Casey M. Holliday

Home

Research Interests

Vertebrate Functional Morphology & Evolution

 

Archosaur Adductor Chamber Homology: integration of musculoskeletal and topological criteria in jaw muscle homology

C. M. Holliday and L. M. Witmer. 2007. Journal of Morphology 268:457-484.

Download pdf

The homology of jaw muscles in reptiles has been difficult to ascertain because of the divergent skulls extant groups, such as lizards, crocodilians, and birds, have evolved. This was the first study to incorporate data from muscle attachments with topological patterns of the trigeminal nerve, blood vessels, and other soft tissues in order to identify evolutionarily similar structures. The study used dissection, vascular injection, CT scanning and a number of other methods to study the anatomy of the adductor chamber in over 100 extant taxa. With these new data, the study reviewed and synonymized nervous and muscular structures  from previous analyses conducted over the past century and made several new findings.

 — Despite their extreme morphological differences, birds and lizards share many similar soft-tissue topological patterns and the trigeminal nerve and its smaller branches can be used to identify muscles.

— However, certain muscles in birds have undergone significant shifts in attachment position, such as M. adductor mandibulae posterior, which in many taxa attaches on the lateral surface of the mandible, rather than the medial surface (as found in lizards and crocs).

— Crocodylians (extant crocodilians) have significantly modified the topology of the jaw muscles and trigeminal nerve such that M. pseudotemporalis does not occupy portions of the dorsotemporal fossa and lies lateral, rather than medial to the maxillary nerve.

— M. adductor mandibulae medialis is relatively easy to identify in lizards because of its attachments to a large aponeurosis (the bodenaponeurosis). However, a lack of clear correlates makes the identification of this muscle tenuous in extant archosaurs.

— M. intramandibularis is not likely a separate muscle in crocodylians, turtles, and some birds, but instead simply the ventral portion of a temporal muscle (e.g., M. pseudotemporalis superficialis in crocs) that has a fibrocartilaginous sesamoid in it.

—Smaller sensory branches of the trigeminal nerve (e.g., n. anguli oris, n. supraorbitalis) project to homologous skin surfaces  (e.g., the rictus, temporal region) regardless of head shape suggesting evolutionarily conservative cephalic dermatomes are present in reptiles and can be used as topological criteria in tests of homology.

These data shed new light on the evolution of the modern archosaurian, and reptilian conditions and will not only serve as a basic anatomical atlas of living animals, but also form the anatomical foundation for further studies of head anatomy in fossil taxa such as non-avian dinosaurs and crocodyliforms.

 

 

Funded by: National Science Foundation: IBN-0407735, IBN-9601174, IOB-0343744; Contract grant sponsors: The Jurassic Foundation; UCMP Sam Welles Fund; Society of Vertebrate Paleontology; OU Student Enhancement Award; OU Graduate Student Senate; OU Departments of Biological and Biomedical Sciences.

Select Images for High Resolution Figures

 

Fig 1. The trigeminal topological paradigm. Neuromuscular topological organization of the adductor chamber in left dorsal view, as shown in schematic of Sphenodon. A: Major muscle compartments defined by their positions relative to the trigeminal divisions. B: Individual muscles within each compartment. gMM, maxillomandibular ganglion; gV1, ophthalmic ganglion; mAMI, Musculus (M) adductor mandibulae internus; mAME, M. adductor mandibulae externus; mAMEM, M. adductor mandibulae externus medialis; mAMEP, M. adductor mandibulae externus profundus; mAMES, M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mCID, M. constrictor internus dorsalis; mLPt, M. levator pterygoideus; mPPt, M. protractor pterygoideus; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPTd+v, M. pterygoideus dorsalis and ventralis; mTP, M. tensor periorbitae;V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve. Fig. 2. Cladogram depicting phylogenetic relationships of focal taxa and outgroups used in this study. Numerical codes indicate nodal taxa: 1, Amniota; 2, Sauropsida; 3, Diapsida; 4, Lepidosauria; 5, Archosauria; 6, Neornithes; 7, Paleognathae; 8, Neognathae; 9, Neoaves. Topology follows Gauthier (1986), Cracraft (1986), Brochu (1999), Cracraft and Clarke (2001), and Mayr and Clarke (2003). Fig. 3. Overview of adductor chamber and its contents. A: Reference image of axial section through Iguana iguana depicting the location of the slice schematized in B-D. B-D: Schematics of axial sections of plesiomorphic sauropsid adductor chamber in left caudal view. B: Major regions and muscular subunits of adductor chamber using musculoskeletal criteria. C: Major muscular subunits using trigeminal topological paradigm criteria. D: Major muscles of interest discussed in this paper. bs, basisphenoid; ept, epipterygoid; gV, trigeminal ganglion; ls, laterosphenoid; mAMI, Musculus (M) adductor mandibulae internus; mAME, M. adductor mandibulae externus; mAMEP, M. adductor mandibulae externus profundus; mAMEM, M. adductor mandibulae externus medialis; mAMES, M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mCID, M. constrictor internus dorsalis; mLPt, M. levator pterygoideus; ml, membrane limitans; mn, mandible; mPPt, M. protractor pterygoideus; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPT, M. pterygoideus; mTP, M. tensor periorbitae; pa, parietal; po, postorbital; pt, pterygoid; pr, prootic; sq, squamosal;V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve.
Fig. 4. Skulls of representative sauropsid taxa in left lateral view indicating attachment areas of important muscles. A: Sphenodon punctatus. B: Alligator mississippiensis. C: Struthio camelus. D: Ardea herodias. mAMI, Musculus (M) adductor mandibulae internus; mAME, M. adductor mandibulae externus; mAMEP, M. adductor mandibulae externus profundus; mAMEM, M. adductor mandibulae externus medialis; mAMES, M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mCID, M. constrictor internus dorsalis; mLPt, M. levator pterygoideus; mPPt, M. protractor pterygoideus; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPT, M. pterygoideus; mTP, M. tensor periorbitae. Fig. 5. Schematics of serial, horizontal sections of the left adductor chamber of Alligator mississippiensis in dorsal view. A-E: Sections proceed dorsal to ventral. F: Denotes location of sections in head. a, vIO, infraorbital artery and vein; a, vJU, jugal artery and vein; a, vM, mandibular artery and vein; a, vMM, maxillomandibular artery and vein; an, angular; ar, articular; aTO, temporoorbital artery; ce, cerebrum; ch, choana; ct, cartilago transiliens; dvs, dural venous sinus; ec, ectopterygoid; gMN; harderian gland; gV, trigeminal ganglion; h, hypophysis; ju, jugal; lb, lateral bridge of the laterosphenoid; ls, laterosphenoid; mAMEP, M. adductor mandibulae externus profundus; mAMEM, M. adductor mandibulae externus medialis; mAMES, M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mBM, M. branchiomandibularis; mDM, M. depressor mandibulae; mIRA, M. intramandibularis; mOD, M. obiquus dorsalis; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPTd, M. pterygoideus dorsalis; mPTv, M. pterygoideus ventralis; mRD, M. rectus dorsalis; mRL, M. rectus lateralis; mRV, M. rectus ventralis; mTP, M. tensor periorbitae; nAO, ramus to the corner of the mouth (anguli oris) of the mandibular nerve; nPTc, caudal branch of the pterygoid ramus of the mandibular nerve; pa, parietal; pe, periorbita; pr, prootic; ptb, pterygoid buttress; qj, quadratojugal; qu, quadrate; ri, rictus; sa, surangular; t, tarsus for M. depressor auriculae inferioris; V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve. Fig. 6. Schematics of serial, horizontal sections of the left adductor chamber of Struthio camelus in dorsal view. A-E: Sections proceed dorsal to ventral. F: Denotes location of sections in head. ar, articular; bs, basisphenoid; dp, diploe; gLA, lacrimal gland; gMN, Harderian gland; ju, jugal, l, labyrinth; ls, laterosphenoid; mAME, musculus (M) adductor mandibulae externus; mAMEP, M. adductor mandibulae externus profundus; mAMES; M. adductor mandibulae externus superficialis; mAMP; M. adductor mandibulae posterior; mDM, M. depressor mandibulae; mIRA; M. intramandibularis; mOD, M. obliquus dorsalis; mPPq, M. protractor quadratus; mPPt, M. protractor pterygoideus; mPSTp; M. pseudotemporalis profundus; mPSTs; M. pseudotemporalis superficialis; mPTd, M. pterygoideus dorsalis; mPTv, M. pterygoideus ventralis; mRD, M. rectus dorsalis; mRL, M. rectus lateralis; mRM, M. rectus medialis; mRV, M. rectus ventralis; mTP, M. tensor periorbitae; pe, periorbita; pop; postorbital process; q, quadrate; ri, rictus; rOP, ophthalmic rete; sf, superficial fatty tissue; sq, squamosal; tc, tympanic cavity; V2, maxillary nerve; V3, mandibular nerve.
Fig. 7. Major features of the adductor chamber of Iguana iguana in left lateral view. Image is composite based on CT data for skeletal anatomy and dissections for soft-tissue anatomy. A: Head skeleton. B: Superficial dissection (M. levator anguli oris omitted). C: Intermediate depth. D: Deep dissection. aTO, temporoorbital artery; aTS, superficial temporal artery; mAMEM, musculus (M) adductor mandibulae externus medialis; mAMEP, M. adductor mandibulae externus profundus; mAMES, M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mLPt, M. levator pterygoideus; mPPt, M. protractor pterygoideus; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPT, M. pterygoideus; nAO, ramus to the corner of the mouth (anguli oris) of the mandibular nerve; nCA, caudal ramus of the mandibular nerve; nCID, motor ramus to the constrictor internus dorsalis muscles of the mandibular nerve; nFR, frontal ramus of the ophthalmic nerve; nPT, pterygoid ramus of the mandibular nerve; nSO, supraorbital ramus of the maxillary nerve; pa, parietal; po, postorbital; pr, prootic; pt, pterygoid; qu, quadrate; sq, squamosal; V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve. Fig. 8. Major features of the adductor chamber of Alligator mississippiensis in left lateral view. Image is composite based on CT data for skeletal anatomy and dissections for soft-tissue anatomy. A: Head skeleton. B: Superficial dissection. C: Intermediate depth. D: Deep dissection. E: deepest dissection. aTO, temporoorbital artery; aTS, superficial temporal artery; ct, cartilago transiliens; eam, external acoustic meatus; gV, trigeminal ganglion; ju, jugal; lb, lateral bridge of the laterosphenoid; ls, laterosphenoid; mAMEM, musculus (M) adductor mandibulae medialis; mAMEP, M. adductor mandibulae externus profundus; M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mIRA, M. intramandibularis; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPTd, M. pterygoideus dorsalis; mPTv, M. pterygoideus ventralis; nAO, ramus to the corner of the mouth (anguli oris) of the mandibular nerve; nCA, caudal ramus of the mandibular nerve; nCID, motor ramus to the constrictor internus dorsalis muscles of the mandibular nerve; nFR, frontal ramus of the ophthalmic nerve; nJU, jugal branch of the maxillary nerve; nPTc, caudal branch of the pterygoid ramus of the mandibular nerve; nPTr, rostral branch of the pterygoid ramus of the mandibular nerve; nSO, supraorbital branch of the maxillary nerve; po, postorbital; ptb, pterygoid buttress; qj, quadratojugal; V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve. Fig. 9. Major features of the adductor chamber of Phoebastria immutabilis in left lateral view. Image is composite based on CT data for skeletal anatomy and dissections for soft-tissue anatomy. A: Head skeleton. B: Superficial dissection (jugal omitted). C: Intermediate depth. D: Deep dissection. aOC, occipital artery; aTO, temporoorbital artery; aTS, superficial temporal artery; eam, external acoustic meatus; mAMEP musculus (M) adductor mandibulae externus profundus; M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mIRA, M. intramandibularis; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPTd, M. pterygoideus dorsalis; mPTv, M. pterygoideus ventralis; mPPq, M. protractor quadratus; mPPt, M. protractor pterygoideus; mPSTa, M. pseudotemporalis superficialis pars absconditum; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPTd, M. pterygoideus dorsalis; mPTv, M. pterygoideus ventralis; nAO, ramus to the corner of the mouth (anguli oris) of the mandibular nerve; nCA, caudal ramus of the mandibular nerve; nCID, motor ramus to the constrictor internus dorsalis muscles of the mandibular nerve; nFR, frontal ramus of the ophthalmic nerve; nJU, jugal branch of the maxillary nerve; nPT, pterygoid ramus of the mandibular nerve; nSO, supraorbital branch of the maxillary nerve; qu, quadrate; 1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve.
Fig. 10. Musculoskeletal patterns of right mandible in representative diapsid clades in medial view. A: Lepidosauria. B: Crocodylia. C: Palaeognathae. D: Neognathae. Note: pterygoideus muscles are not figured for sake of clarity. cp, coronoid process; ct, cartilago transiliens; mAMEM, musculus (M) adductor mandibulae externus medialis; mAMEP, M. adductor mandibulae externus profundus; M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mIRA, M. intramandibularis; mmf, medial mandibular fossa; mmp, medial mandibular process; rap, retroarticular process. Fig. 11. Musculoskeletal patterns of the right dorsotemporal fossa in representative diapsid clades in dorsal view. A: Lepidosauria. B: Crocodylia. C: Paleognathae. D: Neoaves. ls, laterosphenoid; mAMEM, musculus (M) adductor mandibulae externus medialis; mAMEP, M. adductor mandibulae externus profundus; M. adductor mandibulae externus superficialis; mPSTs, M. pseudotemporalis superficialis; mTP, M. tensor periorbitae; pa, parietal; po, postorbital; pr, prootic; sq; squamosal. Fig. 12. Topological patterns of muscles, nerves, and vessels in the adductor chamber of sauropsids. Orientation as in Figure 1. A: Plesiomorphic condition common to Lepidosauria and Testudines. B: Extant crocodylian condition. C: Typical extant avian condition. ?, unclear presence of mAMEM; aPR, profundus branch of the temporoorbital artery; aSP, sphenopalatine artery; aST, stapedial artery; aTO, temporoorbital artery; aTR, rostral trigeminal artery; gMM, maxillomandibular ganglion; gV1, ophthalmic ganglion; mAMEM, musculus (M) adductor mandibulae externus medialis; mAMEP, M. adductor mandibulae externus profundus; mAMES, M. adductor mandibulae externus superficialis; mAMP, M. adductor mandibulae posterior; mLPt, M. levator pterygoideus; mPPt, M. protractor pterygoideus; mPSTp, M. pseudotemporalis profundus; mPSTs, M. pseudotemporalis superficialis; mPT, M. pterygoideus; mTP, M. tensor periorbitae; nAO, ramus to the corner of the mouth (anguli oris) of the mandibular nerve; nCA, caudal ramus of the mandibular nerve; nCID, motor ramus to the constrictor internus dorsalis muscles of the mandibular nerve; nFR, frontal ramus of the ophthalmic nerve; nJU, jugal branch of the maxillary nerve; nPT, pterygoid ramus of the mandibular nerve; nPTc, caudal branch of the pterygoid ramus of the mandibular nerve; nPTr, rostral branch of the pterygoid ramus of the mandibular nerve; nSO, supraorbital branch of the maxillary nerve;V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve; vSP, sphenopalatine vein.
Fig. 13. Parsimony analysis of muscle homology hypotheses within the dorsotemporal fossa of crocodylians (i.e., Crocodylian Homology Hypotheses [CHH] A-D). A: Plesiomorphic condition common to lepidosaurs, turtles, and birds. Color codes are the same as in Fig. 12. B: Four separate hypotheses of muscle homology listing the number of topological and muscular character state changes (n = x) away from the plesiomorphic condition. CHHA is the most parsimonious homology hypothesis. See Fig. 4 for muscle attachments. aTO, temporoorbital artery; dtf, dorsotemporal fossa; gV, trigeminal ganglion; mAMEM, musculus (M) adductor mandibulae externus medialis; mAMEP; M. adductor mandibulae externus profundus; mAMEPc, caudal belly of mAMEP; mAMEPr; rostral belly of mAMEP; mINT, M. intermedius; mPTd, M. pterygoideus dorsalis; mPTdm, M. pterygoideus dorsalis pars minimus; nPT, pterygoid ramus of the mandibular nerve; nSO, supraorbital branch of the maxillary nerve; V1, ophthalmic nerve; V2, maxillary nerve; V3, mandibular nerve. Fig. 14. Postulated dermatome loci of topologically informative sensory nerves. A: Lepidosauria (Iguana iguana). B: Crocodylia (Alligator mississippiensis). C: Neornithes (Anas platyrhynchos). dtf, dorsotemporal fossa; eam, external acoustic meatus; nAD, dorsal alveolar branch of the maxillary nerve; nAO, ramus to the corner of the mouth (anguli oris) of the mandibular nerve; nAV, ventral alveolar branch of the mandibular nerve; nCA, caudal ramus of the mandibular nerve; nEC, external cutaneous branch of the mandibular nerve, nFR, frontal ramus of the ophthalmic nerve; nJU, jugal branch of the maxillary nerve; nMU, muscular branches of the mandibular nerve; nSO, supraorbital branch of the maxillary nerve; or, orbit; ri, rictus.