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Dental Patterning in the Earliest Sharks: Implications for Tooth Evolution

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Dental Patterning in the Earliest Sharks: Implications for Tooth Evolution JOURNAL OF MORPHOLOGY 00:00–00 (2013) 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 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 sug- gests 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 proto- cols “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 con- tinuous tooth replacement over the life of an individual. These teeth are arranged in files that physically move over the jaws from the inside (lin- gual) 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
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