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. 2020 Nov;237(5):870-889.
doi: 10.1111/joa.13256. Epub 2020 Aug 13.

The evolution of the pectoral extrinsic appendicular and infrahyoid musculature in theropods and its functional and behavioral importance

Jeremy J Klingler  1
Affiliations

The evolution of the pectoral extrinsic appendicular and infrahyoid musculature in theropods and its functional and behavioral importance

Jeremy J Klingler. J Anat. 2020 Nov.

Abstract

Birds have lost and modified the musculature joining the pectoral girdle to the skull and hyoid, called the pectoral extrinsic appendicular and infrahyoid musculature. These muscles include the levator scapulae, sternomandibularis, sternohyoideus, episternocleidomastoideus, trapezius, and omohyoideus. As non-avian theropod dinosaurs are the closest relatives to birds, it is worth investigating what conditions they may have exhibited to learn when and how these muscles were lost or modified. Using extant phylogenetic bracketing, osteological correlates and non-osteological influences of these muscles are identified and discussed. Compsognathids and basal Maniraptoriformes were found to have been the likeliest transition points of a derived avian condition of losing or modifying these muscles. Increasing needs to control the feather tracts of the neck and shoulder, for insulation, display, or tightening/readjustment of the skin after dynamic neck movements may have been the selective force that drove some of these muscles to be modified into dermo-osseous muscles. The loss and modification of shoulder protractors created a more immobile girdle that would later be advantageous for flight in birds. The loss of the infrahyoid muscles freed the hyolarynx, trachea, and esophagus which may have aided in vocal tract filtering.

Keywords: alligator; birds; dinosaur; infrahyoid muscles; pectoral extrinsic appendicular muscles; theropod.

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Figures

Figure 1
Figure 1
Comparative figure of reptilian and avian hyoids in ventral view. (a) Varanus hyoid. (b) Alligator hyoid. (c) Columba livia hyoid. Abbreviations: (AP) anterior process, (BH) basihyal, (CBI) ceratobranchial I, (CH) ceratohyal, (EB) epibranchial, (LP) lingual process/entoglossal, (PG) paraglossal, (UH) urohyal. Note the large variation in hyoid form between sprawling reptiles and birds.
Figure 2
Figure 2
Comparative figure of reptilian and avian sterna in ventral views. (a) Iguana. (b) Alligator. (c) Palaeognath bird, Rhea americana (JMB 22726). (d) Neognath bird, Columba livia. Note the articulation of the interclavicle bone to the sternum in sprawling reptiles
Figure 3
Figure 3
Trapezius and cucullaris muscles. (a) Alligator trapezius in right lateral view (anterior is to the right). (b) Avian cucullaris cervicis and cucullaris capitis seen on the skin of the neck (cut down the ventral midline and reflected back – anterior is to the right and posterior is to the left seen over the shoulders)
Figure 4
Figure 4
Alligator neck muscles. (a) Lateral view of the extrinsic appendicular musculature in Alligator. (b) Line drawing detailing muscles of the cervical region
Figure 5
Figure 5
Alligator infrahyoid muscles. (a) Ventral view of the infrahyoid and ventral extrinsic appendicular muscles in Alligator. (b) Line drawing highlighting muscles of interest. Red dashed lines outline the extent of the episternum. Dashed black lines separate the right and left sternomandibularis‐sternohyoid complexes
Figure 6
Figure 6
Ventral view of the alligator hyoid. The left ceratobranchial is flared outward to better expose attachment points of hyoid musculature
Figure 7
Figure 7
Theropod scapulae. (a) Muscle scarring in Allosaurus (UMNH VP 10131). (b) Sulcus in Teratophoneus (UMNH VP 21100) along the anteromedial edge of the scapular blade. These features indicate the presence of both the trapezius and levator scapulae
Figure 8
Figure 8
Splenial of Allosaurus (BYU 759/2028) with a prominence possibly indicative of the attachment of the sternomandibularis
Figure 9
Figure 9
Dinosaur sterna. (a) Camarasaurus lentus sternal plate (CM 11338). (b) Line drawing of the sternal plate of Carnotaurus sastrei (MACN‐CH 894). Redrawn from Bonaparte et al. (1990). (c) Line drawing of the sternum of Gorgosaurus libratus (CMNFV 2120). Redrawn from Lambe (1917). (d) Sternum of the oviraptor Hagryphus giganteus, based on Anzu. (e) Sternum of Bambiraptor feinbergi (KUVP 129737). AMP =anteromedial projection; AMR =anteromedial rugosities; CSA =coracosternal articulation; ISA =intersternal articulation; SR =articular surface for sternal ribs. Observe that among sauropods and earlier‐diverging theropods there are processes and extensions (possibly indicative of muscular attachment) in the anteromedial region of the sternum, whereas among later‐diverging theropods the front edge of the sternum is devoid of features
Figure 10
Figure 10
Phylogenetic summary of character evolution of neck muscles. Red lines indicate a more plesiomorphic condition. Blue lines indicate a more avian, derived condition. Purple lines represent a transitional range. As seen, the Compsognathidae and Ornithomimosauria represent an important transitional range of morphology. Compsognathids likely still possessed reptilian‐like muscles but still possessed some key aspects of avian traits, whereas ornithomimids (maniraptoriforms in general) possessed many avian traits and likely at least had reduced muscles
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