Evolution of the Muscles of Facial Expression in a Monogamous Ape: Evaluating the Relative Influences of Ecological and Phylogenetic Factors in Hylobatids

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Evolution of the Muscles of Facial Expression in a Monogamous Ape: Evaluating the Relative Influences of Ecological and Phylogenetic Factors in Hylobatids THE ANATOMICAL RECORD 294:645–663 (2011) Evolution of the Muscles of Facial Expression in a Monogamous Ape: Evaluating the Relative Influences of Ecological and Phylogenetic Factors in Hylobatids ANNE M. BURROWS,1,2* RUI DIOGO,3 BRIDGET M. WALLER,4 5 4,6,7 CHRISTOPHER J. BONAR, AND KATJA LIEBAL 1Department of Physical Therapy, Duquesne University, Pittsburgh, Pennsylvania 2Department of Anthropology, University of Pittsburgh, Pittsburgh, Pennsylvania 3Department of Anthropology, Center for the Advanced Study of Hominid Paleobiology, George Washington University, Washington, District of Columbia 4Department of Psychology, University of Portsmouth, Portsmouth, United Kingdom 5Dallas World Aquarium, Dallas, Texas 6Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 7Department of Psychology, Freie Universita¨t Berlin, Berlin, Germany ABSTRACT Facial expression is a communication mode produced by facial (mimetic) musculature. Hylobatids (gibbons and siamangs) have a poorly documented facial display repertoire and little is known about their facial musculature. These lesser apes represent an opportunity to test hypotheses related to the evolution of primate facial musculature as they are the only hominoid with a monogamous social structure, and thus live in very small groups. Primate species living in large groups with numerous social relationships, such as chimpanzees and rhesus macaques, have been shown to have a complex fa- cial display repertoire and a high number of discrete facial muscles. The present study was designed to examine the relative influence of social struc- ture and phylogeny on facial musculature evolution by comparing facial musculature complexity among hylobatids, chimpanzees, and rhesus maca- ques. Four faces were dissected from four hylobatid species. Morphology, attachments, three-dimensional relationships, and variation among speci- mens were noted and compared to rhesus macaques and chimpanzees. Microanatomical characteristics of the orbicularis oris muscle were also compared. Facial muscles of hylobatids were generally gracile and less com- plex than both the rhesus macaque and chimpanzee. Microanatomically, the orbicularis oris muscle of hylobatids was relatively loosely packed with mus- cle fibers. These results indicate that environmental and social factors may have been important in determining morphology and complexity of facial musculature in the less social hylobatids and that they may not have experi- enced as strong selection pressure for mimetic muscle complexity as other, more social primates. Anat Rec, 294:645–663, 2011. VC 2011 Wiley-Liss, Inc. Key words: communication; mimetic muscle; gibbon; siamang; facial muscle *Correspondence to: Anne M. Burrows, Department of Received 6 July 2010; Accepted 29 December 2010 Physical Therapy, Duquesne University, 600 Forbes Ave., DOI 10.1002/ar.21355 Pittsburgh, PA 15282. Fax: 412-396-4399. E-mail: burrows@duq. Published online 2 March 2011 in Wiley Online Library edu (wileyonlinelibrary.com). VC 2011 WILEY-LISS, INC. 646 BURROWS ET AL. Hylobatids, the gibbons and siamangs [Primates: foraging parties that later re-group (Goodall, 1986; de Hominoidea: Hylobatidae (Groves, 2005)], are small, ar- Waal, 1997; Stumpf, 2007), hylobatid groups typically do boreal, and territorial lesser apes found throughout the not fission (Leighton, 1987; Bartlett, 2007). Territorial evergreen forests of southeast Asia including Indonesia, defense is common between and within hylobatid taxa Eastern India, Vietnam, Laos, Cambodia, and Southern and seems to be one of the functions of the loud vocaliza- China (Rowe, 1996; Bartlett, 2008). Together with tion known as ‘‘duetting,’’ a stereotyped long-distance humans and the great apes (chimpanzees, bonobos, goril- song performed by a mated pair. There is compelling evi- las, and orangutans) they comprise the superfamily dence that these duets are species-specific and gender- Hominoidea (Groves, 2001, 2005). All species are cur- specific (Carpenter, 1940; Mitani, 1988; Geissmann, rently classified as endangered or critically endangered 2002; Fan et al., 2009). making insights into their behavior, ecology, and evolu- Outside of interactions with family members and regu- tionary morphology imperative (Cunningham and Moot- lar morning duetting to defend territory, hylobatids lead nick, 2009; IUCN Red Book, 2010; Thinh et al., 2010). a relatively subdued social life when compared to the During evolution of the hominoids, hylobatids were African hominids (chimpanzees, bonobos, and gorillas) the first to branch off, around 17 million years ago (Flea- and spend very little time socializing with conspecifics in gle, 1984; Pilbeam, 1996; Cunningham and Mootnick, general. Unlike chimpanzees, who spend up to 20% of 2009). Although it is clear that hylobatids form a mono- their daily activity budget socializing, hylobatids spend phyletic clade to the exclusion of the great apes, there is less than 5% of their daily activity budget socializing, no clear consensus about the phylogenetic and taxo- presumably due to a lack of social partners and neces- nomic relationships among the family Hylobatidae with sity for social bonding (Leighton, 1987; Dunbar, 1993). no definitive number of species or number of genera Despite the fact that hylobatids socialize less, their daily (Prouty et al., 1983; Hall et al., 1998; Groves, 2001, activity patterns are highly synchronized, probably coor- 2005; Roos and Geissmann, 2001; Mootnick and Groves, dinated through observation of the other group mem- 2005; Takacs et al., 2005; Cunningham and Mootnick, bers, but not by communicating with them. Their 2009; Thinh et al., 2010). Currently, four genera are rec- limited communicative repertoire may result from this ognized by most authors: the small-bodied (around 5 kg) lack of necessity (Chivers, 1976). Hylobates (including H. agilis, H. albibarbis, H. klossii, All primates communicate with conspecifics using a H. lar, H. moloch, H. muelleri, and H. pileatus), Nomas- variety of modalities including visual communication. cus (including N. concolor, N. gabriellae, N. hainanus, One close-proximity method of visual communication N. siki, and N. leucogenys), and Bunopithecus (B. hoo- used by many primates is facial expression, the produc- lock), and the larger-bodied (around 10 kg) Symphalan- tion, and neural processing of facial movements (Darwin, gus (S. syndactylus). The genera Hylobates, Nomascus, 1872; Burrows, 2008). They serve, in a communicative and Bunopithecus are gibbons, in contrast with Sympha- setting, to signal the sender’s emotional/motivational langus, which is the only extant member of the sia- intent and territorial intentions, they are used in mate/ mangs. Species are grouped into these genera primarily kin recognition, and/or function in agonistic and concilia- based upon differences in chromosome number (Cun- tory displays (Darwin, 1872; Andrew, 1963; van Hooff, ningham and Mootnick, 2009). 1972; Schmidt and Cohn, 2001; Burrows, 2008). Primate Unlike the great apes (Hominidae), hylobatids show facial expressions are movements of the cartilage of the remarkable behavioral, ecological, and morphological external ear and the alar cartilages of the nose, the skin uniformity. All hylobatids are brachiators with long of the face, the vibrissae, and the lips, eyelids, and na- upper limbs and digits (Leighton, 1987; Fleagle, 1999). res. These facial movements are produced by the facial They live in densely foliated trees, are primarily frugivo- musculature, or the mimetic musculature, which is pos- rous (except for S. syndactylus, which eats primarily sessed by all mammals. This musculature is derived young leaves), and are characterized by loud, long-dis- from the second (hyoid) pharyngeal arch, is innervated tance vocalizations (Raemaekers, 1984; Leighton, 1987; by the facial nerve/seventh cranial nerve, and is unique Bartlett, 2007; Cunningham and Mootnick, 2009). Hylo- among all other skeletal muscle in attaching directly batids are especially remarkable in that they are the into the dermis of the face/neck (Young, 1957; Gasser, only monogamous ape and group size is drastically 1967). smaller than chimpanzees, bonobos, and gorillas, averag- Our conceptualization of primate facial musculature ing only four individuals: a mated male and female with morphology and evolution is traditionally rooted in the their infant and a sub-adult offspring (Carpenter, 1940; organization of the phylogeny of primates. Generally, the Chivers, 1984; MacKinnon and MacKinnon, 1984). lower primates, such as lorises, galagos, lemurs, and Although there are reports of multi-male and multi- tarsiers, have been thought to possess a small number of female groups, mated monogamous male/female pairs is relatively simple, undifferentiated muscles with little by and large a characteristic trait across all hylobatid complexity (complexity is defined here as number and genera (Leighton, 1987; Bartlett, 2007). Although there size of muscles and how interconnected they are with is a dominance hierarchy in chimpanzees and gorillas one another, so that a high number of small muscles with one male generally monopolizing access to the with discrete attachment sites equals great complexity reproductive-aged females, dominance hierarchies seem and a lower number of larger muscles with intercon- to be absent in hylobatids (Kleiman, 1977; Gittins and nected attachments equals lower complexity). On the Raemaekers, 1980; Palombit, 1996; Bartlett, 2007, 2008). other hand, monkeys, apes,
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