Anne M. Burrows

Muscles of facial expression in the chimpanzee (Pan troglodytes): descriptive, comparative and phylogenetic contexts.

Facial expressions are a critical mode of non‐vocal communication for many mammals, particularly non‐human primates. Although chimpanzees (Pan troglodytes) have an elaborate repertoire of facial signals, little is known about the facial expression (i.e. mimetic) musculature underlying these movements, especially when compared with some other catarrhines. Here we present a detailed description of the facial muscles of the chimpanzee, framed in comparative and phylogenetic contexts, through the dissection of preserved faces using a novel approach. The arrangement and appearance of muscles were noted and compared with previous studies of chimpanzees and with prosimians, cercopithecoids and humans. The results showed 23 mimetic muscles in P. troglodytes, including a thin sphincter colli muscle, reported previously only in adult prosimians, a bi‐layered zygomaticus major muscle and a distinct risorius muscle. The presence of these muscles in such definition supports previous studies that describe an elaborate and highly graded facial communication system in this species that remains qualitatively different from that reported for other non‐human primate species. In addition, there are minimal anatomical differences between chimpanzees and humans, contrary to conclusions from previous studies. These results amplify the importance of understanding facial musculature in primate taxa, which may hold great taxonomic value.

The facial expression musculature in primates and its evolutionary significance.

Facial expression is a mode of close‐proximity non‐vocal communication used by primates and is produced by mimetic/facial musculature. Arguably, primates make the most‐intricate facial displays and have some of the most‐complex facial musculature of all mammals. Most of the earlier ideas of primate mimetic musculature, involving its function in facial displays and its evolution, were essentially linear “scala natural” models of increasing complexity. More‐recent work has challenged these ideas, suggesting that ecological factors and social systems have played a much larger role in explaining the diversity of structures than previously believed. The present review synthesizes the evidence from gross muscular, microanatomical, behavioral and neurobiological studies in order to provide a preliminary analysis of the factors responsible for the evolution of primate facial musculature with comparisons to general mammals. In addition, the unique structure, function and evolution of human mimetic musculature are discussed, along with the potential influential roles of human speech and eye gaze. BioEssays 30:212–225, 2008.

Selection for universal facial emotion

Facial expression is heralded as a communication system common to all human populations, and thus is generally accepted as a biologically based, universal behavior. Happiness, sadness, fear, anger, surprise, and disgust are universally recognized and produced emotions, and communication of these states is deemed essential in order to navigate the social environment. It is puzzling, however, how individuals are capable of producing similar facial expressions when facial musculature is known to vary greatly among individuals. Here, the authors show that although some facial muscles are not present in all individuals, and often exhibit great asymmetry (larger or absent on one side), the facial muscles that are essential in order to produce the universal facial expressions exhibited 100% occurrence and showed minimal gross asymmetry in 18 cadavers. This explains how universal facial expression production is achieved, implies that facial muscles have been selected for essential nonverbal communicative function, and yet also accommodate individual variation.

Brief communication: MaqFACS: A muscle-based facial movement coding system for the rhesus macaque.

Over 125 years ago, Charles Darwin (1872) suggested that the only way to fully understand the form and function of human facial expression was to make comparisons with other species. Nevertheless, it has been only recently that facial expressions in humans and related primate species have been compared using systematic, anatomically based techniques. Through this approach, large-scale evolutionary and phylogenetic analyses of facial expressions, including their homology, can now be addressed. Here, the development of a muscular-based system for measuring facial movement in rhesus macaques (Macaca mulatta) is described based on the well-known FACS (Facial Action Coding System) and ChimpFACS. These systems describe facial movement according to the action of the underlying facial musculature, which is highly conserved across primates. The coding systems are standardized; thus, their use is comparable across laboratories and study populations. In the development of MaqFACS, several species differences in the facial movement repertoire of rhesus macaques were observed in comparison with chimpanzees and humans, particularly with regard to brow movements, puckering of the lips, and ear movements. These differences do not seem to be the result of constraints imposed by morphological differences in the facial structure of these three species. It is more likely that they reflect unique specializations in the communicative repertoire of each species.

Paedomorphic Facial Expressions Give Dogs a Selective Advantage

How wolves were first domesticated is unknown. One hypothesis suggests that wolves underwent a process of self-domestication by tolerating human presence and taking advantage of scavenging possibilities. The puppy-like physical and behavioural traits seen in dogs are thought to have evolved later, as a byproduct of selection against aggression. Using speed of selection from rehoming shelters as a proxy for artificial selection, we tested whether paedomorphic features give dogs a selective advantage in their current environment. Dogs who exhibited facial expressions that enhance their neonatal appearance were preferentially selected by humans. Thus, early domestication of wolves may have occurred not only as wolf populations became tamer, but also as they exploited human preferences for paedomorphic characteristics. These findings, therefore, add to our understanding of early dog domestication as a complex co-evolutionary process.

Facial musculature in the rhesus macaque (Macaca mulatta): evolutionary and functional contexts with comparisons to chimpanzees and humans

Facial expression is a common mode of visual communication in mammals but especially so in primates. Rhesus macaques (Macaca mulatta) have a well‐documented facial expression repertoire that is controlled by the facial/mimetic musculature as in all mammals. However, little is known about the musculature itself and how it compares with those of other primates. Here we present a detailed description of the facial musculature in rhesus macaques in behavioral, evolutionary and comparative contexts. Formalin‐fixed faces from six adult male specimens were dissected using a novel technique. The morphology, attachments, three‐dimensional relationships and variability of muscles were noted and compared with chimpanzees (Pan troglodytes) and with humans. The results showed that there was a greater number of facial muscles in rhesus macaques than previously described (24 muscles), including variably present (and previously unmentioned) zygomaticus minor, levator labii superioris alaeque nasi, depressor septi, anterior auricularis, inferior auricularis and depressor supercilii muscles. The facial muscles of the rhesus macaque were very similar to those in chimpanzees and humans but M. mulatta did not possess a risorius muscle. These results support previous studies that describe a highly graded and intricate facial expression repertoire in rhesus macaques. Furthermore, these results indicate that phylogenetic position is not the primary factor governing the structure of primate facial musculature and that other factors such as social behavior are probably more important. The results from the present study may provide valuable input to both biomedical studies that use rhesus macaques as a model for human disease and disorder that includes assessment of facial movement and studies into the evolution of primate societies and communication.

GibbonFACS: a muscle-based facial movement coding system for hylobatids

The evolution and function of human and nonhuman primate facial expression can be better understood through multispecies comparative analyses. Anatomically based coding systems (Facial Action Coding Systems [FACS]) are developed to enable such analyses because they are standardized and systematic and aid identification of homologous expressions underpinned by similar muscle contractions. To date, FACS has been developed for humans, and subsequently modified for chimpanzees and rhesus macaques. Through detailed examination of facial anatomy and spontaneous movement, here we present a FACS for hylobatids (gibbons and siamangs): apes living in small groups and often thought not to display extensive facial movement. We identified and described 18 independent facial movements (Action Units and Action Descriptors) in the hylobatid face, and compared to humans, chimpanzees, and rhesus macaques. The findings show that the facial movement capacity of hylobatids bears great similarity to species living in much larger groups. The findings could be explained by phylogenetic inertia (especially because pair-bonding is likely to have emerged from social living) and/or the social demands of pair-bonding.

Noggin inhibits postoperative resynostosis in craniosynostotic rabbits

Inhibition of bone formation after surgery to correct craniosynostosis would alleviate the need for secondary surgeries and decrease morbidity and mortality. This study used a single dose of Noggin protein to prevent resynostosis and improve postoperative outcomes in a rabbit model of craniosynostosis.

Scaling of the first ethmoturbinal in nocturnal strepsirrhines: Olfactory and respiratory surfaces

Turbinals (scroll bones, turbinates) are projections from the lateral wall of the nasal fossa. These bones vary from simple folds to branching scrolls. Conventionally, maxilloturbinals comprise the respiratory turbinals, whereas nasoturbinals and ethmoturbinals comprise olfactory turbinals, denoting the primary type of mucosa that lines these conchae. However, the first ethmoturbinal (ETI) appears exceptional in the variability of it mucosal covering. Recently, it was suggested that the distribution of respiratory versus olfactory mucosae varies based on body size or age in strepsirrhine primates (lemurs and lorises). The present study was undertaken to determine how the rostrocaudal distribution of olfactory epithelium (OE) versus non‐OE scales relative to palatal length in strepsirrhines. Serially sectioned heads of 20 strepsirrhines (10 neonates, 10 adults) were examined for presence of OE on ETI, rostral to its attachment to the nasal fossa wall (lateral root). Based on known distances between sections of ETI, the rostrocaudal length of OE was measured and compared to the length lined solely by non‐OE (primarily respiratory epithelium). In 13 specimens, the total surface area of OE versus non‐OE was calculated. Results show that the length of non‐OE scales nearly isometrically with cranial length, while OE is more negatively allometric. In surface area, a lesser percentage of non‐OE exists in smaller species than larger species and between neonates and adults. Such results are consistent with recent suggestions that the olfactory structures do not scale closely with body size, whereas respiratory structures (e.g., maxilloturbinals) may scale close to isometry. In primates and perhaps other mammals, variation in ETI morphology may reflect dual adaptations for olfaction and endothermy. Anat Rec, 2007.

The Evolution of Exudativory in Primates

Table of Contents for The Evolution of Exudativory in Primates List of contributors Dedication Acknowledgements Forward: Robert D. Martin 1. Introduction Leanne T. Nash and Anne M. Burrows 2. Nutritional and digestive challenges to being a gum-feeding primate Michael L. Power 3. Exudativory in primates: interspecific patterns Andrew C. Smith 4. The ecology of exudate production and exudate feeding in Saguinus and Callimico Paul A. Garber and Leila M. Porter 5. Influences on gum feeding in primates Andrew C. Smith 6. Gummivory in cheirogaleids: primitive retention or adaptation to hypervariable environments? Fabien G.S. Genin, Judith C. Masters, and Jorg U. Ganzhorn 7. Seasonality in gum and honeydew feeding in gray mouse lemurs Marine Joly-Radko and Elke Zimmermann 8. Comparative ecology of exudate feeding by Asian slow lorises (Nycticebus) K.A.I. Nekaris, C.R. Starr, R.L. Collins, and A. Navarro-Montes 9. Exudativory and primate skull form Matthew J. Ravosa, Russell T. Hogg, and Christopher J. Vinyard 10. A comparative analysis of the articular cartilage in the temporomandibular joint of gouging and non-gouging New World monkeys Amy L. Mork, Walter E. Horton, Jr., and Christopher J. Vinyard 11. Galago dental adaptations to exudativory: Its not the toothcomb that counts Anne M. Burrows and Leanne T. Nash 12. A guide to galago diversity: Getting a grip on how best to chew gum Isobel R. Stephenson, Simon K. Bearder, Guiseppe Donati, and Johann Karlsson 13. Tongue morphology in infant and adult bushbabies (Otolemur spp.) Beth A. Docherty, Laura J. Alport, Kunwar P. Bhatnagar, Anne M. Burrows, and Timothy D. Smith 14. Adaptive profile versus adaptive specialization: Fossils and gummivory in primate evolution Alfred L. Rosenberger Index