Advertisement

The Origin and Evolution of Mammalian Head Muscles with Special Emphasis on the Facial Myology of Primates and Modern Humans

  • Rui DiogoEmail author
  • Vance Powell
Chapter
Part of the Fascinating Life Sciences book series (FLS)

Abstract

In this chapter we focus mainly on from where the head and neck muscles arose and how they evolved within the three major extant mammalian clades: monotremes, marsupials, and placentals. Within placentals, we pay special attention to primates, the group that includes our species, Homo sapiens. In fact, primates are an emblematic case study to show that, within the fascinating morphological diversity of hard and soft tissues of the head, including the jaws and the muscles that move them, the most evolvable and diverse ones are a group of muscles that is characteristic of, and played a crucial evolutionary role in, the Mammalia: the muscles of facial expression. As an example of mammalian diversity and also of an issue that is fundamental for the evolution of our own species as well as to illustrate the highly complex linkage between the evolutionary history of muscles, external characters, behavior, and ecology, we briefly comment on the relationships between facial expression, color patterns, mobility, and social group size during primate and human evolution. Furthermore, we also provide comments about data that have been made available in developmental studies on the ontogeny of the mammalian head muscles as an example of how developmental and evo-devo data can be combined with comparative anatomy in order to provide a more integrative understanding of the evolutionary history of the mammalian head.

Keywords

Human Facial Expression Behavior Evo-devo 

References

  1. Adams LA (1919) A memoir on the phylogeny of the jaw muscles in recent and fossils vertebrates. Ann NY Acad Sci 28:51–166CrossRefGoogle Scholar
  2. Allen WL, Stevens M, Higham JP (2014) Character displacement of Cercopithecini primate visual signals. Nat Commun 5:4266PubMedCrossRefPubMedCentralGoogle Scholar
  3. Andrew RJ (1963) Evolution of facial expression. Science 142:1034–1041PubMedCrossRefPubMedCentralGoogle Scholar
  4. Barghusen HR (1968) The lower jaw of cynodonts (Reptilia, Therapsida) and the evolutionary origin of mammal-like adductor jaw musculature. Postilla 116:1–49Google Scholar
  5. Barghusen HR (1986) On the evolutionary origin of the therian tensor veli palatini and tensor tympani muscles. In: Hotton N, MacLean PD, Roth JJ, Roth EC (eds) The ecology and biology of mammal-like reptiles. Smithsonian Institution Press, Washington, DC, pp 253–262Google Scholar
  6. Bemis WE (1984) Paedomorphosis and the evolution of Dipnoi. Paleobiology 10:293–307CrossRefGoogle Scholar
  7. Bemis WE (1986) Feeding mechanisms of living Dipnoi: anatomy and function. J Morphol 190(Suppl 1):249–275CrossRefGoogle Scholar
  8. Bischoff TLW (1840) Description Anatomique du Lepidosiren paradoxa. Ann Sci Nat 14(Ser 2):116–159Google Scholar
  9. Boas JEV, Paulli S (1908) The elephant head – studies in the comparative anatomy of the organs of the head of the Indian elephant and other mammals, 1: the facial muscles and the proboscis. Gustav Fischer, JenaCrossRefGoogle Scholar
  10. Brand-Saberi B (2002) Vertebrate myogenesis. Springer-Verlag, Heidelberg, BerlinCrossRefGoogle Scholar
  11. Brock GT (1938) The cranial muscles of the Gecko – a general account with a comparison of muscles in other gnathostomes. Proc Zool Soc Lond (Ser B) 108:735–761Google Scholar
  12. Bryant MD (1945) Phylogeny of Nearctic Sciuridae. Am Midland Nat 33:257–390CrossRefGoogle Scholar
  13. Burrows AM (2008) The facial expression musculature in primates and its evolutionary significance. BioEssays 30:212–225PubMedCrossRefPubMedCentralGoogle Scholar
  14. Burrows AM, Smith TD (2003) Muscles of facial expression in Otolemur with a comparison to Lemuroidea. Anat Rec 274:827–836CrossRefGoogle Scholar
  15. Burrows AM, Waller BM, Parr LA, Bonar CJ (2006) Muscles of facial expression in the chimpanzee (Pan troglodytes): descriptive, comparative and phylogenetic contexts. J Anat 208:153–167PubMedCrossRefPubMedCentralGoogle Scholar
  16. Butler AB, Hodos W (2005) Comparative vertebrate neuroanatomy: evolution and adaptation. Wiley Interscience, HobokenCrossRefGoogle Scholar
  17. Carroll AM, Wainwright PC (2003) Functional morphology of feeding in the sturgeon, Scaphirhyncus albus. J Morphol 256:270–284PubMedCrossRefPubMedCentralGoogle Scholar
  18. Carvajal JJ, Cox D, Summerbell D, Rigby PW (2001) A BAC transgenic analysis of the Mrf4/Myf5 locus reveals interdigitated elements that control activation and maintenance of gene expression during muscle development. Development 128(10):1857–1868PubMedPubMedCentralGoogle Scholar
  19. Cohen SR, Chen L, Trotman CA, Burdi AR (1993) Soft-palate myogenesis: a developmental field paradigm. Cleft Palate Craniofac J 30:441–446PubMedCrossRefPubMedCentralGoogle Scholar
  20. Cohen SR, Chen LL, Burdi AR, Trotman CA (1994) Patterns of abnormal myogenesis in human cleft palates. Cleft Palate Craniofac J 31(5):345–350PubMedCrossRefPubMedCentralGoogle Scholar
  21. Crompton AW (1963) The evolution of the mammalian jaw. Evolution 17:431–439CrossRefGoogle Scholar
  22. Crompton AW, Parker P (1978) Evolution of the mammalian masticatory apparatus: the fossil record shows how mammals evolved both complex chewing mechanisms and an effective middle ear, two structures that distinguish them from reptiles. Am Sci 66(2):192–201PubMedPubMedCentralGoogle Scholar
  23. Cuvier G, Laurillard L (1849) Recueil de planches de myologie, vol 3. Anatomie Comparée, ParisGoogle Scholar
  24. Czajkowski MT, Rassek C, Lenhard DC, Bröhl D, Birchmeier C (2014) Divergent and conserved roles of Dll1 signaling in development of craniofacial and trunk muscle. Dev Biol 395(2):307–316PubMedCrossRefPubMedCentralGoogle Scholar
  25. Danforth CH (1913) The myology of Polyodon. J Morphol 24:107–146CrossRefGoogle Scholar
  26. Didier DA (1987) Myology of the pectoral, branchial, and jaw regions of the ratfish Hydrolagus colliei (Holocephali). Honors Projects, paper 46, Illionois Wesleyan UniversityGoogle Scholar
  27. Didier DA (1995) Phylogenetic systematics of extant chimaeroid fishes (Holocephali, Chimaeroidei). Am Mus Novit 3119:86Google Scholar
  28. Diogo R (2007) On the origin and evolution of higher-clades: osteology, myology, phylogeny and macroevolution of bony fishes and the rise of tetrapods. Science, EnfieldGoogle Scholar
  29. Diogo R (2008) Comparative anatomy, homologies and evolution of the mandibular, hyoid and hypobranchial muscles of bony fish and tetrapods: a new insight. Anim Biol 58:123–172CrossRefGoogle Scholar
  30. Diogo R (2009) The head musculature of the Philippine colugo (Dermoptera: Cynocephalus volans), with a comparison to tree-shrews, primates and other mammals. J Morphol 270:14–51PubMedCrossRefPubMedCentralGoogle Scholar
  31. Diogo R, Abdala V (2007) Comparative anatomy, homologies and evolution of the pectoral muscles of bony fish and tetrapods: a new insight. J Morphol 268:504–517PubMedCrossRefPubMedCentralGoogle Scholar
  32. Diogo R, Abdala V (2010) Muscles of vertebrates: comparative anatomy, evolution, homologies and development. Taylor & Francis, OxfordCrossRefGoogle Scholar
  33. Diogo R, Molnar JL (2014) Comparative anatomy, evolution and homologies of the tetrapod hindlimb muscles, comparisons with forelimb muscles, and deconstruction of the forelimb-hindlimb serial homology hypothesis. Anat Rec 297:1047–1075CrossRefGoogle Scholar
  34. Diogo R, Santana SE (2017) Evolution of facial musculature and relationships with facial color patterns, mobility, social group size, development, birth defects and asymmetric use of facial expressions. In: Russel R, Dols JMF (eds) The science of facial expression. Oxford University Press, Oxford, pp 133–152Google Scholar
  35. Diogo R, Tanaka EM (2014) Development of fore- and hindlimb muscles in GFP-Transgenic axolotls: morphogenesis, the tetrapod Bauplan, and new insights on the forelimb-hindlimb enigma. J Exp Zool B Mol Dev Evol 322:106–127PubMedCrossRefPubMedCentralGoogle Scholar
  36. Diogo R, Wood B (2012) Comparative anatomy and phylogeny of primate muscles and human evolution. Taylor & Francis, OxfordGoogle Scholar
  37. Diogo R, Wood BA (2013) The broader evolutionary lessons to be learned from a comparative and phylogenetic analysis of primate muscle morphology. Biol Rev 88:988–1001PubMedCrossRefPubMedCentralGoogle Scholar
  38. Diogo R, Ziermann JM (2014) Development of fore- and hindlimb muscles in frogs: morphogenesis, homeotic transformations, digit reduction, and the forelimb-hindlimb enigma. J Exp Zool B Mol Dev Evol 322:86–105PubMedCrossRefPubMedCentralGoogle Scholar
  39. Diogo R, Ziermann JM (2015) Muscles of chondrichthyan paired appendages: comparison with osteichthyans, deconstruction of the fore-hindlimb serial homology dogma, and new insights on the evolution of the vertebrate neck. Anat Rec 298:513–530CrossRefGoogle Scholar
  40. Diogo R, Hinits Y, Hughes SM (2008a) Development of mandibular, hyoid and hypobranchial muscles in the zebrafish: homologies and evolution of these muscles within bony fishes and tetrapods. BMC Dev Biol 8:24–46PubMedCrossRefPubMedCentralGoogle Scholar
  41. Diogo R, Abdala V, Lonergan N, Wood BA (2008b) From fish to modern humans – comparative anatomy, homologies and evolution of the head and neck musculature. J Anat 213:391–424PubMedCrossRefPubMedCentralGoogle Scholar
  42. Diogo R, Abdala V, Aziz MA, Lonergan N, Wood BA (2009a) From fish to modern humans – comparative anatomy, homologies and evolution of the pectoral and forelimb musculature. J Anat 214:694–716PubMedCrossRefPubMedCentralGoogle Scholar
  43. Diogo R, Wood BA, Aziz MA, Burrows A (2009b) On the origin, homologies and evolution of primate facial muscles, with a particular focus on hominoids and a suggested unifying nomenclature for the facial muscles of the Mammalia. J Anat 215:300–319PubMedCrossRefPubMedCentralGoogle Scholar
  44. Diogo R, Linde-Medina M, Abdala V, Ashley–Ross MA (2013a) New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma. Biol Rev 88:196–214PubMedCrossRefPubMedCentralGoogle Scholar
  45. Diogo R, Murawala P, Tanaka EM (2013b) Is salamander hindlimb regeneration similar to that of the forelimb? Anatomical and morphogenetic analysis of hindlimb muscle regeneration in GFP transgenic axolotls as a basis for regenerative and developmental studies. J Anat 10:459–468Google Scholar
  46. Diogo R, Nacu E, Tanaka EM (2014) Is salamander limb regeneration really perfect? Anatomical and morphogenetic analysis of forelimb muscle regeneration in GFP-transgenic axolotls as a basis for regenerative, developmental and evolutionary studies. Anat Rec 297:1076–1089CrossRefGoogle Scholar
  47. Diogo R, Esteve-Altava B, Smith C, Boughner JC, Rasskin-Gutman D (2015a) Anatomical network comparison of human upper and lower, newborn and adult, and normal and abnormal limbs, with notes on development, pathology and limb serial homology vs. homoplasy. PLoS One 10:e0140030PubMedCrossRefPubMedCentralGoogle Scholar
  48. Diogo R, Kelly R, Christiaen L, Levine M, Ziermann JM, Molnar J, Noden D, Tzahor E (2015b) A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature 520:466–473PubMedCrossRefPubMedCentralGoogle Scholar
  49. Diogo R, Ziermann JM, Linde-Medina M (2015c) Is evolutionary biology becoming too politically correct? A reflection on the scala naturae, phylogenetically basal clades, anatomically plesiomorphic taxa, and ‘lower’ animals. Biol Rev 90:502–521PubMedCrossRefPubMedCentralGoogle Scholar
  50. Diogo R, Ziermann JM, Linde-Medina M (2015d) Specialize or risk disappearance – empirical evidence of anisomerism based on comparative and developmental studies of gnathostome head and limb musculature. Biol Rev 90:964–978PubMedCrossRefPubMedCentralGoogle Scholar
  51. Diogo R, Bello-Hellegouarch G, Kohlsdorf T, Esteve-Altava B, Molnar J (2016) Comparative myology and evolution of marsupials and other vertebrates, with notes on complexity, Bauplan, and “Scala Naturae”. Anat Rec 299:1224–1255CrossRefGoogle Scholar
  52. Diogo R, Molnar JL, Wood BA (2017) Bonobo anatomy reveals stasis and mosaicism in chimpanzee evolution, and supports bonobos as the most appropriate extant model for the common ancestor of chimpanzees and humans. Nat Sci Rep 7:608CrossRefGoogle Scholar
  53. Diogo R, Ziermann JM, Molnar J, Siomava N, Abdala V (2018) Muscles of chordates: development, homologies and evolution. Taylor & Francis, OxfordCrossRefGoogle Scholar
  54. Edgeworth FH (1935) The cranial muscles of vertebrates. Cambridge University Press, CambridgeGoogle Scholar
  55. Epperlein H-H, Khattak S, Knapp D, Tanaka EM, Malashichev Y (2012) Neural crest does not contribute to the neck and shoulder in the Axolotl (Ambystoma mexicanum). PLoS One 7:e52244PubMedCrossRefPubMedCentralGoogle Scholar
  56. Ericsson R, Knight R, Johanson Z (2013) Evolution and development of the vertebrate neck. J Anat 222:67–78PubMedCrossRefPubMedCentralGoogle Scholar
  57. Gasser RF (1967) The development of the facial muscles in man. Am J Anat 120:357–376CrossRefGoogle Scholar
  58. Gaupp E (1896) A. Ecker’s und R. Wiedersheim’s Anatomie des Frosches, part 1. Friedrich Vieweg und Sohn, BraunschweigGoogle Scholar
  59. Gaupp E (1912) De Reichertsche Theorie. (Hammer-, amboss- und Kerferfrage). Arch Anat Physiol Suppl:1–416Google Scholar
  60. Goodrich ES (1958) Studies on the structure and development of vertebrates. Dover Publications, New YorkGoogle Scholar
  61. Gopalakrishnan S, Comai G, Sambasivan R, Francou A, Kelly RG, Tajbakhsh S (2015) A cranial mesoderm origin for esophagus striated muscles. Dev Cell 34:694–704PubMedCrossRefPubMedCentralGoogle Scholar
  62. Greenwood PH (1977) Notes on the anatomy and classification of elopomorph fishes. Bull Br Mus Nat Hist (Zool) 32:65–103Google Scholar
  63. Grimaldi A, Parada C, Chai Y (2015) A comprehensive study of soft palate development in mice. PLoS One 10(12):e0145018PubMedCrossRefPubMedCentralGoogle Scholar
  64. Harel I, Nathan E, Tirosh-Finkel L, Zigdon H, Guimarães-Camboa N, Evans SM, Tzahor E (2009) Distinct origins and genetic programs of head muscle satellite cells. Dev Cell 16:822–832PubMedCrossRefPubMedCentralGoogle Scholar
  65. Haugen I-BK (2002) Neuromuscular organization of mammalian extraocular muscles. Rap Hogskolen Buskerud 36:1–56Google Scholar
  66. House EL (1953) A myology of the pharyngeal region of the albino rat. Anat Rec 116:363–381PubMedCrossRefPubMedCentralGoogle Scholar
  67. Huber E (1930a) Evolution of facial musculature and cutaneous field of trigeminus – Part I. Q Rev Biol 5:133–188CrossRefGoogle Scholar
  68. Huber E (1930b) Evolution of facial musculature and cutaneous field of trigeminus – Part II. Q Rev Biol 5:389–437CrossRefGoogle Scholar
  69. Huber E (1931) Evolution of facial musculature and expression. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  70. Jarvik E (1963) The composition of the intermandibular division of the head in fishes and tetrapods and the diphyletic origin of the tetrapod tongue. Kungl Sven Veten Handl 9:1–74Google Scholar
  71. Johanson Z (2003) Placoderm branchial and hypobranchial muscles and origins in jawed vertebrates. J Vert Paleont 23:735–749CrossRefGoogle Scholar
  72. Jollie M (1982) Ventral branchial musculature and synapomorphies questioned. Zool J Linnean Soc 75:35–47CrossRefGoogle Scholar
  73. Jouffroy FK (1971) Musculature des membres. In: Grassé PP (ed) Traité de Zoologie, XVI: 3 (Mammifères). Masson et Cie, Paris, pp 1–475Google Scholar
  74. Jouffroy FK, Lessertisseur J (1971) Particularités musculaires des Monotrémes – musculature post-craniénne. In: Grassé PP (ed) Traité de Zoologie, XVI: 3 (Mammifères). Masson et Cie, Paris, pp 679–836Google Scholar
  75. Jouffroy FK, Saban R (1971) Musculature peaucière. In: Grassé PP (ed) Traité de Zoologie, XVI: 3 (Mammifères). Masson et Cie, Paris, pp 477–611Google Scholar
  76. Kardong KV (2002) Vertebrates: comparative anatomy, function, evolution, 3rd edn. McGraw-Hill, New YorkGoogle Scholar
  77. Kardong KV (2011) Vertebrates: comparative anatomy, function, evolution, 7th edn. Mcgraw-Hill, BostonGoogle Scholar
  78. Kesteven HL (1942–1945) The evolution of the skull and the cephalic muscles. Mem Austr Mus 8:1–361CrossRefGoogle Scholar
  79. Kingdon J (1992) Facial patterns as signals and masks. In: Jones S (ed) The Cambridge encyclopedia of human evolution. Cambridge University Press, Cambridge, pp 161–165Google Scholar
  80. Kingdon J (2007) Primate visual signals in noisy environments. Folia Primatol (Basel) 78:389–404CrossRefGoogle Scholar
  81. Kishimoto H, Yamada S, Kanahashi T, Yoneyama A, Imai H, Matsuda T, Takeda T, Kawai K, Suzuki S (2016) Three-dimensional imaging of palatal muscles in the human embryo and fetus: development of levator veli palatini and clinical importance of the lesser palatine nerve. Dev Dyn 245:123–131PubMedCrossRefPubMedCentralGoogle Scholar
  82. Kleinteich T, Haas A (2007) Cranial musculature in the larva of the caecilian, Ichthyophis kohtaoensis (Lissamphibia: Gymnophiona). J Morphol 268:74–88PubMedCrossRefPubMedCentralGoogle Scholar
  83. Knight RD, Mebus K, Roehl HH (2008) Mandibular arch muscle identity is regulated by a conserved molecular process during vertebrate development. J Exp Zool Mol Dev Evol 310B:355–369CrossRefGoogle Scholar
  84. Köntges G, Lumsden A (1996) Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development 122:3229–3242PubMedPubMedCentralGoogle Scholar
  85. Larsen JH, Guthrie DJ (1975) The feeding system of terrestrial tiger salamanders (Ambystoma tigrinum melanostictum Baird). J Morphol 147:137–154PubMedCrossRefPubMedCentralGoogle Scholar
  86. Lauder GV, Shaffer HB (1985) Functional morphology of the feeding mechanism in aquatic ambystomatid salamanders. J Morphol 185:297–326PubMedCrossRefPubMedCentralGoogle Scholar
  87. Lautenschlager S, Gill P, Luo ZX, Fagan MJ, Rayfield EJ (2017) Morphological evolution of the mammalian jaw adductor complex. Biol Rev Camb Philos Soc 92(4):1910–1940PubMedCrossRefPubMedCentralGoogle Scholar
  88. Lescroart F, Kelly RG, Le Garrec JF, Nicolas JF, 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
  89. 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(5):1446–1451PubMedCrossRefPubMedCentralGoogle Scholar
  90. Lightoller GS (1928a) The action of the m. mentalis in the expression of the emotion of distress. J Anat 62:319–332PubMedPubMedCentralGoogle Scholar
  91. Lightoller GS (1928b) The facial muscles of three orangutans and two cercopithecidae. J Anat 63:19–81PubMedPubMedCentralGoogle Scholar
  92. Lightoller GS (1934) The facial musculature of some lesser primates and a Tupaia. Proc Zool Soc Lond 1934:259–309CrossRefGoogle Scholar
  93. Lightoller GS (1939) V. Probable homologues. A study of the comparative anatomy of the mandibular and hyoid arches and their musculature – Part I. Comparative myology. Trans Zool Soc Lond 24:349–382CrossRefGoogle Scholar
  94. Lightoller GS (1940a) The comparative morphology of the platysma: a comparative study of the sphincter colli profundus and the trachelo-platysma. J Anat 74:390–396PubMedPubMedCentralGoogle Scholar
  95. Lightoller GS (1940b) The comparative morphology of the M. caninus. J Anat 74:397–402PubMedPubMedCentralGoogle Scholar
  96. Lightoller GS (1942) Matrices of the facialis musculature: homologization of the musculature in monotremes with that of marsupials and placentals. J Anat 76:258–269PubMedPubMedCentralGoogle Scholar
  97. Lubosch W (1914) Vergleischende anatomie der kaumusculatur der Wirbeltiere, in fünf teilen: 1 – die kausmukulatur der Amphibien. Jen Z Naturwiss 53:51–188Google Scholar
  98. Mallat J (1997) Shark pharyngeal muscles and early vertebrate evolution. Acta Zool 78:279–294CrossRefGoogle Scholar
  99. Marion E (1905) Mandibular and pharyngeal muscles of Acanthias and Raia. Am Nat 39:891–924CrossRefGoogle Scholar
  100. 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 436:347–355PubMedCrossRefPubMedCentralGoogle Scholar
  101. Millot J, Anthony J (1958) Anatomie de Latimeria chalumnae – I, squelette, muscles, et formation de soutiens. CNRS, ParisGoogle Scholar
  102. Minkoff EC, Mikkelsen P, Cunningham WA, Taylor KW (1979) The facial musculature of the opossum (Didelphis virginiana). J Mammal 60:46–57CrossRefGoogle Scholar
  103. Miyake T, McEachran JD, Hall BK (1992) Edgeworth’s legacy of cranial muscle development with an analysis of muscles in the ventral gill arch region of batoid fishes (Chondrichthyes: Batoidea). J Morphol 212:213–256PubMedCrossRefPubMedCentralGoogle Scholar
  104. Murie J, Mivart ST (1869) On the anatomy of the Lemuroidea. Trans Zool Soc Lond 7:1–113CrossRefGoogle Scholar
  105. Noden DM, Francis-West P (2006) The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:1194–1218PubMedCrossRefPubMedCentralGoogle Scholar
  106. Noden DM, Schneider RA (2006) Neural crest cells and the community of plan for craniofacial development: historical debates and current perspectives. In: Saint-Jeannet J (ed) Neural crest induction & differentiation – advances in experimental medicine and biology, vol 589. Landes Bioscience, Georgetown, pp 1–31CrossRefGoogle Scholar
  107. Osse JWM (1969) Functional morphology of the head of the perch (Perca fluviatilis L.): an electromyographic study. Neth J Zool 19:289–392CrossRefGoogle Scholar
  108. Owen R (1841) Description of the Lepidosiren annectens. Trans Linn Soc Lond 18:327–361CrossRefGoogle Scholar
  109. Parada C, Han D, Chai Y (2012) Molecular and cellular regulatory mechanisms of tongue myogenesis. J Dent Res 91:528–535PubMedCrossRefPubMedCentralGoogle 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 cranialmost somites revealed by long-term fate mapping in the Mexican axolotl (Ambystoma mexicanum). Evol Dev 9:566–578PubMedCrossRefPubMedCentralGoogle Scholar
  112. Pollard HB (1892) On the anatomy and phylogenetic position of Polypterus. Zool Jahrb 5:387–428Google Scholar
  113. Preuschoft S (2000) Primate faces and facial expressions. Soc Res 67:245–271Google Scholar
  114. Reichert KB (1937) Über die Visceralbogen der Wirbelthiere im Allgemeinen und deren Metamorphosen bei den Vögeln und Säugethieren. Arch Anat Physiol Wissensch Med 1837:120–220Google Scholar
  115. Reilly S, Lauder GV (1989) Kinetics of tongue projection in Ambystoma tigrinum: quantitative kinematics, muscle function and evolutionary hypotheses. J Morphol 199:223–243PubMedCrossRefPubMedCentralGoogle Scholar
  116. Reilly S, Lauder GV (1990) The evolution of tetrapod feeding behavior: kinematic homologies in prey transport. Evolution 44:1542–1557PubMedCrossRefPubMedCentralGoogle Scholar
  117. Reilly S, Lauder GV (1991) Prey transport in the tiger salamander: quantitative electromyography and muscle function in tetrapods. J Exp Zool 260:1–17CrossRefGoogle Scholar
  118. Rodríguez-Vázquez JF, Sakiyama K, Abe H, Amano O, Murakami G (2016) Fetal Tendinous connection between the tensor tympani and tensor veli palatini muscles: a single digastric muscle acting for morphogenesis of the cranial base. Anat Rec 299:474–483CrossRefGoogle Scholar
  119. Ruge G (1885) Über die Gesichtsmuskulatur der Halbaffen. Morph Jahrb 11:243–315Google Scholar
  120. Ruge G (1897) Über das peripherische Gebiet des nervus facialis boi Wirbelthieren, vol 3. Festschr f Gegenbaur, LeipzigGoogle Scholar
  121. Ruge G (1910) Verbindungen des Platysma mit der tiefen Muskulatur des Halses beim Menschen. Morph Jahrb 41:708–724Google Scholar
  122. Saban R (1968) Musculature de la tête. In: Grassé PP (ed) Traité de Zoologie, XVI: 3 (Mammifères). Masson et Cie, Paris, pp 229–472Google Scholar
  123. Saban R (1971) Particularités musculaires des Monotrémes—musculature de la tête. In: Grassé PP (ed) Traité de Zoologie, XVI: 3 (Mammifères). Masson et Cie, Paris, pp 681–732Google Scholar
  124. Santana SE, Dobson SD, Diogo R (2014) Plain faces are more expressive: comparative study of facial color, mobility and musculature in primates. Biol Letters 10:20140275CrossRefGoogle Scholar
  125. Schaeffer JP (1929) Some problems in genesis and development with special reference to the human palate. Int J Orthod 15:291–310Google Scholar
  126. Schmidt KL, Cohn JF (2001) Human facial expressions as adaptations: evolutionary questions in facial expression research. Yearb Phys Anthropol 44:3–24CrossRefGoogle Scholar
  127. Schumacher GH (1973) The head muscles and hyolaryngeal skeleton of turtles and crocodilians. In: Gans C, Parsons TS (eds) Biology of the reptilia, vol 14. Academic Press, New York, pp 101–199Google Scholar
  128. Sefton EM, Bhullar BAS, Mohaddes Z, Hanken J (2016) Evolution of the head-trunk interface in tetrapod vertebrates. eLife 5:e09972PubMedCrossRefPubMedCentralGoogle Scholar
  129. Seiler R (1971a) A comparison between the facial muscles of Catarrhini with long and short muzzles. In: Proc. 3rd Int. Congr. Primat., Zürich 1970, vol l. Karger, Basel, pp 157–162Google Scholar
  130. Seiler R (1971b) Facial musculature and its influence on the facial bones of catarrhinous Primates. I. Morphol Jahrb 116:122–142Google Scholar
  131. Seiler R (1971c) Facial musculature and its influence on the facial bones of catarrhine Primates. II. Morphol Jahrb 116:147–185Google Scholar
  132. Seiler R (1971d) Facial musculature and its influence on the facial bones of catarrhine Primates. III. Morphol Jahrb 116:347–376Google Scholar
  133. Seiler R (1971e) Facial musculature and its influence on the facial bones of catarrhine Primates. IV. Morphol Jahrb 116:456–481Google Scholar
  134. Seiler R (1974a) Muscles of the external ear and their function in man, chimpanzees and Macaca. Morphol Jahrb 120:78–122Google Scholar
  135. Seiler R (1974b) Particularities in facial muscles of Daubentonia madagascariensis (Gmelin 1788). Folia Primatol 22:81–96PubMedCrossRefPubMedCentralGoogle Scholar
  136. Seiler R (1975) On the facial muscles in Perodicticus potto and Nycticebus coucang. Folia Primatol 23:275–289PubMedCrossRefPubMedCentralGoogle Scholar
  137. Seiler R (1979) Criteria of the homology and phylogeny of facial muscles in primates including man. I. Prosimia and Platyrrhina. Morphol Jahrb 125:191–217Google Scholar
  138. Seiler R (1980) Ontogenesis of facial muscles in primates. Morphol Jahrb 126:841–864Google Scholar
  139. Sewertzoff AN (1928) The head skeleton and muscles of Acipenser ruthenus. Acta Zool-Stockholm 9:193–319CrossRefGoogle Scholar
  140. Shearman RM, Burke AC (2009) The lateral somitic frontier in ontogeny and phylogeny. J Exp Biol Mol Dev Evol 312B:602–613Google Scholar
  141. Sherwood CC, Hof PR, Holloway RL, Semendeferi K, Gannon PJ, Frahm HD, Zilles K (2005) Evolution of the brainstem orofacial motor system in primates: a comparative study of trigeminal, facial, and hypoglossal nuclei. J Hum Evol 48:45–84PubMedCrossRefPubMedCentralGoogle Scholar
  142. Smith KK (1992) The evolution of the mammalian pharynx. Zool J Linnean Soc 104:313–349CrossRefGoogle Scholar
  143. Smith KK (1994) Development of craniofacial musculature in Monodelphis domestica (Marsupialia: Didelphidae). J Morphol 222:149–173PubMedCrossRefPubMedCentralGoogle Scholar
  144. Sokoloff AJ, Deacon TW (1992) Musculotopic organization of the hypoglossal nucleus in the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 324:81–93PubMedCrossRefPubMedCentralGoogle Scholar
  145. Sprague JM (1942) The hyoid apparatus of Neotoma. J Mammal 23:405–411CrossRefGoogle Scholar
  146. Sprague JA (1943) The hyoid region of placental mammals with special reference to the bats. Am J Anat 72:385–472CrossRefGoogle Scholar
  147. Sprague JA (1944a) The hyoid region in the insectivora. Am J Anat 74:175–216CrossRefGoogle Scholar
  148. Sprague JA (1944b) The innervation of the pharynx in the rhesus monkey, and the formation of the pharyngeal plexus in primates. Anat Rec 90:197–208CrossRefGoogle Scholar
  149. Surlykke A, Miller LA, Møhl B, Andersen BB, Christensen-Dalsgaard J, Buhl Jørgensen M (1993) Echolocation in two very small bats from Thailand Craseonycteris thonglongyai and Myotis siligorensis. Behav Ecol Sociobiol 33(1):1–12CrossRefGoogle Scholar
  150. Symington J (1898) The marsupial larynx. J Anat Physiol 33:31–49PubMedPubMedCentralGoogle Scholar
  151. Tada M, Kuratani S (2015) Evolutional and developmental understanding of the spinal accessory nerve. Zool Lett 1:4CrossRefGoogle Scholar
  152. Tajbakhsh S, Rocancourt D, Cossu G et al (1997) Redefining the genetic hierarchies controlling skeletal myogenesis: Pax-3 and Myf-5 act upstream of MyoD. Cell 89:127–138PubMedCrossRefPubMedCentralGoogle Scholar
  153. Terminologia Anatomica (1998) Federative Committee on anatomical terminology. Georg Thieme, StuttgardGoogle Scholar
  154. Theis S, Patel K, Valasek P et al (2010) The occipital lateral plate mesoderm is a novel source for vertebrate neck musculature. Development 137:2961–2971PubMedCrossRefPubMedCentralGoogle Scholar
  155. Wiley EO (1979a) Ventral gill arch muscles and the interrelationships of gnathostomes, with a new classification of the vertebrata. J Linn Soc Lond (Zool) 67:149–179CrossRefGoogle Scholar
  156. Wiley EO (1979b) Ventral gill arch muscles and the phylogenetic interrelationships of Latimeria. Occ Pap Calif Acad Sci 134:56–67Google Scholar
  157. Wilga CD, Wainwright PC, Motta PJ (2000) Evolution of jaw depression mechanisms in aquatic vertebrates: insights from Chondrichthyes. Biol J Linn Soc 71:165–185CrossRefGoogle Scholar
  158. Witmer LM (1995) Homology of facial structures in extant archosaurs (birds and crocodilians), with special reference to paranasal pneumaticity and nasal conchae. J Morphol 225:269–327PubMedCrossRefGoogle Scholar
  159. Ziermann J, Miyashita T, Diogo R (2014) 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

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of AnatomyHoward UniversityWashington, DCUSA
  2. 2.CASHP, Department of AnthropologyGeorge Washington UniversityWashington, DCUSA

Personalised recommendations