for chondrichthyans

Fig. 8. Palatal views of the anterior basicranium and palatoquadrates in three Paleozoic gnathostomes with shark-like dentitions. (A) Doliodus problematicus, from tomographic analysis of NBMG 10127/1a; (B) Ptomacanthus anglicus, a Devonian acanthodian (after Brazeau, 2009); Triodus sessilis, MB f 1419.4 (holotype), a Permian xenacanth shark. The width of the ethmoid region occupied by teeth is indicated by a black double-headed arrow. This space is occupied by three tooth families in Doliodus, 12 or 13 in Ptomacanthus and four or five in Triodus. Anterior to top. Scale bars 5 10 mm. eth, ethmoidal cartilage of basicranium; pq, palatoquadrate.

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(Jarvik 1977) or gnthostomes (Rosen et al., 1981). As a corollary, ‘symphyseal’ and anteriormost paired tooth families may be secondarily rather than primitively associated with the palatoquadrates in elasmobranchs. This observation carries important implications for investigations of tooth development, showing that ‘normal’ oral teeth can form in the absence of jaw cartilage. Thus, oral tooth development in modern elasmobranchs (confined only to jaw cartilage) does not provide a complete developmental model for chondrichthyans or gnathostomes generally. There appears to be a correlation in gnathostomes between the lack of a palatoquadrate symphysis and presence in the anterior basicranium of a bucco-hypophyseal canal which, like tooth patterning, is apparently maintained by shh modulation (Khonsari et al., 2013). Shark Dentitions; Ancestral or Apomorphic? The evolutionary origins of gnathostome teeth are still controversial, with two predominating but opposed hypotheses; simply expressed, these are the classical “outside-in” hypothesis, according to which teeth arose as developmentally modified, ectodermally derived skin denticles (Hertwig, 1874; Huysseune et al., 2009, 2010), and the “inside-out” hypothesis, in which tooth families arose from developmentally modified (perhaps endodermally derived) pharyngeal denticles (Smith and Coates, 1998). Whatever the case, the appearance of an inhibitory field within the oral epithelium arguably represents a more significant step in the evolution of oral teeth, as it created a region isolated from surrounding denticles giving rise to the dental lamina (Reif, 1982). Oropharyngeal and skin denticles in Doliodus and modern elasmobranchs differ in size and morphology from all but the smallest posterior jaw teeth (Miller et al., 2003). Gradation from “normal” head scales to tooth-like cheek and lip denticles has been observed in Lower Devonian ischnacanthids (a group of bony, spine-bearing fishes commonly classified as acanthodians), but these tooth-like denticles are located external to the jaws and oral teeth (Blais et al., 2011). Nevertheless, some of these “transitional” denticles are arranged in well-organized rows similar to modern elasmobranch tooth families. This not only indicates the existence of a tooth-like regulatory mechanism in epithelial tissues external to the mandibular arch in ischnacanthids, but it also suggests a process of sequential iterative denticle initiation along well-defined extra-oral pathways, resembling the labial-to-lingual pathways that regulate oral tooth development in modern sharks. The oral dental lamina in gnathostomes may have arisen by heterotopic co-option of extra-oral tissues forming tooth-like lip denticles (Soukup et al., Journal of Morphology

2008), but the conjunction of oral tooth whorls and tooth-like extra-oral denticle whorls in ishchnacanthids suggests the existence of at least two distinct ectodermal laminae in these fishes, one associated with the jaws and another located external to them. From these observations, the dental lamina of modern sharks apparently represents only one of several patterns of epithelial odontogenic laminae that evolved in early jawed vertebrates. A variety of other patterns is found in living osteichthyans. For example, teeth are formed superficially and not in a dental lamina in Gadus (Holmbakken and Fosse, 1973), but in Esox, a permanent but discontinuous lamina is supposedly present (Friedmann, 1897). In the Tetraodontidae, a permanent dental lamina is present and teeth are regularly replaced in an organized pattern, though not in a sharklike manner (Pflugfelder, 1930). It has been suggested that presence of a dental lamina is a synapomorphy of crown-group gnathostomes (osteichthyans plus chondrichthyans; Soukup et al., 2008), but it is also possible that dental laminae evolved independently in different gnathostome lineages. A shark-like dental lamina capable of generating a highly modular series of tooth families has not been found in living osteichthyans (Fraser and Smith, 2011). The presence of edentulous osteichthyan-like marginal jaw bones (dentary, maxilla) in a placoderm (Entelognathus; Zhu et al., 2013) is still of uncertain phylogenetic significance, but is perhaps further evidence that placoderms never possessed shark-like tooth families. Although the lower symphyseal or parasymphyseal tooth whorls of some Paleozoic osteichthyans (e.g., Onychodus, Psarolepis; Zhu et al., 1999; Andrews et al., 2006) resemble shark-like tooth families, short whorl-like arrangements of first generation teeth are known to be produced in the zebrafish due only to space constraints (Van der Heyden et al., 2000) and it is possible that osteichthyan and chondrichthyan tooth whorls do not share a common evolutionary origin. A sharklike oral dentition, consisting only of tooth families, has a restricted phylogenetic distribution within gnathostomes and may represent an apomorphic feature which perhaps unites chondrichthyans with certain “acanthodians” (e.g., Ptomacanthus, Nostolepis scotica; Brazeau, 2009; Burrow and Turner, 2010). This possibility is strengthened by phylogenetic analyses in which “acanthodians” occupy a basal position on the chondrichthyan stem (Zhu et al., 2013). CONCLUSIONS Doliodus confirms that “shark-like” tooth patterning (with new teeth formed lingually at fixed positions within a dental lamina, extending along the entire oral margin) was already present in

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early chondrichthyans approximately 400Ma. Furthermore, regional specialization in the dentition of Doliodus (indicated by monognathic and dignathic heterodonty) suggests a level of developmental modularity and compartmentalization in the dentition of early chondrichthyans equal in sophistication to that seen in modern predaceous ram-feeding sharks. On the other hand, Doliodus also reveals features in its dentition that are atypical of modern sharks, such as a slow rate of tooth formation, retention of postfunctional teeth in tooth whorls, and upper anterior teeth that are not associated with jaw cartilage. Thus, Doliodus provides valuable insights into the early evolution of the “shark-like” dentition in chondrichthyans, but also raises important new questions about the evolution of teeth in gnathostomes. ACKNOWLEDGMENTS The authors thank Eckhard Witten, Roman Khonsari, and anonymous reviewers for reading earlier versions of this paper and making suggestions for improvement. LITERATURE CITED Andrews M, Long J, Ahlberg P, Barwick R, Campbell K. 2006. The structure of the sarcopterygian Onychodus jandemarrai n. sp. from Gogo, Western Australia: With a functional interpretation of the skeleton. Trans R Soc Edinb Earth Sci 96: 197–307. Blais SA, MacKenzie LA, Wilson MVH. 2011. Tooth-like scales in Early Devonian eugnathostomes and the ‘outside-in’ hypothesis for the origins of teeth in vertebrates. J Vert Paleontol 31:1189–1199. Botella H. 2006. The oldest fossil evidence of dental lamina sharks. J Vert Paleontol 26:1002–1003. Botella H, Valenzuela-Rıos JI, Martınez-P erez C. 2009. Tooth replacement rates in early chondrichthyans: A qualitative approach. Lethaia 42:365–376. Brazeau M. 2009. The braincase and jaws of a Devonian ‘acanthodian’ and modern gnathostome origins. Nature 475:305– 308. Breder CM. 1942. The shedding of teeth by Carcharias littoralis (Mitchill). Copeia 1942:42–44. Burrow CJ, Turner S. 2010. Reassessment of “Protodus” scoticus from the Early Devonian of Scotland. In: Elliott DK, Maisey JG, Yu X, Miao D, editors. Morphology, Phylogeny and Paleobiogeography of Fossil Fishes. Munich: Verlag Pfeil. pp 123–144. De Beer G. 1937. The Development of the Vertebrate Skull. Oxford: Clarendon Press. 552 p. Fraser GJ, Smith MM. 2011. Evolution of developmental pattern for vertebrate dentitions: An oro-pharyngeal specific mechanism. J Exp Zool 316B:99–112. Fraser GJ, Graham A, Smith AA. 2006. Developmental and evolutionary origins of the vertebrate dentition: Molecular controls for spatio-temporal organisation of tooth sites in osteichthyans. J Exp Zool 306:183–203. Fraser GJ, Bloomquist RF, Streelman JT. 2008. A periodic pattern generator for dental diversity. BMC Biol 6:32. Friedmann E. 1897. In: Schwalbe G, editor. Morphologische Arbeiten, Beitr€ age zur Zahnentwicklung der Knockenfische, Vol. 5. Jena: Verlag Fischer. pp 545–582.

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