Secondary palate development is characterized by the formation of two palatal shelves on the maxillary prominences, which fuse in the midline in mammalian embryos. However, in reptilian species, such as turtles, crocodilians, and lizards, the palatal shelves of the secondary palate develop to a variable extent and morphology. While in most Squamates, the palate is widely open, crocodilians develop a fully closed secondary palate. Here, we analyzed developmental processes that underlie secondary palate formation in chameleons, where large palatal shelves extend horizontally toward the midline. The growth of the palatal shelves continued during post-hatching stages and closure of the secondary palate can be observed in several adult animals. The massive proliferation of a multilayered oral epithelium and mesenchymal cells in the dorsal part of the palatal shelves underlined the initiation of their horizontal outgrowth, and was decreased later in development. The polarized cellular localization of primary cilia and Sonic hedgehog protein was associated with horizontal growth of the palatal shelves. Moreover, the development of large palatal shelves, supported by the pterygoid and palatine bones, was coupled with the shift in Meox2, Msx1, and Pax9 gene expression along the rostro-caudal axis. In conclusion, our results revealed distinctive developmental processes that contribute to the expansion and closure of the secondary palate in chameleons and highlighted divergences in palate formation across amniote species.

Department of Anatomy Histology and Embryology Faculty of Veterinary Medicine University of Veterinary and Pharmaceutical Sciences Brno Czechia

Department of Developmental Biology Institute of Experimental Medicine Czech Academy of Sciences Prague Czechia

Department of Experimental Biology Faculty of Science Masaryk University Brno Czechia

Department of Histology and Embryology Faculty of Medicine Masaryk University Brno Czechia

Department of Radiation Dosimetry Nuclear Physics Institute Czech Academy of Sciences Prague Czechia

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czechia

Laboratory of Computed Tomography Central European Institute of Technology Brno University of Technology Brno Czechia

Laboratory of Mammalian Evolutionary Genetics Institute of Animal Physiology and Genetics Czech Academy of Sciences Brno Czechia

Laboratory of Molecular Morphogenesis Institute of Animal Physiology and Genetics Czech Academy of Sciences Brno Czechia

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Abramyan J., Leung K. J., Richman J. M. (2014). Divergent palate morphology in turtles and birds correlates with differences in proliferation and BMP2 expression during embryonic development. PubMed DOI PMC

Abramyan J., Richman J. M. (2015). Recent insights into the morphological diversity in the amniote primary and secondary palates. PubMed DOI PMC

Anderson C. V., Deban S. M. (2010). Ballistic tongue projection in chameleons maintains high performance at low temperature. PubMed DOI PMC

Anderson C. V., Deban S. M. (2012). Thermal effects on motor control and in vitro muscle dynamics of the ballistic tongue apparatus in chameleons. PubMed DOI

Andrews R. M. (2007). Effects of temperature on embryonic development of the veiled chameleon, PubMed DOI

Andrews R. M., Donoghue S. (2004). Effects of temperature and moisture on embryonic diapause of the veiled chameleon ( PubMed DOI

Brugmann S. A., Allen N. C., James A. W., Mekonnen Z., Madan E., Helms J. A. (2010). A primary cilia-dependent etiology for midline facial disorders. PubMed DOI PMC

Buchtová M., Zahradněček O., Balková S., Tucker A. S. (2013). Odontogenesis in the veiled chameleon ( PubMed DOI

Bush J. O., Jiang R. (2012). Palatogenesis: morphogenetic and molecular mechanisms of secondary palate development. PubMed DOI PMC

Crompton A. (1995).

Daza J. D., Mapps A. A., Lewis P. J., Thies M. L., Bauer A. M. (2015). Peramorphic traits in the tokay gecko skull. PubMed DOI

Diaz J. R. E., Trainor P. A. (2019).

Diaz R. E., Anderson C. V., Baumann D. P., Kupronis R., Jewell D., Piraquive C., et al. (2015). The veiled chameleon ( PubMed

Diaz R. E., Shylo N. A., Roellig D., Bronner M., Trainor P. A. (2019). Filling in the phylogenetic gaps: induction, migration, and differentiation of neural crest cells in a squamate reptile, the veiled chameleon ( PubMed DOI

Diaz R. E., Trainor P. A. (2015). Hand/foot splitting and the ’re-evolution’ of mesopodial skeletal elements during the evolution and radiation of chameleons. PubMed DOI PMC

Dosedělová H., Štěpánková K., Zikmund T., Lesot H., Kaiser J., Novotný K., et al. (2016). Age-related changes in the tooth-bone interface area of acrodont dentition in the chameleon. PubMed DOI PMC

Duldulao N. A., Lee S., Sun Z. (2009). Cilia localization is essential for in vivo functions of the Joubert syndrome protein Arl13b/Scorpion. PubMed DOI PMC

Ferguson M. W. (1981a). Review: the value of the American alligator ( PubMed

Ferguson M. W. (1981b). The structure and development of the palate in PubMed DOI

Ferguson M. W. (1987). Palate development: mechanisms and malformations. PubMed DOI

Ferguson M. W. (1988). Palate development. PubMed

Grbic D., Saenko S. V., Randriamoria T. M., Debry A., Raselimanana A. P., Milinkovitch M. C. (2015). Phylogeography and support vector machine classification of colour variation in panther chameleons. PubMed DOI PMC

Greene R. M., Pratt R. M. (1976). Developmental aspects of secondary palate formation. PubMed

Hampl M., Cela P., Szabo-Rogers H. L., Bosakova M. K., Dosedelova H., Krejci P., et al. (2017). Role of primary cilia in odontogenesis. PubMed DOI PMC

Hanken J., Thorogood P. (1993). Evolution and development of the vertebrate skull: the role of pattern formation. PubMed DOI

Haycraft C. J., Banizs B., Aydin-Son Y., Zhang Q., Michaud E. J., Yoder B. K. (2005). Gli2 and Gli3 localize to cilia and require the intraflagellar transport protein polaris for processing and function. PubMed DOI PMC

Hedges S. B. (2012). Amniote phylogeny and the position of turtles. PubMed DOI PMC

Hernández-Jaimes C., Jerez A., Ramírez-Pinilla M. P. (2012). Embryonic development of the skull of the Andean lizard PubMed DOI PMC

Herrel A., Redding C. L., Meyers J. J., Nishikawa K. C. (2014). The scaling of tongue projection in the veiled chameleon, PubMed DOI

Huangfu D., Anderson K. V. (2005). Cilia and Hedgehog responsiveness in the mouse. PubMed DOI PMC

Huangfu D., Liu A., Rakeman A. S., Murcia N. S., Niswander L., Anderson K. V. (2003). Hedgehog signalling in the mouse requires intraflagellar transport proteins. PubMed DOI

Iordansky N. (2016). Functional relationships in the jaw apparatus of the chameleons and the evolution of adaptive complexes.

Iwabe N., Hara Y., Kumazawa Y., Shibamoto K., Saito Y., Miyata T., et al. (2005). Sister group relationship of turtles to the bird-crocodilian clade revealed by nuclear DNA-coded proteins. PubMed DOI

Jankowski R. (2013).

Jin J. Z., Ding J. (2006). Analysis of Meox-2 mutant mice reveals a novel postfusion-based cleft palate. PubMed DOI

Jin J. Z., Ding J. (2015). Strain-dependent gene expression during mouse embryonic palate development. PubMed DOI PMC

Johnson M. L. (1933). The time and order of appearance of ossification centers in the albino mouse. DOI

Jones M. E., Werneburg I., Curtis N., Penrose R., O’higgins P., Fagan M. J., et al. (2012). The head and neck anatomy of sea turtles (Cryptodira: Chelonioidea) and skull shape in testudines. PubMed DOI PMC

Kanazawa E., Mochizuki K. (1974). The time and order of appearance of ossification centers in the hamster before birth. PubMed DOI

Kimmel C. B., Sidlauskas B., Clack J. A. (2009). Linked morphological changes during palate evolution in early tetrapods. PubMed DOI PMC

Krmpotić-Nemanić J., Vinter I., Marusić A. (2006). Relations of the pterygoid hamulus and hard palate in children and adults: anatomical implications for the function of the soft palate. PubMed DOI

Le Pabic P., Ng C., Schilling T. F. (2014). Fat-Dachsous signaling coordinates cartilage differentiation and polarity during craniofacial development. PubMed DOI PMC

Li J., Johnson C. A., Smith A. A., Hunter D. J., Singh G., Brunski J. B., et al. (2016). Linking suckling biomechanics to the development of the palate. PubMed PMC

Mo R., Freer A. M., Zinyk D. L., Crackower M. A., Michaud J., Heng H. H., et al. (1997). Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. PubMed

Mohamed R. (2018). Anatomical and radiographic study on the skull and mandible of the common opossum. PubMed DOI PMC

Namkoong B. (2015).

Ollonen J., Da Silva F. O., Mahlow K., Di-Poï N. (2018). Skull development, ossification pattern, and adult shape in the emerging lizard model organism. PubMed DOI PMC

Pinto B. J., Card D. C., Castoe T. A., Diaz R. E., Nielsen S. V., Trainor P. A., et al. (2019). The transcriptome of the veiled chameleon ( PubMed DOI

Presley R., Steel F. L. (1978). The pterygoid and ectopterygoid in mammals. PubMed DOI

Rice R., Connor E., Rice D. P. (2006). Expression patterns of Hedgehog signalling pathway members during mouse palate development. PubMed DOI

Richman J. M., Buchtová M., Boughner J. C. (2006). Comparative ontogeny and phylogeny of the upper jaw skeleton in amniotes. PubMed DOI

Rieppel O. (1993). Studies on skeleton formation in reptiles. v. Patterns of ossification in the skeleton of DOI

Rieppel O., Crumly C. (2009). Paedomorphosis and skull structure in DOI

Romer A. S. (1956).

Schock E. N., Chang C. F., Youngworth I. A., Davey M. G., Delany M. E., Brugmann S. A. (2016). Utilizing the chicken as an animal model for human craniofacial ciliopathies. PubMed DOI PMC

Sheil C. A. (2005). Skeletal development of PubMed DOI

Shi J., Zhao Y., Galati D., Winey M., Klymkowsky M. W. (2014). Chibby functions in PubMed DOI PMC

Sperber G. H., Sperber S. M., Guttmann G. D. (eds) (2012).

Stower M. J., Diaz R. E., Fernandez L. C., Crother M. W., Crother B., Marco A., et al. (2015). Bi-modal strategy of gastrulation in reptiles. PubMed DOI

Tamarin A. (1982). The formation of the primitive choanae and the junction of the primary and secondary palates in the mouse. PubMed DOI

Tokita M., Chaeychomsri W., Siruntawineti J. (2013). Developmental basis of toothlessness in turtles: insight into convergent evolution of vertebrate morphology. PubMed DOI

Tolley K. A., Herrel A. (2015).

Wheatley D. N., Wang A. M., Strugnell G. E. (1996). Expression of primary cilia in mammalian cells. PubMed DOI

Yu K., Ornitz D. M. (2011). Histomorphological study of palatal shelf elevation during murine secondary palate formation. PubMed DOI PMC

Zahradnicek O., Buchtova M., Dosedelova H., Tucker A. S. (2014). The development of complex tooth shape in reptiles. PubMed DOI PMC

Zhang Z., Song Y., Zhao X., Zhang X., Fermin C., Chen Y. (2002). Rescue of cleft palate in Msx1-deficient mice by transgenic Bmp4 reveals a network of BMP and Shh signaling in the regulation of mammalian palatogenesis. PubMed

Zheng Y., Wiens J. J. (2016). Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. PubMed DOI

Zhou J., Gao Y., Lan Y., Jia S., Jiang R. (2013). Pax9 regulates a molecular network involving Bmp4, Fgf10, Shh signaling and the Osr2 transcription factor to control palate morphogenesis. PubMed DOI PMC

X-ray microtomography imaging of craniofacial hard tissues in selected reptile species with different types of dentition

Contrast enhanced X-ray computed tomography imaging of amyloid plaques in Alzheimer disease rat model on lab based micro CT system