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Diversity of Heads, Jaws, and Cephalic Muscles in Amphibians

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Part of the book series: Fascinating Life Sciences ((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.

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References

  • Alberch P, Gale EA (1986) Pathways of cytodifferentiation during the metamorphosis of the epibranchial cartilage in the salamander Eurycea bislineata. Dev Biol 117:233–244

    Article  Google Scholar 

  • Alberch P, Lewbart G, Gale EA (1985) The fate of larval chondrocytes during the metamorphosis of the epibranchial in the salamander, Eurycea bislineata. Development 88:71–83

    CAS  Google Scholar 

  • Alcalde L, Barg M (2006) Chondrocranium and cranial muscle morphology in Lysapsus and Pseudis tadpoles (Anura: Hylidae: Hylinae). Acta Zool 87:91–100

    Article  Google Scholar 

  • Alley KE (1989) Myofiber turnover is used to retrofit frog jaw muscles during metamorphosis. Am J Anat 184:1–12

    Article  CAS  PubMed  Google Scholar 

  • Alley KE, Omerza FF (1998) Neuromuscular remodeling and myofiber turnover in Rana pipiens’ jaw muscles. Cell Tissues Organs 164:46–58

    Article  Google Scholar 

  • Altig R, Johnston GF (1989) Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol Monogr 3:81–109

    Article  Google Scholar 

  • AmphibiaWeb (2018) University of California, Berkeley. https://amphibiaweb.org. Accessed 14 Feb 2018

  • Bauer WJ (1992) A contribution to the morphology of the m. interhyoideus posterior (VII) of urodele Amphibia. Zool Jb Anat 122:129–139

    Google Scholar 

  • Bauer WJ (1997) A contribution to the morphology of visceral jaw-opening muscles of urodeles (Amphibia: Caudata). J Morphol 233:77–97

    Article  PubMed  Google Scholar 

  • Bemis WE, Schwenk K, Wake M (1983) Morphology and function of the feeding apparatus in Dermophis mexicanus (Amphibia: Gymnophiona). Zool J Linnean Soc 77:75–96

    Article  Google Scholar 

  • Bininda-Emonds ORP, Jeffery JE, Richardson MK (2003) Is sequence heterochrony an important evolutionary mechanism in mammals? J Mamm Evol 10:335–361

    Article  Google Scholar 

  • Birchmeier C, Brohmann H (2000) Genes that control the development of migrating muscle precursor cells. Curr Opin Cell Biol 12:725–730

    Article  CAS  PubMed  Google Scholar 

  • Bothe I, Dietrich S (2006) The molecular setup of the avian head mesoderm and its implication for craniofacial myogenesis. Dev Dyn 235:2845–2860

    Article  CAS  PubMed  Google Scholar 

  • Callery EM, Elinson RP (2000) Thyroid hormone-dependent metamorphosis in a direct developing frog. PNAS 97:2615–2620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Callery EM, Fang H, Elinson RP (2001) Frogs without polliwogs: evolution of anuran direct development. BioEssays 23:233–241

    Article  CAS  PubMed  Google Scholar 

  • 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 52–81

    Google Scholar 

  • Carroll RL (2007) The Palaeozoic ancestry of salamanders, frogs and caecilians. Zool J Linnean Soc 150:1–140

    Article  Google Scholar 

  • Carroll RL, Holmes R (1980) The skull and jaw musculature as guides to the ancestry of salamanders. Zool J Linnean Soc 68:1–40

    Article  Google Scholar 

  • 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:e95151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chanoine C, Hardy S (2003) Xenopus muscle development: from primary to secondary myogenesis. Dev Dyn 226:12–23

    Article  PubMed  Google Scholar 

  • Cihak R, Kralovec K, Rocek Z (2002) Developmental origin of the frontoparietal bone in Bombina variegata (Anura: Discoglossidae). J Morphol 255:122–129

    Article  Google Scholar 

  • Couly GF, Coltey PM, Douarin NML (1993) The triple origin of skull in higher vertebrates: a study in quail-chick chimeras. Development 117:409–429

    CAS  PubMed  Google Scholar 

  • 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 129:1061–1073

    CAS  PubMed  Google Scholar 

  • Creuzet S, Couly G, Douarin NML (2005) Patterning the neural crest derivatives during development of the vertebrate head: insights from avian studies. J Anat 207:447–459

    Article  PubMed  PubMed Central  Google Scholar 

  • Dean MN (2003) Suction feeding in the Pipid frog, Hymenochirus boettgeri: kinematic and behavioral considerations. Copeia 4:879–886

    Article  Google Scholar 

  • Deban SM, Olson WM (2002) Suction feeding by a tiny predatory tadpole. Nature 420:41–42

    Article  CAS  PubMed  Google Scholar 

  • Deban SM, O’Reilly JC, Nishikawa KC (2001) The evolution of the motor control of feeding in amphibians. Am Zool 41:1280–1298

    Google Scholar 

  • Diogo R, Abdala V (2010) Muscles of vertebrates—comparative anatomy, evolution, homologies and development. CRC Press, Enfield

    Google Scholar 

  • 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 66:3267–3276

    Article  PubMed  Google Scholar 

  • 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 8:1–22

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 468–593

    Google Scholar 

  • Duellman WE, Trueb L (1994) Biology of Amphibians. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • 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 112:227–239

    Article  PubMed  Google Scholar 

  • Edgeworth FH (1935) The cranial muscles of vertebrates. Cambridge at the University Press, London

    Google Scholar 

  • 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 259–276

    Google Scholar 

  • Ericsson R, Olsson L (2004) Patterns of spatial and temporal visceral arch muscle development in the Mexican Axolotl (Ambystoma mexicanum). J Morphol 261:131–140

    Article  PubMed  Google Scholar 

  • 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 231:237–247

    Article  PubMed  Google Scholar 

  • 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 310:345–354

    Article  PubMed  Google Scholar 

  • 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 90:264–272

    Article  Google Scholar 

  • Ericsson R, Knight R, Johanson Z (2013) Evolution and development of the vertebrate neck. J Anat 222:67–78

    Article  PubMed  Google Scholar 

  • Fabrezi M, Lobo F (2009) Hyoid skeleton, its related muscles, and morphological novelties in the frog Lepidobatrachus (Anura, Ceratophryidae). Anat Rec 292:1700–1712

    Article  Google Scholar 

  • Falck P, Joss J, Olsson L (2000) Cranial neural crest cell migration in the Australian lungfish, Neoceratodus forsteri. Evol Dev 2:179–185

    Article  CAS  PubMed  Google Scholar 

  • 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):74–98

    Article  Google Scholar 

  • Ford LS, Cannatella DC (1993) The major clades of frogs. Herpetol Monogr 7:94–117

    Article  Google Scholar 

  • 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 242:151–204

    Google Scholar 

  • Francis ETB (1934) IV The muscles. In: The anatomy of the salamander. Oxford University Press, London, pp 48–75

    Google Scholar 

  • 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 297:370–371

    Article  Google Scholar 

  • Gegenbaur C (1878) Elements of comparative anatomy. Macmillan, London

    Google Scholar 

  • 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 33:239–250

    Article  Google Scholar 

  • Goodrich ES (1930) Studies on the structure and development of vertebrates. Dover, London

    Book  Google Scholar 

  • Gould SJ (1977) Ontogeny and phylogeny. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Graham A, Smith A (2001) Patterning the pharyngeal arches. BioEssays 23:54–61

    Article  CAS  PubMed  Google Scholar 

  • 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 304:1–8

    Google Scholar 

  • 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 1–16

    Google Scholar 

  • Haas A (1996) Das larvale Cranium von Gastrotheca riobambae und seine Metamorphose (Amphibia, Anura, Hylidae), vol 36. Verhandlungen des naturwissenschaftlichen Vereins, Hamburg, pp 33–162

    Google Scholar 

  • Haas A (2001) Mandibular arch musculature of anuran tadpoles; with comments on homologies of amphibian jaw muscles. J Morphol 247:1–33

    Article  CAS  PubMed  Google Scholar 

  • Haas A (2003) Phylogeny of frogs as inferred from primarily larval characters (Amphibia: Anura). Cladistics 19:23–89

    PubMed  Google Scholar 

  • 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 238:109–141

    Article  CAS  PubMed  Google Scholar 

  • 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 58:251–264

    CAS  Google Scholar 

  • Hanken J, Gross JB (2005) Evolution of cranial development and the role of neural crest: insights from amphibians. J Anat 207:437–446

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 211:95–118

    Article  CAS  PubMed  Google Scholar 

  • 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 264:1349–1354

    Article  CAS  Google Scholar 

  • 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 291:375–388

    Article  CAS  Google Scholar 

  • 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 16:822–832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Helms JA, Codero D, Tapadia MD (2005) New insights into craniofacial morphogenesis. Development 132:851–861

    Article  CAS  PubMed  Google Scholar 

  • Hillis DM (1991) The phylogeny of amphibians: current knowledge and the role of cytogenetics. In: Amphibian cytogenetics and evolution. Academic Press, San Diego, pp 7–31

    Chapter  Google Scholar 

  • Hirasawa T, Kuratani S (2015) Evolution of the vertebrate skeleton: morphology, embryology, and development. Zool Lett 1:2

    Article  Google Scholar 

  • Huang R, Zhi Q, Izpisua-Belmonte J-C, Christ B, Patel K (1999) Origin and development of the avian tongue muscles. Anat Embryol 200:137–152

    Article  CAS  Google Scholar 

  • Huxley TH (1858) On the theory of the vertebrate skull. The Croonian lecture. Proc. Roy. Soc., London

    Google Scholar 

  • Iordansky NN (1992) Jaw muscles of the Urodela and Anura: some features of development, functions, and homology. Zool Jb Anat 122:225–232

    Google Scholar 

  • Iordansky NN (1996) Evolution of the musculature of the jaw apparatus in the Amphibia. Advances in Amphibian Research in the Former Soviet Union 1:3–26

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Johansen K, Hanson D (1968) Functional anatomy of the hearts of lungfishes and amphibians. Am Zool 8:191–210

    Article  CAS  PubMed  Google Scholar 

  • 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 272:1492–1512

    Article  PubMed  Google Scholar 

  • 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 8:1–63

    Article  Google Scholar 

  • Kleinteich T, Haas A (2007) Cranial musculature in the larva of the caecilian, Ichthyophis kohtaoensis (Lissamphibia: Gymnophiona). J Morph 268:74–88

    Article  PubMed  Google Scholar 

  • 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 10:531–536

    Article  PubMed  Google Scholar 

  • 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 222:41–55

    Article  PubMed  Google Scholar 

  • Kusakabe R, Kuratani S (2005) Evolution and developmental patterning of the vertebrate skeletal muscles: perspectives from the lamprey. Dev Dyn 234:824–834

    Article  PubMed  Google Scholar 

  • Lauder GV, Reilly SM (1988) Functional design of the feeding mechanism in salamanders: causal bases of ontogenetic changes in function. J Exp Biol 134:219–233

    Google Scholar 

  • 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 137:3269–3279

    Article  CAS  PubMed  Google Scholar 

  • 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 112:1446–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 24:349–402

    Article  Google Scholar 

  • Lubosch W (1914) Vergleichende Anatomie der Kaumuskeln der Wirbeltiere, in fünf Teilen. Erster Teil: Die Kaumuskeln der Amphibien. Jen Z Naturwissenschaften 53:51–188

    Google Scholar 

  • 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 7:1–151

    Google Scholar 

  • Lynn WG (1961) Types of amphibian metamorphosis. Am Zool 1:151–161

    Article  Google Scholar 

  • Manzano A, Abdala V (2003) The depressor mandibulae muscle in Anura. Alytes 20:93–131

    Google Scholar 

  • 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 436:347–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McBratney-Owen B, Iseki S, Bamforth S, Olsen B, Morriss-Kay G (2008) Development and tissue origins of the mammalian cranial base. Dev Biol 322:121–132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McClearn D, Noden DM (1988) Ontogeny of architectural complexity in embryonic quail visceral arch muscles. Am J Anat 183:277–293

    Article  CAS  PubMed  Google Scholar 

  • McDiarmid RW, Altig R (1999) Tadpoles: the biology of anuran larvae. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Mickoleit G (2004) Phylogenetische Systematik der Wirbeltiere. Verlag Dr. Friedrich Pfeil, München

    Google Scholar 

  • 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 130:1353–1365

    Article  CAS  PubMed  Google Scholar 

  • Müller H (2006) Ontogeny of the skull, lower jaw, and hyobranchial skeleton of Hypogeophis rostratus (Amphibia: Gymnophiona: Caeciliidae) revisited. J Morphol 267:968–986

    Article  PubMed  Google Scholar 

  • Müller H, Oommen OV, Bartsch P (2005) Skeletal development of the direct-developing caecilian Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae). Zoomorphology 124:171–188

    Article  Google Scholar 

  • 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 135:647–657

    Article  CAS  PubMed  Google Scholar 

  • 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):263–276

    Article  PubMed  Google Scholar 

  • Nishikawa A, Hayashi H (1995) Spatial, temporal and hormonal regulation of programmed muscle cell death during metamorphosis of the frog Xenopus laevis. Differentiation 59:207–214

    Article  CAS  PubMed  Google Scholar 

  • Noden DM (1978) The control of avian cephalic neural crest cytodifferentiation: I. Skeletal and connective tissues. Dev Biol 67:296–312

    Article  CAS  PubMed  Google Scholar 

  • Noden DM (1983) The role of the neural crest in patterning of avian cranial skeletal, connective, and muscle tissues. Dev Biol 96:144–165

    Article  CAS  PubMed  Google Scholar 

  • Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218

    Article  CAS  PubMed  Google Scholar 

  • Nussbaum RA (1983) The evolution of a unique dual jaw-closing mechanism in caecilians (Amphibia: Gymnophiona) and its bearing on caecilian ancestry. J Zool 199:545–554

    Article  Google Scholar 

  • 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 153–190

    Google Scholar 

  • 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 229:105–120

    Article  PubMed  Google Scholar 

  • 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 237:354–367

    Article  CAS  PubMed  Google Scholar 

  • Olsson L, Ericsson R, Cerny R (2005) Vertebrate head development: segmentation, novelties, and homology. Theory Biosci 124:145–163

    Article  PubMed  Google Scholar 

  • 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 127:5367–5378

    CAS  PubMed  Google Scholar 

  • Piatt J (1935) A comparative study of the hyobranchial apparatus and throat musculature in the Plethodontidae. J Morphol 57:213–251

    Article  Google Scholar 

  • Piatt J (1938) Morphogenesis of the cranial muscles of Ambystoma punctatum. J Morphol 63:531–587

    Article  Google Scholar 

  • 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 9:566–578

    Article  PubMed  Google Scholar 

  • Piekarski N, Gross JB, Hanken J (2014) Evolutionary innovation and conservation in the embryonic derivation of the vertebrate skull. Nat Commun 5:5661 9pp

    Article  CAS  PubMed  Google Scholar 

  • Platt JB (1898) The development of the cartilaginous skull and of the branchial and hypoglossal musculature in Necturus. Morphologisches Jahrbuch 25:377–463

    Google Scholar 

  • 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 131:349–362

    Article  Google Scholar 

  • Porro LB, Richards CT (2017) Digital dissection of the model organism Xenopus laevis using contrast-enhanced computed tomography. J Anat 231:169–191

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 84:105–195

    Google Scholar 

  • 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 61:543–583

    Article  PubMed  Google Scholar 

  • 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 115:790–799

    Article  CAS  PubMed  Google Scholar 

  • 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 191:205–214

    Article  PubMed  Google Scholar 

  • 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 137:2927–2937

    Article  CAS  PubMed  Google Scholar 

  • Reiss JO (1997) Early development of chondrocranium in the tailed frog Ascaphus truei (Amphibia: Anura): implications for anuran palatoquadrate homologies. J Morphol 231:63–100

    Article  CAS  PubMed  Google Scholar 

  • Reiss JO (2002) The phylogeny of amphibian metamorphosis. Zoology 105:85–96

    Article  PubMed  Google Scholar 

  • 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 42:393–401

    CAS  PubMed  Google Scholar 

  • 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 134:3065–3075

    Article  CAS  PubMed  Google Scholar 

  • 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 412–415

    Google Scholar 

  • Ruibal R, Thomas E (1988) The obligate carnivorous larvae of the frog, Lepidobatrachus laevis (Leptodactylidae). Copeia 1988(3):591–604

    Article  Google Scholar 

  • Sadaghiani B, Thiébaud CH (1987) Neural crest development in the Xenopus laevis embryo, studied by interspecific transplantation and scanning electron microscopy. Dev Biol 124:91–110

    Article  CAS  PubMed  Google Scholar 

  • Sambasivan R, Kuratani S, Tajbakhsh S (2011) An eye on the head: the development and evolution of craniofacial muscles. Development 138:2401–2415

    Article  CAS  PubMed  Google Scholar 

  • Santagati F, Rijli FM (2003) Cranial neural crest and the building of the vertebrate head. Nat Rev Neurosci 4:806–820

    Article  CAS  PubMed  Google Scholar 

  • 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 105:18806–18811

    Article  PubMed  PubMed Central  Google Scholar 

  • Sauka-Spengler T, Bronner-Fraser M (2008) A gene regulatory network orchestrates neural crest formation. Nat Rev Mol Cell Biol 9:557

    Article  CAS  PubMed  Google Scholar 

  • Schilling TF, Kimmel CB (1997) Musculoskeletal patterning in the pharyngeal segments of the zebrafish embryo. Development 124:2945–2960

    CAS  PubMed  Google Scholar 

  • Schlosser G (2003) Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui. Anat Embryol 206:215–227

    Article  Google Scholar 

  • 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 226:189–212

    Article  CAS  PubMed  Google Scholar 

  • 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 50:94–128

    Article  CAS  PubMed  Google Scholar 

  • Schneider RA (1999) Neural crest can form cartilages normally derived from mesoderm during development of the avian head skeleton. Dev Biol 208:441–455

    Article  CAS  PubMed  Google Scholar 

  • 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. Natuurkunde

    Google Scholar 

  • Sefton EM, Piekarski N, Hanken J (2015) Dual embryonic origin and patterning of the pharyngeal skeleton in the axolotl (Ambystoma mexicanum). Evol Dev 17:175–184

    Article  CAS  PubMed  Google Scholar 

  • Sefton EM, Bhullar B-AS, Mohaddes Z, Hanken J (2016) Evolution of the head-trunk interface in tetrapod vertebrates. elife 5:e09972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 104:5907–5912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e3914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith KK (2002) Sequence heterochrony and the evolution of development. J Morphol 252:82–97

    Article  PubMed  Google Scholar 

  • Sokol OM (1969) Feeding in the pipid frog Hymenochirus boettgeri (Tornier). Herpetologica 25:9–24

    Google Scholar 

  • 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 89:127–138

    Article  CAS  PubMed  Google Scholar 

  • Tata JR (2006) Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol Cell Endocrinol 246:10–20

    Article  CAS  PubMed  Google Scholar 

  • Taylor EH (1969) Skulls of gymnophiona and their significance in the taxonomy of the group. University of Kansas Publications, Lawrence, Kan

    Google Scholar 

  • 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 137:2961–2971

    Article  CAS  PubMed  Google Scholar 

  • Trainor PA, Krumlauf R (2001) Hox genes, neural crest cells and branchial arch patterning. Curr Opin Cell Biol 13:698–705

    Article  CAS  PubMed  Google Scholar 

  • Trueb L, Hanken J (1992) Skeletal Development in Xenopus laevis (Anura: Pipidae). J Morphol 214:1–41

    Article  CAS  PubMed  Google Scholar 

  • Vera Candioti MF (2005) Morphology and feeding in tadpoles of Ceratophrys cranwelli (Anura: Leptodactylidae). Acta Zool 86:1–11

    Article  Google Scholar 

  • 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 30:79–118

    Article  Google Scholar 

  • Visser MHC (1963) The cranial morphology of Ichthyophis glutinosus (Linné) and Ichthyophis monochrous (Bleeker). Ann Univ Stellenbosch A 38:67–102

    Google Scholar 

  • Wada N, Nohno T, Kuratani S (2011) Dual origins of the prechordal cranium in the chicken embryo. Dev Biol 356:529–540

    Article  CAS  PubMed  Google Scholar 

  • Wake MH, Hanken J (1982) Development of the skull of Dermophis mexicanus (Amphibia: Gymnophiona), with comments on skull kinesis and amphibian relationships. J Morphol 173:203–223

    Article  PubMed  Google Scholar 

  • Wake MH, Exbrayat J-M, Delsol M (1985) The development of the chondrocranium of Typhlonectes compressicaudus (Gymnophiona), with comparison to other species. J Herpetol 19:68–77

    Article  Google Scholar 

  • Weisbecker V, Mitgutsch C (2010) A large-scale survey of heterochrony in anuran cranial ossification patterns. J Zool Syst Evol Res 48:332–347

    Article  Google Scholar 

  • Wilkinson M, Nussbaum RA (1997) Comparative morphology and evolution of the lungless caecilian Atretochoana eiselti (Taylor) (Amphibia: Gymnophiona: Typhlonectidae). Biol J Linn Soc 62:39–109

    Google Scholar 

  • Ziermann JM (2008) Evolutionäre Entwicklung larvaler Cranialmuskulatur der Anura und der Einfluss von Sequenzheterochronien. Dr. PhD, Friedrich Schiller University Jena

    Google Scholar 

  • 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 296:1031–1048

    Article  Google Scholar 

  • Ziermann JM, Diogo R (2014) Cranial muscle development in frogs with different developmental modes: direct development vs. biphasic development. J Morphol 275:398–413

    Article  PubMed  Google Scholar 

  • Ziermann JM, Olsson L (2007) Patterns of spatial and temporal cranial muscle development in the African clawed frog, Xenopus laevis (Anura: Pipidae). J Morphol 268:791–804

    Article  PubMed  Google Scholar 

  • 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 94:101–112

    Article  Google Scholar 

  • 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:584–604

    Google Scholar 

  • 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 172:771–802

    Article  Google Scholar 

  • 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 

  • 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

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Ziermann JM, Diogo R, Noden DM (2018) Neural crest and the patterning of vertebrate craniofacial muscles. Genesis J Genet Dev 56:e23097

    Google Scholar 

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

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Ziermann, J.M. (2019). Diversity of Heads, Jaws, and Cephalic Muscles in Amphibians. In: Ziermann, J., Diaz Jr, R., Diogo, R. (eds) Heads, Jaws, and Muscles. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-93560-7_7

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