Dental Patterning in the Earliest Sharks: Implications for Tooth Evolution

JOURNAL OF MORPHOLOGY 00:00–00 (2013)

John G. Maisey,1* Susan Turner,2 Gavin J.P. Naylor,3 and Randall F. Miller4

1Department of Vertebrate Paleontology, American Museum of Natural History, Central Park West, New York, New York 10024-5192 2Department of Geosciences, Queensland Museum, Hendra, Queensland 4011, Australia 3Hollings Marine Laboratory and Department of Biology, College of Charleston, South Carolina 29412 4Steinhammer Palaeontology Laboratory, New Brunswick Museum, Saint John, New Brunswick E2K 1E5, Canada

ABSTRACT Doliodus problematicus is the oldest occurs prior to the “lock in” that characterizes line- known fossil shark-like fish with an almost intact den- ages and makes them both recognizable and defin- tition (Emsian, Lower Devonian, c. 397Ma). We provide able. Oral teeth of living elasmobranchs (sharks a detailed description of the teeth and dentition in D. and rays) display a characteristic development problematicus, based on tomographic analysis of pattern that was evidently “locked in” very early NBMG 10127 (New Brunswick Museum, Canada). Comparisons with modern shark dentitions suggest in the evolution of chondrichthyans (the group of that Doliodus was a ram-feeding predator with a denti- jawed vertebrates to which sharks, rays, and chi- tion adapted to seizing and disabling prey. Doliodus maeroid fishes belong). Until now, however, infor- provides several clues about the early evolution of the mation about dental patterning in the earliest “shark-like” dentition in chondrichthyans and also chondrichthyans came mostly from disarticulated raises new questions about the evolution of oral teeth fossil teeth. Herein, we describe the almost intact in jawed vertebrates. As in modern sharks, teeth in battery of oral teeth from Doliodus problematicus Doliodus were replaced in a linguo-labial sequence (Fig. 1; NBMG 10127, Lower Devonian, New within tooth families at fixed positions along the jaws Brunswick, Canada, 397 Ma; Kennedy and (12–14 tooth families per jaw quadrant in NBMG Gibling, 2011), the oldest known tooth-bearing 10127). Doliodus teethwerereplacedmuchmoreslowly than in modern sharks. Nevertheless, its tooth forma- shark with a relatively intact oral dentition (Miller tion was apparently as highly organized as in modern et al., 2003; Turner, 2004). Tomographic scanning elasmobranchs, in which future tooth positions are and segmentation analysis (or “digital prepara- indicated by synchronized expression of shh at fixed tion,” whereby structures are extracted virtually loci within the dental epithelium. Comparable dental from surrounding rock) of NBMG 10127 provided arrays are absent in osteichthyans, placoderms, and a means to investigate and reconstruct its denti- many “acanthodians”; a “shark-like” dentition, there- tion (Fig. 2). Doliodus has been resolved cladisti- fore, may be a synapomorphy of chondrichthyans and cally as a stem chondrichthyan (i.e., below the gnathostomes such as Ptomacanthus. The upper ante- evolutionary divergence of elasmobranchs and rior teeth in Doliodus were not attached to the palato- their holocephalan sister group; Pradel et al., quadrates, but were instead supported by the ethmoid region of the prechordal basicranium, as in some other 2011). Prior to the discovery of NBMG 10127, Paleozoic taxa (e.g., Triodus, Ptomacanthus). This suggests that the chondrichthyan dental lamina was origi- nally associated with prechordal basicranial cartilage Contract grant sponsor: Herbert and Evelyn Axelrod Research as well as jaw cartilage, and that the modern elasmo- Chair in Paleoichthyology (American Museum of Natural His- branch condition (in which the oral dentition is con- tory); Contract grant sponsor: National Science Foundation fined to the jaws) is phylogenetically advanced. Thus, [Award No. 1036488 (Collaborative Research: Jaws and Backbone: oral tooth development in modern elasmobranchs does Chondrichthyan Phylogeny and a Spine for the Vertebrate Tree of not provide a complete developmental model for chon- Life)]; Contract grant sponsor: George Frederic Matthew Research Grants [New Brunswick Museum (to J.G.M and S.T)]. drichthyans or gnathostomes. J. Morphol. 000:000–000, 2013. VC 2013 Wiley Periodicals, Inc. *Correspondence to: John G. Maisey; Department of Vertebrate Paleontology, American Museum of Natural History, Central Park KEY WORDS: chondrichthyan; teeth; evolution; Doliodus; West at 79th Street, New York, NY 10024-5192. E-mail: Devonian [email protected]

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

Vertebrates exhibit a wide range of development Published online 00 Month 2013 in patterns. This is a reﬂection of the developmental Wiley Online Library (wileyonlinelibrary.com). ﬂux and evolutionary experimentation that often DOI 10.1002/jmor.20242

VC 2013 WILEY PERIODICALS, INC. 2 J.G. MAISEY ET AL. stem holocephalans (e.g., Helodus, Debeerius; Pat- terson, 1965; Grogan and Lund, 2000) but are absent in modern chimaeroids, which instead pos- sess large tritoral toothplates.

MATERIAL AND METHODS 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, Camp- bellton Formation, Emsian, late Lower Devonian, Campbellton, N.B. (Fig. 1). Scanned 2007 at the University of Texas High- Resolution 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 Fig. 1. Doliodus problematicus, NBMG 10127/1a, New Bruns- 75 mm (maximum field of view 77.91953 mm), reconstruction off- wick Museum. Ventral surface of the head. Scale bar 5 50 mm. set 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 Doliodus was known only from isolated diplodont “RK_SinoRingProcSimul” (parameters set: binwidth 5 21, best of (bicuspid) teeth and short tooth whorls (Wood- 5 5 11). Reconstructed with beam hardening coefficients (0, 0.75, 0.1, and 0.05) 1,190 final slices. ward, 1892; Traquair, 1893). This fossil provides Scan analysis and segmentation protocols: Mimics 3 64 Ver- evidence of highly regulated oral tooth develop- sion 14 (Materialize, Technologielaan 15, 3000 Leuven, Bel- ment like that found in modern sharks, implying gium); teeth were segmented individually and objects were the presence of a shark-like dental lamina (an saved as stereolithography (STL) files. Tooth images were ectodermal fold, developed during embryogenesis, screen-captured using Snagit software (TIFF 3 400%) and sub- in which the oral teeth are formed). The fossil also sequently aligned using Photoshop. The holotype of Triodus sessilis Jordan, 1849 (MB f 1419.4, reveals that, unlike in modern elasmobranchs, not Museum fur Naturkunde, Berlin) from Lebach, Germany, was all the upper teeth were attached to the jaws. This also examined as part of this investigation. observation has profound implications for The tooth terminology applied here is straightforward evolutionary-developmental models about verte- (uppers, lowers, left, and right). The unpaired upper teeth are brate teeth, because it suggests that part of the termed mesial rather than symphyseal because they are not dental lamina in Doliodus was not constrained to associated with any jaw symphysis. the mandibular arch. Teeth in modern sharks are arranged in a highly structured way, to optimize both biome- chanical 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). Fig. 2. Doliodus problematicus,(A), (B), segmented upper and All modern elasmobranchs have their teeth lower teeth in occlusion; (A) dorsal view, (B) ventral view. (C) arranged in families, but none possesses tooth oral view of separated upper and lower teeth. Ant, anterior; mes, whorls. Tooth families are also present in extinct mesial unpaired tooth family. Scale bars 5 10 mm.

Journal of Morphology DENTAL PATTERNING IN EARLY SHARKS 3 DESCRIPTION was rendered individually. This permitted a Initial tomographic analysis of NBMG 10127/1a detailed examination and comparison of each whorl and also allowed the entire preserved denti- revealed the teeth preserved in almost natural tion to be reconstituted in lingual, labial, and positions, with upper and lower teeth locked other views (Figs. 3–5). These views illustrate the together (Figs. 1 and 2). It also confirmed that the range of morphological variation found within the dentition consists entirely of tooth whorls rather dentition, allowing comparison with modern elas- than separate teeth (Turner, 2004), each whorl cor- mobranchs. Doliodus teeth differ in shape and size responding to a single tooth row (5 tooth family) around the jaw, with a general diminution in size in a modern shark (Fig. 2A,B). An almost complete toward the back of the mouth. Anterior teeth have battery of lower teeth is present, but the upper larger, more upright principal cusps and are wider dentition is less complete, with some whorls miss- than those farther posteriorly. The overall ing and others slightly displaced from their origi- arrangement of teeth is, thus, very reminiscent of nal position. As preserved, the teeth on one side of a modern shark dentition, with the obvious caveat the head are crowded together, while those on the that no modern elasmobranch has diplodont other are separated, suggesting there has been (bicuspid) teeth. postmortem disturbance. This may account for the In addition to this expected variation related to missing upper teeth (which could be preserved in tooth position, other differences in tooth shape, adjacent pieces of matrix that were not scanned). size, and inclination of the main tooth cusps (het- The first paired upper teeth occlude with corre- erodonty) were noted (summarized in Fig. 6); the sponding lower ones, but only the upper dentition upper and lower tooth morphology in Doliodus dif- has a mesial tooth row. The preliminary analysis fers according to position along the jaw ramus revealed 12–14 tooth rows in each lower jaw quad- (monognathic heterodonty), and between corre- rant and approximately the same number (allow- sponding upper and lower teeth (dignathic hetero- ing for missing teeth) of upper rows (Fig. 2C). The donty). Monognathic heterodonty in Doliodus number of tooth families in Doliodus was presum- includes variation in tooth size and shape. As ably as consistent as in modern elasmobranchs, shown in Figure 6, anterior lower teeth are much but this can only be confirmed when additional narrower than the lateral ones; for example, the articulated specimens become available. widest lower tooth depicted here (LR8) is more This analysis also revealed that the palatoqua- than double the width of the first (LR1). Tooth drates in NBMG 10127 are widely separated by the width diminishes rapidly from position 9 posteri- ethmoid region anteriorly and lack a median sym- orly (especially after position 11). The diplodont physis. However, the dentition forms a continuous principal cusps of the anterior teeth also diverge buccal arcade, so that the upper mesial and first at a more acute angle than those farther posteri- paired tooth families are located directly below the orly, mainly because of increased inclination of the basicranium instead of on jaw cartilage (Maisey posterior cusp (cf. UR1, UR8, UR10). Dignathic et al., 2009). A comparable arrangement is reported heterodonty in NBMG 10127 includes disparity in here in the Permian xenacanth Triodus sessilis the width and robustness of corresponding upper (e.g., MB f 1419.4; Fig. 8C). A similar arrangement and lower teeth (Fig. 6). For example, upper ante- also occurs in the early Devonian (Lochkovian, c. rior teeth (e.g., UM, UR1) are 20–25% narrower 410Ma) shark-like “acanthodian” Ptomacanthus than corresponding lower ones (LR1), whereas (Brazeau, 2009). At least part of the upper oral den- upper teeth farther posteriorly are 15–20% wider tition in all these forms is, therefore, associated and considerably more robust than the lowers with cartilage presumed to belong to the prechordal (e.g., UR5 and 8 versus LR5 and 8). Additionally, part of the basicranium, rather than with the man- the posterior cusp in UR5–8 is inclined more pos- dibular arch. Furthermore, the upper mesial and teriorly than in the corresponding lower teeth. first paired tooth families in NBMG 10127 lie within a shallow transverse recess in the ethmoid region. This recess closely resembles the tooth- bearing oral groove of the palatoquadrates. DISCUSSION Although the dental lamina is not preserved in the Heterodonty in Early Shark-like specimen, a thin, dark mineralized layer is present Gnathostomes immediately beneath the teeth (Miller et al., 2003). Although many of the teeth revealed by tomo- This corresponds topographically to the basement graphic analysis of NBMG 10127 are complete, membrane of modern elasmobranchs, to which the only the largest cusplets were revealed by the teeth are attached. The tooth-bearing recesses of scan. It was unfortunately not possible to deter- the jaw cartilages and ethmoid region, thus, pre- mine number of smaller cusplets accurately, sumably all contained parts of the dental lamina. although this could probably be accomplished at A more refined segmentation analysis was sub- higher scan resolutions. The distribution of the sequently conducted, whereby each tooth whorl largest cusplets nevertheless corroborates Turner’s

Journal of Morphology 4 J.G. MAISEY ET AL.

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 5mm.

(2004) evidence for monognathic heterodonty in is potentially useful for estimating the oral posi- cusplet organization in Doliodus. tions of isolated Devonian shark teeth (e.g., Leono- Although no modern shark has diplodont teeth, dus, Portalodus, Aztecodus, Anareodus, the heterodonty seen in the dentition of Doliodus Mamberodus; Mader, 1986; Long and Young, 1995; seems closest to that of modern sharks with Hairapetian et al., 2008; Botella et al., 2009). For “tearing-type” dentitions (e.g., the sand tiger example, teeth from the Aztec Siltstone (Middle/ shark, Carcharias taurus), suggesting that this Upper Devonian, Givetian-Frasnian boundary) of ancient (397Ma) Devonian shark was an active Antarctica described by Long and Young (1995) predator, possibly analogous to modern ram- include strongly asymmetrical forms (e.g., Azteco- feeding sharks which typically accelerate and dus harmsenae and Anareodus statei) which could overtake their prey. A similar feeding strategy has represent teeth from the distal part of the denti- also been postulated in the late Devonian Clado- tion, as well as larger, more symmetrical forms selache (Williams, 2001). By contrast, Ptomacan- (e.g., Portalodus bradshawae) that could represent thus has many more tooth families than Doliodus lateral teeth. (its upper dentition has over 60; Brazeau, 2009), Small intermediate cusplets are present between but these display virtually no heterodonty apart the main cusps in Doliodus (Traquair, 1893; from a slight enlargement of the upper teeth in Turner, 2004; Ginter et al., 2010), although these the ethmoid region (a “clutching-type” dentition, were not resolved clearly by the tomographic anal- analogous to that of the modern suction-feeding ysis. Based on an investigation of isolated Dolio- bamboo shark, Chiloscyllium). Thus, a wide spec- dus teeth, Turner (2004) found a correlation trum of functionally divergent feeding patterns is between tooth size and the number of cusplets, recognizable among the earliest gnathostomes and suggested that smaller teeth (often with a sin- with shark-like dentitions. gle intermediate cusplet) pertained to the distal Besides providing a means to establish the origi- portion of the tooth series and that larger ones nal position of isolated Doliodus tooth whorls in (usually with three or more cusplets) came from the jaw, the heterodonty revealed by NBMG 10127 the main (lateral) part of the dentition. The

Journal of Morphology DENTAL PATTERNING IN EARLY SHARKS 5

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 5mm. exposed teeth in NBMG 10127 generally corrobo- 1942). Studies of tooth development in modern rate that interpretation, but because many of fishes reveal that multirowed dentitions result them are broken it is not possible to provide quan- from sequential iterative tooth initiation along titative data about cusplet variation. well-defined mesial-to-distal and labial-to-lingual It is unclear whether tooth whorls are phyloge- pathways (Smith, 2003; Huysseune and Witten, netically ancestral for gnathostomes, although 2006; Fraser et al., 2006; Fraser et al., 2008). It similar oral tooth whorls are also present in some has been suggested that diversity in vertebrate acanthodians and early osteichthyans (Reif, 1982; dentition patterns may have arisen at least in Janvier, 1996; Brazeau, 2009; Blais et al., 2011) part through evolutionary changes in antagonistic and occasionally in Leonodus. Doliodus has been interactions regulating these pathways across the classified as an omalodontid (Ginter et al., 2010), tooth morphogenetic field (Zhang et al., 2009). but most omalodontids have separate rather than Sonic hedgehog (shh) has been identified as a key fused teeth. The oldest known chondrichthyan regulator of tooth induction in the modern cat- teeth (Leonodus carlsi Mader, 1986; Lower Devo- shark, Scyliorhinus canicula (Smith et al., 2009), nian, Lockhovian-Pragian) are typically separate, as well as in scale development (e.g., in zebrafish; but one pathological example was described by Sire and Akimenko, 2004). The developmental Botella (2006) of two teeth fused together at their expression of shh within catshark dental epithe- base. lium is confined to loci coincident with teeth at alternating iterative jaw positions, so that each locus establishes the precise sequential timing for Tooth Replacement in Doliodus development of successive replacement teeth The highly organized arrangement of oral teeth within each tooth family. Nevertheless, alternating observed in Doliodus could only result from highly tooth succession in the catshark is but one of regulated developmental patterning. In modern many replacement patterns recognized in modern elasmobranchs, successive teeth are added to the elasmobranchs (Strasburg, 1963), at one extreme lingual (buccal) end of each tooth family (Tomes, including the simultaneous replacement of teeth 1876), while postfunctional teeth are typically in every family (e.g., the cookiecutter shark, shed from the labial end of each series (Breder, Isistius).

Journal of Morphology 6 J.G. MAISEY ET AL.

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 5mm.

In NBMG 10127, the largest and most lingually strained by developmental expression patterns positioned tooth in each family often has an identical to those found in modern elasmobranchs, incomplete base and is only weakly attached to probably including synchronized developmental the lingual process of the preceding tooth. More- expression of shh at many loci within its dental over, this tooth is often misaligned with those in epithelium. It is still unclear what regulates the front (Fig. 7). The lingually positioned teeth are position of tooth families within the dental lamina located deep within the dental recess of each jaw of living gnathostomes; ﬁeld theories hypothesize cartilage (Fig. 7E); that is, in a corresponding posi- the existence of morphogens traveling over the tion to the dental lamina in modern elasmo- jaw and initiating teeth at successive loci at par- branchs. These poorly attached, lingually ticular times, implying general control of the positioned teeth are thus interpreted as the onto- whole dentition; clone theories posit the existence genetically newest ones that were being added, in of inhibition zones around individual teeth, imply- shark-like fashion, to the lingual end of each fam- ing that new teeth can form only when cells are ily. This interpretation is consistent with the pres- released from inhibition (Huysseune and Witten, ence of a tooth-forming dental lamina possessing 2006). Whatever the case, Doliodus demonstrates odontogenic properties similar to that of modern that the evolution of “shark-like” tooth develop- elasmobranchs. Additionally, misaligned lingual ment occurred 400 Ma or even earlier. teeth are present in many families (e.g., LL1, 3, 5, Successive teeth in NBMG 10127 show a 6, 8; LR1, 3, 5, 11; UM, UR1, 5, 6; Figs. 3–5). If marked increase in size labio-lingually, the largest new teeth were being added to many whorls teeth in each family being three or four times simultaneously in Doliodus, its tooth succession taller than the smallest (Figs. 5 and 7). Tooth may have been regulated across adjacent tooth width also increases labio-lingually along each families and was perhaps even synchronized family. In modern adult elasmobranchs, teeth are around the entire dental arcade. Tooth replace- replaced rapidly (usually over a few weeks or ment in Doliodus was, therefore, apparently con- months; Moss, 1972; Luer et al., 1990; Overstrom,

Journal of Morphology DENTAL PATTERNING IN EARLY SHARKS 7

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 have also been suggested in other Paleozoic chon- matched in shape and size. However, in juveniles, drichthyans (e.g., Cladoselache, Ctenacanthus; the ontogenetically earliest teeth may show a con- Williams, 2001). As in Doliodus, the smallest teeth siderable discrepancy in size if body growth ini- tially 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 indi- viduals 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 Fig. 7. First lower right tooth whorl (LR1 in Figs. 3–6), illus- Doliodus, large ﬁn spines and a continuous sha- trating variation in successive tooth size and shape. Successive green of dermal denticles covering the head and cusps are numbered 1–5. As in modern elasmobranchs, Cusp 1 body (Miller et al., 2003). Instead, tooth replace- formed earlier and is positioned labially. Cusp 5 was the last to ment may have been far slower in Doliodus than form and is positioned lingually, within the dental groove of the lower jaw (seen in cross section below the tooth whorl). The base in modern adult elasmobranchs, with perhaps of Cusp 5 has not completely formed and the cusp is misaligned, fewer than 10 teeth produced per family over its showing that it was poorly attached to the rest of the whorl. entire lifespan. Slow rates of tooth replacement Scale bar 5 1mm.

Journal of Morphology 8 J.G. MAISEY ET AL. in those forms occupy a postfunctional position on lated tooth whorls recovered from the same the jaw surface (although each tooth is separate, locality may indicate mortalities rather than shed rather than forming a tooth whorl). The arrange- teeth, because they seem to include functional as ment of teeth in NBMG 10127 suggests that iso- 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 overly- ing 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 Chlamydose- lachus 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.InDoliodus, 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 Tri- bodus, (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.

Journal of Morphology DENTAL PATTERNING IN EARLY SHARKS 9 (Jarvik 1977) or gnthostomes (Rosen et al., 1981). 2008), but the conjunction of oral tooth whorls and As a corollary, ‘symphyseal’ and anteriormost tooth-like extra-oral denticle whorls in ishchnacan- paired tooth families may be secondarily rather thids suggests the existence of at least two distinct than primitively associated with the palatoqua- ectodermal laminae in these fishes, one associated drates in elasmobranchs. This observation carries with the jaws and another located external to important implications for investigations of tooth them. development, showing that ‘normal’ oral teeth can From these observations, the dental lamina of form in the absence of jaw cartilage. Thus, oral modern sharks apparently represents only one of tooth development in modern elasmobranchs (con- several patterns of epithelial odontogenic laminae fined only to jaw cartilage) does not provide a com- that evolved in early jawed vertebrates. A variety plete developmental model for chondrichthyans or of other patterns is found in living osteichthyans. gnathostomes generally. For example, teeth are formed superficially and There appears to be a correlation in gnathos- not in a dental lamina in Gadus (Holmbakken and tomes between the lack of a palatoquadrate sym- Fosse, 1973), but in Esox, a permanent but discon- physis and presence in the anterior basicranium of tinuous lamina is supposedly present (Friedmann, a bucco-hypophyseal canal which, like tooth pat- 1897). In the Tetraodontidae, a permanent dental terning, is apparently maintained by shh modula- lamina is present and teeth are regularly replaced tion (Khonsari et al., 2013). in an organized pattern, though not in a shark- like manner (Pflugfelder, 1930). It has been suggested that presence of a dental lamina is a syna- Shark Dentitions; Ancestral or Apomorphic? pomorphy of crown-group gnathostomes The evolutionary origins of gnathostome teeth (osteichthyans plus chondrichthyans; Soukup are still controversial, with two predominating but et al., 2008), but it is also possible that dental lam- opposed hypotheses; simply expressed, these are inae evolved independently in different gnathos- the classical “outside-in” hypothesis, according to tome lineages. A shark-like dental lamina capable which teeth arose as developmentally modified, of generating a highly modular series of tooth fam- ectodermally derived skin denticles (Hertwig, ilies has not been found in living osteichthyans 1874; Huysseune et al., 2009, 2010), and the (Fraser and Smith, 2011). The presence of edentu- “inside-out” hypothesis, in which tooth families lous osteichthyan-like marginal jaw bones (den- arose from developmentally modified (perhaps tary, maxilla) in a placoderm (Entelognathus; Zhu endodermally derived) pharyngeal denticles et al., 2013) is still of uncertain phylogenetic sig- (Smith and Coates, 1998). Whatever the case, the nificance, but is perhaps further evidence that pla- appearance of an inhibitory field within the oral coderms never possessed shark-like tooth families. epithelium arguably represents a more significant Although the lower symphyseal or parasymphy- step in the evolution of oral teeth, as it created a seal tooth whorls of some Paleozoic osteichthyans region isolated from surrounding denticles giving (e.g., Onychodus, Psarolepis; Zhu et al., 1999; rise to the dental lamina (Reif, 1982). Andrews et al., 2006) resemble shark-like tooth Oropharyngeal and skin denticles in Doliodus families, short whorl-like arrangements of first and modern elasmobranchs differ in size and mor- generation teeth are known to be produced in the phology from all but the smallest posterior jaw zebrafish due only to space constraints (Van der teeth (Miller et al., 2003). Gradation from Heyden et al., 2000) and it is possible that “normal” head scales to tooth-like cheek and lip osteichthyan and chondrichthyan tooth whorls do denticles has been observed in Lower Devonian not share a common evolutionary origin. A shark- ischnacanthids (a group of bony, spine-bearing like oral dentition, consisting only of tooth fami- fishes commonly classified as acanthodians), but lies, has a restricted phylogenetic distribution these tooth-like denticles are located external to within gnathostomes and may represent an apo- the jaws and oral teeth (Blais et al., 2011). Never- morphic feature which perhaps unites chon- theless, some of these “transitional” denticles are drichthyans with certain “acanthodians” (e.g., arranged in well-organized rows similar to modern Ptomacanthus, Nostolepis scotica; Brazeau, 2009; elasmobranch tooth families. This not only indi- Burrow and Turner, 2010). This possibility is cates the existence of a tooth-like regulatory mech- strengthened by phylogenetic analyses in which anism in epithelial tissues external to the “acanthodians” occupy a basal position on the mandibular arch in ischnacanthids, but it also chondrichthyan stem (Zhu et al., 2013). suggests a process of sequential iterative denticle initiation along well-defined extra-oral pathways, CONCLUSIONS resembling the labial-to-lingual pathways that reg- ulate oral tooth development in modern sharks. Doliodus confirms that “shark-like” tooth pat- The oral dental lamina in gnathostomes may have terning (with new teeth formed lingually at fixed arisen by heterotopic co-option of extra-oral tissues positions within a dental lamina, extending along forming tooth-like lip denticles (Soukup et al., the entire oral margin) was already present in

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