An Integrative View of Lepidosaur Cranial Anatomy, Development, and Diversification

  • Raul E. DiazJrEmail author
  • Paul A. Trainor
Part of the Fascinating Life Sciences book series (FLS)


There are over 10,300 recognized reptile species in the lineage Lepidosauria whose members utilize almost every mode of locomotion except powered flight. They exhibit a diverse array of feeding mechanisms such as the ballistic tongue projection and retraction system of chameleons to the snake macrostomate mode of eating prey larger than their body width. Lepidosauria also exhibit specialized cranial ornamentation and diverse cranioskeletal architecture. The diversity across over 10,300 species makes it unfeasible to conduct an exhaustive review in a short chapter. Herein, we focus our efforts on four phylogenetically, sensory, and phenotypically divergent taxa, the tuatara (Rhynchocephalia: Sphenodon punctatus) and three squamate reptiles: the desert grassland whiptail lizard (Teiidae: Aspidoscelis uniparens), veiled chameleon (Chamaeleonidae: Chamaeleo calyptratus), and the African house snake (Boaedon fuliginosus). While chondro- and osteocranial architecture, cranial muscle, and cranial nerves have been described for various taxa, most reports focus on different taxa but do not provide a description of all three of these tissues for the same species. Herein we present an integrative view of tissue differentiation of the cranium for the latter three species and also develop a reference for future comparative study of the squamate cranium. In addition, we briefly discuss topics as varied as the role of the embryonic cranial base in shaping the adult postorbital skull and the homology of some skeletal elements and jaw adductor musculature as well as the conservation of cranial nerves across Lepidosauria


Lepidosauria Rhynchocephalia Squamata Cranial muscles Chondrocranium Skull Cranial nerves Embryo 


  1. Anderson CV, Higham TE (2014) Chameleon anatomy. In: The biology of chameleons. University of California Press, London, pp 7–56Google Scholar
  2. Apesteguía S, Jones MEH (2012) A late cretaceous “tuatara” (Lepidosauria: Sphenodontinae) from South America. Cretac Res 34:154–160 CrossRefGoogle Scholar
  3. Apesteguia S, Novas FE (2003) Large cretaceous sphenodontian from Patagonia provides insight into lepidosaur evolution in Gondwana. Nature 425:609–612CrossRefGoogle Scholar
  4. Auen EL, Langebartel DA (1977) The cranial nerves of the colubrid snakes Elaphe and Thamnophis. J Morphol 154:205–222CrossRefGoogle Scholar
  5. Bellairs A d’A, Kamal AM (1981) The chondrocranium and the development of the skull in recent reptiles. In: Gans C, Parsons TS (eds) Biology of the reptilia, vol 11. Academic Press, London, pp 1–263Google Scholar
  6. Bhatt S, Diaz R, Trainor PA (2013) Signals and switches in mammalian neural crest cell differentiation. Cold Spring Harb Perspect Biol 5:a008326CrossRefPubMedPubMedCentralGoogle Scholar
  7. Boback SM, Dichter EK, Mistry HL (2012) A developmental staging series for the African house snake, Boaedon (Lamprophis) fuliginosus. Zoology 115:38–46 CrossRefGoogle Scholar
  8. Brandley MC, Huelsenbeck JP, Wiens JJ (2008) Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms. Evolution 62:2042–2064CrossRefGoogle Scholar
  9. Chai Y, Jiang X, Ito Y, Bringas P, Han J, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127:1671–1679PubMedGoogle Scholar
  10. Couly GF, Coltey PM, Le Douarin NM (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429 Google Scholar
  11. Cree A (2014) Tuatara: biology and conservation of a venerable survivor. Canterbury University Press, ChristchurchGoogle Scholar
  12. Cundall D (1986) Variations of the cephalic muscles in the colubrid snake genera Entechinus, Opheodrys, and Symphimus. J Morphol 187:1–21CrossRefGoogle Scholar
  13. Cundall D, Gans C (1979) Feeding in water snakes: an electromyographic study. J Exp Zool 209:189–207CrossRefGoogle Scholar
  14. Cundall D, Irish F (2008) The snake skull. In: Biology of the reptilia, Volume 20. The skull of Lepidosauria. Society for the Study of Amphibians and Reptiles, Ithaca, pp 349–392 Google Scholar
  15. Curtis N, Jones ME, Evans SE, O’Higgins P, Fagan M (2009) Visualizing muscle anatomy using three-dimensional computer models—an example using the head and neck muscles of Sphenodon. Palaeontol Electron 12:7TGoogle Scholar
  16. Daza JD, Diogo R, Johnston P, Abdala V (2011) Jaw adductor muscles across Lepidosaurs: a reappraisal. Anat Rec 294:1765–1782CrossRefGoogle Scholar
  17. Daza JD, Stanley EL, Wagner P, Bauer AM, Grimaldi DA (2016) Mid-cretaceous amber fossils illuminate the past diversity of tropical lizards. Sci Adv 2:e1501080CrossRefPubMedPubMedCentralGoogle Scholar
  18. De Beer G (1937) Development of the vertebrate skull. Oxford University Press, New York, NYGoogle Scholar
  19. Dendy A (1909) The intracranial vascular system of sphenodon. Proc R Soc B 81:403–427CrossRefGoogle Scholar
  20. Diaz RE, Bertocchini F, Trainor PA (2017) Lifting the veil on reptile embryology: the veiled chameleon (Chamaeleo calyptratus) as a model system to study reptilian development. Methods Mol Biol 1650:269–284CrossRefGoogle Scholar
  21. Diaz RE, Trainor PA (2015) Hand/foot splitting and the “re-evolution” of mesopodial skeletal elements during the evolution and radiation of chameleons. BMC Evol Biol 15:184 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Diogo R, Abdala V (2010) Muscles of vertebrates: comparative anatomy, evolution, homologies and development. Science Publishers, EnfieldCrossRefGoogle Scholar
  23. Diogo R, Kelly RG, Christiaen L, Levine M, Ziermann JM, Molnar JL, Noden DM, Tzahor E (2015) A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature 520:466–473 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Edgeworth FH (1935) The cranial muscles of vertebrates. Cambridge University Press, LondonGoogle Scholar
  25. El-Toubi MR, Soliman MA (1967) Studies on the osteology of the family Lacertidae in Egypt. I. The skull. Proc Zool Soc United Arab Repub 2:219–257Google Scholar
  26. Estes R, De Queiroz K, Gauthier JA (1988) Phylogenetic relationships within Squamata. In: Phylogenetic relationships of the lizard families essays commemorating Charles L. Camp. Stanford University Press, Stanford, pp 119–281Google Scholar
  27. Evans SE (2003) At the feet of the dinosaurs: the early history and radiation of lizards. Biol Rev Camb Philos Soc 78:513–551CrossRefGoogle Scholar
  28. Evans S, Jones M (2010) The origins, early history and diversification of lepidosauromorph reptiles. New Asp Mesozoic Biodivers 132:105–126, CrossRefGoogle Scholar
  29. Fischer JG (1852) Die Gehirnnerven der saurier anatomisch untersucht. Abh Naturw Ver Hambg 2:115–212Google Scholar
  30. Fraser NC, Benton MJ (1989) The Triassic reptiles Brachyrhinodon and Polysphenodon and the relationships of the sphenodontids. Zool J Linnean Soc 96:413–445CrossRefGoogle Scholar
  31. Gans C, Gaunt AS, Adler K (2008) Biology of the reptilia. Volume 20. Morphology H. The skull of Lepidosauria. Society for the Study of Amphibians and Reptiles, New YorkGoogle Scholar
  32. Gans C, Northcutt RG, Ulinski P (1979) Biology of the reptilia, Volume 10. Neurology B. Academic Press, London, New York and San FranciscoGoogle Scholar
  33. Gans C, Wever EG (1976) Ear and hearing in sphenodon puncatus. Proc Natl Acad Sci U S A 73:4244–4246CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gauthier JA, Kearney M, Maisano JA, Rieppel O, Behlke ADB (2012) Assembling the squamate tree of life: perspectives from the phenotype and the fossil record. Bull Peabody Museum Nat Hist 53:3–308CrossRefGoogle Scholar
  35. Gignac PM, Kley NJ (2014) Iodine-enhanced micro-CT imaging: methodological refinements for the study of the soft-tissue anatomy of post-embryonic vertebrates. J Exp Zool Part B Mol Dev Evol 322:166–176CrossRefGoogle Scholar
  36. Gignac PM, Kley NJ, Clarke JA, Colbert MW, Morhardt AC, Cerio D, Cost IN, Cox PG, Daza JD, Early CM, Echols MS, Henkelman RM, Herdina AN, Holliday CM, Li Z, Mahlow K, Merchant S, Müller J, Orsbon CP, Paluh DJ, Thies ML, Tsai HP, Witmer LM (2016) Diffusible iodine-based contrast-enhanced computed tomography (diceCT): an emerging tool for rapid, high-resolution, 3-D imaging of metazoan soft tissues. J Anat 228:889–909. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Gisi J (1907) Das gehirn von Hatteria punctata. Zool Jahrb (Anat) 25:1–166Google Scholar
  38. Greer AE (1991) Limb reduction in squamates: identification of the lineages and discussion of the trends. J Herpetol 25:166 CrossRefGoogle Scholar
  39. Gunther A (1867) Contribution to the anatomy of Hatteria. Philos Trans R Soc London 157:1–34CrossRefGoogle Scholar
  40. Haas G (1973) Muscles of the jaws and associated structures in the Rhynchocephalia and Squamata. In: Gans C, Parsons TS (eds) Biology of the reptilia, vol 4. Academica Press, New York and London, pp 285–490Google Scholar
  41. Hall BK (2008) The neural crest and neural crest cells: discovery and significance for theories of embryonic organization. J Biosci 33:781–793CrossRefGoogle Scholar
  42. Haluska F, Alberch P (1983) The cranial development of Elaphe obsoleta (Ophidia, colubridae). J Morphol 178:37–55. CrossRefPubMedGoogle Scholar
  43. Hay JM, Sarre SD, Lambert DM, Allendorf FW, Daugherty CH (2010) Genetic diversity and taxonomy: a reassessment of species designation in tuatara (Sphenodon: Reptilia). Conserv Genet 11:1063–1081. CrossRefGoogle Scholar
  44. Heckert AB, Lucas SG, Rinehart LF, Hunt AP (2008) A new genus and species of sphenodontian from the ghost ranch coelophysis quarry (upper triassic: apachean), rock point formation, New Mexico, USA. Palaeontology 51:827–845. CrossRefGoogle Scholar
  45. Herrera-Flores JA, Stubbs TL, Benton MJ (2017) Macroevolutionary patterns in Rhynchocephalia: is the tuatara (Sphenodon punctatus) a living fossil? Palaeontology 60:319–328CrossRefGoogle Scholar
  46. Hutchinson MN, Skinner A, Lee MSY (2012) Tikiguania and the antiquity of squamate reptiles (lizards and snakes). Biol Lett 8:665–669 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Islam A, Ashiq S (1972) The cranial nerves of Uromastix hardwicki gray. Biologia (Bratisl) 18:51–73Google Scholar
  48. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM (2002) Tissue origins and interactions in the mammalian skull vault. Dev Biol 241:106–116 CrossRefGoogle Scholar
  49. Johnston P (2011) Cranial muscles of the anurals Leiopelma hochstetteri and Ascaphus truei and the homologies of the mandibular adductors in Lissamphibia and other gnathostomes. J Morphol 272:1492–1512CrossRefGoogle Scholar
  50. Johnston P (2014) Homology of the jaw muscles in lizards and snakes-a solution from a comparative gnathostome approach. Anat Rec 297:574–585CrossRefGoogle Scholar
  51. Jones MEH, Anderson CL, Hipsley CA, Müller J, Evans SE, Schoch RR (2013) Integration of molecules and new fossils supports a Triassic origin for Lepidosauria (lizards, snakes, and tuatara). BMC Evol Biol 13:208. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Jones MEH, Curtis N, O’Higgins P, Fagan M, Evans SE (2009) Head and neck muscles associated with feeding in Sphenodon (Reptilia: Lepidsauria: Rhynchocephalia). Palaeontol Electron 12:1–56Google Scholar
  53. Kamal AM, Abdeen AM (1972) The development of the chondrocranium of the lacertid lizard, Acanthodactylus boskiana. J Morphol 137:289–333CrossRefGoogle Scholar
  54. Khannoon ER, Evans SE (2015) The development of the skull of the Egyptian Cobra Naja h. haje (Squamata: Serpentes: Elapidae). PLoS One 10:e0122185. CrossRefPubMedPubMedCentralGoogle Scholar
  55. Kochva E (1963) Development of the enom gland and trigeminal muscles in Vipera palestinae. Acta Anat 52:49–89CrossRefGoogle Scholar
  56. Kumar S, Stecher G, Suleski M, Hedges SB (2017) TimeTree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol 34:1812–1819. CrossRefPubMedGoogle Scholar
  57. Lakjer T (1926) Studien uber die trirgeminus-versorgte Kaumuskulatur der SauropsidenGoogle Scholar
  58. Langebartel DA (1968) The hyoid and its associated muscles in snakes. Illinois Biological Monographs 38. University of Illinois Press, Champaign, ILGoogle Scholar
  59. Le Douarin NM, Dupin E (2014) The neural crest, a fourth germ layer of the vertebrate embryo: significance in chordate evolution. In: Neural crest cells: evolution, development and disease. Elsevier Inc., New York, pp 3–26CrossRefGoogle Scholar
  60. Luther A (1914) Uber die vom N. trigeminus versorgte Muskulatur der Amphibien, mit einen vergleichenden Ausblick uber den Adductor mandibulae der Gnathostomen, und einem Beitrag zu Verstandnis der organisation der Anuranlarven. Acta Soc Sci Fenn 44:1–151Google Scholar
  61. McBratney-Owen B, Iseki S, Bamforth SD, Olsen BR, Morriss-Kay GM (2008) Development and tissue origins of the mammalian cranial base. Dev Biol 322:121–132 CrossRefPubMedPubMedCentralGoogle Scholar
  62. McClearn D, Noden DM (1988) Ontogeny of architectural complexity in embryonic quail visceral arch muscles. Am J Anat 183:277–293. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Metscher BD (2009) MicroCT for developmental biology: a versatile tool for high-contrast 3D imaging at histological resolutions. Dev Dyn 238:632–640CrossRefGoogle Scholar
  64. Michailovici I, Eigler T, Tzahor E (2015) Chapter One—Craniofacial muscle development. In: Chai YBT (ed) Current topics in developmental biology, Craniofacial development, vol 115. Academic Press, Cambridge, MA, pp 3–30 Google Scholar
  65. Molnar JL, Diaz RE, Skorka T, Dagliyan G, Diogo R (2017) Comparative musculoskeletal anatomy of chameleon limbs, with implications for the evolution of arboreal locomotion in lizards and for teratology. J Morphol 278:1241–1261CrossRefGoogle Scholar
  66. Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218CrossRefGoogle Scholar
  67. Noden DM, Trainor PA (2005) Relations and interactions between cranial mesoderm and neural crest populations. J Anat 207:575–601. CrossRefPubMedPubMedCentralGoogle Scholar
  68. Oelrich TM (1956) The anatomy of the head of Ctenosaura pectinata (Iguanidae). Misc Publ Mus Zool Univ Mich 94:1–122Google Scholar
  69. Palci A, Caldwell MW (2013) Primary homologies of the circumorbital bones of snakes. J Morphol 274:973–986. CrossRefPubMedGoogle Scholar
  70. Pianka ER, Vitt L (2006) Lizards: windows to the evolution of diversity. University of California Press, Berkeley, CAGoogle Scholar
  71. Pough FH, Andrews RM, Cadle JE, Crump ML, Savitsky AH, Kentwood DW (2004) Herpetology as a field of study. In: Herpetology, 3rd edn. Prentice Hall, New York, pp 3–20Google Scholar
  72. Pringle JA (1952) The cranial development of certain South African snakes and the relationship of these groups. Proc Zool Soc London 123:813–866. CrossRefGoogle Scholar
  73. Pyron RA, Burbrink FT, Wiens JJ (2013) A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Evol Biol 13:93CrossRefPubMedPubMedCentralGoogle Scholar
  74. Reeder TW, Townsend TM, Mulcahy DG, Noonan BP, Wood PL Jr, Sites JW Jr, Wiens JJ (2015) Integrated analyses resolve conflicts over Squamate reptile phylogeny and reveal unexpected placements for fossil taxa. PLoS One 10:e0118199. CrossRefPubMedPubMedCentralGoogle Scholar
  75. Rieppel O (1980) The trigeminal jaw adductors of primitive snakes and their homologies with the lacertilian jaw adductors. J Zool 190:447–471CrossRefGoogle Scholar
  76. Rieppel O (1981) The skull and jaw adductor musculature in chameleons. Rev Suisse Zool 88:433–445CrossRefGoogle Scholar
  77. Rieppel O (1988) The development of the trigeminal jaw adductor musculature in teh grass snake Natrix natrix. J Zool 216:743–770CrossRefGoogle Scholar
  78. Romer A (1956) Osteology of the reptiles. University of Chicago Press, ChicagoGoogle Scholar
  79. Romer AS, Parsons TS (1977) The vertebrate body, 5th edn. W. B. Saunders, PhiladelphiaGoogle Scholar
  80. Sambasivan R, Kuratani S, Tajbakhsh S (2011) An eye on the head: the development and evolution of craniofacial muscles. Development 138:2401 LP–2402415 CrossRefGoogle Scholar
  81. Schweitzer R, Zelzer E, Volk T (2010) Connecting muscles to tendons: tendons and musculoskeletal development in flies and vertebrates. Development 137:3347–3347 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Sefton EM, Bhullar B-AS, Mohaddes Z, Hanken J (2016) Evolution of the head-trunk interface in tetrapod vertebrates. elife 5:e09972 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Shapiro MD (2002) Developmental morphology of limb reduction in Hemiergis (Squamata: Scincidae): Chondrogenesis, osteogenesis, and heterochrony. J Morphol 254:211–231CrossRefGoogle Scholar
  84. Starck D (1979) Cranio-cerebral relations in recent reptiles. In: Biology of the reptilia, Neurology, vol 9. Academic Press, London, New York and San Francisco, pp 1–38Google Scholar
  85. Szekely G, Matesz C (1988) Topography and organization of cranial nerve nuclei in the sand lizard, Lacerta agilis. J Comp Neurol 267:525–544CrossRefGoogle Scholar
  86. Szekely G, Matesz C (1993) The efferent system of cranial nerve nuclei: a comparative neuromorphological study. Springer-Verlag, Berlin, Heidelberg, New YorkCrossRefGoogle Scholar
  87. Tanner WW, Avery DF (1982) Buccal floor of reptiles, a summary. Gt Basin Nat 42:273–349 Google Scholar
  88. ten Donkelaar HJ. 1998. Reptiles. Cent Nerv Syst Vertebr:1315–1524.
  89. Trainor PA (2014) Neural crest cells: evolution, development and disease. Academic Press, AmsterdamGoogle Scholar
  90. Uetz P, Freed P, Hosek J (2018) The reptile database.
  91. Wada N, Nohno T, Kuratani S (2011) Dual origins of the prechordal cranium in the chicken embryo. Dev Biol 356:529–540CrossRefGoogle Scholar
  92. Watkinson GB (1906) The cranial nerves of Varanus bivittatus. Morphol Jahrb 35:450–472Google Scholar
  93. Werner G (1962) Das cranium der Bruckenechse, Sphenodon punctatus Gray, von 58 mm Gesamtlange. Z Anat EntwGesch 123:323–368CrossRefGoogle Scholar
  94. Wever EG (1968) The ear of the chameleon: Chamaeleo senegalensis and Chamaeleo quilensis. J Exp Zool 168:423–436CrossRefGoogle Scholar
  95. Whiteside DI (1986) The head skeleton of the Rhaetian Sphenodontid Diphydontosaurus Avonis Gen. Et Sp. Nov. and the modernizing of a living fossil. Philos Trans R Soc B Biol Sci 312:379–430CrossRefGoogle Scholar
  96. Willard WA (1915) The cranial nerves of Anolis carolinensis. Bull Mus Comp Zool Harv 49:15–116Google Scholar
  97. Woltering JM (2012) From lizard to snake; behind the evolution of an extreme body plan. Curr Genomics 13:289–299 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Wu X-C (2003) Functional morphology of the temporal region in the rhynchocephalia. Can J Earth Sci 40:589–607 CrossRefGoogle Scholar
  99. Yi H, Norell MA (2015) The burrowing origin of modern snakes. Sci Adv 1:e1500743 CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of BiologySoutheastern Louisiana UniversityHammondUSA
  2. 2.Stowers Institute for Medical ResearchKansas CityUSA
  3. 3.Department of Anatomy and Cell BiologyUniversity of Kansas Medical CenterKansas CityUSA

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