On the origin, homologies and evolution of primate facial muscles, with a particular focus on hominoids and a suggested unifying nomenclature for the facial muscles of the Mammalia

Abstract

The mammalian facial muscles are a subgroup of hyoid muscles (i.e. muscles innervated by cranial nerve VII). They are usually attached to freely movable skin and are responsible for facial expressions. In this study we provide an account of the origin, homologies and evolution of the primate facial muscles, based on dissections of various primate and non-primate taxa and a review of the literature. We provide data not previously reported, including photographs showing in detail the facial muscles of primates such as gibbons and orangutans. We show that the facial muscles usually present in strepsirhines are basically the same muscles that are present in non-primate mammals such as tree-shrews. The exceptions are that strepsirhines often have a muscle that is usually not differentiated in tree-shrews, the depressor supercilii, and lack two muscles that are usually differentiated in these mammals, the zygomatico-orbicularis and sphincter colli superficialis. Monkeys such as macaques usually lack two muscles that are often present in strepsirhines, the sphincter colli profundus and mandibulo-auricularis, but have some muscles that are usually absent as distinct structures in non-anthropoid primates, e.g. the levator labii superioris alaeque nasi, levator labii superioris, nasalis, depressor septi nasi, depressor anguli oris and depressor labii inferioris. In turn, macaques typically lack a risorius, auricularis anterior and temporoparietalis, which are found in hominoids such as humans, but have muscles that are usually not differentiated in members of some hominoid taxa, e.g. the platysma cervicale (usually not differentiated in orangutans, panins and humans) and auricularis posterior (usually not differentiated in orangutans). Based on our observations, comparisons and review of the literature, we propose a unifying, coherent nomenclature for the facial muscles of the Mammalia as a whole and provide a list of more than 300 synonyms that have been used in the literature to designate the facial muscles of primates and other mammals. A main advantage of this nomenclature is that it combines, and thus creates a bridge between, those names used by human anatomists and the names often employed in the literature dealing with non-human primates and non-primate mammals.

Introduction

In a recent work Diogo et al. (2008) reported the results of their long-term study of the comparative anatomy, homologies and evolution of the head and neck muscles of sarcopterygians (the group comprising tetrapods and bony fish such as coelacanths and dipnoans). The study was mainly based on dissections of numerous non-primate sarcopterygians and a few primates, and on a review of the literature. Its goal was to present the homologies and evolution of the mandibular, hyoid, branchial and hypobranchial muscles of the Sarcopterygii as a whole, thus providing a background for more detailed morphological and taxon-based analyses. Of the nine sarcopterygian taxa featured in the tables of that study, only one, Homo sapiens, was a primate. In the present work we focus on the origin, evolution and homologies of the facial muscles of primates, particularly hominoids.

The facial muscles are a subgroup of the hyoid muscles sensuEdgeworth (1935) (i.e. muscles innervated by cranial nerve VII) (for a recent review, see Diogo et al. 2008). Except for the buccinatorius and mandibulo-auricularis muscles, they are attached to the dermis of the skin and the elastic cartilage of the pinna. They are involved in generating facial expressions during social interactions among conspecifics, as well as in feeding, chemosensation, whisker motility, hearing, vocalization and in human speech (e.g. Burrows, 2008). Unlike most skeletal muscles of vertebrates, the facial muscles usually do not attach via tendons but typically attach via a subcutaneous musculoaponeurotic sheath (e.g. Larrabee & Makielski, 1993). Many anatomical works have provided information about the facial muscles of primates, particularly in the 19th century and the first three quarters of the 20th century (e.g. Owen, 1830–1831; Duvernoy, 1855–1856; Wilder, 1862; Gratiolet & Alix, 1866; Broca, 1869; Bischoff, 1870, 1880; MacAlister, 1871; Champneys, 1872; Murie & Mivart, 1872; Sirena, 1876; Sutton, 1883; Chudzinski, 1885; Deniker, 1885; Ruge, 1885, 1887a,b, 1890, 1897, 1910, 1911; Le Double, 1897; Sperino, 1897; Zuckerlkandl, 1900; Sommer, 1907; Polak, 1908; Virchow, 1915; Sonntag, 1923, 1924a,b; Lightoller, 1925, 1928a,b, 1934, 1939, 1940a,b, 1942; Sullivan & Osgood, 1925; Woollard, 1925; Schreiber, 1928; Huber, 1930a,b, 1931, 1933; Loth, 1931; Edgeworth, 1935; Miller, 1952; Hill, 1953, 1955, 1957, 1959, 1960a,b, 1970, 1974; Shibata, 1959; Gasser, 1967; Schön, 1968; Seiler, 1970, 1971a,b,c,d,e, 1973, 1974a,b, 1975, 1977, 1979a,b, 1980; Jouffroy & Saban, 1971; Swindler & Wood, 1973; Pellatt, 1979a,b; Peng et al. 1982). In recent years, there has been a renewed interest in the comparative anatomy of the primate facial muscles. Burrows and colleagues have been re-examining the presence/absence, configuration and function of the facial muscles of various primates, using a new ‘face mask’ technique in which the superficial facial musculature, skin and fascia are carefully removed from the skull (e.g. Burrows & Smith, 2003; Burrows et al. 2006, in review; Burrows, 2008; Waller et al. 2008a,b; Rogers et al. 2009). They claim that, by using this methodology instead of the more traditional method of removing the skin and attempting to leave behind all of the musculature with the skull, a greater number of facial muscles is preserved. For instance, their results suggest that the muscles of facial expression in the common chimpanzee, Pan troglodytes, are more similar to the arrangement seen in Homo sapiens than previously reported (Burrows et al. 2006). These results were supported by the recent comparative studies of Diogo and colleagues, who used both the traditional dissection method and the new ‘face mask’ technique to reanalyse the facial muscles of primates and compare them with those of other mammals in order to investigate the identity and homologies of the primate muscles in a broader phylogenetic context (e.g. Diogo & Wood, 2008; Diogo et al. 2008; Diogo, 2009).

The present account of the origin, homologies and evolution of the primate facial muscles is based on the results of our own recent dissections of various primates combined with an exhaustive literature review. It includes a significant amount of new data, e.g. the results of our observations of the facial muscles of specimens of Hylobates and Pongo. To our knowledge, this is the first publication providing photographs that show in detail the facial muscles of primates such as hylobatids and orangutans. As we have now dissected specimens of each of the five main extant hominoid groups (Hylobatidae, Ponginae, Gorillini, Panini and Hominini; see Fig. 1), a significant part of this study and of Table 1 will be focused on the hominoids. The results of our observations and comparisons are summarized in Table 1, which presents the best supported hypotheses of homology for the facial muscles discussed in the present work. As stressed by Diogo (2007, 2008, 2009), one of the major problems that researchers face when they compare the muscles of modern humans with those of other primates and with non-primate mammals is the use of different names by different authors to designate the same muscle in the members of different clades, and even of the same clade. In order to reconcile these different nomenclatures we propose a unifying nomenclature for the facial muscles of the Mammalia as a whole that takes into account the data compiled in Table 1 and discussed in the text.

Fig. 1.

Phylogenetic framework for the discussion provided in the present study and the comparison between the head and neck muscles of the genera listed in Table 1 and shown in Figs 2–9, based on Pough et al. (1996), Shoshani et al. (1996), Kardong (2002), Sargis (2002a, b, 2004), Dawkins (2004), Gunnell & Simons (2005), Kemp (2005), Marivaux et al. (2006), Janeka et al. (2007) and Silcox et al. (2007). The Primates, Dermoptera (including colugos or ‘flying lemurs’) and Scadentia (including tree-shrews) are placed in an unresolved trichotomy because the relationships between these three groups remain mainly unresolved (some authors continue to group colugos with tree-shrews, others group tree-shrews with primates and yet others group colugos with primates; see, e.g. Sargis, 2002a, b, 2004; Dawkins, 2004; Marivaux et al. 2006; Janeka et al. 2007; Silcox et al. 2007); the names of the primate subgroups are those used by Shoshani et al. (1996) [modified from Diogo et al. (2008); for more details see this latter work].

Table 1.

Scheme illustrating the authors’ hypotheses regarding the homologies of the facial muscles of adults of representative non-primate and primate mammalian taxa

Fig. 7.

Hylobates lar (Primates): anterolateral view of the facial muscles of an adult specimen (HU-ANA, H01) dissected in the course of this investigation [anterior is to the right; the scale bar shown on the right, at the bottom, corresponds to 1 cm]. BUC, buccinatorius; DES, depressor supercilii; DSN, depressor septi nasi; LAO, levator anguli oris facialis; LELS, levator labii superioris; LELSA, levator labii superioris alaeque nasi; MEN, mentalis; NAS, nasalis; OROC, orbicularis occuli; OROR, orbicularis oris.

Materials and methods

The phylogenetic framework used in the present study, and specifically in the comparisons between the facial musculature of the genera set out in Table 1 and shown in Figs 2–9, is shown in Fig. 1. We dissected the facial muscles of various non-primate and primate mammals and were careful to include in Table 1: (1) a member of the most basal extant mammalian clade, the monotremes (Ornithorhynchus anatinus, or ‘platypus’); (2) a member of the rodents, the Norwegian rat (Rattus norvegicus), because rodents and lagomorphs are included in the clade Glires, which is considered to be the sister-group of the clade Euarchonta (Fig. 1); (3) a member of the tree-shrews (Tupaia sp.), i.e. one of the two groups that are now considered to be the closest living relatives of primates (the other group being the colugos, or ‘flying lemurs’; see Fig. 1); (4) a non-anthropoid primate taxon, the strepsirhine Lepilemur ruficaudatus; (5) a monkey, the cercopithecoid Macaca mulatta; and (6–10) members of each of the five major extant hominoid groups, i.e. Hylobates lar(Hylobatidae), Pongo pygmaeus(Ponginae), Gorilla gorilla(Gorillini), Pan troglodytes (Panini) and Homo sapiens(Hominini). The dissected specimens are from the Colección Mamíferos Lillo of the Universidad Nacional de Tucumán (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), the Smithsonian Institution's National Museum of Natural History (USNM), the Cleveland Metroparks Zoo (CMZ), the Yerkes National Primate Research Center (YNPRC), and the Duke Lemur Center (DLC). The list of specimens examined is given in Appendix 1; the number of specimens dissected is followed by an abbreviation that refers to the state of the specimen (alc, alcohol fixed; fre, fresh; for, formalin embalmed). In our dissections, other than their color, there were no notable differences regarding the attachments, overall configuration and general appearance of the muscles of fresh, alcohol-fixed and formalin-embalmed specimens. Regarding the nomenclature for the facial muscles, we use a system that takes into account the names used by researchers working with non-human primates and non-primate mammals (e.g. Jouffroy & Saban, 1971) and those employed by human anatomists (e.g. Terminologia Anatomica, 1998) (see below). When we cite studies that use a nomenclature that differs from that proposed here, the respective synonymy is given in Table 1. The muscles listed in Table 1 are those that are usually present in adults of the respective taxa; we do not list all of the muscles that occasionally appear as variants in the members of these taxa (e.g. although a few modern humans may have a platysma cervicale, in the vast majority of cases this muscle is lacking; see Diogo et al. 2008). In Table 1, the muscles are listed in the order used by Diogo et al. (2008), which takes into account the homologies and evolutionary history of the hyoid muscles in the sarcopterygian clade as a whole; as done by those authors, we list the extrinsic musculature of the ear (which includes muscles such as, e.g. the obliquus auriculae, transversus auriculae, helicis, tragicus, depressor helicis and/or antitragicus, among others; see Jouffroy & Saban, 1971; Table 1) as a single group. When we use the terms anterior, posterior, dorsal and ventral, we do so in the sense that the terms are used for pronograde tetrapods (e.g. in mammals the eye, and thus the orbicularis oculi, is usually anterior to the ear, and thus to the auricularis superior, and dorsal to the mandible, and thus to the orbicularis oris). Although there is obviously some subjectivity concerning the identification of separate muscles, we followed as strictly as possible the criteria of Edgeworth (1935) for analysing the evidence acquired by others and ourselves, which include criteria such as, e.g. the degree of separation of the fibers, differences in origin and/or insertion, differences in function, orientation of the fibers and/or differences in innervation, among others (see Diogo, 2007, 2008; Diogo et al. 2008).

Fig. 2.

Ornithorhynchus anatinus(Monotremata): lateral view of the deep facial musculature of an adult specimen. Muscles such as the interhyoideus profundus, buccinatorius, orbicularis oris and mentalis are not shown [modified from Lightoller (1942) and Saban (1971); the nomenclature of the structures illustrated follows that used in the present work; anterior is to the right]. CETR, cervicalis transversus; OROC, orbicularis oculi; PLAC, platysma cervicale; PLAM, platysma myoides; SCOS, sphincter colli superficialis.

Pan troglodytes (Primates): lateral view of the facial muscles of an infant specimen (HU-ANA, C104) dissected in the course of this investigation [anterior is to the right; the scale bar shown on the right, at the bottom, corresponds to 1 cm]. DAO, depressor anguli oris; DES, depressor supercilii; DLI, depressor labii inferioris; FRO, frontalis; LELS, levator labii superioris; LELSA, levator labii superioris alaeque nasi; OROC, orbicularis occuli; OROR, orbicularis oris; PLAM, platysma myoides; ZYMA, zygomaticus major; ZYMI, zygomaticus minor.

The definition of homology and its use in systematics and comparative anatomy has been discussed by several authors (e.g. Patterson, 1988; De Pinna, 1991; Agnarsson & Coddington, 2007). The simplest meaning of homology is equivalence of parts (e.g. De Pinna, 1991). In the present work we follow the phylogenetic definition of homology, as proposed by Patterson (1988): homology is equal to synapomorphy. Therefore, following De Pinna (1991), we recognize two main types of muscular homology. ‘Primary homology’ hypotheses are conjectures or hypotheses about the common origin of muscular characters that are established after a careful analysis of criteria such as function, topology and ontogeny (i.e. after the so-called test of similarity). In this study we follow the same methodology that we have employed and carefully explained in previous works (e.g. Diogo, 2007, 2008; Diogo et al. 2008, 2009) and thus take into account all of the lines of evidence obtained either from our dissections or gleaned from the literature in order to formulate such ‘primary homology’ hypotheses (e.g. the innervation of the muscles, their relationships with other muscular structures, their relationships with hard tissues, the configuration/orientation of their fibers, their development, their function, etc.). This is because, as pointed out by Edgeworth (1935), no single criterion is sufficient. For instance, although the innervation of a muscle generally remains constant and corresponds to its segment of origin, there are cases in which the same muscle has different innervations in different taxa (e.g. although wholly of mandibular origin, the intermandibularis of dipnoans is innervated by the Vth and/or VII nerve; Edgeworth, 1935). Also, there are cases in which the same muscle may be ontogenetically derived from different regions and/or segments of the body in different taxa (e.g. the trapezius of Ornithorhynchus is derived from the third branchial muscle-plate, that of Talusia from the second branchial muscle-plate and that of Sus from the first branchial muscle-plate; Edgeworth, 1935). As noted by Edgeworth (1935, p. 224), there are also cases in which ‘an old structure or group of structures may be transformed’ (e.g. the levator hyoideus ‘may be transformed, either partially or wholly, into a depressor mandibulae’).

Following De Pinna (1991), the ‘primary homology’ hypotheses have, however, to pass the second, or ‘hard’, test of homology, i.e. the test of phylogenetic conjunction and congruence (agreement in supporting the same phylogenetic relationships), before they can actually be considered as solid hypotheses of homology, i.e. as ‘secondary homology’ hypotheses. The important point is, thus, that under the phylogenetic definition of homology it is the test of phylogenetic conjunction and congruence that ultimately determines if a hypothesis can, or cannot, be considered as a solid hypothesis of homology. Therefore, if for instance a muscle A of a taxon X and a muscle B of a taxon Y have a similar innervation, function, topology and development but the phylogenetic data available strongly support the idea that muscles A and B were the result of convergent evolution [i.e. that they were acquired independently in evolution and do not correspond to a structure that was present in the last common ancestor (LCA) of A and B], then the phylogenetic criterion has preponderance over the other criteria. As explained above, in the specific case of the present work the phylogenetic framework that we use to investigate and discuss the evolution and homologies of the facial musculature of the taxa listed in Table 1 is shown in Fig. 1. Therefore, following the methodology explained above, if for example an analysis of the data provided by some lines of evidence (e.g. innervation, function and relationships with other muscular and hard structures) indicates that muscles C and D could be homologous (‘primary homology’ hypothesis) but within all mammals muscle C is only present in monotremes and muscle D in modern humans, then we would consider that muscles C and D were probably independently acquired in monotremes and modern humans, respectively, i.e. that these muscles are probably not homologous (i.e. the ‘primary homology’ hypothesis did not pass the ‘hard’ test of homology, that is the test of phylogenetic conjunction and congruence; see Diogo, 2007, 2008, and Diogo et al. 2008, 2009, for more details on this subject). Therefore, the hypotheses of homology that are shown in Table 1 are hypotheses that are phylogenetically congruent with the scenario shown in the cladogram of Fig. 1, i.e. they are ‘secondary homology’ hypotheses sensuDe Pinna (1991).

Results and discussion

The results of our observations and comparisons are summarized in Table 1, and are also partially shown in Figs 2–9. In the sections that follow we comment on the information presented in Table 1, paying special attention to some topics that remain particularly controversial among comparative morphologists.

The origin and plesiomorphic condition of the primate facial muscles

As explained in the recent review of Diogo et al. (2008), the mammalian facial muscles derive from the ventral hyoid muscle interhyoideus, and probably also from at least some dorso-medial hyoid muscles (e.g. cervicomandibularis) of other tetrapods. Monotremes such as the platypus (Ornithorhynchus; Fig. 1) have only 10 distinct facial muscles (not including the extrinsic muscles of the ear), i.e. a platysma cervicale, platysma myoides, interhyoideus profundus, sphincter colli superficialis, cervicalis transversus, orbicularis oculi, naso-labialis, buccinatorius, orbicularis oris and mentalis (Diogo et al. 2008; Diogo, 2009; see Table 1 and Fig. 2).

Rodents such as rats (Fig. 1) have up to 20 distinct facial muscles (Diogo et al. 2008; see Table 1). There is still some controversy regarding certain homologies between the facial muscles of monotremes and of other mammals. However, there is strong supporting evidence for the hypothesis that the occipitalis + auricularis posterior, procerus and dilatator nasi + maxillo-naso-labialis + levator anguli oris facialis of rats correspond to part of the platysma cervicale, naso-labialis and orbicularis oris of monotremes, respectively (Diogo et al. 2008; Table 1). The sternofacialis, interscutularis, zygomaticus major, zygomaticus minor and orbito-termporo-auricularis of rats probably derive from the sphincter colli profundus but it is possible that at least some of the former muscles derive from the platysma cervicale and/or platysma myoides (Diogo et al. 2008; Table 1). The therian mandibulo-auricularis is a deep muscle that is probably derived from the platysma cervicale but it is possible that it is derived, in fact, from deep dorsomedial hyoid muscles such as, e.g. the styloideus (which, together with its derivatives stylohyoideus and digastricus posterior and with the stapedius, are among the few mammalian hyoid muscles that are not considered to be facial muscles) (Diogo et al. 2008; Table 1).

As noted above, colugos (Dermoptera or ‘flying lemurs’) and tree-shrews (Scandentia) are now commonly considered to be the closest living relatives of primates, these three taxa being included in the clade Euarchonta; the clades Glires (lagomorphs + rodents) and Euarchonta make up the clade Euarchontoglires (e.g. Sargis, 2004; Silcox et al. 2007; Fig. 1). Diogo (2009) has recently described the facial muscles of colugos (Fig. 3) and compared them with the facial muscles of tree-shrews and of other mammals. The facial musculature of tree-shrews (Table 1) is similar to that of colugos but the latter lack two muscles that are usually present in the former, the sphincter colli superficialis and mandibulo-auricularis. As both of these muscles are found in rodents, as well as in tree-shrews and at least some primates, they were probably present in the LCA of Euarchontans and Primates (Table 1). Some muscles (e.g. frontalis, auriculo-orbitalis, auricularis superior, zygomatico-orbicularis, corrugator supercilii) are normally present as separate elements in tree-shrews, colugos and primates, but not in rodents (Figs 3–9), but there are also muscles (e.g. dilatator nasi, interscutularis, sternofacialis) that are normally present in the latter group but not in euarchontans. The frontalis, auriculo-orbitalis and auricularis superior of euarchontans probably derive from the orbito-temporo-auricularis of other mammals, whereas the zygomatico-orbicularis and corrugator supercilii probably derive from the orbicularis oculi (see Diogo et al. 2008, Diogo, 2009, and Table 1).

Fig. 3.

Cynocephalus volans (Dermoptera): lateral view of the facial muscles of an adult specimen dissected in the course of this investigation (USNM, 144941), the splenius capitis is also shown. Anteriorly, the nasolabialis was partially cut in order to show the maxillo-naso-labialis [modified from Diogo (2009); the nomenclature of the structures illustrated basically follows that used in the present work, anterior is to the right; the scale bar shown on the right, at the bottom, corresponds to 5 mm]. 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 oculi; 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.

A detailed comparison between the facial muscles of primates, tree-shrews, colugos and other mammals suggests that the facial musculature of the LCA of all primates was probably very similar to that seen in the extant tree-shrew Tupaia (Table 1). Muscles that have been described in the literature as peculiar to primates, e.g. the zygomaticus major and zygomaticus minor, are now commonly accepted as homologues of muscles of other euarchontans. For instance, in the case of the zygomaticus major and minor, these muscles are respectively homologous to the ‘auriculolabialis inferior’ and ‘auriculolabialis superior’ of other mammals (see, e.g. Jouffroy & Saban, 1971; Diogo et al. 2008; Diogo, 2009). The term ‘auriculolabialis’ was used in descriptions of non-primate taxa such as, e.g. tree-shrews and colugos, because, contrary to the usual condition in anthropoids (Figs 4–9), in these taxa the zygomaticus major and minor usually attach posteriorly onto the cartilage of the external ear (Fig. 3). However, attachment to the external ear also occurs in members of the most basal extant primate clade, the strepsirhines (e.g. Ruge, 1885; Lightoller, 1934; Jouffroy & Saban, 1971; Seiler, 1974b, 1975; Burrows & Smith, 2003; this work). According to our dissections, comparisons and review of the literature, the only muscle that is actually often present as a distinct structure in strepsirhines (e.g. Jouffroy & Saban, 1971; Seiler, 1974b, 1975) but not in tree-shrews or colugos (e.g. Le Gros Clark, 1924, 1926; Lightoller, 1934; Jouffroy & Saban, 1971; Diogo, 2009) is the depressor supercilii (Table 1). This muscle derives from the orbicularis oris matrix, and probably corresponds to part of the corrugator supercilii of non-primate taxa (see Diogo et al. 2008; Table 1). As the depressor supercilii is present in strepsirhine and non-strepsirhine primates, it is likely that this muscle was present in the LCA of primates (Table 1).

Fig. 4.

Macaca mulatta (Primates): lateral view of the facial muscles of an adult specimen (HU-ANA, M01) dissected in the course of this investigation, the temporalis is also shown [anterior is to the right; the scale bar shown on the right, at the bottom, corresponds to 1 cm]. DAO, depressor anguli oris; DLI, depressor labii inferioris; FRO, frontalis; LAO, levator anguli oris facialis; LELS, levator labii superioris; LELSA, levator labii superioris alaeque nasi; OROC, orbicularis occuli; OROR, orbicularis oris; PLAC, platysma cervicale; PLAM, platysma myoides; PLAMD, decussating fibers of platysma myoides; TEMP, temporalis; ZYMA, zygomaticus major; ZYMI, zygomaticus minor.

According to most authors (e.g. Murie & Mivart, 1872; Ruge, 1885; Huber, 1930b, 1931; Lightoller 1934; Hill, 1953) and our own observations (see, e.g. Burrows & Smith, 2003; this work), extant strepsirhines share a plesiomorphic configuration with most other therian mammals in which the levator labii superioris and levator labii superioris alaeque nasi are not present as distinct muscles (i.e. these primates have an undifferentiated naso-labialis sensu the present work; Table 1). However, Seiler (1974b) described both a levator labii superioris and a levator labii superioris alaeque nasi in some strepsirhines, e.g. Daubentonia madagascarensis, Eulemur fulvus and Lepilemur ruficaudatus. Seiler (1974b) also described an ‘orbitotemporalis’ and an ‘auricularis anterior’ in these taxa, which would thus correspond to the temporoparietalis and auricularis anterior sensu the present work (see Diogo et al. 2008). However, a detailed analysis of his illustrations indicates that the structures that he designates as ‘orbitotemporalis’ and ‘auricularis anterior’ actually form a continuous auriculo-orbitalis sensu the present work, as is the case in colugos and tree-shrews (e.g. Le Gros Clark, 1924, 1926; Lightoller, 1934; Jouffroy & Saban, 1971; Diogo, 2009) and in the strepsirhine dissections reported by other authors and ourselves (e.g. Murie & Mivart, 1872; Ruge, 1885; Huber, 1930b, 1931; Lightoller, 1934; Hill, 1953; Burrows & Smith, 2003). Another way in which Seiler's reports contradict those of most other researchers concerns the muscles around the mouth. Seiler (1974b, 1975) shows a depressor labii inferioris in the Eulemur, Daubentonia, Nycticebus and Perodicticus (but not in the Lepilemur) specimens dissected by him. However, according to the descriptions of most authors (e.g. Murie & Mivart, 1872; Ruge, 1885; Lightoller, 1928a; Huber, 1930a, 1931) and our own findings (e.g. Burrows & Smith, 2003; this work), strepsirhines do not have a distinct depressor anguli oris or a distinct depressor labii inferioris, thus sharing the plesiomorphic condition of mammals. Further detailed studies on the facial musculature of the oral region of the strepsirhine taxa described by Seiler, as well as of other non-anthropoid primates, are needed to investigate whether or not at least some of these primates have a distinct depressor anguli oris as usually found in monkeys and hominoids.

In summary, the plesiomorphic condition predicted for the LCA of primates is probably similar to that found in extant strepsirhines such as Lepilemur (Table 1). As stressed by Burrows & Smith (2003), the number of facial muscles present in living strepsirhines is higher than that originally reported by authors such as Murie & Mivart (1872) and Huber (1930a, 1931). For instance, Murie & Mivart (1872) reported only seven facial muscles in Otolemur (referred to therein as Galago), grouping all of the muscles associated with the nasal region into a single ‘nasolabial muscle mass’. The supposed lack of complexity seen in strepsirhines was consistent with the anthropocentric, finalistic evolutionary paradigm subscribed to by many anatomists in the last decades of the 19th, and the first decades of the 20th, centuries (e.g. Huber, 1931; see Burrows & Smith, 2003). However, it is now accepted that strepsirhines may have more than 20 facial muscles (e.g. 21 in Lepilemur, without including the extrinsic muscles of the ear; Table 1). In this respect, the works of authors such as, e.g. Lightoller (1934), Seiler (1974b, 1975; which are unfortunately often neglected by non-German-speaking authors) and Burrows & Smith (2003) were crucial to developing a better understanding of the actual complexity of the strepsirhine facial musculature.

Before moving to the next section, we will provide here a brief account of the general function of the facial muscles that are present in strepsirhines. When we refer in the next section to a certain muscle that is not differentiated in strepsirhines but that is present in anthropoids, we will also briefly describe the general function of that muscle. Unless stated otherwise, the functional descriptions provided in the next section are mainly based on what we know about the muscles of those anthropoids that have been the subject of more frequent and rigorous stimulation and/or movement coding studies, e.g. rhesus monkeys, chimpanzees and particularly modern humans (see, e.g. Andrew, 1963; Preuschoft, 2000; Schmidt & Cohn, 2001; Ekman & Friesen, 2003; Waller & Dunbar, 2005; Parr & Waller, 2006; Parr et al. 2005; Waller et al. 2006, 2008a,b; Vick et al. 2007). In Lepilemur(Table 1), a nocturnal, arboreal, territorial, intensive folivore (e.g. Fleagle, 1999), we can reasonably infer muscle function based upon attachments and topology and by comparing these muscles with those of another strepsirhine, the lorisoid Otolemur, for which detailed muscle functions have already been proposed (Burrows & Smith, 2003). The platysma myoides probably draws the oral commissure posteroinferiorly, an action that may be used in social interactions as well as feeding, whereas the platysma cervicale probably elevates the skin of the neck. The occipitalis draws the scalp posteriorly toward the nuchal region, whereas the frontalis elevates the skin/brow over the superciliary region. The auriculo-orbitalis may be used to draw the lateral corner of the eyelid posteroinferiorly or the external ear anterosuperiorly. The corrugator supercilii and depressor supercilii are used to draw the medial edge of the superciliary region inferomedially and inferiorly, respectively. The mandibulo-auricularis may be used to approximate the superior and inferior edges of the external ear, as well as the external ear and mandible. The muscles clustered around the upper lip, including the zygomaticus major and zygomaticus minor muscles, may be used to draw the upper lip and posterior region of the mouth posterosuperiorly, functions that may be used in both social interactions and in use of the vomeronasal organ. As their name indicates, the extrinsic muscles of the ear, as well as the auricularis posterior and auricularis superior, are mostly related to movement of the external ear, whereas the orbicularis oculi and orbicularis oris are primarily associated with movement of the eyes and lips, respectively. The buccinatorius mainly pulls the corner of the mouth laterally and presses the cheek against the teeth. The nasolabialis, maxillo-naso-labialis and levator anguli oris facialis are probably used together in drawing the upper lip and posterior region of the mouth superiorly and medially, which is probably used in social interactions and feeding. The mentalis mainly elevates the skin ventral to the lower lip, whereas the sphincter colli profundus probably draws the skin of the neck posterosuperiorly. Although we have proposed these functions based upon muscle attachments and topology and a comparison to closely related species, ethograms of Lepilemur and other strepsirhines are clearly needed to test these functional hypotheses.

Homologies and evolution of the facial muscles within anthropoids

There are some notable differences between the plesiomorphic condition described above for non-anthropoid primates such as Lepilemur and the condition found in New World and Old World monkeys (Table 1). For example, the mandibulo-auricularis is usually not present as an independent, fleshy muscle in most anthropoids (Table 1; Figs 4–9). It probably corresponds to the stylo-mandibular ligament seen in hominoids such as Homo sapiens and monkeys such as Macaca mulatta (e.g. Lightoller, 1928a, 1934; Jouffroy & Saban, 1971; Diogo et al. 2008), although in the latter species the origin of this ligament is markedly ventral to the ear, i.e. to the usual posterior attachment of the mandibulo-auricularis (e.g. Geist, 1933; this work). According to Huber (1933), fleshy vestiges of the mandibulo-auricularis are, however, found as a ‘rare primitive’ variant in some anthropoid taxa (e.g. macaques; see his Fig. 55). The sphincter colli profundus is also normally absent in anthropoids (Table 1; Figs 4–9) but fleshy vestiges of this muscle have also been described in a few macaque specimens (e.g. Lightoller, 1928a; Huber, 1930b, 1931, 1933).

Contrary to other mammals, most anthropoids have a levator labii superioris, levator labii superioris alaeque nasi and procerus (Table 1; Figs 4–9). These muscles are probably derived from the naso-labialis, although the procerus may possibly be derived from the orbicularis oculi (see Diogo et al. 2008; Table 1). Both the levator labii superioris and levator labii superioris alaeque nasi are normally used in elevating the upper lip and flaring the alar region of the nostril, respectively; these movements are seen in social interactions among rhesus macaques, baboons, chimpanzees and other anthropoids (e.g. Goodall, 1986; Partan, 2002). The levator labii superioris muscle is also used for grooming in chimpanzees and for speech in modern humans (e.g. Calvert & Campbell, 2003; Rogers et al. 2009). The procerus muscle is typically described as drawing the medial portion of the superciliary region inferiorly, wrinkling the skin over the glabella (Waller et al. 2008b). Huber (1930b, 1931, 1933) and Lightoller (1928a) suggested that in Macaca mulatta the procerus is not present as a separate muscle, and Lightoller (1928a) stated that the ‘labii profundus superior’ (i.e. the depressor septi nasi sensu the present work) is also not present as a separate muscle in these monkeys. However, Shibata (1959) and Seiler (1970, 1971c) did describe both muscles inMacaca mulatta; our dissections corroborate the descriptions of these latter authors (Table 1; see, e.g. Fig. 5). Waller et al. (2008b) did not describe a depressor septi nasi in Macaca mulatta but this muscle might well correspond to the small, unlabeled structure that is shown below the nasalis muscle in their Fig. 1. The depressor septi nasi and nasalis of anthropoids are probably derived from the maxillo-naso-labialis (Table 1; Diogo et al. 2008).

Fig. 5.

Macaca mulatta (Primates): anterolateral view of the facial muscles of an adult specimen (HU-ANA, M01) dissected in the course of this investigation [anterior is to the right; the scale bar shown on the right, at the bottom, corresponds to 1 cm]. BUC, buccinatorius; COS, corrugator supercilii; DSN, depressor septi nasi; NAS, nasalis; OROC, orbicularis occuli; OROR, orbicularis oris.

Anthropoids often have a depressor anguli oris and depressor labii inferioris (e.g. Schreiber, 1928; Huber, 1930a, 1931, 1933; see Table 1 and Figs 4–9). These muscles are probably derived from the orbicularis oris matrix; some authors suggested that the depressor anguli oris might be the result of a ventral extension of the levator anguli oris (e.g. Ruge, 1887b; Lightoller, 1928a; Huber, 1930a, 1931; Diogo et al. 2008; Table 1). Generally, the depressor anguli oris and depressor labii inferioris function in anthropoids to draw the corner of the mouth posteroinferiorly and to draw the lower lip inferiorly, respectively. These movements are seen in some displays of facial expression and in some feeding contexts (e.g. Goodall, 1986; Dobson, 2009, in press). Huber (1930b, 1931, 1933) and Shibata (1959) state that the depressor labii inferioris is not present as an independent structure in Macaca mulattaand Macaca cyclopis(note that the muscle named ‘depressor labii inferioris’ in Fig. 471 of Jouffroy & Saban, 1971, which is based on Fig. 1 of Shibata, 1959, corresponds in fact to the ‘incisivus inferioris’ and not to the depressor labii inferioris, sensuShibata, 1959). However, the depressor labii inferioris was found in the Macaca mulatta specimens dissected by authors such as Waller et al. (2008b) as well as by us (Table 1; see Fig. 4).

With regard to the Hominoidea, the number of facial muscles found in the taxa within this clade is essentially the same as that found in Macaca mulatta (Table 1). According to the descriptions available in the literature, the platysma cervicale is usually present in hylobatids (e.g. Sonntag, 1924b; Ruge, 1911; Huber, 1930b, 1931; Loth, 1931; Edgeworth, 1935) and gorillas (e.g. Sullivan & Osgood 1925; Raven, 1950) but is often highly reduced or absent in adult orangutans, panins and modern humans (e.g. Lightoller 1928a; Huber, 1930b, 1931; Loth, 1931; Gasser, 1967). Our dissections corroborate these descriptions (Table 1; see Figs 6–9). The transversus nuchae, found as a variant in the three latter taxa, is often considered to be a vestigial remain/bundle of the platysma cervicale (e.g. Aziz, 1981). Interestingly, Gasser (1967) has shown that the platysma cervicale is present early in the development of modern humans but that it normally disappears as an independent structure in later stages of development. Contrary to the platysma cervicale, the platysma myoides is usually present as a separate structure in adult members of all of the major five extant hominoid taxa (Table 1; Figs 6–9). The occipitalis is also usually present in these five taxa (Table 1; see Fig. 8) but the auricularis posterior is normally not differentiated in the Ponginae (e.g. Sullivan & Osgood, 1925; Lightoller, 1928a; Miller, 1952; Table 1), although it has been described in a few members of this latter subfamily (see, e.g. Winkler, 1989).

Fig. 6.

Hylobates lar (Primates): lateral view of the facial muscles of an adult specimen (HU-ANA, H01) dissected in the course of this investigation [anterior is to the right; the scale bar shown on the right, at the bottom, corresponds to 1 cm]. AUOR, auriculo-orbitalis; AUP, auricularis posterior; AUS, auricularis superior; DAO, depressor anguli oris; DES, depressor supercilii; DLI, depressor labii inferioris; LELS, levator labii superioris; LELSA, levator labii superioris alaeque nasi; OROC, orbicularis occuli; OROR, orbicularis oris; PLAC, platysma cervicale; PLAM, platysma myoides; ZYMA, zygomaticus major; ZYMI, zygomaticus minor.

Fig. 8.

Pongo pygmaeus (Primates): lateral view of the facial muscles of a neonatal specimen (HU-ANA, O01) dissected in the course of this investigation, the masseter is also shown [anterior is to the right; the scale bar shown on the right, at the bottom, corresponds to 1 cm]. AUOR, auriculo-orbitalis; AUS, auricularis superior; COS, corrugator supercilii; DAO, depressor anguli oris; DES, depressor supercilii; DSN, depressor septi nasi; DLI, depressor labii inferioris; FRO, frontalis; LELS, levator labii superioris; LELSA, levator labii superioris alaeque nasi; MAS, masseter; NAS, nasalis; OCC, occipitalis; OROC, orbicularis occuli; OROR, orbicularis oris; PLAM, platysma myoides; PRO, procerus; ZYMA, zygomaticus major; ZYMI, zygomaticus minor.

There is much confusion in the literature about the presence/absence, in apes, of a separate risorius muscle such as that usually (but not always; see, e.g. Standring, 2004) found in modern humans. In humans, the risorius pulls the lip corners backward, stretching the lips, a function that is, interestingly, usually associated with the display of fear (e.g. Ekman & Friesen, 2003). Lightoller (1928a) stated that there are some structures that are often named ‘risorius’ in apes but that probably are not homologous to the risorius of humans, and even to each other, because some of these structures apparently derive from the platysma myoides, others from the depressor anguli oris, and still others from muscles such as the zygomaticus major. Huber (1930a, 1931) argued that the ‘true’ risorius derives from the depressor anguli oris, and that the ‘risorius’ muscles described in Pan are probably not homologous to the ‘true’ risorius because they derive from the platysma myoides, zyzgomaticus major or both. Loth (1931) agreed with the hypothesis that the ‘true’ risorius, i.e. the ‘risorius Santorini’, derives from the depressor anguli oris, proposed that the other ‘risorius’, the ‘platysmarisorius’, derives from the platysma myoides, and suggested that a few modern humans might have both a ‘true’ risorius and a ‘platysmarisorius’. In contrast, in his study of modern human development, Gasser (1967) concluded that the ‘true’ risorius that is usually present in humans derives from the platysma myoides, a view that was supported by Jouffroy & Saban (1971). Based on their own dissections of numerous mammals and a review of the information available in the literature, Diogo et al. (2008) concluded that the muscle risorius that is usually present in humans is probably derived from the platysma myoides, although it cannot be completely discarded that it is partly, or even wholly, derived from the zygomaticus major (Table 1).

Within hylobatids, Seiler (1971d) described a distinct ‘risorius’ in Hylobates agilis, Hylobates lar and Hylobates syndactylus but it is not clear if the structures that he described in the three species are actually homologous to each other. For instance, in his Figs 591 and 592 the ‘risorius’ of Hylobates syndactylus runs more horizontally than that of Hylobates agilis and its fibers have an overall configuration that is somewhat similar to those of the zygomaticus major sensu the present work (i.e. a careful analysis of his figures indicates that the ‘risorius’ of Hylobates agilis might be differentiated from the platysma myoides, whereas the ‘risorius’ of Hylobates syndactylusmight be differentiated from the zygomaticus major). Regarding the Ponginae, according to many assessments (e.g. Sonntag, 1924a; Sullivan & Osgood, 1925; Lightoller, 1928a; Huber, 1930b; Winkler, 1989: Gibbs, 1999; Gibbs et al. 2002), these apes lacks a ‘risorius’ but Seiler (1971d) reported it to be present. Seiler (1971d), as well as authors such as Chudzinski (1885), Huber (1930b, 1931), Raven (1950), Gibbs (1999) and Gibbs et al. (2002), did also report the presence of a ‘risorius’ in gorillas. Chudzinski (1885) stated that the ‘risorius’ of the gorilla that he dissected probably corresponds to the ‘true’ risorius of humans. Huber (1930b, 1931) argued that the ‘risorius’ of gorillas, as well as of chimpanzees, is not a ‘true’ risorius (‘of Santorini’) because it is derived from the platysma myoides and/or zygomaticus major, and not from the depressor anguli oris (however, as explained above, the human risorius probably does derive from the platysma myoides and/or zygomaticus major). The ‘risorius’ of the Gorillaspecimen examined by Raven (1950) is also probably closely related to the platysma myoides. Concerning Pan, Gratiolet & Alix (1866), Sonntag (1923, 1924b), Gibbs (1999) and Gibbs et al. (2002) suggest that, although some individuals have a ‘risorius’, this structure is not completely differentiated from muscles such as the platysma myoides. Sullivan & Osgood (1925) described an ‘upper bundle of the platysma’ in common chimpanzees, which, according to them, corresponds to the ‘true’ risorius of humans. In their work on the facial muscles of chimpanzees, Burrows et al. (2006) described a structure that they suggested might be homologous to the risorius found in most humans and explained that this structure was not described by Pellatt (1979b) in other chimpanzees but that it may correspond to part of the ‘platysma’sensuSonntag (1923).

Among the hominoids dissected for the present study, only modern humans had a well-defined, separate, risorius. In some non-human specimens (e.g. in the chimpanzees PFA 1016 and PFA 1009 but not in PFA 1051 or HUC 104) a few muscular fibers passed posteriorly and superficially (relative to the platysma myoides) to the angle of the mouth but these fibers did not form a distinct, well-defined muscle risorius such as that found in most humans (Table 1).

All of the other facial muscles that are present in macaques (i.e. zygomaticus major, zygomaticus minor, frontalis, auricularis superior, orbicularis oculi, depressor supercilii, corrugator supercilii, levator labii superioris, levator labii superioris alaeque nasi, procerus, buccinatorius, nasalis, depressor septi nasi, levator anguli oris facialis, orbicularis oris, depressor labii inferioris, depressor anguli oris and mentalis) are normally present in extant hylobatids, orangutans, gorillas, panins and humans (Table 1; see Figs 6–9). However, contrary to monkeys and other hominoids, humans, and possibly also gorillas, usually have an auricularis anterior and temporoparietalis (Table 1). Both of these muscles are derived from the auriculo-orbitalis, which, in other hominoids such as chimpanzees, has often been given the name ‘auricularis anterior’, although it actually corresponds to the auricularis anterior plus the temporoparietalis of humans and gorillas (Table 1; Diogo et al. 2008). When present, the temporoparietalis stabilizes the galeal aponeurosis, whereas the auricularis anterior draws the external ear superoanteriorly, closer to the orbit.

General remarks and proposal of a unifying nomenclature for the facial muscles of the Mammalia

The names of the facial muscles that we propose are shown in Table 1; Table 1 also provides a list of more than 300 synonyms that have been used by other authors to designate these muscles. To our knowledge, this is the first time that such a detailed list of synonyms of the facial muscles, not only of primates but also of other mammals, has been compiled in a single study. The fact that more than 300 synonyms have been, and continue to be, used in the literature to describe the facial muscles listed in Table 1 stresses the problem that researchers face when trying to compare the structures of the taxa that they are studying with those described by other authors in other taxa, or even in the same taxa. This is particularly problematic for researchers, such as psychologists or neurobiologists interested in the evolution of facial expressions, who work in fields other than comparative anatomy (e.g. Sherwood et al. 2003; Parr & Waller, 2006; Waller et al. 2006, 2008a,b). One of the main goals of this study was to provide researchers with tools to compare the facial muscles in their study animal with muscles previously described in the literature. Our suggested nomenclature expands on the proposals made in Diogo et al. (2008). A main advantage and strength of our nomenclature is that it combines, and thus creates a bridge between, the names used by human anatomists and by researchers working with non-human primates and non-primate mammals. For example, the terms platysma myoides, platysma cervicale, sphincter colli superficialis, sphincter colli profundus, cervicalis transversus, naso-labialis, sternofacialis, interscutularis, orbito-temporo-auricularis, auriculo-orbitalis and maxillo-naso-labialis are often used to designate the muscles of non-primate mammals (e.g. Jouffroy & Saban, 1971). As some of the muscles that are present in these mammals are directly homologous with muscles that are seen in primates and particularly in strepsirhines (e.g. platysma cervicale, platysma myoides, sphincter colli profundus, auriculo-orbitalis, naso-labialis and maxillo-naso-labialis), it is reasonable to use these names in the descriptions of these primates (and not to use, as is often done in the literature, different names to designate these muscles in primates, e.g. ‘notoplatysma’, ‘tracheloplatysma’, ‘sphincter colli’, ‘auricularis anterior’, ‘levator labii inferioris’ and ‘nasalis’, respectively; see Table 1). At the same time, our nomenclature retains most of the names used for the facial muscles of modern humans as set out in, e.g., the Terminologia Anatomica (1998), for it is also important to maintain the stability of a nomenclature that has been consistently used during various decades in thousands of publications dealing with human anatomy, evolution, psychology and medicine. In fact, regarding the human facial muscles, there are only two differences between our nomenclature and that used in Terminologia Anatomica (1998). Instead of ‘platysma’ we use the name platysma myoides (because the muscle of modern humans corresponds to the platysma myoides and not to the whole ‘platysma’, i.e. platysma myoides + platysma cervicale, of other mammals) and in place of ‘levator anguli oris’ we use the name levator anguli oris facialis [in order to distinguish this facial muscle from the reptilian mandibular muscle that is also designated as ‘levator anguli oris’, Diogo et al. (2008) proposed naming the mammalian facial muscle as levator anguli oris facialis and the reptilian mandibular muscle as levator anguli oris mandibularis] (Table 1).

A consequence of using this unifying nomenclature is that it clearly stresses that the facial muscles present in strepsirhines are in reality essentially the same muscles that are present in non-primate mammals such as tree-shrews (Table 1). The main difference between these taxa is that strepsirhines usually have a muscle, the depressor supercilii, that is usually not differentiated in tree-shrews, and that strepsirhines lack two muscles that are often present in tree-shrews, the sphincter colli superficialis and the peculiar, small zygomatico-orbicularis (Table 1). It is interesting to note that each of the three non-primate taxa listed in Table 1 has at least one derived, peculiar muscle that is not differentiated in any other taxa listed in Table 1. So, for instance, Ornithorhynchus has a cervicalis transversus, Rattus has a sternofacialis and interscutularis and Tupaia has a zygomatico-orbicularis. This supports the idea that evolution is not directed ‘towards’ a goal, and surely not ‘towards’ primates and modern humans; each taxon has its own particular mix of primitive and derived anatomical structures, which is the result of its unique evolutionary history (Diogo et al. 2008, 2009). That is why we use the term correspond, because muscles such as the zygomatico-orbicularis are not ‘ancestral’ to the muscles of primates. The zygomatico-orbicularis simply corresponds to a part of the orbicularis oculi that, in taxa such as Tupaia, became sufficiently differentiated to deserve being recognized as a separate muscle (Table 1; see also Diogo et al. 2008; Diogo, 2009).

Regarding the evolution of the facial muscles within the primates, the muscles present in macaques are essentially the same muscles that are seen in hominoids, with a few exceptions (Table 1). These monkeys do not have distinct risorius, auricularis anterior and temporoparietalis muscles such as those found in hominoids such as humans but have muscles that are usually not differentiated in some hominoid taxa, e.g. the platysma cervicale (usually not differentiated in orangutans, panins and hominins) and the auricularis posterior (usually not differentiated in orangutans). Overall, monkeys and hominoids have more facial muscles than strepsirhines and, among the taxa listed in Table 1, modern humans, together with gorillas, have the greatest number of facial muscles; this is consistent with the important role played by facial expression in anthropoids in general and in modern humans in particular (e.g. Burrows, 2008). However, the evidence presented in this study, as well as in Burrows & Smith (2003) and Burrows et al. (2006), shows that the difference between the number of facial muscles present in modern humans and hominoids such as hylobatids, chimpanzees and orangutans, and between the number of muscles seen in these latter hominoids and strepsirhines, is not as marked as previously thought (see, e.g. Huber 1930b, 1931). In fact, it is important to stress that the display of complex facial expressions in a certain taxon is not only related to the number of facial muscles. It is also related to the subdivisions, arrangements of the fibers, topology, biochemistry and microanatomical mechanical proprieties of these muscles, as well as to the peculiar osteological and external features, and the specific social group characteristics and ecological setting of the members of that taxon (see, e.g. Andrew, 1963; Preuschoft, 2000; Schmidt & Cohn, 2001; Burrows et al. 2006; Burrows, 2008; Waller et al. 2008a,b; Dobson, 2009, in press; Rogers et al. 2009; Burrows & Cohn, in press). A main goal of the present study was precisely to stimulate and help anatomists, functional morphologists and other researchers such as psychologists, neurobiologists and developmental biologists to undertake future works that will hopefully lead to a more comprehensive, multidisciplinary understanding of the evolution of the facial muscles and facial expressions in primates, and in mammals in general.

Appendix 1List of mammalian specimens dissected

Cynocephalus volans: USNM, 144941, 1 (alc); USNM, uncatalogued, 1 (alc). Didelphis albiventris: CML 5971, 1 (alc). Homo sapiens: GWU-ANA, 1–16, 16 (for). Hylobates lar: HU-ANA, H01, 1 (for). Lepilemur ruficaudatus: HU-ANA, L01, 1 (for). Lutreolina crassicaudata: CML 4114, 1 (alc). Macaca mulatta: HU-ANA, M01, 1 (for); YNPRC, M1–9, 9 (for). Monodelphis dimidiata: CML 4118, 1 (alc). Otolemur garnettii: DLC, OG1–10, 10 (for). Otolemur crassicaudatus: DLC, OC1–12, 12 (for). 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); YNPRC, C1–2, 2 (for); CMZ, C1–2, 2 (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.: USNM, 87244, 1 (alc), USNM, uncatalogued, 1 (alc).