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New Data on the Late Cretaceous Lizard

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New Data on the Late Cretaceous Lizard Anais da Academia Brasileira de Ciências (2018) (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201820170563 www.scielo.br/aabc | www.fb.com/aabcjournal New data on the Late Cretaceous lizard Dicothodon bajaensis (Squamata, Borioteiioidea) from Baja California, Mexico reveals an unusual tooth replacement pattern in squamates MARÍA LUISA CHAVARRÍA-ARELLANO1, TIAGO R. SIMÕES2 and MARISOL MONTELLANO-BALLESTEROS3 1Universidad Nacional Autónoma de México, Posgrado en Ciencias Biológicas, Instituto de Geología, Investigación Científica, Copilco Cd. Universidad, Coyoacán, 04510, Ciudad de México, CDMX, México 2University of Alberta, Department of Biological Sciences, 11645, Saskatchewan Drive, Edmonton, Alberta, T6G 2E9, Canada 3Universidad Nacional Autónoma de México, Instituto de Geología, Investigación Científica, Copilco Cd. Universidad, Coyoacán, 04510, Ciudad de México, CDMX, México Manuscript received on July 21, 2017; accepted for publication on December 18, 2017 ABSTRACT Borioteiioids comprise an extinct family of squamates that inhabited the Northern Hemisphere during the Cretaceous and were characterized by varying patterns of tooth replacement and dental morphology. Understanding the evolution of these tooth replacement patterns has, however, been largely hampered by an extremely fragmentary fossil record. Here we present new information on Dicothodon bajaensis from the Campanian of Baja California (Mexico), so far known only from isolated teeth and jaw fragments. Among abundant new materials there are ten maxillae and five dentaries belonging to distinct ontogenetic stages. Whereas juveniles display active tooth replacement, older specimens show no evidence of replacement. Dicothodon bajaensis is therefore inferred to have had arrested tooth replacement later in ontogeny. This provides the first evidence of cessation of tooth replacement during late ontogeny in lizards (living or extinct). This replacement type is also an evolutionary intermediate between the typical lizard replacement pattern, observed in some borioteiioids (e.g., Bicuspidon) and the complete absence of tooth replacement since early ontogeny as observed in other borioteiioids (e.g., Polyglyphanodon). Key words: Campanian, dental morphology, Mexico, North America, Squamata, tooth replacement. INTRODUCTION and amphisbaenians), is placed lingually to the tooth row. Each replacement tooth eventually migrates Tooth replacement in most reptiles occurs throughout labially and enters the pulp cavity of the functional their whole life (Edmund 1960, 1969, Osborn tooth through a resorption pit located at the base of 1974, Berkovitz 2000). Older functional teeth are the latter, and continues to develop within it until periodically shed and substituted by replacement the functional tooth is shed (Edmund 1960, Cooper teeth that are continuously formed in a dental 1966). This process is observed in a vast number of lamina which, within squamates (lizards, snakes squamate lineages (e.g., most iguanians, geckoes, Correspondence to: María Luisa Chavarría-Arellano cordylids, lacertids, teiioids, and scincids), but some E-mail: [email protected] important deviations from this pattern may occur. An Acad Bras Cienc (2018) 2 MARÍA LUISA CHAVARRÍA-ARELLANO, TIAGO R. SIMÕES and MARISOL MONTELLANO-BALLESTEROS An unusual replacement pattern occurs within homoplastic to the acrodontan condition (Borsuk- acrodontan lizards (agamids and chameleons), in Bialynicka 1996, Simões et al. 2015). which tooth replacement occurs during embryonic The ontogenetic and evolutionary patterns developmental stages, but ceases in post-embryonic concerning tooth development and replacement in ontogeny in the posterior tooth series (although borioteiioids - a clade from the Late Cretaceous new teeth continue to be added posteriorly on the of North America, East Asia, and Europe (Gao tooth row until later in ontogeny). The anteriormost and Norell 2000, Folie and Codrea 2005, maxillary and dentary teeth in acrodontans are still Nydam et al. 2007) - is, on the other hand, more replaced during post-embryonic ontogeny, but enigmatic. Arrested tooth replacement has been even among those, tooth replacement ceases during identified in North American borioteiioids, such as early ontogeny (Cooper et al. 1970, Cooper and Polyglyphanodon sternbergi (Nydam and Cifelli Poole 1973). In some extreme cases, there is no 2005) and also suggested for Peneteius aquilonius tooth replacement at all during post-embryonic life, (Nydam et al. 2000). However, most Cretaceous such as in the agamids Calotes (Edmund 1960) and North American lizards, apart from Po. sternbergi, Uromastyx (Cooper and Poole 1973). Recently, it have a very limited record and specimen sample has been identified that in agamids and chameleons size (mostly being fragmentary jaws and isolated the cessation of replacement occurs due to a teeth), thus, preventing a thorough understanding of dramatic reduction in the size of the successional the patterns of tooth replacement during ontogeny lamina (which becomes vestigial), thus, not (Nydam et al. 2000, 2007, 2013). Additionally, producing any tooth germs for replacement tooth even for Pe. aquilonius and Po. sternbergi there generations (Richman and Handrigan 2011, are still important unanswered questions regarding Buchtová et al. 2013). their tooth replacement patterns. For instance, it is Among fossil squamates, important clues known that juvenile and adults of Po. sternbergi regarding patterns of tooth development and lacked tooth replacement (Nydam and Cifelli replacement have been discovered in the last 2005), but it is unknown at which ontogenetic stage decades. Some of these findings have elucidated that replacement ceased. important questions and given new insights into the evolutionary history of mosasaurs, snakes and Here we report on and describe numerous new acrodontans (Nydam et al. 2000, Caldwell et al. materials of the fossil lizard Dicothodon bajaensis 2003, Budney et al. 2006, Caldwell 2007, Luan et al. Nydam et al. 2007 from the Campanian of Baja 2009, Simões et al. 2015). Concerning the evolution California, Mexico (Chavarría-Arellano 2014, of acrodonty and arrested tooth development, García-Alcantara 2016, Montellano-Ballesteros et two particular fossil squamate lineages are of al. 2005, 2008, Romo de Vivar 2011). These new great relevance: priscagamids and borioteiioids. specimens offer a unique opportunity to re-examine Priscagamids lived during the Late Cretaceous in tooth replacement patterns in D. bajaensis, and Mongolia, China and Central Asia (Nessov 1988, therefore shed some light on the patterns of tooth Borsuk-Bialynicka 1996) and exhibited a similar development and replacement among borioteiioids pattern of arrested tooth replacement to that seen from the Cretaceous of North America. Importantly, in acrodontans. Priscagamids are considered to be an unusual pattern of replacement is observed that the sister clade to Acrodonta (Gauthier et al. 2012, might be unique to borioteiioids, as it is thus far Simões et al. 2017, Pyron 2017) and thus, their unknown from any other clade of squamates, either pattern of tooth replacement has been considered living or extinct. An Acad Bras Cienc (2018) BORIOTEIIOID REVEALS UNIQUE TOOTH REPLACEMENT 3 MATERIALS AND METHODS to the outcrops of the ‘El Gallo’ Formation, in the area of El Rosario, Baja California, Mexico. The Observations and measurements on dental specimens were collected on the surface, by screen- morphology, tooth replacement patterns, and washing in four different microsites (Figure 1): overall morphology of tooth bearing bones in D. Evelia, 0km, Scorpio, and CADAEL. The materials bajaensis were performed using a wide range of were subsequently transported to and prepared techniques. These include: personal observations at the Laboratorio de Paleontología, Instituto de of the referred specimens using dissecting Geología, Universidad Nacional Autónoma de stereomicroscopes (Olympus SZ61), radiographic México (UNAM), in Mexico City, using mechanical images (X Mind Satelec), three-dimensional micro preparation techniques (entomological needles and computer-tomography scans (CT scans) were taken air scribes). at Laboratorio Nacional de Manufactura Aditiva, Measurements: The length of the dentaries Digitalización 3D y Tomografía Computarizada, was measured from the first tooth position to UNAM (Nikon Metrology XT H 225 at 215 kV the last tooth position. Dentary height was taken and 32 uA with an exposure time of 500 ms). from the base of exposed tooth crown of last The software myVGL 3.0 was used to create the tooth position to the ventral edge of the jaw. The two-dimensional images, and high resolution length of the maxillae was performed from the last photographs (Nikon D3300 digital camera). posterior molariform tooth to the first molariform Drawings were created using Adobe Photoshop tooth, as most maxillae are too incomplete for a CC 14.0. Additionally, we obtained pictures of whole maxilla length measure. The relative sizes Adamisaurus magnidentatus (MgR- III/5, MgR- of replacement teeth were taken from the CT scan III/3, MgR-III/1 and MgR-II/50) donated by Dr. data, following the guidelines of Delgado et al. Adam Halanski. (2003). Functional and replacement tooth crown The fossil materials of Dicothodon bajaensis heights were taken from the tooth apex to a line were collected during multiple field trip seasons circumscribing
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