Review article
Measuring the evolution of facial ‘expression’ using multi-species FACS

https://doi.org/10.1016/j.neubiorev.2020.02.031Get rights and content

Highlights

  • Facial Action Coding Systems (FACS) are useful tools for facial behaviour measurement.

  • FACS is objective, anatomically based and systematic.

  • FACS have been created to facilitate cross-species comparison.

  • Homology is indicated by stereotypy, physical and anatomical similarity, and presence across multiple species.

  • FACS can help determine homology of facial behaviour across species.

Abstract

Darwin observed that form, and in his view, meaning, of facial behaviour (observable changes in the appearance of the face, often termed facial ‘expression’) is similar between a wide range of species and concluded that this must be due to a shared ancestral origin. Yet, as with all social behaviours, exactly how to define similarity and determine homology is debated. Facial behaviour is linked to specific facial muscle movements, so one important factor in determining homology is the anatomical basis of facial behaviours that appear similar in both appearance and social function. The Facial Action Coding System (FACS) was developed for the scientific measurement of human facial behaviour and is based on individual facial muscle movements (Ekman and Friesen, 1978). FACS has since been modified for use with various non-human primate species (chimpanzees, macaques, hylobatids, orangutans) and domestic species (dogs, cats, horses). These FACS can be used to trace continuity of form in facial behaviour across species and build a better understanding of the evolution of facial communication in mammals.

Introduction

The evolution of modern Homo sapiens is thought to have been accompanied by rapid cognitive and behavioural change equipping modern humans with many complex and unique traits (Tomasello, 2008). Some of the most complex and interesting aspects of human mind and behaviour are therefore unique to humans. Human language, for example, is not found in other species and is thus thought to have evolved fairly recently in the hominid lineage, possibly as recently as 50,000 years ago (e.g. Klein, 2017). Such uniqueness renders a comparative approach to some aspects of cognition and behaviour challenging, as scientists need to investigate the precursors to these traits without the option of examining clear, unambiguous counterparts in other extant primates. Human facial behaviour (observable changes in the appearance of the face, often termed facial ‘expression’), in stark contrast, has an abundant array of similar phenomena (in both form and function) throughout the primate order and in other mammals (Waller and Micheletta, 2013). This broad continuity across species suggests that facial expression evolved long before the arrival of modern humans, and that human facial behaviours are rooted in evolutionarily ancient displays. In comparison to some other human traits, scientists are therefore presented with a much easier task when trying to understand the evolutionary trajectory and function of facial behaviour.

Despite the excellent scientific opportunity presented by the existence of similar facial behaviour across species, there are still considerable theoretical and methodological challenges. The field of comparative facial communication research has attracted (and continues to attract) divergent theoretical approaches. First, scientists disagree on which criteria are needed to identify behaviours of shared descent, and thus how to identify unambiguous counterparts. Second, facial behaviours form part of a complex system of production (in the sender) and perception (in the receiver), in which we (the scientists) take part when we make observations. We argue that precise and objective methodology is therefore essential when studying facial behaviours in any species, to avoid biasing observations with our own categorical and emotional interpretation. For example, chimpanzee bared-teeth faces are perceived as more similar to human smiles when the underlying emotion is judged as similar, suggesting observers find it hard to distinguish meaning from form (Waller et al., 2007). Here, we review the development of objective anatomically based systems for the measurement of facial behaviour across species. The Facial Action Coding System (FACS) was originally developed for humans (Hjortsjo, 1969; Ekman et al., 2002; Ekman and Friesen, 1978) and has since been modified for use with several other animal species. We strongly advocate the use of these systems for comparative facial behaviour analysis and discuss how these can be used to better understand the evolution of facial behaviour.

Section snippets

How can we identify homologous facial behaviour?

“As scientists we want to know how justified our feelings of familiarity and understanding are and to what extent our impressions of oddity are based simply on anthropocentrism. To a biologist these questions translate into the question of whether a common heritage disposes us to understand some of the primate facial displays but not others, or whether the perceived similarities and dissimilarities are only superficial and disappear on closer examination.” (Preuschoft and van Hooff, 1995, p.

What is FACS?

The investigation of human facial non-verbal communication has been greatly facilitated and standardised by the development of the Facial Action Coding System (FACS: Ekman et al., 2002; Ekman and Friesen, 1978). Prior to this, the human facial behaviour field was reliant on more subjective methods and did not have a systematic way to assess the muscular components of facial behaviour (and thus help determine homology, see above). Duchenne de Boulogne (1862), however, was the first scientist to

The development of multi-species FACS

FACS has been modified for use with non-human species to facilitate objective facial behaviour measurement. However, there are important assumptions in this endeavour that should be taken into account. The human FACS is based on the assumption that what can be observed by a scientist is similar to what is perceived during human-human social interaction. Thus, the units of FACS (AUs) are assumed to be reasonable units of human perception. This makes sense when investigating human-human

Applications of multi-species FACS

Despite the increase in the number of FACS systems available, there are relatively few studies using this tool to answer questions about the evolution and function of facial behaviours. However, the studies that are available demonstrate how FACS can be a powerful tool to inform us about 1) the phylogenetic link between the facial behaviours of humans and other animals, 2) the cognitive mechanisms underpinning the production and perception of facial behaviours, and 3) the social and ecological

Conclusion and future directions

Comparative analysis of facial behaviour across species attracts different methods and theoretical approaches. Following on from the seminal work of Preuschoft and van Hooff (1995), we argue that to be considered homologous across species, and therefore similar through common descent, facial behaviours need to demonstrate the following: a stereotyped and recognisable form (as defined by the recognition of conspecifics), similarity of multiple elements, homology of underlying facial musculature

Acknowledgements

We would like to thank Mariska Kret, Eliza Bliss-Moreau and Jorg Massen for inviting us to be part of this special issue. We would also like to thank everyone who has contributed to the development and management of the different animal FACS systems. We also thank the funders for the various FACS systems (to us and others): Leverhulme Trust (ChimpFACS and NetFACS), NIH (MaqFACS), British Academy (modification of MaqFACS for crested macaques), Waltham Foundation (DogFACS), DFG (GibbonFACS) and

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