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Diversity of Heads, Jaws, and Cephalic Muscles in Amphibians

  • Janine M. ZiermannEmail author
Chapter
Part of the Fascinating Life Sciences book series (FLS)

Abstract

Living amphibians include caecilians, salamanders, and frogs. They share many features like a biphasic lifestyle with aquatic larvae and terrestrial adults, cranial skeletal elements that are derived from neural crest cells and mesoderm, and muscles derived from branchiomeric mesoderm and somites. Meckel’s cartilage, which forms the larval lower jaw, derives, for example, from mandibular arch neural crest cells. Mandibular arch mesoderm gives rise to the intermandibularis muscle, which forms the floor of the mouth, and the adductor mandibulae muscles, which are laterally located muscles that close the jaw. For the following arches (hyoid and branchial arches), similarities in muscles and cartilages can also be found. However, taking a closer look, it turns out that amphibians differ also in many things. Direct development evolved in all three taxa as did neoteny, i.e., the specimens reach sexual maturity while still having larval characters. The crania range from robust in caecilians to very light in anurans. Neural crest cells contribute in different amounts to the same cranial structures as the skull roof, and in all muscle groups, some muscles changed their attachments, others are only present in one or two taxa, and again others developed several heads. The knowledge of the diversity and in particular the similarities of amphibian crania and cranial muscles can help us to shed light onto the anatomy of the last common ancestor of tetrapods and onto variations in head anatomy and development in amniotes, which include reptiles and mammals.

Keywords

Branchiomeric muscles Cephalic muscles Metamorphosis Chondrocranium 

Notes

Acknowledgment

The helpful review from Virginia Abdala improved the quality of the text.

References

  1. Alberch P, Gale EA (1986) Pathways of cytodifferentiation during the metamorphosis of the epibranchial cartilage in the salamander Eurycea bislineata. Dev Biol 117:233–244CrossRefGoogle Scholar
  2. Alberch P, Lewbart G, Gale EA (1985) The fate of larval chondrocytes during the metamorphosis of the epibranchial in the salamander, Eurycea bislineata. Development 88:71–83Google Scholar
  3. Alcalde L, Barg M (2006) Chondrocranium and cranial muscle morphology in Lysapsus and Pseudis tadpoles (Anura: Hylidae: Hylinae). Acta Zool 87:91–100CrossRefGoogle Scholar
  4. Alley KE (1989) Myofiber turnover is used to retrofit frog jaw muscles during metamorphosis. Am J Anat 184:1–12PubMedCrossRefGoogle Scholar
  5. Alley KE, Omerza FF (1998) Neuromuscular remodeling and myofiber turnover in Rana pipiens’ jaw muscles. Cell Tissues Organs 164:46–58CrossRefGoogle Scholar
  6. Altig R, Johnston GF (1989) Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol Monogr 3:81–109CrossRefGoogle Scholar
  7. AmphibiaWeb (2018) University of California, Berkeley. https://amphibiaweb.org. Accessed 14 Feb 2018
  8. Bauer WJ (1992) A contribution to the morphology of the m. interhyoideus posterior (VII) of urodele Amphibia. Zool Jb Anat 122:129–139Google Scholar
  9. Bauer WJ (1997) A contribution to the morphology of visceral jaw-opening muscles of urodeles (Amphibia: Caudata). J Morphol 233:77–97PubMedCrossRefGoogle Scholar
  10. Bemis WE, Schwenk K, Wake M (1983) Morphology and function of the feeding apparatus in Dermophis mexicanus (Amphibia: Gymnophiona). Zool J Linnean Soc 77:75–96CrossRefGoogle Scholar
  11. Bininda-Emonds ORP, Jeffery JE, Richardson MK (2003) Is sequence heterochrony an important evolutionary mechanism in mammals? J Mamm Evol 10:335–361CrossRefGoogle Scholar
  12. Birchmeier C, Brohmann H (2000) Genes that control the development of migrating muscle precursor cells. Curr Opin Cell Biol 12:725–730PubMedCrossRefGoogle Scholar
  13. Bothe I, Dietrich S (2006) The molecular setup of the avian head mesoderm and its implication for craniofacial myogenesis. Dev Dyn 235:2845–2860PubMedCrossRefGoogle Scholar
  14. Callery EM, Elinson RP (2000) Thyroid hormone-dependent metamorphosis in a direct developing frog. PNAS 97:2615–2620PubMedCrossRefGoogle Scholar
  15. Callery EM, Fang H, Elinson RP (2001) Frogs without polliwogs: evolution of anuran direct development. BioEssays 23:233–241PubMedCrossRefGoogle Scholar
  16. Cannatella DC (1999) 4. Architecture: cranial and axial musculoskeleton. In: McDiarmid RW, Altig R (eds) Tadpoles—the biology of anuran larvae, vol 1. The University of Chicago Press, Chicago, pp 52–81Google Scholar
  17. Carroll RL (2007) The Palaeozoic ancestry of salamanders, frogs and caecilians. Zool J Linnean Soc 150:1–140CrossRefGoogle Scholar
  18. Carroll RL, Holmes R (1980) The skull and jaw musculature as guides to the ancestry of salamanders. Zool J Linnean Soc 68:1–40CrossRefGoogle Scholar
  19. Castellanos R, Xie Q, Zheng D, Cvekl A, Morrow BE (2014) Mammalian TBX1 preferentially binds and regulates downstream targets via a tandem T-site repeat. PLoS One 9:e95151PubMedPubMedCentralCrossRefGoogle Scholar
  20. Chanoine C, Hardy S (2003) Xenopus muscle development: from primary to secondary myogenesis. Dev Dyn 226:12–23PubMedCrossRefGoogle Scholar
  21. Cihak R, Kralovec K, Rocek Z (2002) Developmental origin of the frontoparietal bone in Bombina variegata (Anura: Discoglossidae). J Morphol 255:122–129CrossRefGoogle Scholar
  22. Couly GF, Coltey PM, Douarin NML (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429PubMedGoogle Scholar
  23. Couly G, Creuzet S, Bennaceur S, Vincent C, Douarin NML (2002) Interactions between Hox-negative cephalic neural crest cells and the foregut endoderm in patterning the facial skeleton in the vertebrate head. Development 129:1061–1073PubMedGoogle Scholar
  24. Creuzet S, Couly G, Douarin NML (2005) Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies. J Anat 207:447–459PubMedPubMedCentralCrossRefGoogle Scholar
  25. Dean MN (2003) Suction feeding in the Pipid frog, Hymenochirus boettgeri: kinematic and behavioral considerations. Copeia 4:879–886CrossRefGoogle Scholar
  26. Deban SM, Olson WM (2002) Suction feeding by a tiny predatory tadpole. Nature 420:41–42PubMedCrossRefGoogle Scholar
  27. Deban SM, O’Reilly JC, Nishikawa KC (2001) The evolution of the motor control of feeding in amphibians. Am Zool 41:1280–1298Google Scholar
  28. Diogo R, Abdala V (2010) Muscles of vertebrates—comparative anatomy, evolution, homologies and development. CRC Press, EnfieldCrossRefGoogle Scholar
  29. Diogo R, Wood B (2012) Violation of Dollo’s law: evidence of muscle reversions in primate phylogeny and their implications for the understanding of the ontogeny, evolution, and anatomical variations of modern humans. Evolution 66:3267–3276PubMedCrossRefGoogle Scholar
  30. Diogo R, Hinits Y, Hughes SM (2008) Development of mandibular, hyoid and hypobranchial muscles in the zebrafish: homologies and evolution of these muscles within bony fishes and tetrapods. BMC Dev Biol 8:1–22CrossRefGoogle Scholar
  31. 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 520:466–473PubMedPubMedCentralCrossRefGoogle Scholar
  32. Drüner L (1901) Zungenbein-, Kiemenbogen- und Kehlkopf-Skelet, -Muskeln und Nerven von Siredon (Larvenform). Studien zur Anatomie der Zungenbein-, Kiemenbogen-und Kehlkopfmusculatur der Urodelen. 2. T. Z. J Anat 468–593Google Scholar
  33. Duellman WE, Trueb L (1994) Biology of Amphibians. Johns Hopkins University Press, BaltimoreGoogle Scholar
  34. Dulcey Cala CJ, Tarazona OA, Ramìrez-Pinilla MP (2009) The morphology and post-hatching development of the skull of Bolitoglossa nicefori (Caudata: Plethodontidae): developmental implications of recapitulation and repatterning. Zoology 112:227–239PubMedCrossRefGoogle Scholar
  35. Edgeworth FH (1935) The cranial muscles of vertebrates. Cambridge at the University Press, LondonGoogle Scholar
  36. Elinson RP (2013) Metamorphosis in a frog that does not have a tadpole. In: Shi Y-B (ed) Current topics in developmental biology, vol 103. Academic Press, Burlington, pp 259–276Google Scholar
  37. Ericsson R, Olsson L (2004) Patterns of spatial and temporal visceral arch muscle development in the Mexican Axolotl (Ambystoma mexicanum). J Morphol 261:131–140PubMedCrossRefGoogle Scholar
  38. Ericsson R, Cerny R, Falck P, Olsson L (2004) The role of cranial neural crest cells in visceral arch muscle positioning and morphogenesis in the Mexican axolotl, Ambystoma mexicanum. Dev Dyn 231:237–247PubMedCrossRefGoogle Scholar
  39. Ericsson R, Joss J, Olsson L (2008) The fate of cranial neural crest cells in the Australian lungfish (Neoceratodus forsteri). J Exp Zool B Mol Dev Evol 310:345–354PubMedCrossRefGoogle Scholar
  40. Ericsson R, Ziermann JM, Piekarski N, Schubert G, Joss J, Olsson L (2009) Cell fate and timing in the evolution of neural crest and mesoderm development in the head region of amphibians and lungfishes. Acta Zool 90:264–272CrossRefGoogle Scholar
  41. Ericsson R, Knight R, Johanson Z (2013) Evolution and development of the vertebrate neck. J Anat 222:67–78PubMedCrossRefPubMedCentralGoogle Scholar
  42. Fabrezi M, Lobo F (2009) Hyoid skeleton, its related muscles, and morphological novelties in the frog Lepidobatrachus (Anura, Ceratophryidae). Anat Rec 292:1700–1712CrossRefGoogle Scholar
  43. Falck P, Joss J, Olsson L (2000) Cranial neural crest cell migration in the Australian lungfish, Neoceratodus forsteri. Evol Dev 2:179–185PubMedCrossRefGoogle Scholar
  44. Fan X, Loebel DA, Bildsoe H, Wilkie EE, Qin J, Wang J, Tam PP (2016) Tissue interactions, cell signaling and transcriptional control in the cranial mesoderm during craniofacial development. AIMS Genet 3(1):74–98CrossRefGoogle Scholar
  45. Ford LS, Cannatella DC (1993) The major clades of frogs. Herpetol Monogr 7:94–117CrossRefGoogle Scholar
  46. Fox H (1959) A study of the development of the head and pharynx of the larval Urodele Hynobius and its bearing on the evolution of the vertebrate head. Philos Trans R Soc Lond 242:151–204Google Scholar
  47. Francis ETB (1934) IV The muscles. In: The anatomy of the salamander. Oxford University Press, London, pp 48–75Google Scholar
  48. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, de Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297:370–371CrossRefGoogle Scholar
  49. Gegenbaur C (1878) Elements of comparative anatomy. Macmillan, LondonGoogle Scholar
  50. Goldberg J, Candioti FV, Akmentins MS (2012) Direct-developing frogs: ontogeny of Oreobates barituensis (Anura: Terrarana) and the development of a novel trait. Amphibia-Reptilia 33:239–250CrossRefGoogle Scholar
  51. Goodrich ES (1930) Studies on the structure and development of vertebrates. Dover, LondonCrossRefGoogle Scholar
  52. Gould SJ (1977) Ontogeny and phylogeny. Harvard University Press, Cambridge, MAGoogle Scholar
  53. Graham A, Smith A (2001) Patterning the pharyngeal arches. BioEssays 23:54–61PubMedCrossRefGoogle Scholar
  54. Gross JB, Hanken J (2005) Cranial neural crest contributes to the bony skull vault in adult Xenopus laevis: insights from cell labeling studies. J Exp Zool B Mol Dev Evol 304:1–8Google Scholar
  55. Gross JB, Hanken J (2008). Segmentation of the vertebrate skull: neural-crest derivation of adult cartilages in the clawed frog, Xenopus laevis. Annual meeting of the Society for Integrative and Comparative Biology, p 1–16Google Scholar
  56. Haas A (1996) Das larvale Cranium von Gastrotheca riobambae und seine Metamorphose (Amphibia, Anura, Hylidae), vol 36. Verhandlungen des naturwissenschaftlichen Vereins, Hamburg, pp 33–162Google Scholar
  57. Haas A (2001) Mandibular arch musculature of anuran tadpoles; with comments on homologies of amphibian jaw muscles. J Morphol 247:1–33PubMedCrossRefGoogle Scholar
  58. Haas A (2003) Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19:23–89Google Scholar
  59. Haas A, Richards SJ (1998) Correlations of cranial morphology, ecology, and evolution in Australian suctorial tadpoles of the Genera Litoria and Nyctimystes (Amphibia: Anura: Hylidae: Pelodryadinae). J Morph 238:109–141PubMedCrossRefGoogle Scholar
  60. Hall BK (1980) Tissue interactions and the initiation of osteogenesis and chondrogenesis in the neural crest-derived mandibular skeleton of the embryonic mouse as seen in isolated murine tissues and in recombinations of murine and avian tissues. Development 58:251–264Google Scholar
  61. Hanken J, Gross JB (2005) Evolution of cranial development and the role of neural crest: insights from amphibians. J Anat 207:437–446PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hanken J, Klymkowsky MW, Summers CH, Seufert DW, Ingebrigsten N (1992) Cranial ontogeny in the direct-developing frog, Eleutherodactylus coqui (Anura: Leptodactylidae), analysed using whole-mount immunohistochemistry. J Morphol 211:95–118PubMedCrossRefGoogle Scholar
  63. Hanken J, Klymkowsky MW, Alley KE, Jennings DH (1997) Jaw muscle development as evidence for embryonic repatterning in direct-developing frogs. Proc R Soc Lond B 264:1349–1354CrossRefGoogle Scholar
  64. Hanken J, Carl TF, Richardson MK, Olsson L, Schlosser G, Osabutey CK, Klymkowsky MW (2001) Limb development in a “nonmodel” vertebrate, the direct-developing frog Eleutherodactylus coqui. J Exp Zool B Mol Dev Evol 291:375–388CrossRefGoogle Scholar
  65. Harel I, Nathan E, Tirosh-Finkel L, Zigdon H, Guimaraes-Camboa N, Evans SM, Tzahor E (2009) Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16:822–832PubMedPubMedCentralCrossRefGoogle Scholar
  66. Helms JA, Codero D, Tapadia MD (2005) New insights into craniofacial morphogenesis. Development 132:851–861PubMedCrossRefGoogle Scholar
  67. Hillis DM (1991) The phylogeny of amphibians: current knowledge and the role of cytogenetics. In: Amphibian cytogenetics and evolution. Academic Press, San Diego, pp 7–31CrossRefGoogle Scholar
  68. Hirasawa T, Kuratani S (2015) Evolution of the vertebrate skeleton: morphology, embryology, and development. Zool Lett 1:2CrossRefGoogle Scholar
  69. Huang R, Zhi Q, Izpisua-Belmonte J-C, Christ B, Patel K (1999) Origin and development of the avian tongue muscles. Anat Embryol 200:137–152PubMedCrossRefGoogle Scholar
  70. Huxley TH (1858) On the theory of the vertebrate skull. The Croonian lecture. Proc. Roy. Soc., LondonGoogle Scholar
  71. Iordansky NN (1992) Jaw muscles of the Urodela and Anura: some features of development, functions, and homology. Zool Jb Anat 122:225–232Google Scholar
  72. Iordansky NN (1996) Evolution of the musculature of the jaw apparatus in the Amphibia. Advances in Amphibian Research in the Former Soviet Union 1:3–26Google Scholar
  73. Jiang X, Iseki S, Maxson RE, Sucov HM, Morriss-Kay GM (2002) Tissue origins and interactions in the mammalian skull vault. Dev Biol 241:106–116PubMedCrossRefGoogle Scholar
  74. Johansen K, Hanson D (1968) Functional anatomy of the hearts of lungfishes and amphibians. Am Zool 8:191–210PubMedCrossRefGoogle Scholar
  75. Johnston P (2011) Cranial muscles of the anurans Leiopelma hochstetteri and Ascaphus truei and the homologies of the mandibular adductors in Lissamphibia and other gnathostomes. J Morphol 272:1492–1512PubMedCrossRefGoogle Scholar
  76. Kesteven HL (1942–45) The evolution of the skull and the cephalic muscles: a comparative study of their development and adult morphology. Part I. The fishes. Australian Museum Memoir 8:1–63CrossRefGoogle Scholar
  77. Kleinteich T, Haas A (2007) Cranial musculature in the larva of the caecilian, Ichthyophis kohtaoensis (Lissamphibia: Gymnophiona). J Morph 268:74–88PubMedCrossRefGoogle Scholar
  78. Kundrát M, Joss JM, Smith MM (2008) Fate mapping in embryos of Neoceratodus forsteri reveals cranial neural crest participation in tooth development is conserved from lungfish to tetrapods. Evol Dev 10:531–536PubMedCrossRefGoogle Scholar
  79. Kuratani S, Adachi N, Wada N, Oisi Y, Sugahara F (2013) Developmental and evolutionary significance of the mandibular arch and prechordal/premandibular cranium in vertebrates: revising the heterotopy scenario of gnathostome jaw evolution. J Anat 222:41–55PubMedCrossRefGoogle Scholar
  80. Kusakabe R, Kuratani S (2005) Evolution and developmental patterning of the vertebrate skeletal muscles: perspectives from the lamprey. Dev Dyn 234:824–834PubMedCrossRefGoogle Scholar
  81. Lauder GV, Reilly SM (1988) Functional design of the feeding mechanism in salamanders: causal bases of ontogenetic changes in function. J Exp Biol 134:219–233Google Scholar
  82. Lescroart F, Kelly RG, Le Garrec J-F, Nicolas J-F, Meilhac SM, Buckingham M (2010) Clonal analysis reveals common lineage relationships between head muscles and second heart field derivatives in the mouse embryo. Development 137:3269–3279PubMedCrossRefPubMedCentralGoogle Scholar
  83. Lescroart F, Hamou W, Francou A, Théveniau-Ruissy M, Kelly RG, Buckingham M (2015) Clonal analysis reveals a common origin between nonsomite-derived neck muscles and heart myocardium. Proc Natl Acad Sci 112:1446–1451PubMedCrossRefPubMedCentralGoogle Scholar
  84. Lightoller G (1939) Probable homologues. A study of the comparative anatomy of the mandibular and hyoid arches and their musculature. Part I. Comparative myology. Trans Zool Soc London 24:349–402CrossRefGoogle Scholar
  85. Lubosch W (1914) Vergleichende Anatomie der Kaumuskeln der Wirbeltiere, in fünf Teilen. Erster Teil: Die Kaumuskeln der Amphibien. Jen Z Naturwissenschaften 53:51–188Google Scholar
  86. Luther A (1914) Über die vom N. trigeminus versorgte Muskulatur der Amphibien mit einem vergleichenden Ausblick über den Adductor mandibulae der Gnathostomen, und einem Beitrag zum Verständnis der Organisation der Anurenlarven. Acta Societatis Scientiarum Fennicæ 7:1–151Google Scholar
  87. Lynn WG (1961) Types of amphibian metamorphosis. Am Zool 1:151–161CrossRefGoogle Scholar
  88. Manzano A, Abdala V (2003) The depressor mandibulae muscle in Anura. Alytes 20:93–131Google Scholar
  89. Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP, Koentges G (2005) Neural crest origins of the neck and shoulder. Nature 436:347–355PubMedPubMedCentralCrossRefGoogle Scholar
  90. McBratney-Owen B, Iseki S, Bamforth S, Olsen B, Morriss-Kay G (2008) Development and tissue origins of the mammalian cranial base. Dev Biol 322:121–132PubMedPubMedCentralCrossRefGoogle Scholar
  91. McClearn D, Noden DM (1988) Ontogeny of architectural complexity in embryonic quail visceral arch muscles. Am J Anat 183:277–293PubMedCrossRefGoogle Scholar
  92. McDiarmid RW, Altig R (1999) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, ILGoogle Scholar
  93. Mickoleit G (2004) Phylogenetische Systematik der Wirbeltiere. Verlag Dr. Friedrich Pfeil, MünchenGoogle Scholar
  94. Miller CT, Yelon D, Stainier DYR, Kimmel CB (2003) Two endothelin 1 effectors, hand2 and bapx1, pattern ventral pharyngeal cartilage and the jaw joint. Development 130:1353–1365PubMedCrossRefGoogle Scholar
  95. Müller H (2006) Ontogeny of the skull, lower jaw, and hyobranchial skeleton of Hypogeophis rostratus (Amphibia: Gymnophiona: Caeciliidae) revisited. J Morphol 267:968–986PubMedCrossRefGoogle Scholar
  96. Müller H, Oommen OV, Bartsch P (2005) Skeletal development of the direct-developing caecilian Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae). Zoomorphology 124:171–188CrossRefGoogle Scholar
  97. Nathan E, Monovich A, Tirosh-Finkel L, Harrelson Z, Rousso T, Rinon A, Harel I, Evans SM, Tzahor E (2008) The contribution of Islet1-expressing splanchnic mesoderm cells to distinct branchiomeric muscles reveals significant heterogeneity in head muscle development. Development 135:647–657PubMedPubMedCentralCrossRefGoogle Scholar
  98. Naumann B, Warth P, Olsson L, Konstantinidis P (2017) The development of the cucullaris muscle and the branchial musculature in the Longnose Gar (Lepisosteus osseus, Lepisosteiformes, Actinopterygii) and its implications for the evolution and development of the head/trunk interface in vertebrates. Evol Dev 19(6):263–276PubMedCrossRefGoogle Scholar
  99. Nishikawa A, Hayashi H (1995) Spatial, temporal and hormonal regulation of programmed muscle cell death during metamorphosis of the frog Xenopus laevis. Differentiation 59:207–214PubMedCrossRefGoogle Scholar
  100. Noden DM (1978) The control of avian cephalic neural crest cytodifferentiation: I. Skeletal and connective tissues. Dev Biol 67:296–312PubMedCrossRefGoogle Scholar
  101. Noden DM (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96:144–165PubMedCrossRefGoogle Scholar
  102. Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218PubMedCrossRefPubMedCentralGoogle Scholar
  103. Nussbaum RA (1983) The evolution of a unique dual jaw-closing mechanism in caecilians (Amphibia: Gymnophiona) and its bearing on caecilian ancestry. J Zool 199:545–554CrossRefGoogle Scholar
  104. O’Reilly JC, Deban SM, Nishikawa KC (2002) Derived life history characteristics constrain the evolution of aquatic feeding behavior in adult amphibians. In: Aerts P, D’Août K, Herrel A, Van Damme R (eds) Topics in functional and ecological vertebrate morphology. Shaker, Maastricht, pp 153–190Google Scholar
  105. Olsson L, Hanken J (1996) Cranial neural-crest migration and chondrogenic fate in the oriental fire-bellied toad Bombina orientalis: defining the ancestral pattern of head development in anuran amphibians. J Morphol 229:105–120PubMedCrossRefGoogle Scholar
  106. Olsson L, Falck P, Lopez K, Cobb J, Hanken J (2001) Cranial neural crest cells contribute to connective tissue in cranial muscles in the anuran amphibian, Bombina orientalis. Dev Biol 237:354–367PubMedCrossRefGoogle Scholar
  107. Olsson L, Ericsson R, Cerny R (2005) Vertebrate head development: segmentation, novelties, and homology. Theory Biosci 124:145–163PubMedCrossRefGoogle Scholar
  108. Pasqualetti M, Ori M, Nardi I, Rijli FM (2000) Ectopic Hoxa2 induction after neural crest migration results in homeosis of jaw elements in Xenopus. Development 127:5367–5378PubMedGoogle Scholar
  109. Piatt J (1935) A comparative study of the hyobranchial apparatus and throat musculature in the Plethodontidae. J Morphol 57:213–251CrossRefGoogle Scholar
  110. Piatt J (1938) Morphogenesis of the cranial muscles of Ambystoma punctatum. J Morphol 63:531–587CrossRefGoogle Scholar
  111. Piekarski N, Olsson L (2007) Muscular derivatives of the cranial most somites revealed by long-term fate mapping in the Mexican axolotl (Ambystoma mexicanum). Evol Dev 9:566–578PubMedCrossRefPubMedCentralGoogle Scholar
  112. Piekarski N, Gross JB, Hanken J (2014) Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull. Nat Commun 5:5661 9ppPubMedPubMedCentralCrossRefGoogle Scholar
  113. Platt JB (1898) The development of the cartilaginous skull and of the branchial and hypoglossal musculature in Necturus. Morphologisches Jahrbuch 25:377–463Google Scholar
  114. Ponssa ML, Candioti MFV (2012) Patterns of skull development in anurans: size and shape relationship during postmetamorphic cranial ontogeny in five species of the Leptodactylus fuscus Group (Anura: Leptodactylidae). Zoomorphology 131:349–362CrossRefGoogle Scholar
  115. Porro LB, Richards CT (2017) Digital dissection of the model organism Xenopus laevis using contrast-enhanced computed tomography. J Anat 231:169–191PubMedCrossRefGoogle Scholar
  116. Pusey HK (1943) On the head of the liopelmid frog, Ascaphus truei. I. The chondrocranium, jaws, arches, and muscles of a partly-grown larva. Quart J Micr Sci 84:105–195Google Scholar
  117. Pyron RA, Wiens JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61:543–583PubMedCrossRefGoogle Scholar
  118. Rana MS, Théveniau-Ruissy M, De Bono C, Mesbah K, Francou A, Rammah M, Domínguez JN, Roux M, Laforest B, Anderson RH, Mohun T, Zaffran S, Christoffels VM, Kelly RG (2014) Tbx1 coordinates addition of posterior second heart field progenitor cells to the arterial and venous poles of the heart. Circ Res 115:790–799PubMedCrossRefGoogle Scholar
  119. Reilly SM (1987) Ontogeny of the Hyobranchial apparatus in the salamanders Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): the ecological morphology of two neotenic strategies. J Morphol 191:205–214PubMedCrossRefGoogle Scholar
  120. Reisoli E, De Lucchini S, Nardi I, Ori M (2010) Serotonin 2B receptor signaling is required for craniofacial morphogenesis and jaw joint formation in Xenopus. Development 137:2927–2937PubMedCrossRefGoogle Scholar
  121. Reiss JO (1997) Early development of chondrocranium in the tailed frog Ascaphus truei (Amphibia: Anura): implications for anuran palatoquadrate homologies. J Morphol 231:63–100PubMedCrossRefGoogle Scholar
  122. Reiss JO (2002) The phylogeny of amphibian metamorphosis. Zoology 105:85–96PubMedCrossRefGoogle Scholar
  123. Rijli FM, Gavalas A, Chambon P (1998) Segmentation and specification in the branchial region of the head: the role of the Hox selector genes. Int J Dev Biol 42:393–401PubMedGoogle Scholar
  124. Rinon A, Lazar S, Marshall H, Büchmann-Møller S, Neufeld A, Elhanany-Tamir H, Taketo MM, Sommer L, Krumlauf R, Tzahor E (2007) Cranial neural crest cells regulate head muscle patterning and differentiation during vertebrate embryogenesis. Development 134:3065–3075PubMedCrossRefGoogle Scholar
  125. Rocek Z (1989) Developmental patterns of the ethmoidal region of the anuran skull. In: Fortschritte der Zoologie/progress in zoology, Splechtna and Hilgers, vol 35. Gustav Fischer, Stuttgart, pp 412–415Google Scholar
  126. Ruibal R, Thomas E (1988) The obligate carnivorous larvae of the frog, Lepidobatrachus laevis (Leptodactylidae). Copeia 1988(3):591–604CrossRefGoogle Scholar
  127. Sadaghiani B, Thiébaud CH (1987) Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol 124:91–110PubMedCrossRefGoogle Scholar
  128. Sambasivan R, Kuratani S, Tajbakhsh S (2011) An eye on the head: the development and evolution of craniofacial muscles. Development 138:2401–2415PubMedCrossRefGoogle Scholar
  129. Santagati F, Rijli FM (2003) Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci 4:806–820PubMedCrossRefGoogle Scholar
  130. Sato T, Kurihara Y, Asai R, Kawamura Y, Tonami K, Uchijima Y, Heude E, Ekker M, Levi G, Kurihara H (2008) An endothelin-1 switch specifies maxillomandibular identity. Proc Natl Acad Sci U S A 105:18806–18811PubMedPubMedCentralCrossRefGoogle Scholar
  131. Sauka-Spengler T, Bronner-Fraser M (2008) A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9:557PubMedCrossRefGoogle Scholar
  132. Schilling TF, Kimmel CB (1997) Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 124:2945–2960PubMedGoogle Scholar
  133. Schlosser G (2003) Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui. Anat Embryol 206:215–227PubMedCrossRefGoogle Scholar
  134. Schlosser G, Roth G (1995) Nerves in tadpoles of Discoglossus pictus: distribution of cranial and rostral spinal nerves in tadpoles of the frog Discoglossus pictus (Discoglossidae). J Morph 226:189–212PubMedCrossRefGoogle Scholar
  135. Schlosser G, Roth G (1997) Evolution of nerve development in Frogs II: modified development of the peripheral nervous system in the direct-developing frog Eleutherodactylus coqui (Leptodactylidae). Brain Behav Evol 50:94–128PubMedCrossRefGoogle Scholar
  136. Schneider RA (1999) Neural crest can form cartilages normally derived from mesoderm during development of the avian head skeleton. Dev Biol 208:441–455PubMedCrossRefGoogle Scholar
  137. Sedra SN, Michael IM (1957) The development of the skull, visceral arches, larynx and visceral muscles of the South African clawed toad, Xenopus laevis (Daudin) during the process of metamorphosis (from Stage 55 to Stage 66). Amsterdam, Verhandelingen der Koninklijke Nederlandse Akademie van Wetenschappen, AFD. NatuurkundeGoogle Scholar
  138. Sefton EM, Piekarski N, Hanken J (2015) Dual embryonic origin and patterning of the pharyngeal skeleton in the axolotl (Ambystoma mexicanum). Evol Dev 17:175–184PubMedCrossRefGoogle Scholar
  139. Sefton EM, Bhullar B-AS, Mohaddes Z, Hanken J (2016) Evolution of the head-trunk interface in tetrapod vertebrates. elife 5:e09972PubMedPubMedCentralCrossRefGoogle Scholar
  140. Shih HP, Gross MK, Kioussi C (2007) Cranial muscle defects of Pitx2 mutants result from specification defects in the first branchial arch. Proc Natl Acad Sci 104:5907–5912PubMedCrossRefPubMedCentralGoogle Scholar
  141. Slater BJ, Liu KJ, Kwan MD, Quarto N, Longaker MT (2009) Cranial osteogenesis and suture morphology in Xenopus laevis: a unique model system for studying craniofacial development. PLoS One 4:e3914PubMedPubMedCentralCrossRefGoogle Scholar
  142. Smith KK (2002) Sequence heterochrony and the evolution of development. J Morphol 252:82–97PubMedCrossRefGoogle Scholar
  143. Sokol OM (1969) Feeding in the pipid frog Hymenochirus boettgeri (Tornier). Herpetologica 25:9–24Google Scholar
  144. Tajbakhsh S, Rocancourt D, Cossu G, Buckingham M (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89:127–138PubMedCrossRefPubMedCentralGoogle Scholar
  145. Tata JR (2006) Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol Cell Endocrinol 246:10–20PubMedCrossRefGoogle Scholar
  146. Taylor EH (1969) Skulls of gymnophiona and their significance in the taxonomy of the group. University of Kansas Publications, Lawrence, KanGoogle Scholar
  147. Theis S, Patel K, Valasek P, Otto A, Pu Q, Harel I, Tzahor E, Tajbakhsh S, Christ B, Huang R (2010) The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development 137:2961–2971PubMedCrossRefPubMedCentralGoogle Scholar
  148. Trainor PA, Krumlauf R (2001) Hox genes, neural crest cells and branchial arch patterning. Curr Opin Cell Biol 13:698–705PubMedCrossRefGoogle Scholar
  149. Trueb L, Hanken J (1992) Skeletal Development in Xenopus laevis (Anura: Pipidae). J Morphol 214:1–41PubMedCrossRefGoogle Scholar
  150. Vera Candioti MF (2005) Morphology and feeding in tadpoles of Ceratophrys cranwelli (Anura: Leptodactylidae). Acta Zool 86:1–11CrossRefGoogle Scholar
  151. Vera Candioti F, Grosso J, Haad B, Pereyra MO, Bornschein MR, Borteiro C, Costa P, Kolenc F, Pie MR, Proaño B (2016) Structural and heterochronic variations during the early ontogeny in toads (Anura: Bufonidae). Herpetol Monogr 30:79–118CrossRefGoogle Scholar
  152. Visser MHC (1963) The cranial morphology of Ichthyophis glutinosus (Linné) and Ichthyophis monochrous (Bleeker). Ann Univ Stellenbosch A 38:67–102Google Scholar
  153. Wada N, Nohno T, Kuratani S (2011) Dual origins of the prechordal cranium in the chicken embryo. Dev Biol 356:529–540PubMedCrossRefGoogle Scholar
  154. Wake MH, Hanken J (1982) Development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J Morphol 173:203–223PubMedPubMedCentralCrossRefGoogle Scholar
  155. Wake MH, Exbrayat J-M, Delsol M (1985) The development of the chondrocranium of Typhlonectes compressicaudus (Gymnophiona), with comparison to other species. J Herpetol 19:68–77CrossRefGoogle Scholar
  156. Weisbecker V, Mitgutsch C (2010) A large-scale survey of heterochrony in anuran cranial ossification patterns. J Zool Syst Evol Res 48:332–347CrossRefGoogle Scholar
  157. Wilkinson M, Nussbaum RA (1997) Comparative morphology and evolution of the lungless caecilian Atretochoana eiselti (Taylor) (Amphibia: Gymnophiona: Typhlonectidae). Biol J Linn Soc 62:39–109Google Scholar
  158. Ziermann JM (2008) Evolutionäre Entwicklung larvaler Cranialmuskulatur der Anura und der Einfluss von Sequenzheterochronien. Dr. PhD, Friedrich Schiller University JenaGoogle Scholar
  159. Ziermann JM, Diogo R (2013) Cranial muscle development in the model organism Ambystoma mexicanum: implications for tetrapod and vertebrate comparative and evolutionary morphology and notes on ontogeny and phylogeny. Anat Rec 296:1031–1048CrossRefGoogle Scholar
  160. Ziermann JM, Diogo R (2014) Cranial muscle development in frogs with different developmental modes: direct development vs. biphasic development. J Morphol 275:398–413PubMedCrossRefGoogle Scholar
  161. Ziermann JM, Olsson L (2007) Patterns of spatial and temporal cranial muscle development in the African clawed frog, Xenopus laevis (Anura: Pipidae). J Morphol 268:791–804PubMedCrossRefGoogle Scholar
  162. Ziermann JM, Infante C, Hanken J, Olsson L (2013) Morphology of the cranial skeleton and musculature in the obligate carnivorous tadpole of Lepidobatrachus laevis (Anura: Ceratophryidae). Acta Zool 94:101–112CrossRefGoogle Scholar
  163. Ziermann JM, Mitgutsch C, Olsson L (2014a) Analyzing developmental sequences with Parsimov—a case study of cranial muscle development in anuran larvae. J Exp Zool B Mol Dev Evol 322B:584–604Google Scholar
  164. Ziermann JM, Miyashita T, Diogo R (2014b) Cephalic muscles of cyclostomes (hagfishes and lampreys) and Chondrichthyes (sharks, rays and holocephalans): comparative anatomy and early evolution of the vertebrate head muscles. Zool J Linnean Soc 172:771–802CrossRefGoogle Scholar
  165. Ziermann JM, Fahimuddin F, Forrester A, Singh S (2017a) The cardiopharyngeal field in the light of evolutionary medicine—implications for human syndromes. J Hum Anat 1:10 https://medwinpublishers.com/JHUA/JHUA16000110.pdf Google Scholar
  166. Ziermann JM, Clement AM, Ericsson R, Olsson L (2017b) Cephalic muscle development in the Australian lungfish, Neoceratodus forsteri. J Morphol 279:494.  https://doi.org/10.1002/jmor.20784 CrossRefPubMedGoogle Scholar
  167. Ziermann JM, Freitas R, Diogo R (2017c) Muscle development in the shark Scyliorhinus canicula: implications for the evolution of the gnathostome head and paired appendage musculature. Front Zool 14:1–17.  https://doi.org/10.1186/s12983-12017-10216-y. CrossRefGoogle Scholar
  168. Ziermann JM, Diogo R, Noden DM (2018) Neural crest and the patterning of vertebrate craniofacial muscles. Genesis J Genet Dev 56:e23097Google Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of AnatomyHoward University college of medicineWashington, DCUSA

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