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Fphys-09-00278 ORIGINAL RESEARCH published: 28 March 2018 doi: 10.3389/fphys.2018.00278 Skull Development, Ossification Pattern, and Adult Shape in the Emerging Lizard Model Organism Pogona vitticeps: A Comparative Analysis With Other Squamates Joni Ollonen 1, Filipe O. Da Silva 1, Kristin Mahlow 2 and Nicolas Di-Poï 1* 1 Program in Developmental Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland, 2 Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Berlin, Germany The rise of the Evo-Devo field and the development of multidisciplinary research tools at Edited by: various levels of biological organization have led to a growing interest in researching for Paul Trainor, Stowers Institute for Medical new non-model organisms. Squamates (lizards and snakes) are particularly important Research, United States for understanding fundamental questions about the evolution of vertebrates because Reviewed by: of their high diversity and evolutionary innovations and adaptations that portrait a Raul Diaz, striking body plan change that reached its extreme in snakes. Yet, little is known Southeastern Louisiana University, United States about the intricate connection between phenotype and genotype in squamates, Nathan Michael Young, partly due to limited developmental knowledge and incomplete characterization of University of California, San Francisco, United States embryonic development. Surprisingly, squamate models have received limited attention *Correspondence: in comparative developmental studies, and only a few species examined so far can be Nicolas Di-Poï considered as representative and appropriate model organism for mechanistic Evo-Devo nicolas.di-poi@helsinki.fi studies. Fortunately, the agamid lizard Pogona vitticeps (central bearded dragon) is one Specialty section: of the most popular, domesticated reptile species with both a well-established history in This article was submitted to captivity and key advantages for research, thus forming an ideal laboratory model system Craniofacial Biology and Dental and justifying his recent use in reptile biology research. We first report here the complete Research, a section of the journal post-oviposition embryonic development for P. vitticeps based on standardized staging Frontiers in Physiology systems and external morphological characters previously defined for squamates. Received: 12 January 2018 Whereas the overall morphological development follows the general trends observed Accepted: 08 March 2018 Published: 28 March 2018 in other squamates, our comparisons indicate major differences in the developmental Citation: sequence of several tissues, including early craniofacial characters. Detailed analysis of Ollonen J, Da Silva FO, Mahlow K and both embryonic skull development and adult skull shape, using a comparative approach Di-Poï N (2018) Skull Development, integrating CT-scans and gene expression studies in P. vitticeps as well as comparative Ossification Pattern, and Adult Shape in the Emerging Lizard Model embryology and 3D geometric morphometrics in a large dataset of lizards and snakes, Organism Pogona vitticeps: A highlights the extreme adult skull shape of P. vitticeps and further indicates that Comparative Analysis With Other Squamates. Front. Physiol. 9:278. heterochrony has played a key role in the early development and ossification of squamate doi: 10.3389/fphys.2018.00278 skull bones. Such detailed studies of embryonic character development, craniofacial Frontiers in Physiology | www.frontiersin.org 1 March 2018 | Volume 9 | Article 278 Ollonen et al. Skull Development of Pogona vitticeps patterning, and bone formation are essential for the establishment of well-selected squamate species as Evo-Devo model organisms. We expect that P. vitticeps will continue to emerge as a new attractive model organism for understanding developmental and molecular processes underlying tissue formation, morphology, and evolution. Keywords: Pogona vitticeps, lizard, squamate, embryogenesis, skull, model organism BACKGROUND rarely consider the presence of heterochronic shifts at different levels of organogenesis, in contrast to the standardized SES The wide recognition of the importance to connect the field system, thus making embryonic comparisons between squamate of evolution with developmental biology (Evo-Devo) in a species extremely challenging (Werneburg, 2009). mechanistic perspective, alongside with both the development of While previous embryonic descriptions of squamates have new multidisciplinary research tools and the employment of new largely focused on non-venomous and oviparous species, only a types of molecular data in modern comparative developmental few species examined so far can be considered as representative approaches have led to an explosion of interest for new model and appropriate model organism for detailed Evo-Devo studies. organisms. In particular, squamate reptiles (lizard and snakes) In particular, a lack of developmental information for agamid are becoming popular animal models among evolutionary lizards (Agamidae) is particularly surprising given the fact developmental biologists because of their high morphological that they are a widespread, diverse iguanian group with a and genetic diversity as well as exceptional anatomical and well-known ecology, life-history, and behavior (Witten, 1993; physiological innovations. Squamate models are particularly Zoffer and Mazorlig, 1997; Doneley, 2006; Cogger, 2014). At useful for shedding light onto the multiple genotype-phenotype the developmental level, complete staging tables for both pre- paths taken in the evolution of amniotes and for understanding and post-oviposition development have been reported for two fundamental questions about the evolution of morphological agamid species, Agama impalearis (El Mouden et al., 2000) diversity, including extreme body form such as limb loss and and Calotes versicolor (Muthukkarruppan et al., 1970). However, axial skeleton elongation (Gomez et al., 2008; Di-Poï et al., incomplete developmental information is available for some 2010; Head and Polly, 2015; Kvon et al., 2016; Leal and Cohn, more popularly known, domesticated species such as the central 2016). For these purposes, developmental staging tables based bearded dragon Pogona vitticeps, with only a few recent reports on external embryonic features have been reported for multiple focusing on limb and/or genital development using different lizard and snake species from different families (Tables 1, 2). non-standardized staging systems (Melville et al., 2016; Whiteley These staging tables are indispensable tools to describe the timing et al., 2017). P. vitticeps has been increasingly used in recent of developmental events in a specific taxon, and can be directly reptile biology research (see, e.g., Tzika et al., 2015; Di-Poï and used for the comparison of developmental dynamics across Milinkovitch, 2016; Melville et al., 2016; Whiteley et al., 2017) species. Such comparative studies in squamates have expanded because this species forms an ideal laboratory model system the comparative bases of tooth, axial skeleton, skull, limb, and to examine developmental and molecular processes underlying genital development (Tables 1, 2), and have played an important tissue morphology and evolution. This model has several unique role for establishing evolutionary patterns among vertebrates. In characteristics shared by the genus Pogona and relevant for many cases, however, the staging tables are fragmented and do scientific research, including e.g., relatively large size, broad not cover all external features and/or the whole developmental triangular head, flattened bodies, heterogeneous body scales with period of particular squamate species; as a consequence, complete elongated spiny scales, variable skin coloration, acrodont teeth, tables exist for only a small sample of lizard and snake species chromosomal- or temperature-dependent sex determination, (Tables 1, 2). In addition, whereas the complete intra-uterine and primitive venom glands (Witten, 1993; de Vosjoli and development of Zootoca vivipara (Dufaure and Hubert, 1961) Maillou, 1996; Zoffer and Mazorlig, 1997; Ezaz et al., 2005; Fry and the more recent Standard Event System (SES) developed by et al., 2006; Cogger, 2014; Whiteley et al., 2017). Similarly to Werneburg (2009) have been adopted as the preferred references other oviparous lizard models proposed for Evo-Devo studies— for comparisons of embryonic characters (Wise et al., 2009; the leopard gecko Eublepharis macularius (Vickaryous and Roscito and Rodrigues, 2012a,b; Polachowski and Werneburg, McLean, 2011), the genus Anolis (Sanger et al., 2008), and 2013; Werneburg et al., 2015; Melville et al., 2016; Rapp Py- the veiled chameleon Chamaeleo calyptratus (Diaz and Trainor, Daniel et al., 2017), many studies have used other staging tables or 2017)— P. vitticeps has a well-established history in captivity and even independent staging criteria. Importantly, the latter studies hatchlings are easily raised to adulthood, enabling breeding lines to be established. For examples, a variety of color morphs and scaleless Eda-mutants already exists as popular pets (de Vosjoli Abbreviations: Evo-Devo, Evolutionary and developmental; CT, micro- and Maillou, 1996; Di-Poï and Milinkovitch, 2016). Importantly, computed tomography; SES, Standard Event System; dpo, days post-oviposition; PTA, phosphotungstic acid; SVL, snout-vent length; TL, total length; PFA, P. vitticeps also combines several key advantages
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