JOURNAL OF MORPHOLOGY 270:1451 (2009)

The Head and Neck Muscles of the Philippine Colugo (Dermoptera: Cynocephalus volans), With a Comparison to Tree-Shrews, Primates, and Other Mammals
Rui Diogo*
Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology, George Washington University, Washington, DC ABSTRACT The colugos, or ying lemurs (Dermoptera), are arboreal gliding mammals that are commonly grouped with tree-shrews (Scandentia) and Primates in the superorder Euarchonta. However, little is known about the head and neck muscles of these gliding mammals. This raises difculties for the discussion of not only the functional morphology and evolution of colugos, but also the origin, evolution, functional morphology, and phylogenetic relationships of the Euarchonta as a whole, and thus also of our own clade, the Primates. In this work, I describe the head and neck muscles of the colugo Cynocephalus volans, and compare these muscles with those of other mammals, either dissected by me or described in the literature. My observations and comparisons indicate that, with respect to the number of muscles, the plesiomorphic condition for euarchontans as well as for primates is more similar to that found in extant tree-shrews than in extant colugos. This is because various muscles that were probably plesiomorphically present in the euarchontan and primate clades, as, e.g., the stylohyoideus, mandibulo-auricularis, cleido-occipitalis, omohyoideus, and sternohyoideus, are not present as independent elements in extant colugos. These observations and comparisons also indicate that various laryngeal and facial muscles that are present in modern humans were absent in the last common ancestor of extant primates. J. Morphol. 270:1451, 2009.
2008 Wiley-Liss, Inc.

KEY WORDS: anatomy; colugos; Dermoptera; evolution; head muscles; homologies; mammals; primates; Scandentia; tree-shrews

Extant colugos, or ying lemurs (Dermoptera), are arboreal gliding mammals found in South-east Asia. Many authors recognize a single extant dermopteran genus, Cynocephalus, with two species, the Philippine C. volans and the Sundaic C. variegatus (e.g., Dawkins, 2004). However, some researchers argue that the appropriate names for these two taxa are Cynocephalus volans and Galeopterus variegatus (e.g., Stafford and Szalay, 2000; Marivaux et al., 2006; Janecka et al., 2007). In the past, colugos were often considered to be closely related with bats, an arrangement that was appealing because many researchers believed that bats evolved from gliding ancestors. However, this view was strongly contradicted by molecular clad 2008 WILEY-LISS, INC.

istic studies and is now commonly discarded by most researchers. As recently stressed by Gunnell and Simmons (2005; p 211), regardless of the genes sampled or the phylogenetic methods used, bats never group with primates or dermopterans; multiple analyses of nuclear and mitochondrial gene sequences have resoundingly refuted the hypothesis that bats are archontan mammals (i.e., that they are closely related to dermopterans, treeshrews and/or primates); instead, molecular studies uniformly place bats in a Laurasiatheria clade. In fact, molecular studies have consistently supported a clade Euarchonta, which includes extant dermopterans, Primates, and tree-shrews (Scandentia). This clade is now accepted by most of the authors (Silcox et al., 2007). Within Euarchonta, consistent molecular support for the traditional grouping of primates and tree-shrews has been lacking, with a Scandentia-Dermoptera link being supported by some recent molecular and morphological studies (Silcox et al., 2007). Interestingly, the most recent and most complete molecular cladistic analysis (using two independent approaches: searching multispecies genome alignments for phylogenetically informative rare genomic changes and constructing phylogenetic trees from 14 kilobases of nuclear genes) strongly suggested that colugos are the closest living relatives of Primates (Janecka et al., 2007). Despite being closely related to and possibly even the closest extant relatives of our own clade, the Primates, very little is known about the soft tissues and particularly the head and neck muscles of colugos. The scarce information that has been published in the literature about these muscles and that was actually based on a dissection of these mammals was provided in works that
*Correspondence to: Rui Diogo, Center for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, 2110 G St. NW, Washington, DC 20052. E-mail: Rui_Diogo@hotmail.com Published online 16 September 2008 in Wiley InterScience (www.interscience.wiley.com) DOI: 10.1002/jmor.10666

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1872) was primarily interested on the myology of bats; Leche (1886) mainly described dermopteran postcranial structures; Thewissen and Babcock (1991, 1993) compared the wing muscles of bats and the propatagial muscles of dermopterans; Stafford and Szalays (2000) work primarily focused on dermopteran craniodental functional morphology and taxonomy; Gunnell and Simmons (2005) were mainly interested in the origin and phylogeny of bats. The lack of knowledge about the head and neck musculature of colugos raises difculties for the discussion of not only functional morphology and the evolution of these mammals, but also the origin, evolution, functional morphology, and phylogenetic relationships of the Euarchonta as a whole, and thus also of the Primates. In this work, I describe the head and neck muscles of the colugo Cynocephalus volans, and compare these muscles with those of members of closely related groups such as tree-shrews and primates, as well as of other mammalian clades, including the phylogenetically plesiomorphic monotremes. MATERIALS AND METHODS
I begin by setting out the phylogenetic framework for the discussion provided in this article and the comparison between the head and neck muscles of the ve taxa listed in Appendix 18. 1) Monotremes are the sister-group of marsupials 1 placentals; 2) Rodentia (including, e.g., rats) and Lagomorpha (including, e.g., rabbits) are often included in a clade (Glires) that is closely related to the Euarchonta, i.e., to the group comprising extant Primates, Dermoptera (colugos or ying lemurs), and Scandentia (tree-shrews); 3) within the Euarchonta, some authors continue to group Primates with tree-shrews; recent molecular studies have, however, provided more support for a closer relationship between colugos and tree-shrews or between Primates and colugos (see above and also, e.g., Stafford and Szalay, 2000; Sargis, 2002a,b, 2004; Dawkins, 2004; Gunnell and Simmons, 2005; Marivaux et al., 2006; Janeka et al., 2007; Silcox et al., 2007); 4) Within the Dermoptera, I follow the nomenclature used by Dawkins (2004) and many other authors, who recognize a single extant dermopteran genus, Cynocephalus, with two species, the Philippine C. volans and the Sundaic C. variegatus (see earlier). As explained in the Introduction, one of the main aims of this work is to describe the head and neck muscles of C. volans and to compare these muscles with those of other mammals. I have, therefore, carefully chosen to include in Appendices 18: 1) a member of the phylogenetically most plesiomorphic extant mammalian clade, the monotremes (Ornithorhynchus anatinus); 2) a member of the rodents, namely the Norwegian rat (Rattus norvegicus), because rats are often considered to be anatomically generalized" therian mammals, but at the same time are closely related to Euarchonta (see above); 3) a member of the colugos (Cynocephalus volans); 4) a member of the treeshrews (Tupaia sp.); and 5) a member of the Primates, Homo sapiens. It should be noted that apart from dissecting specimens of the ve taxa listed in these Appendix 1 also dissected specimens of and/or undertook an extensive review of the information provided in the literature for various other euarchontan and non-euarchontan mammalian taxa. The mammalian speci mens dissected are from the Coleccion Mamferos Lillo of the Universidad Nacional de Tucuman (CML), the Primate Foundation of Arizona (PFA), the Department of Anatomy (GWU-ANA) and the Department of Anthropology (GWU-ANT) of the George Washington University, the Department of Anatomy of Howard University (HU-ANA), and the National Museum of Natural

Fig. 1. Cynocephalus volans: Lateral view of the facial muscles, the splenius capitis is also shown; anteriorly, the nasolabialis was partially cut in order to show the maxillo-naso-labialis (anterior is to the right; muscles shown in darker red are deeper than [medial to] those shown in lighter red). AUOR, auriculo-orbitalis; AUP, auricularis posterior; AUS; auricularis superior; FRO, frontalis; LAO, levator anguli oris facialis; MEN, mentalis; MNL, maxillo-naso-labialis; NASL, naso-labialis; OCC, occipitalis; OROC, orbicularis occuli; OROR, orbicularis oris; PLAC, platysma cervicale; PLAM, platysma myoides; SCOP, sphincter colli profundus; SPLE, splenius capitis; ZYMA, zygomaticus major; ZYMI, zygomaticus minor; ZYOR, zygomatico-orbitalis.

History (USNM). The nomenclature of Diogo (2007, 2008), which refers mainly to bony sh and non-mammalian tetrapods, was reconciled with the nomenclature used by researchers working with mammals (for a review, see, e.g., Saban, 1968, 1971; Jouffroy and Saban, 1971) and namely with primates and humans (e.g., The Federative Committee on Anatomical Terminology; Terminologia Anatomica, 1998). When cited articles use a nomenclature that differs from that followed here, the respective synonymy is given in Appendix 1,3,5, and 7. It should be noted that the Homo sapiens muscles that are listed in Appendices 18 are those muscles that are usually present in adult humans, i.e., I am not listing all the muscles that can occasionally be found as variations and/or abnormalities in humans (see, e.g., Huber, 1931; see also, e.g., Wood, 1866, 1867a,b, 1868, 1870; Anderson, 1880; Shattock, 1882; Parsons, 1898; Taylor, 1925; Wells and Thomas, 1927; Chi, 1937; Pettersen et al., 1979; Aziz, 1981; Gibbs, 1999). When I refer to the anterior, posterior, dorsal, and ventral regions of the body, I do so in the sense the terms are used for pronograde tetrapods (e.g., the forelimb is anterior to the hind limb, the sternum is ventral to the thoracic part of the vertebral column) (see Figs. 14). The list of mammalian specimens examined for the present work is given below. The number of specimens examined is followed by an abbreviation that refers to the state of the specimen (alc, alcohol xed; fre, fresh; for, formalin embalmed). The dissections and anatomical drawings were made using a Wild M5 dissecting microscope equipped with a camera lucida. Cynocephalus volans: USNM, 144941, 1 (alc); USNM, uncatalogued, 2 (alc). Didelphis albiventris: CML 5971, 1 (alc); Homo sapiens: GWU-ANA, 1-16, 16 (for); Lutreolina crassicaudata: CML 4114, 1 (alc); Monodelphis dimidiata: CML 4118, 1 (alc); Ornithorhynchus anatinus: USNM, 13678, 1 (alc); USNM, uncatalogued, 1 (alc); Pan troglodytes: PFA, 1016, 1 (fre); PFA, 1009, 1 (fre); PFA, 1051, 1 (alc.); HU-ANA, C104, 1 (for); GWU-ANT, 01, 1 (for); GWU-ANT, 02, 1 (for); Pongo pygmaeus: HU-ANA, O01, 1 (for); GWU-ANT, 01, 1 (for); Rattus norvegicus: USNM, uncatalogued, 2 (alc); Thylamys venustus: CML 5586, 1 (alc); Tupaia sp.: UNSM, 87244, 1 (alc); USNM, uncatalogued, 1 (alc).

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241 242 243 244 245 246 247 248 249 250 251 C 252 O 253 L 254 O 255 R 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280 281 282 283 C 284 O 285 L 286 O 287 R 288 289 290 291 292 293 294 295 296 297 298 299 300

Fig. 2. Cynocephalus volans: Postero-ventro-lateral view of the masseter, buccinatorius, pterygoideus medialis, temporalis, digastricus anterior, digastricus posterior, jugulohyoideus, sternomastoideus, cleidomastoideus, mylohyoideus, and splenius capitis (anterior is to the right; muscles shown in darker red are deeper than [medial to] those shown in lighter red). BUC, buccinatorius; CMA, cleidomastoideus; DIA, DIP, digastricus anterior and digastricus posterior; eam, external acoustic meatus; JUH, jugulohyoideus; l-sty-mnd, stylomandibular ligament; MAP, MAS, pars profunda and pars supercialis of masseter; mnd, mandible; MPT, pterygoideus medialis; MYH, mylohyoideus; SMA, sternomastoideus; SPLE, splenius capitis; TEMP, temporalis.

Fig. 4. Cynocephalus volans: Lateral view of the laryngeal muscles and of the pharyngeal muscle cricothyroideus; this latter muscle and the lateral surface of the thyroid cartilage were partially cut in order to show the deeper (more medial) muscles (anterior is to the left, dorsal to the top; muscles shown in darker red are deeper than [medial to] those shown in lighter red). ARY, arytenoideus; CRAL, cricoarytenoideus lateralis; CRAP, cricoarytenoideus posterior; cric, cricoid cartilage; CRTO, CRTR, pars obliqua and pars recta of cricothyroideus; epigl, epiglottis; THARI, THARS, pars intermedia and pars superioris of thyroarytenoideus; thyr, thyroid cartilage.

RESULTS In this section, I describe the mandibular, hyoid, branchial, pharyngeal, laryngeal, and hypobranchial muscles of the colugo specimens dissected. In those cases in which there are differences between my observations and the scarce data that are available in the literature about these muscles, these differences will be mentioned. The order in which the muscles are described mainly follows that used in Appendix 18.

Mandibular Muscles Although exceptions may occur, the mandibular muscles sensu Edgeworth (1935) are considered to be derived from branchial arch 1 (mandibular arch) and generally innervated by the Vth cranial nerve (see Diogo, 2007, for a recent review). Eight mandibular muscles are present as independent elements in the colugos dissected: the mylohyoideus, digastricus anterior, masseter, temporalis, pterygoideus lateralis, tensor tympani, tensor veli palatini, and pterygoideus medialis (Figs. 2 and 3). The anterior portion of the mylohyoideus (Fig. 2) is mainly aponeurotic and attached to the ventromedial surface of the mandible. Posteriorly, this muscle reaches the hyoid bone, while medially it meets its counterpart on a median raphe. The posterior portion of the digastricus anterior (Fig. 2) is connected to the digastricus posterior (a hyoid muscle: see below) by a short tendinous intersection. Its anterior portion attaches to the angle of the mandible. The digastricus anterior does not meet its counterpart at the midline.
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Fig. 3. Cynocephalus volans: Ventro-lateral view of the genioglossus, geniohyoid, styloglossus, hyoglossus, sternothyroid, sternohyoid, palatoglossus, tensor veli palatini, levator veli palatini, pterygopharyngeus, salpingopharyngeus, stylopharyngeus, jugulohyoideus, and constrictor pharyngis inferior; the mandible, zygomaticus arch and part of the orbit were removed (anterior is to the right; muscles shown in darker red are deeper than [medial to] those shown in lighter red). eam, external acoustic meatus; GEG, genioglossus; GEH, geniohyoideus; GLOP, glossopharyngeus; HYG, hyoglossus; IPC, constrictor pharyngis inferior; JUH, jugulohyoideus; LVP, levator veli palatini; mapr, mastoid process; PAG, palatoglossus; PAP, palatopharyngeus; PTEP, pterygopharyngeus; ptha, pterygoid hamulus; SALP, salpingopharyngeus; STEH, sternohyoideus; STG, styloglossus; STP, stylopharyngeus; STT, sternothyroideus; TVP, tensor veli palatini.

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The masseter (Fig. 2) mainly originates from the zygomatic arch and maxilla and is subdivided into a supercial bundle (supercialis), a deep bundle (profundus), and a zygomatico-mandibular bundle. The zygomatico-mandibular bundle is sometimes considered to be an independent muscle (e.g., Stafford and Szalay, 2000), but in the colugos I dissected this bundle is deeply mixed with the other masseter bundles. The supercial bundle attaches to the posteroventrolateral surface of the mandible, just ventrolaterally to the attachment of the deep bundle. The zygomatico-mandibularis bundle is deeply mixed with the medial bers of the deep bundle, as well as with the lateral bers of the temporalis, attaching mainly to the lateral margin of the coronoid process. The temporalis (Fig. 2) is not clearly subdivided into supercial and deep bundles, and there is also no distinct pars suprazygomatica sensu Saban (1968). It originates on a broad temporal fossa, but does not meet its counterpart at the midline. Ventrally, it mainly attaches to the medial and dorsal surfaces of the coronoid process. The pterygoideus medialis (Fig. 2) is not subdivided. It originates on the pterygoid process and attaches to the posteroventromedial margin of the mandible. The pterygoideus lateralis originates dorsolaterally to the medial pterygoid and attaches to the condylar process of the mandible, although it is also partially connected to the capsule lying between this process and the neurocranium. It is not subdivided into supercial and deep heads. The tensor tympani and tensor veli palatini (Fig. 3) are small muscles originating on the auditory tube and surrounding structures. The tensor tympani attaches to the malleus, whereas the tensor veli palatini passes laterally to the levator veli palatini (a pharyngeal muscle: see below) in order to attach on the soft palate and on the pterygoid hamulus (Fig. 3). Hyoid Muscles The hyoid muscles sensu Edgeworth (1935) are considered to be derived from branchial arch 2 (hyoid arch) and usually innervated by the VIIth cranial nerve (see Diogo, 2007, for a recent review). Apart from the extrinsic musculature of the ear (including facial muscles as, e.g., helicis, tragicus, and/or antitragicus), the colugos dissected have 22 hyoid muscles: jugulohyoideus, digastricus posterior, stapedius, platysma cervicale, platysma myoides, occipitalis, auricularis posterior, sphincter colli profundus, zygomaticus major, zygomaticus minor, frontalis, auriculo-orbitalis, auricularis superior, orbicularis oculi, zygomatico-orbicularis, corrugator supercilii, naso-labialis, buccinatorius, maxillo-naso-labialis, levator anguli oris facialis, orbicularis oris, and mentalis (Figs. 13). Of these 22 muscles, the rst three are the only ones that

are not facial muscles sensu, e.g., Huber (1930a,b, 1931). The digastricus posterior (Fig. 2) originates on the mastoid process and is connected anteroventrally to the digastricus anterior (a mandibular muscle) by a short tendinous intersection (see above). The jugulohyoideus (Figs. 2 and 3) originates on the mastoid process, medially to the digastricus posterior, and inserts mainly on the ligament connecting the neurocranium to the hyoid as well as on the proximal surface of this latter structure. The stapedius is a very small muscle running from the neurocranium to the stapes. Saban (1968) states that the stylohyoideus meets its counterpart at the ventral midline. However, the stylohyoideus is not present as an independent structure in the colugos dissected by me or by authors such as Gunnel and Simmons (2005). Saban (1968) apparently confused the stylohyoideus with the sphincter colli profundus: the colugo specimens dissected lack a stylohyoideus but, contrary to what was stated by Saban (1968), they do have a sphincter colli profundus (Fig. 1), which effectively meets its counterpart at the ventral midline (see below). Posteriorly, the platysma cervicale (Fig. 1) is blended with a thick fascia covering the dorsal surface of the neck. Only a few bers of this muscle meet their counterparts at the dorsal midline of the neck. The anterodorsal bers of the platysma cervicale attach to the zygomatic arch, wheras its anteroventral bers run to the posterodorsal region of the mouth, blending with the zygomaticus minor and the orbicularis oris (Fig. 1). The platysma myoides (Fig. 1) is blended with the platysma cervicale, running from the anteroventral margin of the mandible and posteroventral region of the mouth to the forelimb and forming part of the propatagial complex (related to gliding in colugos). Leche (1886) and Jouffroy and Saban (1971) stated that the propatagial complex of dermopterans has a dorsal muscle that is formed in part by the platysma myoides and in part by a jugalis propatagii and a ventral muscle that was named ventrale Schicht (ventral layer) by Leche (1886). However, Thewissen and Babcocks (1991, 1993) detailed analysis of the conguration and innervation of these muscles has pointed out that the dorsal muscle is exclusively innervated by the facial nerve, whereas the ventral one is exclusively innervated by cervical spinal nerves. The dorsal and ventral propatagial muscles of colugos, thus, probably correspond to the platysma myoides and to part of the panniculus carnosus of other mammals, respectively. The occipitalis (Fig. 1) has a medial portion that is anteriorly blended with the frontalis, and a lateral portion that runs anteroventrolaterally to attach to the posterior surface of the ear, thus covering part of the lateral margin of the auricularis
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posterior. Posteriorly, these two portions are deeply blended to each other and attach to the nuchal region of the skull. The auricularis posterior (Fig. 1) runs from this latter region to the posterior surface of the ear. The mandibulo-auricularis is absent as an independent, eshy muscle. In the position usually occupied by this muscle lies a strong fascial sheet connecting the posterior edge of the mandible to the bony external auditory meatus (which, according to Lightoller, 1934, may well correspond to the mandibulo-auricularis of other mammals and to the stylo-mandibular ligament of modern humans: Fig. 2). The sphincter colli profundus (Fig. 1) is deep to the platysma myoides and to the platysma cervicale. Dorsally, it blends with these muscles. Ventrally, it meets its counterpart at the ventral midline. The sphincter colli supercialis does not seem to be present as an independent muscle in the colugos dissected. Jouffroy and Saban (1971) stated that this muscle is present in colugos, but this is because they were considering the ventral muscle of the propatagial complex of dermopterans as probably homologous to the sphincter colli supercialis of other mammals. As explained earlier, this ventral propatagial muscle is actually innervated by cervical spinal nerves and not by the facial nerve; it very likely corresponds to part of the panniculus carnosus of other mammals (see above). The zygomaticus major (auriculabialis inferior: e.g., Jouffroy and Saban, 1971; this work) is supercial to the platysma cervicale, running from the anteroventral region of the ear to the posterodorsal region of the mouth, where it blends with the orbicularis oris (Fig. 1). The zygomaticus minor (auriculabialis superior: e.g., Jouffroy and Saban, 1971; this work) is blended with the orbicularis oculi, dorsally, and with both the orbicularis oris and the nasolabialis, ventrally (Fig. 1). The posterior portion of the frontalis (Fig. 1) is blended with the occipitalis, whereas its anterior portion is blended with the nasolabialis. It meets its counterpart at the dorsal midline. The auriculoorbitalis (Fig. 1) lies deep to both the orbicularis oculi and frontalis. As its name indicates, it runs from the auricular region to the orbital region, where it blends with the orbicularis oculi. The auricularis superior (Fig. 1) originates on the galea aponeurotica, near the dorsal midline, and runs ventrally, passing supercially to the frontalis and occipitalis and attaching on the anterodorsal region of the ear (Fig. 1). The orbicularis oculi (Fig. 1) is a broad muscle surrounding the eye. The posteromedial bers of this muscle are blended with a thin group of bers that lies deep to the dorsal portion of the zygomaticus minor and run posteroventrally to attach to the dorsal surface of the zygomatic arch (Fig. 1). This thin group of bers is blended medially with the temporal fascia
Journal of Morphology

covering the temporalis, and probably corresponds to the zygomatico-orbicularis sensu Le Gros Clark, 1924 (Fig. 1). Dorsal to the eye, and deep to the frontalis and orbicularis oculi, lies the small corrugator supercilii, which is attached to the skin/fascia covering the superior orbital margin, and possibly also to part of this latter bony structure. The nasolabialis (Fig. 1) is a broad muscle that meets its counterpart at the dorsal midline. Posterodorsomedially it blends with the frontalis. It runs ventrally to attach to the upper lip, covering a signicant part of the broad orbicularis oris (Fig. 1) in lateral view. The posterior portion of the maxillo-naso-labialis (Fig. 1) is blended with the orbicularis oris and the orbicularis oculi, although it is mainly supercial to the latter. Its anterior portion extends to the region of the snout, being supercial to, and somewhat mixed with, the levator anguli oris facialis (Fig. 1). The mentalis (Fig. 1) is well-developed, lying deep to the orbicularis oris and to the platysma myoides and meeting its counterpart at the ventral midline. It attaches to the anteroventral surface of the mandible. The levator anguli oris facialis (Fig. 1) is deep to the maxillo-naso-labialis, running from the maxilla, dorsally, to the upper lip, ventrally (I use the name levator anguli oris facialis to distinguish this muscle from the levator anguli oris mandibularis of some non-mammalian tetrapods, which is a mandibular, and not a hyoid, muscle: Diogo, 2007, 2008). The buccinatorius (Fig. 2) lies deep to the other facial muscles. Posteriorly, it is attached to both the ventrolateral surface of the maxilla and the dorsolateral surface of the mandible. Anteriorly it blends with both the levator anguli oris facialis and orbicularis oris. Branchial, Pharyngeal, and Laryngeal Muscles The branchial muscles sensu lato of Edgeworth (1935) may be divided into three main groups. The rst group includes the true branchial muscles, which are subdivided into: A) the branchial muscles sensu stricto that are directly associated with the movements of the branchial arches and that in mammals are usually innervated by the glossopharyngeal nerve (CNIX) and represented by the subarcualis rectus III (found in adult extant monotremes), subarcualis rectus II (found in adult extant marsupials), and subarcualis rectus I (which corresponds to the ceratohyoideus and possibly to the stylopharyngeus of monotremes, marsupials and placentals: Smith, 1992; Noden and Francis-West, 2006; Diogo et al., in press); B) the branchial muscles that are instead mainly associated with the pectoral girdle and that in mammals are primarily innervated by the accessory nerve (CNXI) and represented by muscles such as the acromiotrapezius, spinotrapezius, cleido-occipitalis,

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cleidomastoideus, sternomastoideus, trapezius, and/or sternomastoideus. The second group includes the pharyngeal muscles, which are only present as independent elements in extant mammals and are considered to be derived from arches 46 and usually innervated by the vagus nerve (CNX; the mammalian stylopharyngeus, which is considered to be derived from the third arch and is primarily innervated by the glossopharyngeal nerve, is grouped here with the true branchial muscles, and not with the pharyngeal muscles: see above). The third group includes the laryngeal muscles, which are considered to be derived from arches 46 and are usually innervated by the vagus nerve (CNX). The colugos dissected have six true branchial muscles sensu this work: the ceratohyoideus, stylopharyngeus (see above), acromiotrapezius, spinotrapezius, cleidomastoideus, and sternomastoideus (Fig. 3). The stylopharyngeus (Fig. 3) originates on the proximal surface of the hyoid apparatus. Most of its bers attach to the pharyngeal connective tissue surrounding the hyoid, although some of them are possibly blended with those of pharyngeal muscles such as the palatopharyngeus and the constrictor pharyngis medius. The ceratohyoideus is a small muscle lying deep to the hyoglossus and running from the distal margin of the lesser cornu of the hyoid to the greater cornu of the hyoid. Contrary to what is suggested in Figure 4 of Leche (1886), in the colugos dissected by me, there is clearly a sternomastoideus and a cleidomastoideus; each of these two muscles attaches anteriorly to the mastoid process by a thin and long tendon (Fig. 2). Posteriorly the sternomastoideus attaches to the sternum, with some of its bers meeting its counterpart at the ventral midline. The cleidomastoideus also attaches to the sternum, but does not meet its counterpart at the ventral midline. Macalister (1872) and Gunnell and Simmons (2005) stated that the spinotrapezius and acromiotrapezius are not present as independent structures in colugos. However, the colugos I dissected do have a distinct spinotrapezius and a distinct acromiotrapezius. The former mainly inserts on the scapular spine, whereas the latter mainly inserts on the acromion. This conguration was also found in the specimens examined by Leche (1886; see, e.g., his Fig. 8). As stated by Macalister (1872), in colugos the trapezius complex (5 acromiotrapezius 1 spinotrapezius of the present work) does not reach the cranium anteriorly and does not attach to the clavicle posteriorly; i.e., it probably does not include a cleido-trapezius" sensu Kardong (2002) nor a cleido-occipitalis sensu the present work (Appendices 5,6). The colugos dissected have eight pharyngeal muscles: constrictor pharyngis medius, constrictor pharyngis inferior, constrictor pharyngis superior,

pterygopharyngeus, palatopharyngeus, levator veli palatini, salpingopharyngeus, and cricothyroideus (which is a pharyngeal muscle, and not a laryngeal muscle as it is sometimes erroneously suggested in the literature: see, e.g., Edgeworth, 1935; Saban, 1968, 1971) (Figs. 3 and 4). The constrictor pharyngis inferior (Fig. 3) is poorly differentiated into a pars thyropharyngea running from the dorsal pharyngeal wall to the thyroid cartilage and a pars cricopharyngea running from the dorsal pharyngeal wall to the cricoid cartilage. The constrictor pharyngis medius connects the dorsal pharyngeal wall to the lesser cornu of the hyoid. My dissections indicate that there is a glossopharyngeus (5 part of constrictor pharyngis superior: Fig. 3) in the specimens examined, running from the tongue to the dorsal pharyngeal wall and possibly also inserting on the hyoid and/or on the pharyngeal connective tissue surrounding this structure. It is possible that, apart from attaching to the tongue, some of the bers of the constrictor pharyngis superior also blend anteriorly with those of the buccinatorius, i.e., that the contrictor pharyngis superior includes both a glossopharyngeus and a buccopharyngeus (sensu Sprague 1942, 1943, 1944a,b). The palatopharyngeus (Fig. 3) is deeply blended with the salpingopharyngeus. Most of its bers run from the soft palate to the lateral pharyngeal wall. However, there is a thin, distinct group of bers that lies laterally to the main body of the palatopharyngeus and runs from the soft palate to apparently attach to the dorsal pharyngeal wall. This group of bers of the palatopharyngeus probably corresponds to the sphincter palatopharyngeus sensu Edgeworth (1935). The salpingopharyngeus (Fig. 3) runs from the auditory tube to the lateral and dorsal pharyngeal walls. The levator veli palatini (Fig. 3) also originates on the auditory region, posteriorly to the tensor veli palatini (a mandibular muscle: see above), running posteromedially to this muscle to attach to the soft palate. Ventrally to these two muscles lies the pterygopharyngeus (Fig. 3), which originates on the pterygoid hamulus and inserts on the dorsal pharyngeal wall, laterally to the palatopharyngeus and salpingopharyngeus. The cricothyroideus (Fig. 4) is divided into a pars obliqua and a pars recta, which are well separated from each other by a prominent anteroventrolateral crest of the cricoid cartilage. The pars recta is supercial to the pars obliqua, mainly running anteriorly and anterodorsally from the anterior surface of this crest to the posteroventral margin of the thyroid cartilage. It meets its counterpart at the ventral midline, below the larynx. The pars obliqua runs from both the posterior margin of the crest and the main body of the cricoid cartilage to the posterodorsal margin of the thyroid cartilage; it does not reach the dorsal midline above the larynx.
Journal of Morphology

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Four laryngeal muscles are present as independent elements in the colugos dissected: thyroarytenoideus, cricoarytenoideus lateralis, arytenoideus, and cricothyroideus posterior (Fig. 4). The thyroarytenoideus (Fig. 4) connects the ventral portion of the thyroid cartilage to the arytenoid cartilage. It is mainly divided into a posterior, medial bundle and an anterior, lateral bundle, which probably correspond respectively to the pars intermedia and pars superioris (sensu Starck and Schneider, 1960) (Fig. 4). The anterior, lateral bundle is in turn subdivided into a more posterior, deep section and a more anterior, supercial section. Some of the bers of this latter section are fused dorsally to those of the muscle cricoarytenoideus posterior: this section of the thyroarytenoideus, thus, probably corresponds to the ceratoarytenoideus lateralis (sensu Harrison, 1995). The cricoarytenoideus posterior (Fig. 4) runs from the dorsal surface of the cricoid cartilage, posteriorly, to the arytenoid cartilage, anteriorly. It meets its counterpart in a median raphe, dorsally to the larynx. The arytenoideus (Fig. 4) is a small muscle connecting the right and left arytenoid cartilages. The cricoarytenoideus lateralis (Fig. 4) lies ventrally to the cricoarytenoideus posterior, running from the anterior margin of the cricoid cartilage to the arytenoid cartilage. Hypobranchial Muscles According to Edgeworth (1935: 189), the hypobranchial muscles are developed from the anterior myotomes of the body and thus are intrusive elements of the head; they retain a spinal innervation and may also be innervated by the XIth and XIIth nerves, but usually do not receive any branches from the Vth, VIIth, IXth, and Xth nerves (see Diogo, 2007, for a recent review). Apart from the intrinsic musculature of the tongue (including hypobranchial muscles such as the longitudinalis superior, longitudinalis inferior, transversus linguae, and/or verticalis linguae), seven hypobranchial muscles are present as independent structures in the colugos dissected: geniohyoideus, genioglossus, hyoglossus, styloglossus, palatoglossus, sternohyoideus, and sternothyroideus (Fig. 3). The geniohyoideus (Fig. 3) is attached posteriorly to the hyoid bone; anteriorly, it does not reach the mandibular symphysis, inserting on the mandible laterally to this symphysis. It contacts its counterpart at the midline but is not deeply fused to it. The genioglossus (Fig. 3) is a broad muscle that lies medially to the geniohyoideus and connects the portion of the mandible lying laterally to the mandibular symphysis to the hyoid bone and to the tongue. According to Edgeworth (1935), the hyoglossus of colugos corresponds to the hyoglossus 1 thyrohyoideus of other mammals. These muscles seem to be effectively fused to each other
Journal of Morphology

in the colugo specimens I dissected. In these specimens, the hyoglossus (Fig. 4) is markedly extended posteriorly, attaching not only to the tongue and the hyoid bone but also to the posterior margin of the thyroid cartilage. The styloglossus (Fig. 3) is a long muscle lying laterally to the genioglossus and hyoglossus and running from an expanded tip of the stylohyal and its surrounding structures, posteriorly, to the tongue, anteriorly. There is a thin group of bers lying dorsomedially to the hyoglossus, which mainly connects the lateral wall of the oropharynx to the posterolateral surface of the tongue; this group of bers probably corresponds to the palatoglossus sensu (Edgeworth, 1935; and Saban, 1968) (Fig. 3). The sternohyoideus (Fig. 3) runs from the pectoral girdle to the hyoid bone, being subdivided into two bundles. The posterior one reaches the posterior margin of the thyroid cartilage and then contacts, via a broad but thin tendon, the anterior bundle, which extends anteriorly to attach to the lesser cornu of the hyoid. Neither of these two bundles meets its counterpart at the ventral midline. The sternothyroideus (Fig. 3) lies dorsolaterally to the sternohyoideus, connecting the pectoral girdle to the posterior margin of the thyroid cartilage. DISCUSSION In Appendices 18, I list the mandibular, hyoid, branchial, pharyngeal, laryngeal, and hypobranchial muscles found in the colugos dissected and compare these muscles with those of tree-shrews such as Tupaia, of primates such as humans, of rodents such as rats, and of a member of the phylogenetically most basal mammal extant group (monotremes), the platypus. As explained earlier, in addition to dissecting specimens of the ve taxa included in these Appendices, I also dissected specimens of and/or undertook an extensive review of the information provided in the literature for various other mammalian taxa, such as lemuroid, lorisoid, tarsioid, and non-human anthropoid primates (sensu Shoshani et al., 1996), other treeshrews, other rodents, and numerous other mammals, including marsupials and the other extant member of the monotremes, the echidna. It should be noted that the position of Cynocephalus, Tupaia, and Homo in these Appendices is arbitrary, i.e., the fact that these two latter genera are placed next to each other does not necessarily mean that the author considers that colugos cannot be the closest living relatives of primates (see Introduction). As a great part of the data obtained from my dissections, comparisons and review of the literature is provided in Appendices 18, here I will briey summarize the information presented in those Appendices and discuss the head and neck muscles of colugos in an evolutionary and phylogenetic context.

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

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In general, the number of head and neck muscles present in extant colugos is somewhat similar to that found in extant tree-shrews (Appendices 18) and in extant primates such as lemuroids (e.g., Murie and Mivart, 1872; Ruge, 1885; Parsons, 1898; Sonntag, 1924; Huber, 1930b, 1931; Lightoller, 1934; Edgeworth, 1935; Hill, 1953; Starck and Schneider, 1960; Saban, 1968; Jouffroy and Saban, 1971; Seiler, 1979, 1980; Jablonski, 1986; Burrows and Smith, 2003). As can be seen in Appendices 1 and 2, extant colugos and extant primates such as humans have eight mandibular muscles. Extant tree-shrews such as Tupaia have nine mandibular muscles, because they have an intermandibularis anterior (5 anterior part of mylohyoid sensu Le Gros Clark, 1924: Appendix 1). However, in other extant tree-shrews, as, e.g., Ptilocercus, this latter muscle is not present as an independent element (Le Gros Clark, 1926); i.e., these tree-shrews also have eight mandibular muscles, as do colugos and many primates. Colugos have three nonfacial hyoid muscles: the jugulohyoideus, digastricus posterior, and stapedius (Appendices 3,4). Extant tree-shrews such as Tupaia (Appendices 3,4) and Ptilocercus (e.g., Le Gros Clark, 1926; Sprague, 1944a) have these three muscles plus a stylohyoideus. This latter muscle, as well as the digastricus posterior and stapedius, is also present in most primates (e.g., Sonntag, 1924; Saban, 1968), including humans (Appendices 3,4). As the stylohyoideus is present in most non-euarchontan placental mammals and in most tree-shrews and primates, it is very likely that this muscle was present in the last common ancestor of primates, colugos and tree-shrews and then secondarily lost in colugos (Appendices 3,4). In phylogenetically derived primates such as humans, the jugulohyoideus is not present as an independent element. However, this muscle is present in phylogenetically plesiomorphic primates such as strepsirhines, and was very likely present in the last common ancestor of extant primates (e.g., Lightoller, 1934; Saban, 1968). The evolution and homologies of the mammalian facial muscles have been, and continue to be, the subject of much controversy (e.g., Ruge, 1885, 1897, 1910; Boas and Paulli, 1908; Lightoller, 1928a,b, 1934, 1940a,b, 1942; Huber, 1930a,b, 1931; Edgeworth, 1935; Andrew, 1963; Gasser, 1967; Jouffroy and Saban, 1971; Saban, 1971; Seiler, 1971a,b,c,d,e, 1974a,b, 1975, 1979, 1980; Minkoff et al., 1979; Preuschoft, 2000; Schmidt and Cohn, 2001; Burrows and Smith, 2003; Burrows et al., 2006; Burrows, 2008). Although it is clearly beyond the scope of this article to review the origin and evolution of the facial muscles within the Mammalia as a whole, it can be said that some of the hypotheses that are proposed in Appendix 3 and shown in Appendix 4 (arrows) regarding the evolution and homologies of these muscles are in fact well supported by the

data now available. For instance, the data available on, e.g., topology, functional morphology, development, and innervation strongly suggest that the platysma cervicale, platysma myoides, occipitalis, auricularis posterior and some of the extrinsic muscles of the ear (e.g., antitragicus, helicis and/or transversus and obliquus auriculae) of mammals very likely have a common phylogenetic and ontogenetic origin (e.g., Boas and Paulli, 1908; Huber, 1930a,b, 1931; Gasser, 1967; Jouffroy and Saban, 1971; Saban, 1971; this work). Also, it seems clear, in face of the data available, that mammalian muscles such as the interhyoideus profundus, sphincter colli supercialis, sphincter colli profundus, naso-labialis, levator labii superioris, levator labii superioris alaeque nasi, buccinatorius, dilatator nasi, maxillo-naso-labialis, nasalis, depressor septi nasi, levator anguli oris facialis, orbicularis oris, depressor labii inferioris, depressor anguli oris, and/or mentalis derive from the interhyoideus of non-mammalian tetrapods (e.g., Gasser 1967; Jouffroy and Saban, 1971; Saban, 1971; Seiler, 1971a,b,c,d,e, 1974a,b, 1975, 1979, 1980; this work). However, as explained in Appendix 3 and shown in Appendix 4 (dotted arrows), even a detailed, updated overall analysis of the data obtained from my dissections and available in the literature does not allow us to satisfactorily answer some of the questions that have been puzzling anatomists for decades. For instance, it is still not clear if the therian mandibulo-auricularis (a muscle that is usually deep to all the other mammalian facial muscles) is phylogenetically more related to the other facial muscles than to deeper dorso-median muscles such as the stylohyoideus, digastricus posterior, jugulohyoideus, and stapedius (e.g., Lightoller, 1934; Jouffroy and Saban, 1971; Seiler, 1971a,b,c,d,e, 1974a,b, 1975, 1979, 1980; this work). Also, it is commonly accepted that muscles such as the zygomaticus major, zygomaticus minor, orbito-temporo-auricularis, frontalis, auriculo-orbitalis, temporoparietalis, auricularis anterior, and auricularis superior derive from the sphincter colli profundus and/or supercialis, but Seiler (1971a,b,c,d,e, 1974a,b, 1975, 1979, 80), based on his comparative and developmental studies, argues that at least some of these muscles may derive from the platysma cervicale and/or myoides (Appendices 3,4). A detailed comparative analysis of the development and innervation of the hyoid muscles of various key mammalian groups, including monotremes, as well as of several other vertebrates, is clearly needed to clarify these and other controversial issues regarding the origin, homologies, and evolution of the mammalian facial muscles and to test the hypotheses proposed in Appendices 3 and 4. I plan to undertake such an analysis in a future work. Despite the controversies regarding the homologies and evolution of the facial muscles within the Mammalia as a whole, the dissections, comparisons,
Journal of Morphology

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and review of the literature undertaken in the present work clearly indicate that, within the Euarchonta, the overall conguration of the facial muscles of extant colugos is actually very similar to that found in extant tree-shrews such as Tupaia and in extant lower primates such as strepsirhines (e.g., Ruge, 1885; Le Gros Clark, 1924, 1926; Huber, 1930a,b; Lightoller, 1934; this work). For instance, all these taxa have a characteristic zygomaticus minor (auriculolabialis superior) originating posterior to, and blending with, the orbicularis oris, and a zygomaticus major (auriculolabialis inferior) originating on the ear region and sometimes blending with the platysma myoides (Fig. 1, compare with, e.g., plate I of Lightoller, 1934). As explained by Saban (1968), the presence of both a zygomaticus minor and a zygomaticus major, and the origin of the latter in the ear region and not on the zygomatic arch, are features that are not commonly found in, and are apomorphic for, placental mammals. Extant colugos, tree-shrews and lemurs also have muscles such as the frontalis, auricularis superior, auriculo-orbitalis, and corrugator supercilii, which are usually not differentiated into independent elements in non-euarchontan mammals, including in closely related groups (see above) such as rodents (Appendices 3,4; see also, e.g., Boas and Paulli, 1908; Huber, 1930a,b, 1931; Gasser, 1967; Jouffroy and Saban, 1971; Saban, 1971; this work). However, it should be noted that not all the facial muscles present in extant tree-shrews such as Tupaia and/or in extant plesiomorphic primates such as lemurs are present in extant colugos. For instance, in extant colugos the mandibulo-auricularis is not present as an independent, eshy muscle (Appendices 3,4). This muscle is present in treeshrews such as Tupaia (Appendices 3,4) and Ptilocercus (e.g., Le Gros Clark, 1926). Although it is missing in primates such as humans (Appendices 3,4), it is also present in plesiomorphic primates such as strepsirhines, and was very likely present in the last common ancestor of extant primates (e.g., Huber, 1930a,b; Lightoller, 1934; Jouffroy and Saban, 1971). As this muscle is also present in numerous non-euarchontan placental mammals, it was very likely present in the last common ancestor of tree-shrews, colugos and primates and secondarily lost in colugos (Appendices 3,4; see also, e.g., Boas and Paulli, 1908; Huber, 1930a,b, 1931; Edgeworth, 1935; Jouffroy and Saban, 1971). The sphincter colli profundus and platysma cervicale are present in extant colugos and extant treeshrews such as Tupaia and Ptilocercus, as well as in most non-euarchontan placental mammals (Appendices 3,4; see also, e.g., Jouffroy and Saban, 1971). These two muscles are missing in humans but are present in various other primates, including plesiomorphic primates such as strepsirhines (e.g., Ruge, 1885; Huber, 1930a,b, 1931; Lightoller,
Journal of Morphology

1934; Edgeworth, 1935; Jouffroy and Saban, 1971). Therefore, both these muscles were very likely present in the last common ancestor of colugos, tree-shrews, and primates, as well as in the last common ancestor of extant primates. The sphincter colli supercialis is present in tree-shrews such as Tupaia, as well as in numerous non-euarchontan mammals, including rodents and lagomorphs, and was thus very likely also present in the last common ancestor of colugos, primates, and tree-shrews (Appendices 3,4; see also, e.g., Boas and Paulli, 1908; Huber, 1930a,b, 1931; Edgeworth, 1935, Jouffroy and Saban, 1971). It is sometimes stated in the literature that extant primates lack a sphincter colli supercialis, but according to authors such as Jouffroy and Saban (1968) this muscle is present in some strepsirhine primates such as the lemuroid Propithecus. Therefore, the presence of this muscle may also be plesiomorphic for primates, i.e., it may have been independently lost within dermopteran and primate evolution. The zygomatico-orbicularis is a small muscle that runs from the orbital region to the zygomatic arch and that is missing in most mammals (e.g., Ruge, 1885, 1897, 1910; Boas and Paulli, 1908; Lightoller, 1928a,b, 1934, 1940a,b, 1942; Huber, 1930,a,b, 1931; Edgeworth, 1935; Andrew, 1963; Gasser, 1967; Jouffroy and Saban, 1971; Saban, 1971; Seiler, 1971a,b,c,d,e, 1974a,b, 1975, 1979, 1980; Minkoff et al., 1979; Preuschoft, 2000; Schmidt and Cohn, 2001; Burrows and Smith, 2003; Burrows et al., 2006). It was described in Tupaia by Le Gros Clark (1924) and then in Ptilocercus by Le Gros Clark (1926) (although Le Gros Clark, 1926, described the zygomatico-mandibularis as part of the orbicularis oculi, he clearly stated that this it is a well-developed and strong muscle in Ptilocercus). As explained in the section earlier, the thin group of bers lying ventromedially to the auriculo-orbitalis and connecting the orbicular region to the zygomatic arch in the colugos dissected corresponds very likely to the zygomaticoorbicularis of tree-shrews. It possibly also corresponds to the thin group of bers of the lemur specimen illustrated in Lightollers (1934) Figure 4, which apparently originates in the orbital region, ventromedially to the auriculo-labialis, and to run posteroventrally to attach to the zygomatic arch. A detailed comparative study of the facial muscles of a large number of euarchontans is needed to clarify if the zygomatico-orbicularis was present in the last common ancestor of colugos, primates, and tree-shrews. I plan to undertake such a study in a future work. The branchial muscles ceratohyoideus, spinotrapezius, cleido-occipitalis, and sternomastoideus are not present as independent muscles in modern humans (Appendices 5,6), but are present in various other primates, including plesiomorphic primates such as lemuroids and/or lorisoids (e.g., Murie

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and Mivart, 1872; Sonntag, 1924; Edgeworth, 1935; Sprague, 1944b; Hill, 1953; Jouffroy, 1962; Saban, 1968). These muscles are also present in extant colugos and extant tree-shrews, as well as in numerous other mammals. They were thus very likely present in the last common ancestor of colugos, tree-shrews and primates (Appendices 5,6; see also, e.g., Jouffroy, 1971). The spinotrapezius is present as an independent, distinct muscle in the colugo specimens dissected by Leche (1886) and by me (see section above). Interestingly, according to authors such as Edgeworth (1935), Le Gros Clark (1924, 1926), Hill (1953), Jouffroy (1962, 1971), and George (1977), the spinotrapezius is not present as a independent muscle in extant tree-shrews and in extant primates: it is instead completely fused with other muscular structures to form the trapezius of these mammals (Appendices 5,6). If further studies corroborate that the spinotrapezius is effectively absent as an independent element in all extant tree-shrews and primates, this could possibly constitute a potential synapomorphic feature to support a close relationship between treeshrews and primates (see Introduction). Extant colugos and extant primates such as humans have eight pharyngeal muscles, whereas extant tree-shrews such as Tupaia have seven. The pterygopharyngeus is absent as an independent muscle in Tupaia and in modern humans (it isprobably included in the constrictor pharyngis superior: Appendices 5,6). However, it is present as an independent element in various non-human primates, and was probably present in the last common ancestor of the extant primate taxa (e.g., Edgeworth, 1935; Kanagasuntheram, 19521954; Saban, 1968). As this muscle is also present in extant colugos and in numerous other mammalian taxa, it was very likely plesiomorphically present in euarchontans and then independently lost within the evolutionary history of tree-shrews and of primates (Appendices 5,6; see also, e.g., Edgeworth, 1935; House, 1953; Saban, 1968). The pharyngeal muscle uvulae, as well as the laryngeal muscles vocalis and arytenoideus obliquus, are only present as independent elements in a few phylogenetically derived primates, such as humans; the presence of these muscles is clearly apomorphic for the order Primates (Appendices 5,6; see also, e.g., Edgeworth, 1935; Negus, 1949; DuBrul, 1958; Starck and Schneider, 1960; Saban, 1968; Wind, 1970; Crelin, 1987; Harrison, 1995). As explained in the section above, in extant colugos the hypobranchial muscle thyrohyoideus is completely fused with the hyoglossus, being thus absent as an independent element. As in most extant tree-shrews, primates, and other placentals the thyrohyoideus is present as an independent muscle, the condition found in extant colugos is clearly apomorphic for euarchontans (Appendices 7,8). The absence of the hypobranchial muscle

omohyoideus in extant colugos also represents an apomorphic condition for the Euarchonta (Appendices 7,8). The hypobranchial muscle palatoglossus is absent as an independent element in the noncolugo and nonprimate mammals listed in Appendices 7 and 8. However, this muscle is present as a distinct element in many non-euarchontan mammals, and was possibly present in the common ancestor of primates, tree-shrews and colugos (e.g., Edgeworth, 1935; Saban, 1968). General Remarks From the discussion earlier, it can thus be said that the last common ancestor of primates, treeshrews, and colugos probably had a mylohyoideus, a digastric anterior, a masseter, a temporalis, a pterygoideus lateralis, a tensor tympani, a tensor veli palatini, a pterygoideus medialis, a stylohyoideus, a jugulohyoideus, a digastricus posterior, a stapedius, a platysma cervicale, a platysma myoides, an occipitalis, an auricularis posterior, a mandibulo-auricularis, a sphincter colli supercialis, a sphincter colli profundus, a zygomaticus major, a zygomaticus minor, a frontalis, an auriculo-orbitalis, an auricularis superior, an orbicularis oculi, a corrugator supercilii, a naso-labialis, a buccinatorius, a maxillo-naso-labialis, a levator anguli oris facialis, an orbicularis oris, a mentalis, a stylopharyngeus, a ceratohyoideus, an acromiotrapezius, a spinotrapezius, a cleido-occipitalis, a cleidooccipitalis, a cleidomastoideus, a sternomastoideus, a constrictor pharyngis medius, a constrictor pharyngis inferior, a cricothyroideus, a constrictor pharyngis superior, a pterygopharyngeus, a palatopharyngeus, a levator veli palatini, a salpingopharyngeus, a thyroarytenoideus, a cricoarytenoideus lateralis, an arytenoideus, a cricoarytenoideus posterior, a geniohyoideus, a genioglossus, a hyoglossus, a styloglossus, a sternohyoideus, a omohyoideus, a sternothyroideus and a thyrohyoideus, and possibly an intermandibularis anterior, a zygomatico-orbicularis, and a palatoglossus (Appendices 1 8). Therefore, with respect to the number of muscles, the last common ancestor of colugos, primates, and tree-shrews, and probably the common ancestor of the extant primate taxa (see above), were very likely more similar to extant tree-shrews than to extant colugos. This is because various muscles that were probably plesiomorphically present in the euarchontan and the primate clades, e.g., the stylohyoideus, mandibulo-auricularis, cleido-occipitalis, omohyoideus, and sternohyoideus, are absent as independent elements in extant colugos. The only muscles that are lacking in extant tree-shrews such as Tupaia and that were probably plesiomorphically present in both the euarchontan and primate clades are the pterygopharyngeus and possibly the palatoglossus (the spinotrapezius is missing in Tupaia, but was probably
Journal of Morphology

24

R. DIOGO

also plesiomorphically absent in the primate clade: see above). Therefore, extant tree-shrews do seem to provide a good living model for the study of not only the osteological (e.g., Jablonski, 1986; Sargis, 2004; Silcox et al., 2007) but also the myological structures of plesiomorphic primates, regardless of how the phylogenetic relationships between them, the colugos, and the primates are interpreted (see Introduction). As extant colugos have some muscles that were probably plesiomorphically present in the rst primates and that are missing in extant tree-shrews, both colugos and treeshrews should, however, be ideally used as living models for the study of basal primates (Appendices 18). It is important to stress that this does not mean that these groups should be seen as ancestors of primates. Actually, the fact that both the colugos and the tree-shrews secondarily lost muscles that were very likely plesiomorphically present in the euarchontan and primate clades clearly stresses that, as is now well-known in theory, but unfortunately often neglected in general textbooks and even in specialized articles, evolution is not directed towards a goal, and surely not towards primates and humans. That is why throughout this article I prefer to use the term Correspond, because the spinotrapezius of extant colugos, for example, is clearly not ancestral to the trapezius of primates and of humans. It simply corresponds to a part of the trapezius complex that, in adult extant colugos, becomes sufciently differentiated to deserve being recognized as an independent muscle. In fact, the number of true branchial muscles (Appendix 6) found in primates such as humans is actually much smaller than that found in most nonprimate mammals (e.g., monotremes such as the platypus usually have eight muscles, rodents such as rats seven, colugos with six, tree-shrews such as Tupaia six, and modern humans have three muscles; Appendix 6). Interestingly, within the various muscular groups analyzed in this article, the only cases in which the number of muscles found in humans is actually clearly greater than that found in extant colugos, tree-shrews, and primates such as strepsirhines, and, importantly, in which humans do exhibit various peculiar muscles that are not present in the vast majority of the other mammals, concern the facial and laryngeal muscles (Appendices 36). Examples of facial and laryngeal muscles that are present in modern humans and lacking in most other mammals, including colugos, treeshrews, and primates such as lemurs, are the risorius, depressor supercilii, levator labii superioris alaeque nasi, depressor septi nasi, depressor labii inferioris, depressor anguli oris, vocalis, and arytenoideus obliquus (Appendices 36). The analysis of the muscular data discussed in this article thus seems to corroborate the crucial role played
Journal of Morphology

by vocal communication and by facial expressions in primate, and namely in human, evolution (e.g., Ruge, 1885, 1897, 1910; Boas and Paulli, 1908; Lightoller, 1928a,b, 1934, 1940a,b, 1942; Huber, 1930, 1931; Edgeworth, 1935; Negus, 1949; DuBrul, 1958; Starck and Schneider, 1960; Andrew, 1963; Gasser, 1967; Saban, 1968, 1971; Wind, 1970; Jouffroy and Saban, 1971; Seiler, 1971, a,b,c,d,e, 1974a,b, 1975, 1979, 1980; Minkoff et al., 1979; Crelin, 1987; Harrison, 1995; Preuschoft, 2000; Schmidt and Cohn, 2001; Burrows and Smith, 2003; Burrows et al., 2006; Burrows, 2008; this work). Before ending this article, I would like to stress that the hypotheses proposed in the paragraphs earlier, as well as in the other parts of the text and in Appendices 18, are simply scientic hypotheses that need to, and hopefully will, be tested by data obtained in the future. As explained in the text and Appendices 18, some issues remain problematic and need to be addressed in future studies. For example, detailed comparative ontogenetic studies of the facial muscles of numerous euarchontans, as well as of other mammals, including monotremes, are clearly needed. As said above, I plan to undertake such studies in future works. But, above all, I hope that the information provided in the present article could stimulate and pave the way for other researchers to undertake future works on the comparative anatomy, functional morphology, development, evolution, and/or phylogeny of the head and neck muscles of euarchontans and of mammals in general. ACKNOWLEDGMENTS I thank M. Carleton, D. Schmidt and L. Gordon (National Museum of Natural History), S. Ktretsch mar, M. Canepa, J. C. Stazonelli and G. Scrocchi (Fundacion Miguel Lillo), R. Walsh and F. Slaby (Department of Anatomy, George Washington University), B. Richmond (Department of Anthropology, George Washington University), M. Aziz (Department of Anatomy, Howard University) and J. Fritz and J. Murphy (Primate Fondation of Arizona) for kindly providing a large part of the specimens analyzed for this study. I am particularly thankful to V. Abdala, N. Lonergan and B. Wood for their assistance and advice, and to F. W. Harrison and an anonymous reviewer for providing helpful suggestions. RD was supported by a George Washington University Presidential Merit Fellowship. LITERATURE CITED
Adams SB, Wheeler JFG, Edgeworth FH. 1929. On the innervation of the platysma and the mandibulo-auricularis. J Anat 63:242252. Anderson RJ. 1880. A variety of the mylopharyngeus and other unusual muscular abnormalities. J Anat Physiol 14:357359.

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Anderson RJ. 1881. The morphology of the muscles of the tongue and pharynx. J Anat Physiol 15:382391. Andrew RJ. 1963. Evolution of facial expression. Science 142:10341041. Aziz MA. 1981. Possible atavistic structures in human aneuploids. Am J Phys Anthropol 54:347353. Aziz MA, Cowie RJ, Skinner CE, Abdi TS, Orzame G. 1998. Are the two heads of the human lateral pterygoid separate muscles? A perspective based on their nerve supply. J Orofac Pain 2:226239. Barrow JR, Capecchi MR. 1999. Compensatory defects associated with mutations in Hoxa1 restore normal palatogenesis to Hoxa2 mutants. Development 126:50115026. Birou G, Garcier JM, Guillot M, Vanneuville G, Chazal J. 1991. A study of the lateral pterygoid muscle: Anatomic sections and CT appearances. Surg Radiol Anat 13:307311. 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. Jena: Gustav Fischer. Bryant MD. 1945. Phylogeny of Nearctic sciuridae. Am Midland Nat 33:257390. Burrows AM. 2008. The facial expression musculature in primates and its evolutionary signicance. Bioessays 30:212225. Burrows AM, Smith TD. 2003. Muscles of facial expression in Otolemur with a comparison to Lemuroidea. Anat Rec 274:827836. 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 208:153167. Chi TK. 1937. An unusual variation of the pharyngeal muscles. J Anat 72:134135. Crelin ES. 1987. The Human Vocal Tract: Anatomy, Function, Development, and Evolution. New York: Vantage Press. Dawkins R. 2004. The ancestors tale A Pilgrimage to the Dawn of Life. Boston: Houghton Mifin. Diogo R. 2007. On the Origin and Evolution of Higher-Clades: Osteology, Myology, Phylogeny and Macroevolution of Bony Fishes and the Rise of Tetrapods. Eneld: Science Publishers. Diogo R. 2008. Comparative anatomy, homologies and evolution of the mandibular, hyoid and hypobranchial muscles of bony sh and tetrapods: A new insight. Anim Biol 58:123172. Diogo R, Lonergan N, Abdala V, Wood BA. From sh to modern humans: comparative anatomy, homologies and evolution of the head and neck. J Anat (in press). DuBrul EL. 1958. Evolution of the Speech Apparatus. Springeld: Thomas. Edgeworth FH. 1935. The Cranial Muscles of Vertebrates. Cambridge: University press. El Haddioui AL, Zouaoui A, Bravetti P, Gaudy JF. 2005. Functional anatomy of the human lateral pterygoid muscle. Surg Radiol Anat 27:271286. Gasser RF. 1967. The development of the facial muscles in man. Am J Anat 120:357376. George RM. 1977. The limb musculature of the Tupaiidae. Primates 18:134. Gibbs S. 1999. Comparative soft tissue morphology of the extant Hominoidea, including man. Unpublished PhD Thesis, The University of Liverpool. Gorniak GC. 1985. Trends in the action of mammalian masticatory muscles. Am Zool 25:331337. Greene EC. 1935. Anatomy of the Rat. New York: Hafner Publishing Co. Gunnell GF, Simmons NB. 2005. Fossil evidence and the origin of bats. J Mammal Evol 12:209246. Harrison DFN. 1995. The Anatomy and Physiology of the Mammalian Larynx. Cambridge: University Press. Hill WCO. 1953. Primates Comparative Anatomy and Taxonomy. I. Strepsirhini. Edinburgh: University Press. House EL. 1953. A myology of the pharyngeal region of the albino rat. Anat Rec 116:363381. Howell AB. 1937a. Morphogenesis of the shoulder architecture, Part V, Monotremata. Q Rev Biol 12:191205.

25

Howell AB. 1937b. Morphogenesis of the shoulder architecture, Part IV, Therian Mammalia. Q Rev Biol 12:440463. Huber E. 1930a. Evolution of facial musculature and cutaneous eld of trigeminus, Part I. Q Rev Biol 5:133188. Huber E. 1930b. Evolution of facial musculature and cutaneous eld of trigeminus, Part II. Q Rev Biol 5:389437. Huber E. 1931. Evolution of Facial Musculature and Expression. Baltimore: The Johns Hopkins University Press. Jablonski NG. 1986. A history of form and function in the primate masticatory apparatus from the ancestral primate through the strepsirhines. In: Swindler DR, Erwin J, editors. Comparative Primate Biology, Systematics, Evolution and Anatomy, Vol. 1. New York: AR Liss. pp 537558. Janecka JE, Miller W, Pringle TH, Wiens F, Zitzmann A, Helgen KM, Springer MS, Murphy WJ. 2007. Molecular and genomic data identify the closest living relative of primates. Science 318:792794. Jarvik E. 1963. The composition of the intermandibular division of the head in shes and tetrapods and the diphyletic origin of the tetrapod tongue. Kungl Sven Veten Handl 9:174. Jarvik E. 1980. Basic Structure and Evolution of Vertebrates. London: Academic Press. Jouffroy FK. 1962. La musculature des membres chez les lemuriens de Madagascar, etude descriptive et comparative. Mammalia 26:1326. Jouffroy FK. 1971. Musculature des membres. In: Grasse PP, ` editor. Traite de Zoologie, XVI: 3 (Mammiferes). Paris: Masson et Cie. pp 1475. Jouffroy FK, Lessertisseur J. 1971. Particularites musculaires des Monotremes, musculature post-cranienne. In: Grasse PP, ` editor. Traite de Zoologie, XVI: 3 (Mammiferes). Paris: Masson et Cie. pp 733836. ` Jouffroy FK, Saban R. 1971. Musculature peauciere. In: Grasse ` PP, editor. Traite de Zoologie, XVI: 3 (Mammiferes). Paris: Masson et Cie. pp 477611. Kanagasuntheram R. 19521954. Observations on the anatomy of the hoolock gibbon. Ceylon J Sci Sect G 5:1164, 69122. Kardong KV. 2002. Vertebrates: Comparative Anatomy, Function, Evolution, 3rd ed. New York: McGraw-Hill. Leche W. 1886. Uber die Saugethiergattung Galeopithecus: eine morphologische untersuchung. Kungl Svenska Vetenskap Akad Stockholm 21:392. Le Gros Clark WE. 1924. The myology of the tree-shrew (Tupaia minor). Proc Zool Soc Lond 1924:461497. Le Gros Clark WE. 1926. On the anatomy of the pen-talied treeshrew (Ptilocercus lowii). Proc Zool Soc Lond 1926:11781309. Lightoller GS. 1928a. The action of the m. mentalis in the expression of the emotion of distress. J Anat 62:319332. Lightoller GS. 1928b. The facial muscles of three orang utans and two Cercopithecidae. J Anat 63:1981. Lightoller GS. 1934. The facial musculature of some lesser primates and a Tupaia. Proc Zool Soc Lond 1934:259309. Lightoller GS. 1940a. The comparative morphology of the platysma: A comparative study of the sphincter colli profundus and the trachelo-platysma. J Anat 74:390396. Lightoller GS. 1940b. The comparative morphology of the M. caninus. J Anat 74:397402. Lightoller GS. 1942. Matrices of the facialis musculature: Homologization of the musculature in monotremes with that of marsupials and placentals. J Anat 76:258269. Macalister A. 1872. The myology of the Cheiroptera. Phil Trans R Soc Lond 162:125171. Marivaux L, Bocat L, Chaimanee Y, Jaeger J-J, Marandat B, Srisuk P, Tafforeau P, Yamee C, Welcomme J-L. 2006. Cynocephalid dermopterans from the Palaeogene of South Asia (Thailand, Myanmar and Pakistan): Systematic, evolutionary and palaeobiogeographic implications. Zool Scripta 35:395 420. Minkoff EC, Mikkelsen P, Cunningham WA, Taylor KW. 1979. The facial musculature of the opossum (Didelphis virginiana). J Mammal 60:4657. Murie J, Mivart StG. 1872. On the anatomy of the Lemuroidea. Trans Zool Soc Lond 7:1113.

Journal of Morphology

26

R. DIOGO
Seiler R. 1980. Ontogenesis of facial muscles in primates. Morphol Jb 126:841864. Shattock SG. 1882. A kerato-thyro-hyoid muscle as a variation in human anatomy. J Anat Physiol 171:124125. Shoshani J, Groves CP, Simons EL, Gunnell GF. 1996. Primate phylogeny: Morphological vs molecular results. Mol Phylogenet Evol 5:102154. Silcox MT, Sargis EJ, Bloch JI, Boyer DM. 2007. Primate origins and supraordinal relationships: Morphological evidence. In: Henke W, Tattersall I, editors. Handbook of Palaeoanthropology, Vol. 2. Primate Evolution and Human Origins. Heidelberg: Springer-Verlag. pp 831859. Smith KK. 1992. The evolution of the mammalian pharynx. Zool J Linn Soc 104:313349. Sokoloff AJ. 2000. Localization and contractile properties of intrinsic longitudinal motor units of the rat tongue. J Neurophysiol 84:827835. Sonntag CF. 1924. The Morphology and Evolution of the Apes and Man. London: John Bale Sons and Danielsson Ltd. Sprague JA. 1942. The hyoid apparatus of Neotoma. J Mammal 23:405411. Sprague JA. 1943. The hyoid region of placental mammals with special reference to the bats. Am J Anat 72:385472. Sprague JA. 1944a. The hyoid region in the Insectivora. Am J Anat 74:175216. Sprague JA. 1944b. The innervation of the pharynx in the rhesus monkey, and the formation of the pharyngeal plexus in primates. Anat Rec 90:197208. Stafford BJ, Szalay FS. 2000. Craniodental functional morphology and taxonomy of dermopterans. J Mammal 81:360385. Starck D, Schneider R. 1960. Respirationsorgane. In: Hofer H, Schultz AH, Starck D, editors. Primatologia III/2. Basel: S. Karger. pp 423587. Sullivan WE, Osgood CW. 1927. The musculature of the superior extremity of the orang-utan, Simia satyrus. Anat Rec 35:193239. Taylor J. 1925. An unusual variation of the omo-hyoid muscle. J Anat 59:331332. The Federative Committee on Anatomical Terminology. 1998. Terminologia Anatomica. Stuttgard: Georg Thieme. Thewissen JGM, Babcock SK. 1991. Distinctive cranial and cervical innervation of wing muscles: New evidence for bat monophyly. Science 251:934936. Thewissen JGM, Babcock SK. 1993. The implications of the propatagial muscles of ying and gliding mammals for archontan systematics. In MacPhee RDE, editor. Primates and their Relatives in Phylogenetic Perspective. New York: Plenum Press. pp 91107. Walker WF, Homberger DG. 1998. Anatomy and Dissection of the Rat, 3rd ed. New York: Freeman Company. Wells LH, Thomas EA. 1927. A note on two abnormal laryngeal muscles in a Zulu. J Anat 61:340343. Whidden HP. 2000. Comparative myology of moles and the phylogeny of the Talpidae (Mammalia, Lipotyphla). Am Museum Novitates 3294:153. Wind J. 1970. On the phylogeny and ontogeny of the human larynx. Groningen: Wolters-Noordhoff. Wood J. 1866. Variations in human myology observed during the Winter session of 1865-1866 at Kings College, London. Proc R Soc Lond 15:229244. Wood J. 1867a. On human muscular variations and their relation to comparative anatomy. J Anat Physiol 1867:4459. Wood J. 1867b. Variations in human myology observed during the Winter session of 18661867 at Kings College, London. Proc R Soc Lond 15:518545. Wood J. 1868. Variations in human myology observed during the Winter session of 18671868 at Kings College, London. R Soc Lond 16:483525. Wood J. 1870. On a group of varieties of the muscles of the human neck, shoulder, and chest, with their transitional forms and homologies in the Mammalia. Philos Trans R Soc Lond 160:83116.

Netter FH. 2006. Atlas of Human Anatomy, 4th ed. Philadelphia: Saunders. Negus VE. 1949. The Comparative Anatomy and Physiology of the Larynx. New York: Hafner Publishing Company. Noden DM, Francis-West P. 2006. The differentiation and morphogenesis of craniofacial muscles. Dev Dyn 235:11941218. Parsons FG. 1898. The muscles of mammals, with special relation to human myology: A course of lectures delivered at the Royal College of Surgeons of England, lecture I, the muscles of the head and neck. J Anat Physiol 32:428450. Peterka HE. 1936. A study of the myology and osteology of tree sciurids with regard to adaptation to arboreal, glissant and fossorial habits. Trans Kansas Acad Sci 39:313332. Pettersen GC, Koltis GG, White MJ. 1979. An examination of the spectrum of anatomic defects and variations found in eight cases of trisomy 13. Amer J Med Genet 3:183210. 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 9:566578. Preuschoft S. 2000. Primate faces and facial expressions. Soc Res 67:245271. Ruge G. 1885. Uber die Gesichtsmuskulatur der Halbaffen. Morph Jb 11:243315. Ruge G. 1897. Uber Das Peripherische Gebiet Des Nervus Facialis Boi Wirbelthieren. Leipzig: Festschr f Gegenbaur. Ruge G. 1910. Verbindungen des platysma mit der tiefen muskulatur des halses beim menschen. Morph Jb 41:708724. Ryan JM. 1986. Comparative morphology and evolution of cheek pouches in rodents. J Morphol 190:2742. Ryan JM. 1989. Evolution of cheek pouches in African pouched rats (Rodentia: Cricetomyinae). J Mammal 70:267274. Saban R. 1968. Musculature de la tete. In: Grasse PP, editor. ` Traite de Zoologie, XVI: 3 (Mammiferes). Paris: Masson et Cie. pp 229472. Saban R. 1971. Particularites musculaires des Monotremes Musculature de la tete. In: Grasse PP, editor. Traite de Zoologie, ` XVI: 3 (Mammiferes). Paris: Masson et Cie. pp 681732. Sargis EJ. 2002a. The postcranial morphology of Ptilocercus lowii (Scandentia, Tupaiidae): An analysis of primatomorphan and volitantian characters. J Mammal Evol 9:137160. Sargis EJ. 2002b. Functional morphology of the forelimb of tupaiids (Mammalia, Scadetia) and its phylogenetic implications. J Mammal 253:1042. Sargis EJ. 2004. New views on tree shrews: The role of tupaiids in primate supraordinal relationships. Evol Anthropol 13:5666. Seiler R. 1971b. Facial musculature and its inuence on the facial bones of catarrhinous primates. I. Morphol Jb 116:122142. Schmidt KL, Cohn JF. 2001. Human facial expressions as adaptations: Evolutionary questions in facial expression research. Yearb Phys Anthropol 44:324. Seiler R. 1971a. A Comparison Between the Facial Muscles of Catarrhini with Long and Short Muzzles. Proc. 3rd Int. Congr. Primat., Zurich 1970, Vol. l. Basel: Karger. pp 157 162. Seiler R. 1971b. Facial musculature and its inuence on the facial bones of catarrhinous primates. I. Morphol Jb 116:122142. Seiler R. 1971c. Facial musculature and its inuence on the facial bones of catarrhine primates. II. Morphol Jb 116:147185. Seiler R. 1971d. Facial musculature and its inuence on the facial bones of catarrhine primates. III. Morphol Jb 116:347 376. Seiler R. 1971e. Facial musculature and its inuence on the facial bones of catarrhine primates. IV. Morphol Jb 116:456 481. Seiler R. 1974a. Muscles of the external ear and their function in man, chimpanzees and Macaca. Morphol Jb 120:78122. Seiler R. 1974b. Particularities in facial muscles of Daubentonia madagascariensis (Gmelin 1788). Folia Primatol 22:8196. Seiler R. 1975. On the facial muscles in Perodicticus potto and Nycticebus coucang. Folia Primatol 23:275289. Seiler R. 1979. Criteria of the homology and phylogeny of facial muscles in primates including man. I. Prosimia and platyrrhina. Morphol Jb 125:191217.

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APPENDIX 1. Mandibular muscles of the adult colugos dissected and of adult representative members of other mammalian taxa Rodentia: Rattus norvegicus (Norwegian rat) Mylohyoideus Mylohyoideus Mylohyoideus Mylohyoideus (posterior part of mylohyoid sensu Le Gros Clark, 1924) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Monotremata; Ornithorhynchus anatinus (Platypus)

Mylohyoideus (as described by Lightoller, (1942) there is a mylohyoideus profundus, a mylohyoideus supercialis and, supercially to the latter, a digastricus anterior; Saban (1971) states that these three structures come from the same embryological anlage) Digastricus anterior Digastricus anterior (anterior belly of digastricus sensu; Greene, 1935) Intermandibularis anterior (transversus mandibularis sensu; Greene, 1935) Digastricus anterior (part of biventer sensu; Leche, 1886) Digastricus anterior

Digastricus anterior (anterior belly of biventer mandibulae sensu; Huber, 1930a,b)

Masseter (as described by Greene (1935), in the Norwegian rats dissected by me the masseter is mainly divided into a deep part with anterior and posterior bundles and a supercial part with anterior and posterior bundles)

Masseter (Masseter 1 zygomatico-mandibularis sensu; Stafford and Szalay, 2000) (in the colugo specimens dissected by me the masseter is subdivided into a supercial bundle, a deep bundle, and a zygomatico-mandibular bundle)

Intermandibularis anterior (anterior part of mylohyoid sensu; Le Gros Clark, 1924, and Sprague, 1944a) (not present as an independent element in Ptilocercus: Le Gros Clark, 1924) Masseter (as described by Le Gros Clark (1924), in the Tupaia specimens dissected by me the masseter is mainly divided into deep, intermediate and supercial bundles)

Masseter (in humans the masseter is usually mainly divided into deep and supercial bundles)

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Masseter (corresponds to the masseter 1 zygomaticomandibularis, and occasionally to the maxillomandibularis, sensu; Saban, 1971) (as shown in Sabans (1971) g. 569, in the platypus specimens dissected by me the masseter is mainly divided into a deep part with anterior and posterior bundles and a supercial part with anterior and posterior bundles) Detrahens mandibulae (some authors consider that the detrahens mandibulae is homologous to the digastricus anterior of other mammals, but it probably corresponds, instead, to part of the adductor mandibulae A2 of nonmammalian tetrapods: Saban, 1968)

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APPENDIX 1. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Temporalis (in the Cynocephalus specimens dissected the temporalis is not clearly divided into supercial and deep bundles, and there is no distinct pars suprazygomatica as that found in Tupaia) Temporalis (in the Tupaia specimens dissected the temporalis is mainly divided into a supercial bundle, a deep bundle, and a pars suprazygomatica sensu e.g., Saban, 1971) Pterygoideus lateralis (Pterygoideus externus sensu Le Gros Clark, 1924, 1926) (as described by Le Gros Clark, 1924, in the Tupaia specimens dissected by me the pterygoideus lateralis is constituted by a single bundle) Pterygoideus lateralis (in the Cynocephalus specimens dissected the pterygoideus lateralis is constituted by a single bundle) Temporalis (Greene (1935) describes the temporalis of rats as an undivided muscle, but as stated by, e.g., Walker and Homberger, 1998, in the specimens dissected by me this muscle is divided into s supercial, anterior bundle and a deep, posterior bundle) Pterygoideus lateralis (Pterygoideus externus sensu Greene, 1935) (in the specimens dissected the pterygoideus lateralis is constituted by a single bundle) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Temporalis (usually described as an undivided muscle, but various authors, as, e.g., Gorniak, 1985, consider that it is in fact often divided into supercial and deep bundles)

Monotremata; Ornithorhynchus anatinus (Platypus)

Journal of Morphology
Pterygoideus lateralis (in humans the pterygoideus lateralis is usually divided into superior and inferior heads: see e.g., Birou et al, 1991; Aziz et al., 1998; El Haddioui et al., 2005)

Temporalis

R. DIOGO

Pterygoideus lateralis (in some parts of Edgeworth (1935) work, he seems to suggest that the pterygoideus lateralis and medialis are both included in the pterygoideus medialis of monotremes and that the pterygoideus lateralis only becomes separated in other extant mammals; the platypus specimens dissected by me have both a pterygoideus lateralis and a pterygoideus medialis) Tensor tympani Tensor veli palatini (as described by Saban (1971), in the platypus specimens dissected by me the tensor veli palatini is present as an independent muscle) Pterygoideus medialis Tensor tympani Tensor veli palatini Tensor tympani Tensor veli palatini Tensor tympani Tensor veli palatini Pterygoideus medialis (Pterygoideus internus sensu; Greene, 1935) Pterygoideus medialis

Tensor tympani Tensor veli palatini

Pterygoideus medialis (Pterygoideus internus sensu Le Gros Clark, 1924, 1926)

Pterygoideus medialis

The nomenclature of the muscles shown in bold follows that of the text; in order to facilitate comparisons, in some cases names often used by other authors to designate a certain muscle/bundle are given in front of that muscle/bundle. Data compiled from evidence provided by my own dissections and comparisons and by a review of the literature. Each of the hypotheses of homology shown in the Appendix is based on a detailed analysis of all the lines of evidence available (e.g., innervation; relation with other muscular structures; relation with hard tissues; conguration/orientation of the bers; development; function; phylogeny; presence/absence/conguration in fossils; etc.) (see also text, Appendix 2 and Figs. 14).

APPENDIX 2. Scheme illustrating the authors hypotheses regarding the homologies of the mandibular muscles of the adult colugos dissected and of adult representative members of other mammalian taxa Rattus (9 muscles) Mylohyoideus Digastricus anterior Interm. anterior Masseter Temporalis Pterygoideus lateralis Tensor tympani Tensor veli palatini Pterygoideus medialis Masseter Temporalis Pterygoideus lateralis Tensor tympani Tensor veli palatini Pterygoideus medialis Mylohyoideus Digastricus anterior Cynocephalus (8 muscles) Tupaia (9 muscles) Mylohyoideus Digastricus anterior Interm. anterior Masseter Temporalis Pterygoideus lateralis Tensor tympani Tensor veli palatini Pterygoideus medialis Homo (8 muscles) Mylohyoideus Digastricus anterior Masseter Temporalis Pterygoideus lateralis Tensor tympani Tensor veli palatini Pterygoideus medialis

Ornithorhynchus (9 muscles)

Ventral Mylohyoideus Digastricus anterior Adductor mandibulae Masseter Detrahens man. Temporalis Pterygoideus lateralis Tensor tympani Tensor veli palatini Pterygoideus medialis

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

The nomenclature of the muscles follows that used in the text. Data compiled from evidence provided by my own dissections and comparisons and by a review of the literature. Each of the homology hypotheses shown in the Appendix 2 is based on detailed analysis of all the lines of evidence available (e.g., innervation; relation with other muscular structures; relation with hard tissues; conguration/orientation of the bers; development; function; phylogeny; presence/absence/conguration in fossils; etc.) (see also text, Appendix 1 and Figs. 14; Ventral, Adductor mandibulae 5 Ventral and adductor mandibulae musculature sensu; Edgeworth, 1935, and Diogo, 2007).

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APPENDIX 3. Hyoid muscles of the adult colugos dissected and of adult representative members of other mammalian taxa (see caption of Appendix 1; see also text, Appendix 3 and Figs. 14) Rodentia: Rattus norvegicus (Norwegian rat) (see text) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Stylohyoideus [Gassers (1967) developmental study suggests that in humans the digastricus posterior, stapedius and stylohyoideus derive from the same anlage]

Monotremata: Ornithorhynchus anatinus (Platypus)

Journal of Morphology
Stylohyoideus [Sprague (1944a) states that the styloglossus of certain treeshrews is innervated by the hypoglossal nerve, but (Le Gros Clark, 1926; Lightoller, 1934) defend that this muscle is innervated by the facial nerve, as in other mammals] Digastricus posterior [as described by Sprague (1944a) my dissections suggest that the digastricus posterior and digastricus anterior of Tupaia are joined by a welldeveloped tendon] Jugulohyoideus (see on the left) Digastricus posterior (the digastricus posterior and digastricus anterior of humans are usually joined by a well-developed tendon) [but present in other extant primates, as (e.g., lemuroids: Lightoller, 1934; Saban, 1968)]

Styloideus [the styloideus sensu (Huber, 1930a) corresponds to the interhyoideus sensu (Edgeworth, 1935) and to the posterior digastric sensu (Parsons, 1898)]

Stylohyoideus (see on the left)

Digastricus posterior (see above)

R. DIOGO

Stapedius

Digastricus posterior [part of biventer sensu (Leche, 1886)] [as described by Saban (1968), my dissections suggest that the digastricus posterior and digastricus anterior of colugos are joined by a tendinous intersection] Jugulohyoideus [mastoideostyloideus sensu (Saban, 1968)] [probably corresponds to part of the stylohyoideus and/or possibly of the digastricus posterior of mammals such as rats: Appendix 4; (e.g., Huber, 1930a, 1931; Saban, 1968)] Stapedius Stapedius Platysma cervicale [part of platysma sensu (Le Gros Clark, 1924) and of notoplatysma sensu (Lightoller, 1934)] Platysma cervicale [part of platysma sensu (Leche, 1886)]

Stapedius [levator hyoideus sensu (Edgeworth, 1935)] Platysma cervicale [the platysma cervicale sensu; Jouffroy and Saban (1971) corresponds to the pars nuchalis of the platysma sensu (Saban, 1971) and to part of the platysma sensu (Lightoller, 1942)]

Stapedius [but present in other primates, as e.g., lemuroids: Jouffroy and Saban, 1971; according to Gasser, (1967), the platysma cervicale [5his nuchal platysma] is present in early developmental stages of humans, disappearing in later stages; Aziz (1981) considers that the transversus nuchae found in some humans is a remaining of the platysma cervicale, but Gasser (1967) describes both a platysma cervicale and a transversus nuchae in early human embryos]

Platysma cervicale [the cranial panniculus sensu Greene (1935) corresponds to my platysma cervicale 1 auriculolabialis inferior [5zygomaticus major]; his supercial portion of the cervical panniculus corresponds to my sphincter colli profundus 1 supercialis; his deep cervical panniculus corresponds to my sternofacialis, which he describes as an upper limb muscle but, as noted by Jouffroy and Saban (1971), is in fact a facial muscle that is probably derived from the sphincter colli profundus: (e.g., Jouffroy and Saban, 1971; Ryan, 1986, 1989; this work)]

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Platysma myoides [platysma myoides superior 1 jugalis propatagii sensu (Leche, 1886) dorsal sheet of propatagial complex sensu (Thewissen and Babcock, 1991, 1993: see text)] (mixed with platysma cervicale) Occipitalis (see on the left) Platysma myoides (mixed with platysma cervicale) Occipitalis [occipitalis 1 cervico-auriculo-occipitalis sensu (Lightoller, 1934): see on the left] Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Platysma myoides [platysma sensu (Netter, 2006) tracheoplatysma sensu (Lightoller, 1940a)]

Monotremata: Ornithorhynchus anatinus (Platypus)

Platysma myoides [probably corresponds to the pars omoidea sensu (Saban, 1971)]

Platysma myoides (blended with platysma cervicale)

[as described by Lightoller (1942) in the platypus specimens dissected by me, there is a bundle of the platysma that is somewhat similar to the occipitalis of the mammals listed on the right, but this bundle is clearly part of the platysma, i.e., it does not constitute an independent muscle] Auricularis posterior (see above) Extrinsic muscles of the ear (see on the left) Auricularis posterior (see above) Extrinsic muscles of the ear (see on the left)

Occipitalis [Gassers (1967) developmental study in humans suggests that the occipitalis, auricularis posterior and transversus nuchae develop from the same anlage]

Auricularis posterior (see above) Extrinsic muscles of the ear (see on the left)

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Extrinsic muscles of the ear [my dissections and comparisons suggest that the platypus has at least some extrinsic muscles of the ear, as suggested by Lightoller (1942); according to Huber (1930a,b, 1931) and Jouffroy and Saban (1971), the mammalian extrinsic muscles of the ear derive from both the platysma and the sphincter colli profundus]

Occipitalis (cranial part of levator auris longus sensu; Greene, 1935) (the occipitalis of Rattus is similar to that of Tupaia and Cynocephalus, i.e., it has a medial portion [occipitalis sensu; Lightoller, 1934] that extends blends with the frontalis and a lateral portion [5cervico-auriculo-occipitalis sensu; Lightoller, 1934] that runs anteroventrolaterally to attach to the posterior surface of the ear; these two portions are blended to each other posteriorly, attaching to the dorsal region of the neck, just medially to the posterior attachment of the auricularis posterior) Auricularis posterior (caudal part of levator auris longus sensu; Greene, 1935: see above) Extrinsic muscles of the ear [examples of extrinsic, facial muscles of the ear present in therian mammals are the obliquus auriculae, transversus auriculae, helicis, tragicus and/or antitragicus: see (e.g., Jouffroy and Saban, 1971)]

Journal of Morphology

31

32

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Mandibulo-auricularis (see on the left) Mandibulo-auricularis [auriculo-mandibularis sensu (e.g., Lightoller, 1934)] (see on the left) [as stated by Lightoller (1934), contrary to lemurs and, e.g., Tupaia, in primates as, e.g., Tarsius and marmosets the mandibuloauricularis is not present as an independent, eshy muscle: it probably corresponds, instead, to a strong fascial sheet connecting the posterior edge of the mandible to the bony external auditory meatus, which might well correspond to the stylo-mandibular ligament of humans; such a conguration is found in the colugos dissected: see text] Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) [probably corresponds to the stylo-mandibular ligament, which is usually present in humans: see on the left; according to Jouffroy and Saban (1971), it may possibly also correspond to the styloauricularis muscle abnormally present in a few humans; the mandibuloauricularis is present as an independent, eshy muscle in various primates, as, e.g., strepsirhines: (e.g., Lightoller, 1934)]

Journal of Morphology R. DIOGO

Monotremata: Ornithorhynchus anatinus (Platypus)

[authors as, e.g., Adams et al. (1929) suggest that the therian mandibulo-auricularis is a preauricular muscle and thus derives from the sphincter colli profundus, but most researchers consider that it is instead a postauricular muscle derived from the platysma: (e.g., Huber, 1930a,b, 1931; Ryan, 1986, 1989) however, a few authors, as, e.g., Lightoller (1934) and Jouffroy and Saban (1971) suggested that the mandibulo-auricularis may in fact be ontogenetically and phylogenetically more related to deeper hyoid muscles such as the stylohyoideus, digastricus posterior, stapedius, and/or jugulohyoideus than to other facial muscles; although I tentatively follow here the most consensual view, I do think that Lightollers hypothesis should not be discarded, because the mandibuloauricularis does usually lie deeper to the other facial muscles and its topology, the orientation of its bers, and its attachments (e.g., on the mandible and/or near the ear region) are in fact similar to those of the deeper hyoid muscles of mammals; also, Seilers (1980) developmental studies of treeshrews and primates seem to suggest that the mandibuloauricularis does not develop from the anlages that give rise to most other facial muscles, but instead from a different, deeper anlage]

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Risorius [authors such as Huber (1930a,b, 1931), suggested that the risorius derives from the sphincter colli profundus; my dissections and comparisons support the conclusions of Jouffroy and Sabans (1971) review, i.e., that the risorius derives instead from the platysma myoides; this latter hypothesis is also supported by the developmental data of Gasser (1967): see, e.g., his g. 10]

Monotremata: Ornithorhynchus anatinus (Platypus)

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Interhyoideus profundus [sphincter colli profundus sensu (Lightoller, 1942); hyomandibularis sensu (Edgeworth, 1935)] Sphincter colli supercialis [corresponds to Hubers (1930a) sphincter colli externus of platypus and sphincter colli of echidna] [Lightoller (1940a) states that Hubers (1930a) sphincter colli supercialis of, e.g., marsupials and rodentscorresponds to his transitus, i.e., to a part of the sphincter colli profundus that passes supercial to the platysma but that originally was deep to it: he says that the rest of the sphincter colli profundus (i.e., everything except the transitus) is absent in all primates, and that it is thus this transitus that gives the primate tracheo-platysma; however, my dissections and comparisons strongly indicate that the conguration of the platysma of primates such as lemurs (e.g., Lightoller, 1934) is in fact similar to that found in, e.g., extant colugos and tree-shrews, i.e., these latter mammals have both a platysma cervicale and a platysma myoides, although these muscles are deeply Sphincter colli supercialis (transitus sensu; Lightoller, 1942) [as explained by Lightoller (1940a, 1942), in rodents such as rats the sphincter colli does also have a part that is supercial to the platysma, i.e., a sphincter colli supercialis] (see text)

Sphincter colli supercialis [probably corresponds to the occipitocervicalis sensu (Lightoller, 1934) and might correspond to the cervicomandibularis sensu (Le Gros Clark, 1926), which was originally described as part of the platysma of Ptilocercus but seems rather to correspond to the sphincter colli supercialis of Tupaia and other mammals]

[it is often stated in the literature that extant primates lack a sphincter colli supercialis, but according to Jouffroy and Saban (1971), this muscle is found in lemuroids such as Propithecus; it should also be noted that Burrows et al. (2006) describe a sphincter colli in chimpanzees, which, according to these authors, is supercial to the platysma; in the human and chimpanzee cadavers dissected by me the sphincter colli supercialis does not seem to be present as an independent muscle]

Journal of Morphology

33

34

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Journal of Morphology R. DIOGO

Sphincter colli profundus [supercial portion of cervical platysma sensu (Greene, 1935); sphincter colli profundus 1 primitive sphincter colli of Figure 6 of Huber (1930a); transitus sensu (Lightoller, 1940a) (deeply blended with the sphincter colli supercialis)] Sphincter colli profundus (see text) Sphincter colli profundus [but present in other primates, as, (e.g., strepsirhines: e.g., Huber, 1931; Lightoller, 1934; Jouffroy and Saban, 1971)] Sternofacialis [deep cervical panniculus sensu, (e.g., Greene, 1935: see platysma cervicale above)]

Monotremata: Ornithorhynchus anatinus (Platypus)

blended to each other; in primates such as humans, the platysma cervicale is usually missing, i.e., the platysma sensu, e.g., Netter, (2006) corresponds to the platysma myoides of other mammals; in fact, it should be stressed that, if we accept, as it is nowadays commonly accepted by most authors, that the sphincter colli of mammals derives from the interhyoideus of other tetrapods, it makes sense to suppose that plesiomorphically the sphincter colli was a supercial muscle, as is the non-mammalian interhyoideus, not a deep muscle] [absent as an independent muscle in the platypus, although part of it might have given rise to facial muscles such as the orbicularis oris, orbicularis oculi, mentalis, and/or naso-maxillo-labialis (which very likely corresponds to the muscles that are designated by the same names in other mammals) and possibly to the sphincter bursae buccalis sensu; Huber 1930a (which, contrary to what was stated by Huber 1930a, probably corresponds to the buccinatoriusof the echidna and to the buccinatorius of other mammals); in the echidna part of the sphincter colli passes deep to other facial muscles, forming the sphincter colli profundus: (e.g., Lightoller, 1942; Jouffroy and Saban, 1971; this work)]

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) (see on the left) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Monotremata: Ornithorhynchus anatinus (Platypus)

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Cervicalis transversus [its position and the orientation of its bers are somewhat similar to those of the interscutularis of nonmonotreme mammals as, e.g., rats; Lightoller (1940a) seems to corroborate the homology of these muscles because he states that there is a cervicalis transversus in rodents; however, according to Jouffroy and Saban (1971), the interscutularis is derived from the pars intermedia of the sphincter colli profundus, while the cervicalis transversus is derived from the pars cervicalis of this latter muscle] (see above) [my dissections and comparisons support Jouffroy and Sabans (1971) hypothesis, i.e.: 1) the zygomaticus major and minor are absent in mammals such as monotremes; 2) in placentals, the zygomaticus is plesiomorphically attached to the zygomatic arch, but in some cases it extends posteriorly to attach to the ear (that is why it is sometimes named auriculolabialis); 3) in a few mammals, such as ungulates, pinnipedes, bats, rodents, treeshrews, and primates, the zygomaticus is divided into supercial (5 auriculolabialis inferior and zygomaticus major sensu; Jouffroy and Saban, 1971) and deep (5 auriculolabialis superior and zygomaticus minor sensu; Jouffroy and Saban, 1971) portions, the former originating ventrally and/or posteriorly to the latter, thus usually lying nearer the ear and being more associated with the platysma that is why some authors argue that it might derive from the Interscutularis (see above) Zygomaticus major [5part or totality of the auriculolabialis sensu (Greene, 1935) zygomatico-labialis supercialis and/or auriculolabialis inferior sensu Jouffroy and Saban, 1971] [my dissections indicate that the auriculolabialis of the Norwegian rat is deeply blended with the platysma myoides: does this means that it is really part of and/or derived from the platysma [see on the left]? Probably not, because as stated by Greene (1935) in other rodents this auriculolabialis is clearly distinct from the platysma myoides, being probably a derivative of the sphincter colli profundus; however, it is possible that some of the mammalian structures that are designated as zygomaticus major and minor and/or auriculolabialis inferior and superior in the literature are really part of and/or Zygomaticus major [in Hubers (1930a) Fig. 27 of the primate ground plan of supercial facial musculature, he suggests that the auriculabialis inferior (5zygomaticus major) derives from the platysma (see on the left), but at least in the case of colugos the former muscle is well distinguished from the latter, because these muscles are in fact perpendicular to each other; there is a signicant difference between Cynocephalus, Lemur and Tupaia: in Cynocephalus the auriculolabialis inferior (5zygomaticus major) is supercial to the platysma cervicale; in Lemur these two muscles lie in the same plane; in Tupaia the auricularis inferior is deep to the platysma cervicale: (e.g., Lightoller, 1934; this work)] Zygomaticus major [auriculolabialis inferior or zygomaticolabialis sensu (Jouffroy and Saban, 1971; Le Gros Clark, 1926; Lightoller, 1934)] (see on the left)

Zygomaticus major [Gassers (1967) developmental study suggests that the zygomaticus major and zygomaticus minor of humans derive from his infraorbital lamina, and not from his mandibular lamina, i.e., they seem to be ontogenetically more related with the facial muscles of the orbit region than with those of the mouth region; interestingly, in earlier stages of human development these two muscles are more separated from each other than in later stages, i.e., in this respect the conguration seen in the early stages is more similar to that seen in adult mammals such as colugos, tree-shrews and lemurs]

Journal of Morphology

35

36

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) derive from the platysma, i.e., that they are not really homologous to the zygomaticus major and minor sensu this work: (e.g., Boas and Paulli, 1908; Huber, 1930a; Edgeworth, 1935; Jouffroy and Saban, 1971) it cannot also be discarded that at least in some cases the zygomaticus major and/or auriculolabialis inferior derive from the platysma, while the zygomaticus minor and/or auriculolabialis superior derive from, e.g., the orbicularis oculi] Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Journal of Morphology R. DIOGO

Zygomaticus minor Zygomaticus minor [auriculolabialis superior sensu (Le Gros Clark, 1926; Lightoller, 1934)] Frontalis Zygomaticus minor Zygomaticus minor [zygomaticus sensu (Greene, 1935); zygomatico-labialis profundus and or auriculolabialis superior sensu (Jouffroy and Saban, 1971)] Orbito-temporo-auricularis [the frontalis sensu (Greene 1935) corresponds to the orbito-temporo-auricularis sensu (Edgeworth, 1935)] Frontalis (my dissections and comparisons indicate that the frontalis and auriculoorbitalis of colugos and Tupaia and the frontalis, temporoparietalis and auricularis anterior of humans, correspond to the orbito-temporo-auricularis of mammals such as rats) Frontalis

Monotremata: Ornithorhynchus anatinus (Platypus)

platysma, although its innervation seems to indicate the contrary; Jouffroy and Saban (1971) explicitly state that these supercial and deep portions correspond very likely to the zygomaticus major and minor of humans, respectively; 4) according to them, in mammals as, e.g., treeshrews and lemurs the zygomatic muscles, and particularly the zygomaticus major, often extend posteriorly in order to attach to the ear, but this trend is reverted in higher primates: e.g., usually in humans both the zygomaticus major and zygomaticus minor originate relatively far from the ear, although in a few /abnormal cases at least one of these muscles might originate on the ear region]

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Auriculo-orbitalis [auriculo-orbitalis or orbito-auricularis sensu (Lightoller, 1934); it might correspond to Tupaias attrahens aurem sensu (Le Gros Clark, 1924), and/or to the Ptilocercus scutularis 1 portio transiens sensu (Le Gros Clark, 1926)] Auriculo-orbitalis (see above; this muscle usually runs from the auricular region to the orbital region, being inferior and/or deep to the frontalis) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Monotremata: Ornithorhynchus anatinus (Platypus)

Temporoparietalis [according to Jouffroy and Saban (1971), this muscle is related to, but different from, the auricularis superior; they state that it corresponds to the temporal part of the frontalis, which is also named epicranio-temporal or orbito-temporalis, and which has a longitudinal orientation and covers the temporal aponeurosis, being often fused in primates with the auriculares anterior and superior and also to part of the galea aponeurotica] Auricularis anterior

[contrary to Ptilocercus, Tupaia seems to only have an auriculo-orbitalis sensu (Lightoller, 1934) i.e., it does not have a separate temporoparietalis and a separate auricularis anterior: see above] Auricularis superior

Auricularis superior

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Orbicularis oculi

Orbicularis oculi

Auricularis superior [auricularis anterior superior of g. 409 of Jouffroy and Saban (1971)] Orbicularis oculi Zygomatico-orbicularis (see text)

Orbicularis oculi Zygomaticoorbicularis (see text)

Journal of Morphology

Corrugator supercilii (see above)

Corrugator supercilii [superciliaris sensu (Jouffroy and Saban, 1971)]

Orbicularis oculi (absent in modern humans but may well be present in primates as, e.g., lemurs: see on the left) Depressor supercilii (the depressor supercillii and corrugator supercilii are probably derived from the orbicularis oris: Appendix IV) Corrugator supercilii

37

38

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Naso-labialis [levator labii superioris sensu (Parsons, 1898; Greene, 1935); pars jugularis of supercial maxillo-naso-labialis sensu (Lightoller, 1940b)] Naso-labialis Naso-labialis [levator labii superioris sensu (Le Gros Clark, 1924)] [not described by Le Gros Clark (1926), but his Fig. 49 suggests that it may also be present in Ptilocercus] Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Levator labii superioris [the levator labii superioris and levator labii superioris alaeque nasi corresponds very likely to the nasolabialis of the other therian mammals listed on the left: Appendix IV; Gassers (1967) developmental study suggests that at least in humans these two muscles appear ontogenetically in the orbital region]

Journal of Morphology R. DIOGO

Levator labii superioris alaeque nasi (see above) Procerus Procerus [nasolabialis supercialis sensu (Ryan, 1989)] [not described by Greene (1935), but seems to be present in the rats dissected by me; see also, e.g., Ryan (1989)] Buccinatorius [not described by Greene (1935), but is clearly present in the rats dissected by me, being in fact subdivided into various sections; (see also, e.g., Ryan, 1989)] Buccinatorius Buccinatorius [not described by Le Gros Clark (1924), but it is clearly present in the Tupaia specimens dissected by me; it is also present in Ptilocercus (see e.g., Le Gros Clark, 1926)] Buccinatorius

Monotremata: Ornithorhynchus anatinus (Platypus)

Naso-labialis [Lightoller (1942) and Saban (1971) state that deep to the cranial (anterior) portion of the orbicularis oculi of the echidna lies a small naso-labialis; according to Lightoller (1942), in the platypus there is a somewhat similar structure, but it is not as differentiated from the other facial musculature as in the echidna; in the platypus specimens dissected by me the naso-labialis does seem to be an independent muscle, being in fact very similar to the naso-labialis of the echidna, see, e.g., g. 4 of Lightoller (1942), which strongly suggests that the naso-labialis derives from a part of the sphincter colli supercialis (transitus sensu Lightoller); see also, e.g., Huber, 1930a; Jouffroy and Saban, 1971]

Buccinatorius [the buccinatorius sensu Lightoller (1942) corresponds to the sphincter bursae buccalis sensu, e.g., Huber (1930a)] [according to Huber (1930a), there is no buccinatorius in the platypus, and the buccinatorius of echidna may well not be homologous with that of other mammals; however, as noted in later works as, e.g., Lightoller (1942) and Jouffroy and Saban (1971), the sphincter bursae buccalis of platypus might actually correspond to the buccinatorius of echidna and/or to the buccinatorius of other mammals]

APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Monotremata: Ornithorhynchus anatinus (Platypus)

Maxillo-naso-labialis

Dilatator nasi [dilatator naris sensu (Greene, 1935; Peterka, 1936)] [I prefer to use the name dilatator nasi because the term dilatator naris is often used to designate the pars alaris of the nasalis: (see, e.g., Jouffroy and Saban, 1971)] Maxillo-naso-labialis [probably includes the maxillo-labialis and nasolabiais profundus sensu (Jouffroy and Saban, 1971; Ryan, 1989)] [not described by Greene (1935), but it is clearly present in the rats dissected by me; (see also, e.g., Ryan, 1989)]

Nasalis [the nasalis and depressor septi nasi of humans probably correspond to the maxillo-naso-labialis of, e.g., rats, colugos, and tree-shrews (e.g., Jouffroy and Saban, 1971; this work)]

Levator anguli oris facialis [levator anguli oris or caninus sensu (Lightoller, 1934); bucco-naso-labialis sensu (Ryan, 1986); buccinatorius sensu (Greene, 1935; Bryant, 1945); pars profunda of maxillo-nasolabialis sensu (Lightoller, 1940b)] [I use the name levator anguli facialis in order to distinguish this muscle from the levator anguli oris mandibularis of some non-mammalian tetrapods, which is a mandibular, and not a hyoid, muscle: (Diogo, 2007, 2008)]

Levator anguli oris facialis

Maxillo-naso-labialis [maxillo-nasalis sensu (Jouffroy and Saban, 1971); it might correspond to the dilator naris, zygomatici and/or erector vibrissae sensu (Le Gros Clark, 1924), and thus might be included in the orbicularis oculi (sensu Le Gros Clark, 1926) of Ptilocercus] Levator anguli oris facialis [levator anguli oris sensu (Le Gros Clark, 1926); incisivus superior 1 caninus sensu (Lightoller, 1934)] [as noted by Lightoller (1934), it is deeply mixed with the orbicularis oris]

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Depressor septi nasi (see above) Levator anguli oris facialis [Gassers (1967) study of human development suggests that the levator anguli oris facialis, orbicularis oris, depressor labii inferioris, depressor anguli oris, and mentalis have a common ontogenetic origin, being derived from his mandibular lamina; (see also, e.g., Sullivan and Osgood, 1927; Jouffroy and Saban, 1971)]

Journal of Morphology

39

40

Journal of Morphology
APPENDIX 3. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Orbicularis oris Mentalis Mentalis [labiorum profundi inferioris sensu (Lightoller, 1934)] Orbicularis oris Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Orbicularis oris Orbicularis oris (see maxillo-naso-labialis above)

Monotremata: Ornithorhynchus anatinus (Platypus)

Orbicularis oris [plicae anguli oris sensu (Huber, 1930a)]

R. DIOGO

Mentalis [present in the platypus, but not in echidna, according to, e.g., Lightoller (1942) and Saban (1971)]

Depressor labii inferioris (see levator anguli oris facialis above) Depressor anguli oris (see levator anguli oris facialis above) Mentalis (see levator anguli oris facialis above)

Appendix 4. Scheme illustrating the authors hypotheses regarding the homologies of the hyoid muscles of the adult colugos dissected and of adult representative members of other mammalian taxa (see caption of Appendix 1)

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Journal of Morphology

The arrows indicate the hypotheses that are most strongly supported by the evidence available; the dotted arrows indicate alternative hypotheses that are supported by some data, but that overall are not as strongly supported by the evidence available as are the hypotheses indicated by solid arrows (e,g., the overall analysis of the data available indicates that the risorius of humans corresponds to part of the platysma myoides of other mammals, but the possibility that the former muscle derives from the zygomaticus major cannot be completely discarded: see text, Appendix 3 and gs. 14; colli. prof., sphincter colli profundus; ex., extrinsic; FACIAL, NONFACIAL, facial and nonfacial muscles; le., levator; mus., muscles; prof., profundus; supe., supercials; tra, transversus).

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APPENDIX 5. Branchial, pharyngeal, and laryngeal muscles of the adult colugos dissected and of adult representative members of other mammalian taxa (see caption of Appendix 1; see also text, Appendix 6 and Figs. 14) Rodentia: Rattus norvegicus (Norwegian rat) Stylopharyngeus Stylopharyngeus Stylopharyngeus Stylopharyngeus Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Journal of Morphology
Ceratohyoideus [the ceratohyoideus sensu (House, 1953) corresponds to the branchiohyoideus sensu (Sprague, 1943), and to the hyoideus latus, brevis and intercornualis sensu (Saban, 1968) (see text)] Ceratohyoideus (see text) Acromiotrapezius (see text) Trapezius [in both Tupaia and Ptilocercus, it is a single, continuous muscle, which probably corresponds to the acromiotrapezius 1 spinotrapezius of other mammals: (e.g., Le Gros Clark, 1924, 1926; George, 1977; this work)] Acromiotrapezius (dorsoscapularis superior, anterior trapezius or trapezius superior sensu; Greene, 1935) (it is somewhat mixed with the spinotrapezius, but is considered to be an independent muscle by many authors: see, e.g., Greene, 1935) Ceratohyoideus [interhyoideus sensu (Le Gros Clark, 1926) (see text)] [absent as an independent muscle in modern humans, but present in other primates (e.g., Sprague, 1944b; Saban, 1968)]

Monotremata: Ornithorhynchus anatinus (Platypus)

Stylopharyngeus [the overall analysis of the data now available on innervation, development, topology and comparative anatomy seems to point out that the mammalian stylopharyngeus is probably not a de novo pharyngeal muscle sensu Edgeworth, but instead a derivative of the branchial musculature sensu stricto: (Smith, 1992; Noden and Francis-West, 2006; Diogo et al., in press; this work)] Ceratohyoideus (see text)

R. DIOGO

Subarcualis rectus III (see text) Acromiotrapezius (anterior trapezius sensu; Saban, 1971) (the anterior and posterior trapezius sensu; Saban, 1971, are well separate in platypus and probably correspond to the acromiotrapezius and spinotrapezius of other mammals)

Spinotrapezius (posterior trapezius sensu Saban, 1971: see above) Spinotrapezius (Dorsoscapularis, inferior posterior trapezius, or trapezius inferior superior sensu Greene, 1935) (see above)

Spinotrapezius (see text)

(see above)

Trapezius [it usually has three parts,. the acromiotrapezius, claviculotrapezius and spinotrapezius sensu, e.g., (Kardong, 2002), which are not differentiated into separate muscles, as is the case in various other mammals; the human claviculotrapezius probably corresponds to part of the trapezius of, e.g., Tupaia, although it may correspond to the cleido-occipitalis of this latter taxon: (e.g., Jouffroy, 1971; Appendix 6)] (see above)

APPENDIX 5. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Monotremata: Ornithorhynchus anatinus (Platypus)

Dorso-cutaneous [present in monotremes as well as in some other mammals; probably derives from part of the trapezius: (e.g., Jouffroy, 1971; Jouffroy and Lessertisseur, 1971)] [according to Edgeworth (1935), the cleido-occipitalis of mammals as, e.g., Tatusia probably corresponds to part of the reptilian trapezius, but the cleido-occipitalis of, e.g., the placental carnivores may well correspond to the part of the reptilian sternocleidomastoideus] Cleido-occipitalis [the cleidooccipitalis sensu; Wood (1870) and Edgeworth (1935) corresponds to the clavotrapezius and cleidooccipitalis cervicalis sensu (Greene, 1935)] [the position and orientation of the bers of the cleido-occipitalis of, e.g., Rattus and Tupaia are more similar to those of the monotreme sternocleidomastoideus than to those of the monotreme trapezius; also, according to Greene (1935), in, e.g., rats the cleido-occipitalis, sternomastoideus, and cleidomastoideus are all innervated by the spinal accessory and third and fourth cervical nerves through the subtrapezial plexus, while the spinotrapezius and acromiotrapezius are innervated by the spinal accessory and second and third cervical nerves through the subtrapezial plexus] Cleidomastoideus Cleido-occipitalis (see on the left) Cleidomastoideus (see text) Cleidomastoideus

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

[but may be present as an independent muscle in a few humans, as well as in various non-human primates: (e.g., Wood, 1870; Hill, 1953; Jouffroy, 1962)] Sternocleidomastoideus (including sternal and clavicular heads, which correspond very likely to the sternomastoideus and cleidomastoideus of other mammals)

Cleidomastoideus [as suggested by Howell (1937a,b) and Saban (1971) in the platypus specimens dissected by me both the sternomastoideus and cleidomastoideus are present as independent muscles] Sternomastoideus Sternomastoideus

Journal of Morphology

Sternomastoideus (see text)

Sternomastoideus

[but present in various nonhuman primates: (e.g., Hill, 1953; Jouffroy, 1962)]

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APPENDIX 5. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Constrictor pharynges medius [Ceratopharyngeus and/or hyopharyngeus sensu (e.g., House, 1953)] Constrictor pharynges medius Constrictor pharynges medius Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Constrictor pharyngismedius (including a pars ceratopharyngea and a pars chondropharyngea) Constrictor pharyngis inferior (see on the left)

Journal of Morphology
Constrictor pharyngis inferior (see on the left) Constrictor pharyngis inferior (see on the left)

Monotremata: Ornithorhynchus anatinus (Platypus)

Constrictor pharyngis (there is only one constrictor of the pharynx in monotremes, but the cricothyroideus and the palatopharyngeus are already differentiated in these mammals)

R. DIOGO

Cricothyroideus [in the platypus specimens dissected by me the cricothyroideus is probably not divided into a pars obliquua and a pars recta; it should be noted that in terms of both its ontogeny and phylogeny the mammalian cricothyroideus is clearly a pharyngeal muscle, and not a laryngeal muscle as it is sometimes suggested in the literature: (e.g., Edgeworth, 1935; Negus, 1949; DuBrul, 1958; Starck and Schneider, 1960; Saban, 1968)]

Constrictor pharyngis inferior [as described by Saban (1968), the constrictor pharyngis inferior of therian mammals is often divided into a pars thryropharyngea attaching on the thyroid cartilage, a pars cricopharyngea attaching on the cricoid cartilage, and a pars intermedia lying between these two myological structures; the pars intermedia is often reduced in mammals as, e.g., primates and is often absent in mammals as, e.g., rodents] Cricothyroideus (including a pars obliquua and a pars profunda: see on the right) Cricothyroideus (including a pars obliquua and a pars recta, which are more separated from each other than in Rattus and Tupaia but are not as separated as in humans) Cricothyroideus (including a pars obliquua and a pars recta)

Cricothyroideus (including a pars obliquua and a pars recta: see on the left)

APPENDIX 5. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Constrictor pharynges superior [glossopharyngeus sensu (House, 1953)] (the constrictor pharyngis superior of rats probably includes only a pars glossopharyngea: see on the left) Constrictor pharynges superior (my dissections indicate that it includes a pars glossopharyngea and possibly a pars buccopharyngea: see text) Constrictor pharynges superior [probably including a pars buccopharyngea, a pars pterygopharyngea (corresponding to the pterygopharyngeus of, e.g., rats and colugos? see on the left), and possibly a pars glossopharyngea: e.g., Sprague, 1944a; this work] Constrictor pharynges superior [including a pars buccopharyngea, a pars pterygopharyngea (corresponding to the pterygopharyngeus of, e.g., rats and colugos? see on the left), a pars mylopharyngea, and a pars glossopharyngea] Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Monotremata: Ornithorhynchus anatinus (Platypus)

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

[according to Edgeworth (1935), the constrictor pharyngis superior is missing in monotremes and was very likely poorly developed in the rst placentals, being probably similar to the glossopharyngeus of, e.g., rats (see on the right); according to him the constrictor pharyngis superior only became a broad muscle as that found in, e.g., humans later in evolution; House, (1953) and Smith (1992) suggest that the pterygopharyngeus of, e.g., rats probably corresponds to part of the constrictor pharyngis superior of humans; in my opinion it is effectively more plausible to assume that the pterygopharyngeus became part of the human constrictor pharyngis superior than to assume that a muscle such as the glossopharyngeus of rats migrated dorsally in order to attach to the hard palate; however, until more data is available, the hypothesis that the pterygopharyngeus of, e.g., rats and colugos might be simply missing or deeply mixed with the palatopharyngeus in mammals such as Tupaia and Homo cannot be discarded: Appendix 6] Pterygopharyngeus (see above) Pterygopharyngeus (see above)

Journal of Morphology
Palatopharyngeus (see on the left)

Palatopharyngeus (in the rats, colugos, and tree-shrews dissected by me it is more blended with the salpingopharyngeus than in humans)

Palatopharyngeus (see on the left)

Palatopharyngeus (see on the left)

[see above; present as an independent element in various nonhuman primates: (e.g., Edgeworth, 1935; Saban, 1968)] Palatopharyngeus (see on the left)

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APPENDIX 5. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Journal of Morphology
Levator veli palatini Levator veli palatini Musculus uvulae [according to Edgeworth, (1935), this muscle is only found in a few mammals such as phylogenetically derived primates, corresponding to part of the palatopharyngeus of other mammals] Levator veli palatini Levator veli palatini [corresponds to part of the palatopharyngeus of monotremes: (e.g., Edgeworth, 1935; Saban, 1968; this work)] Salpingopharyngeus [corresponds to part of the palatopharyngeus of monotremes: (e.g., Edgeworth, 1935; Saban, 1968; this work)] Thyroarytenoideus (mainly divided into supercial and deep bundles) Salpingopharyngeus Salpingopharyngeus Thyroarytenoideus [divided into a posterior, medial section and an anterior, lateral section, which probably correspond respectively to the pars intermedia and pars superioris of g. 69 of Starck and Schneider (1960); the anterior section is subdivided into medial and lateral bundles, the latter being fused with the cricoarytenoideus posterior and thus probably corresponding to the ceratoarytenoideus lateralis sensu, (e.g., Harrison, 1995)] Salpingopharyngeus

Monotremata: Ornithorhynchus anatinus (Platypus)

R. DIOGO

Thyrocricoarytenoideus [the thyrocricoarytenoideus sensu; Saban (1968) corresponds to the thyroarytenoideus sensu (Edgeworth, 1935); it has two bundles, which probably correspond to the thyroarytenoideus and cricoarytenoideus lateralis of other mammals: that is why I prefer to use the name thyrocricoarytenoideus for the monotreme muscle]

Thyroarytenoideus (mainly divided into supercial and deep bundles)

Thyroarytenoideus [often including, e.g., a pars thyroepiglottica, a pars aryepiglottica, a pars superioris, a pars ventricularis, and/or a ceratoarytenoideus lateralis sensu (Saban, 1968, and Harrison, 1995)]

APPENDIX 5. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Monotremata: Ornithorhynchus anatinus (Platypus)

Cricoarytenoideus lateralis

Cricoarytenoideus lateralis

Vocalis [thyroarytenoideus inferior sensu (e.g., Saban, 1968)] [according to, e.g., Edgeworth (1935), the vocalis is only found in a few taxa as, e.g., some phylogenetically derived primates, and corresponds to the medial portion of the thyroarytenoideus of other mammals] Cricoarytenoideus lateralis

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Arytenoideus (interarytenoideus sensu, e.g., Saban, 1971, which is divided into crico-proarytenoideus and ary-proarytenoideus) Arytenoideus Arytenoideus

Cricoarytenoideus lateralis (Cricoarytenoideus ventralis sensu, e.g., Whidden, 2000) (see thyrocricoarytenoideus above) Arytenoideus (Interarytenoideus sensu, e.g., Edgeworth, 1935)

Arytenoideus transversus

Journal of Morphology
Cricoarytenoideus posterior (Cricoarytenoideus dorsalis sensu, e.g., Whidden, 2000)

Cricoarytenoideus posterior [cerato-crico-arytenoideus sensu (Saban, 1971)]

Cricoarytenoideus posterior

Cricoarytenoideus posterior

Arytenoideus obliquus (it is commonly accepted that the arytenoideus transversus and arytenoideus obliquus derive from the arytenoideus of other mammals; however, as the pars aryepiglottica is probably derived from the thyroarytenoideus, it cannot be discarded that the arytenoideus obliquus also derives from this latter muscle, and not from the arytenoideus: e.g., Saban, 1968; Appendix 6) Cricoarytenoideus posterior [including the ceratocricoideus sensu (Harrison, 1995), which, according to this author, is found in about 63% of modern humans]

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Journal of Morphology R. DIOGO

Appendix 6. Scheme illustrating the authors hypotheses regarding the homologies of the branchial pharyngeal and laryngeal muscles of the adult colugos dissected and of adult representative members of other mammalian taxa (see caption of Appendix 4); see also text, Appendix 5 and gs. 14 ;co., constrictor; mus., muscles; post., posterior)

APPENDIX 7. Hypobranchial muscles of the adult colugos dissected and of adult representative members of other mammalian taxa (see caption of Appendix 1 and also text, Appendix 8 and Figs. 14) Rodentia: Rattus norvegicus (Norwegian rat) Geniohyoideus Geniohyoideus Geniohyoideus Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human) Geniohyoideus

Monotremata: Ornithorhynchus anatinus (Platypus)

Geniohyoideus [according to Edgeworth (1935), the geniohyoideus, genioglossus, and hyoglossus of mammals develop ontogenetically at the same time; also according to him, the two former muscles develop internally, whereas the latter develops externally] Genioglossus [as explained by, e.g., Piekarski and Olsson (2007), in mammals as, e.g., dogs the tongue muscles might be innervated by both the hypoglossal [CNXII] and the facial [VII] nerves, thus indicating that at least in some cases these muscles may have a dual origin] Genioglossus [Geniohyoglossus sensu (Le Gros Clark, 1924; 1926)] Genioglossus [not described Genioglossus by Greene (1935), but it is present as an independent structure in the rats dissected by me; authors such as Bryant (1945) state that this muscle is effectively often present in rodents] Intrinsic muscles of the Intrinsic muscles tongue (see on the left) of the tongue (see on the left) Intrinsic muscles of the tongue (see on the left)

Genioglossus

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

Intrinsic muscles of the tongue (see on the left)

Intrinsic muscles of the tongue (according to Saban (1968), the intrinsic muscles of the tongue of amniotes derive from both the genioglossus and hyoglossus: Appendix 8; examples of these muscles are the longitudinalis superior, longitudinalis inferior, transversus linguae, and/or verticalis linguae: (e.g., Anderson, 1881; Edgeworth, 1935; Jarvik, 1963, 1980; Saban, 1968, 1971; Smith, 1992; Sokoloff, 2000)] Hyoglossus Hyoglossus Hyoglossus [as described by, e.g., Edgeworth (1935), in colugos the hyoglossus and thyrohyoideus are very likely fused to each other: see text] Styloglossus

Hyoglossus (see on the left)

Styloglossus [my dissections and comparisons support Edgeworths (1935) suggestion that the styloglossus and palatoglossus of therian mammals likely correspond to part of the hyoglossus of monotremes]

Hyoglossus [hyoglossus 1 chondroglossus sensu (Le Gros Clark, 1926)] [according to Saban (1968), in primates and tree-shrews the hyoglossus is divided into a chondroglossus and a ceratoglossus; this is supported by, e.g., Le Gros Clark (1926) and Sprague (1944a), although this latter author erroneously states that the chondroglossus is part of the genioglossus and not of the hyoglossus] Styloglossus

Styloglossus

Journal of Morphology

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APPENDIX 7. (Continued) Rodentia: Rattus norvegicus (Norwegian rat) Dermoptera: Cynocephalus volans (Philippine colugo) Scandentia: Tupaia sp. (Tree-shrew) Primates: Homo sapiens (Modern human)

Journal of Morphology
[probably not present as a separate muscle Palatoglossus in the Tupaia specimens dissected by me; it is also not described in this and other treeshrew taxa by authors such as Le Gros Clark (1924, 1926)] Sternohyoideus (blended with the Sternohyoideus sternothyroideus)

Monotremata: Ornithorhynchus anatinus (Platypus)

R. DIOGO
Omohyoideus [George (1977) states that this Omohyoideus muscle has no distinct tendinous intersection, (it has superior but Le Gros Clark (1924, 1926) and Sprague and inferior (1944a) describe such an intersection in treebellies, which shrews as, e.g., Tupaia and Ptilocercus] are separated by a distinct tendon) Sternothyroideus Thyrohyoideus Thyrohyoideus

[probably not present as an Palatoglossus (see independent muscle in the text) rats dissected; this is supported by authors such as (Barrow and Capecchi, 1999)] Sternohyoideus [in the platypus specimens Sternohyoideus Sternohyoideus [as examined by me this muscle is blended described by Leche posteriorly with the sternothryroideus, as (1886) and Saban stated by Saban (1971)] (1968) in Cynocephalus the sternohyoideus is divided into an anterior bundle and a posterior bundle: see text] Omohyoideus [as stated by, e.g., Saban (1971), Omohyoideus [not present as an in the platypus specimens dissected by me independent muscle the omohyoideus is anteriorly divided into in the colugos supercial and deep bundles] dissected by me as well as by authors such as Gunnell and Simmons (2005)] Sternothyroideus (see above) Sternothyroideus Sternothyroideus Sternothyroideus Thyrohyoideus [as explained (not present as an above, the thyrohyoideus of independent therian mammals clearly structure in the corresponds to part of the colugos dissected; it sternohyoideus of nonis probably fused to mammalian tetrapods; the hyoglossus: see however, it is not clear if it text) corresponds to part of the monotreme sternohyoideus or, instead, to part of the monotreme sternothyroideus: (e.g., Edgeworth, 1935; Saban, 1968; Appendix 8)]

Appendix 8. Scheme illustrating the authors hypotheses regarding the homologies of the hyppobranchial muscles of the adult colugos dissected and of adult representative members of other mammalian taxa

HEAD AND NECK MUSCLES OF CYNOCEPHALUS VOLANS

(See caption of Appendix 4; see also text, Appendix 7, and gs.14; GENIOHYOIDEUS, RECTUS CERVICIS 5 geniohyoideus and rectus cervicis groups sensu Edgeworth, 1935; in.to., intrinsic muscles of the tongue; mus., muscles).

Journal of Morphology

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