Animals must overcome a range of environmental and ecological challenges to survive and reproduce, with group-living species having to overcome additional social challenges to maximize fitness. Communicative signals can be used to navigate a number of different social situations and may need to become more elaborate as social complexity increases. The social complexity hypothesis for communicative complexity encapsulates this idea, proposing that animal societies with more complex social systems require more complex communication systems (Freeberg et al., 2012).

The social complexity hypothesis has become a topical issue in recent years, with questions regarding the definitions, measurement, and selective pressures driving both social and communicative complexity (Peckre et al., 2019; Raviv et al., 2022). Social complexity as experienced by group members can be affected by the level of differentiation of social relationships, where complexity increases as social relationships become more differentiated (Bergman and Beehner, 2015; Aureli et al., 2022). In a socially complex society, individuals interact frequently with each other in diverse ways and in many different contexts (Freeberg et al., 2012). If the types of interactions that individuals have is constrained, for example, by dominance or kinship, then social complexity decreases (Freeberg et al., 2012). Social complexity is also affected by the predictability or consistency of social interactions (Aureli et al., 2022; Aureli and Schino, 2019). When the behavior of social partners is unpredictable, such as when the dominance hierarchy is unstable, individuals likely perceive the social environment as more complex (Aureli and Schino, 2019). These operational definitions of social complexity are valuable to advance the study of social complexity but are not easy to quantify with a single measure (Kappeler, 2019).

Similarly, communicative complexity is also difficult to quantify. Many studies have used the number of signaling units as a measure of communicative complexity (Peckre et al., 2019). While a useful measure, it is not always apparent what a signaling unit is. For example, calls are sometimes graded on a continuous scale without a clear separation between different call types (Keenan et al., 2013). Fewer studies have investigated the complexity of non-vocal communication (Freeberg et al., 2012; Peckre et al., 2019), but similar issues exist. One previous study quantified the repertoire of facial behavior in macaques by the number of discrete facial expressions that a species displays and found that it was positively correlated with conciliatory tendency and counter-aggression across species (Dobson, 2012). However, classifying facial expressions into discrete categories (e.g., bared-teeth display) does not capture the full range of expressiveness and meanings that the face can convey. For example, subtle morphological variations in bared-teeth displays are associated with different outcomes of social interactions (e.g., affiliation versus submission) in crested macaques (Macaca nigra) (Clark et al., 2020). A better approach is to quantify facial behavior at the level of individual facial muscle movements (Waller et al., 2020), which can be done using the Facial Action Coding System (FACS) (Ekman et al., 2002). In FACS, visible muscle contractions in the face are called Action Units and allow for a detailed and objective description of facial behavior (Waller et al., 2020; Ekman et al., 2002). Indeed, facial mobility, as defined by the number of Action Units that a species has, is positively correlated with group size across non-human primates (Dobson, 2009a). However, isolated muscle movements still do not account for the full diversity of facial behavior because facial muscles often contract simultaneously to produce a large variety of distinct facial expressions.

One promising avenue to approximate complexity in living organisms is to quantify the uncertainty or predictability of a system (Rebout et al., 2021; Sambrook and Whiten, 1997), which are general properties of complex systems (McDaniel and Driebe, 2005; Schuster, 2016). Shannon’s information entropy (Shannon, 1948) is a measure of uncertainty that can be applied to animal communication. Conceptually, entropy measures the potential amount of information that a communication system holds, rather than what is actually communicated (Shannon, 1948; Adami, 2002). Entropy increases along two dimensions: (1) with increasing diversity of signals and (2) as the relative frequency of signal use becomes more balanced. For example, a system with three calls can hold more information than a system with one call and thus would have higher entropy. Likewise, a system with three calls used with equal frequency will have a higher entropy than another system that expresses one call more frequently than the two others. Uncertainty increases with entropy because each communicative event has the potential to derive from a greater number of units. The relative entropy, or uncertainty, of different systems can be compared by calculating the ratio between the observed and maximum entropy of each system.

The predictability and uncertainty of a communication system is also affected by how flexibly signals are used across different social contexts (Aureli et al., 2022). For instance, if signal A is always used in an aggressive context and signal B is always used in an affiliative context, then it is easy to predict the context from the signal. Conversely, if signals A and B are used in both contexts, then predictability is lower, and complexity is higher. Extremely rare signals do not substantially affect the predictability of a system regardless of whether they have high or low specificity since they are seldom observed in the majority of social interactions. Therefore, predictability is highest when signals are both highly context-specific and occur in that context often. Additionally, predictability can be measured directly by training a machine learning classifier to predict the social context that a given signal was used in. Differences in prediction error would approximate the relative uncertainty and complexity, with accuracy being lower in more complex systems. However, as complexity lies somewhere between order and randomness (Sambrook and Whiten, 1997; Adami, 2002), we should still be able to predict the social contexts better than chance, even in a complex system.

Studying closely related species offers a robust means of testing the social complexity hypothesis due to their homologous communication systems. For this reason, macaques (genus Macaca) are excellent taxa to test the social complexity hypothesis. All species have a similar social organization consisting of multi-male, multi-female groups, but vary in social style in ways that are highly relevant to predictions of the social complexity hypothesis. The social styles of macaques consist of several covarying traits that can be ordered along a social tolerance scale ranging from the least (grade 1) to most tolerant (grade 4) (Thierry, 2007; Thierry, 2022). Social interactions for the least tolerant species, such as rhesus (Macaca mulatta) and Japanese (Macaca fuscata) macaques, are generally more constrained by a steep linear dominance hierarchy (Balasubramaniam et al., 2012) and nepotism (Sueur et al., 2011; Thierry and Berman, 2010; Duboscq et al., 2013). Additionally, severe agonistic interactions are more frequent (Duboscq et al., 2013), instances of counter-aggression and reconciliation after conflicts are rare (Balasubramaniam et al., 2012; Duboscq et al., 2013), and formal signals of submission are commonly used (de Waal and Luttrell, 1985; Preuschoft and Schaik, 2000). Combined, these behavioral traits indicate that agonistic interactions of the least tolerant species are more stereotyped and formalized. Thus, the outcome of such interactions is more certain, whereas the opposite is true for the most tolerant species, such as crested and Tonkean (Macaca tonkeana) macaques. The unpredictability in the outcome of agonistic interactions of tolerant macaques potentially results in a social environment that is perceived as more complex by individuals (Aureli and Schino, 2019), where more subtle means of negotiation during conflicts may be necessary.

In this study we compared the facial behavior of three macaque species that vary in their degree of social tolerance and, therefore, social complexity: rhesus (least tolerant), Barbary (Macaca sylvanus, mid-tolerant), and crested macaques (most tolerant). For macaques (and primates in general), the face is central to communication and is a key tool in allowing individuals to achieve their social goals by communicating motivations, emotions, and/or intentions (Waller et al., 2017; Fridlund, 1994). We coded facial behavior at the level of individual visible muscle movements using FACS and recorded all observed unique combinations, rather than classifying facial expressions into discrete categories. Based on the social complexity hypothesis (Freeberg et al., 2012), we expected that tolerant species would have higher communicative complexity, given that their social relationships are less constrained by dominance and have higher overall uncertainty in the outcome of agonistic interactions. Specifically, we predicted the following: (1) relative entropy of facial behavior will be lowest in the rhesus and highest in crested macaques, (2) context specificity of facial behavior will be highest in rhesus and lowest in crested macaques, and (3) social context can be predicted from facial behavior most accurately in rhesus and least accurately in crested macaques. For all three metrics, we expected Barbary macaques to lie somewhere in-between the rhesus and crested macaques.

We investigated the hypothesis that complex societies require more complex communication systems (Freeberg et al., 2012) by comparing the complexity of facial behavior of three species of macaques that vary in their degree of social tolerance and complexity. We defined facial behavior by the unique combinations of muscle movements visible in the face. Doing so allows for a much more precise description of facial behavior and captures subtle differences that are lost if facial expressions are classified as discrete categories. We quantified communicative complexity using three measures of uncertainty and predictability: entropy, context specificity, and prediction error. Collectively, our results suggest that the complexity of facial behavior is higher in species with a more tolerant—and therefore more complex—social style; complexity was highest for crested, followed by Barbary, and lowest in rhesus macaques. In light of what we know about the differences between macaque social systems, our results support the predictions of the social complexity hypothesis for communicative complexity.

The entropy ratio of facial behavior was highest in crested compared to Barbary and rhesus macaques, both overall and within each social context (affiliative, aggressive, submissive). This result suggests that crested macaques use a higher diversity of facial signals within each social context more frequently, resulting in the higher relative uncertainty in their use of facial behavior. Information theory defines information as the reduction in uncertainty once an outcome is learned (Shannon, 1948). By this definition, our data suggest that the facial behavior of crested macaques has the potential to communicate more information, compared to Barbary and rhesus macaques, although this would need to be explicitly tested in future studies. Our findings are in line with predictions of the social complexity hypothesis (Freeberg et al., 2012) given the differences in social styles between tolerant and intolerant macaques. In tolerant macaque societies, social interactions are less constrained by dominance (Balasubramaniam et al., 2012) such that rates of counter-aggression and reconciliation post-conflict are higher (Duboscq et al., 2013; Thierry et al., 2008). Thus, there is a greater variability in the kind of interactions that individuals have, potentially requiring the use of more diverse facial behavior to achieve social goals, particularly during conflicts. Similarly, strongly bonded chimpanzee (Pan troglodytes) dyads exhibit a larger repertoire of gestural communication than non-bonded dyads, presumably due to the former having more varied types of social interactions (Amici and Liebal, 2022).

The overall entropy ratio of rhesus and Barbary macaques was similar, suggesting that they have similar communicative capacity using facial behavior. However, the entropy ratio differed when compared within social contexts; while relative entropy was higher for Barbary macaques in affiliative and submissive contexts, it was higher for rhesus macaques in aggressive contexts. One possible explanation may be due to the use of stereotyped signals of submission and dominance in each species. For example, subordinate rhesus macaques regularly exhibit stereotyped signals of submission (silent-bared-teeth), whereas dominant Barbary macaques regularly exhibit stereotyped threats (round-open-mouth) (de Waal and Luttrell, 1985; Preuschoft and Schaik, 2000). Frequent use of a stereotyped signal within a context reduces the overall diversity of signals, resulting in a lower entropy ratio for submission and aggression in rhesus and Barbary macaques, respectively. It has been suggested that in societies with high power asymmetries between individuals, such as in rhesus macaques, spontaneous signals of submission serve to prevent conflicts from escalating as well as increasing the tolerance of dominant individuals toward subordinates (Preuschoft and Schaik, 2000). In societies with more moderate power asymmetries, such as in Barbary macaques, subordinates may be less motivated to spontaneously submit and thus dominants may need to assert their dominance with formalized threats more frequently (Preuschoft and Schaik, 2000).

While the entropy ratio captures the uncertainty of facial behavior used within a social context, context specificity captures the uncertainty generated when the same facial behavior is used flexibly across different social contexts. Overall, the context specificity of facial behavior was higher for the intolerant rhesus macaques as compared to the more tolerant Barbary and crested macaques across all three social contexts. This pattern occurred for both the mean specificity values and the proportion of Action Unit combinations used that had high (>0.8) specificity. Similarly, a previous study demonstrated that vocal calls of tolerant macaques are less context specific than in intolerant macaques (Rebout et al., 2022). There was not a clear difference in specificity between Barbary and crested macaques; specificity was higher for Barbary macaques in affiliative contexts, similar for both species in aggressive contexts, and higher for crested macaques in submissive contexts. These differences in context specificity of communicative signals across macaque species may be related to differences in power asymmetry in their respective societies, particularly as it relates to the risk of injury. For macaques, bites are far more likely to injure opponents than other types of contact aggression (e.g., grab, slap) and thus provide the best proxy for risk of injury (Thierry, 2022). The percentage of conflicts involving bites is much higher in the less tolerant rhesus macaque, compared to the more tolerant Barbary and crested macaques who have similar low rates of aggression involving bites (Duboscq et al., 2013; Tyrrell et al., 2020). Risky situations may promote the evolution of more conspicuous, stereotypical signals to reduce ambiguity (Clark et al., 2022). Indeed, intolerant macaques such as the rhesus more commonly use formal signals of submission (de Waal and Luttrell, 1985; Preuschoft and Schaik, 2000). In our study, rhesus macaques used facial behavior with high specificity across all contexts but particularly in submissive contexts. If the same facial behavior (or signal in general) is used in multiple social contexts, its meaning may be uncertain and must be deduced from additional contextual cues (Seyfarth and Cheney, 2017). When facial behavior is highly context specific, there is less uncertainty about the meaning of the signal and/or intention of the signaler. In a society where the risk of injury from aggression is high, it may be adaptive for individuals to use signals that are highly context specific or ritualized to reduce uncertainty about its meaning. By contrast, the lower risk of injury in Barbary and crested macaques may allow room for a greater variety of more nuanced behaviors during conflicts as well as higher rates of reconciliation post-conflict (Duboscq et al., 2013; Thierry et al., 2008).

In all three species of macaques, at least some facial muscle movements had low specificity and were therefore used across multiple social contexts that likely differed in valence. This finding is in line with the idea that communicative signals in primates are better interpreted as the signaler announcing its intentions and likely future behavior (Cheney and Seyfarth, 2018; Fischer and Price, 2017), and not necessarily as an expression of emotional state (Waller et al., 2017; Fridlund, 1994; Cheney and Seyfarth, 2018; Barrett et al., 2019).

We found that a random forest classifier was least accurate at predicting social context from facial behavior for crested, followed by Barbary, and then rhesus macaques. The behavior of complex systems is generally harder to predict than simpler ones (McDaniel and Driebe, 2005; Schuster, 2016). Thus, the relatively poorer performance of the classifier in crested macaques suggests that they have the most complex facial behavior. Nevertheless, the classifier was able to predict social context from facial behavior with better accuracy than expected by chance alone for all three species of macaque, including the crested. This result confirms the assumption that facial behavior in macaques is not used randomly and most likely has some communicative or predictive value (Waller et al., 2016). It is worthwhile to reiterate here that completely random (and thus unpredictable) systems are not considered complex (Adami, 2002). Therefore, the species with the highest entropy values, or unpredictability, could be interpreted as having a simpler communication system than a species with a moderately high entropy value or unpredictability. But the communications systems of living organisms are unlikely to be observed as random, otherwise they would not have evolved as signals. Therefore, working under the assumption that animal communication systems cannot possibly be random, we can conclude that the species whose communication system has the highest relative entropy and unpredictability is in fact the most complex (Rebout et al., 2021).

In addition to social complexity, it is possible that other factors are related to the complexity of facial behavior. For example, primates with a larger body size have greater facial mobility (Dobson, 2009a; Santana et al., 2014), which could allow for greater complexity of facial behavior. However, differences in mean body mass across the three macaques species of this study are small (rhesus: 6.5 kg; Barbary: 11.5 kg; crested: 7.4 kg) (Jones et al., 2009) with substantial overlap in body weight across adult individuals of the different species (Smith and Jungers, 1997), and so it is unlikely to explain the differences in the complexity of facial behavior that we report in this study. The degree of terrestriality could also influence the evolution of facial signals due to more limited visibility in the canopy. However, differences in facial mobility across terrestrial and non-terrestrial primates are not significant once body size is controlled for (Dobson, 2009a). Furthermore, all three species included in this study have comparable levels of terrestriality, spending the majority (52–72%) of the time on the ground (Khatiwada et al., 2020; O’Brien and Kinnaird, 1997; El Alami and Chait, 2014). Spatial spread is another factor that could influence the use of facial signals. For example, when group spread is higher, reliance on facial signals could be lower since it is harder to perceive facial signals from a large distance. There are currently no reliable data on spatial spread of the three species of this study in their natural habitat but it could be a good avenue for future studies. It is also important to note that our study is correlational in nature and we cannot determine the direction of the link between social and communicative complexity. It is possible that an increase in communicative complexity evolved first, which then allowed for the evolution of more complex social systems. Finally, effectively, our comparison is limited to three species which is a small sample. However, the methodology we used is applicable to any species for which FACS is available (including other non-human primates, dogs, and horses; Waller et al., 2020), and therefore, we hope that other datasets will complement ours in the future.

Our results on the complexity of facial behavior in macaques is mirrored by previous studies showing that the complexity of vocal calls is similarly higher in tolerant compared to intolerant macaques (Rebout et al., 2022; Rebout et al., 2020). Although not all macaque facial expressions have a vocal component, vocalizations are fundamentally multisensory with both auditory and visual components, where different facial muscle contractions are partly responsible for different-sounding vocalizations (Ghazanfar and Takahashi, 2014). Indeed, some areas of the brain in primates integrate visual and auditory information resulting in behavioral benefits (Ghazanfar and Eliades, 2014). For example, macaques detect vocalizations in a noisy environment faster when mouth movements are also visible, where faster reaction times are associated with a reduced latency in auditory cortical spiking activity (Chandrasekaran et al., 2013). Combined, these findings suggest that the evolution in the complexity of vocal and facial signals in macaques may be linked and the same may be true of primates in general. For instance, humans not only have the most complex calls (language) and gestures, but most likely use the most complex facial behavior as well, given that their general facial mobility is highest among primates (most Action Units) (Ekman et al., 2002; Dobson, 2009b). In lemurs (Lemuriformes), the repertoire size of vocal, visual, and olfactory signals positively correlate with group size and each other, suggesting that complexity in all three communicative modalities coevolved with social complexity (Fichtel and Kappeler, 2022). While the complexity of different communication modalities is likely interlinked and correlated with each other, future studies would ideally integrate signals from all modalities into a single communicative repertoire for each species. While collecting and analyzing data on multiple modalities of communication has historically been a challenge, such endeavors would be an important next step in the study of animal communication (Liebal et al., 2022). By breaking down signaling units to their smallest components, as we have done for facial behavior in this study, we may be able to define a ‘signal’ by temporal co-activation of visual, auditory, and perhaps even olfactory cues, which would provide the most comprehensive picture of animal communication.

The data generated and analyzed in this study, along with the R code used for all statistical analysis is available on GitHub, https://github.com/avrincon/macaque-facial-complexity (copy archived at Rincon, 2022).

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Author details

1. Alan V Rincon

   Department of Psychology, Centre for Comparative and Evolutionary Psychology, University of Portsmouth, Portsmouth, United Kingdom

   Contribution

   Conceptualization, Data curation, Software, Formal analysis, Validation, Investigation, Visualization, Methodology, Writing - original draft, Writing - review and editing

   For correspondence

   avrincon1@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6181-0152

2. Bridget M Waller

   Centre for Interdisciplinary Research on Social Interaction, Department of Psychology, Nottingham Trent University, Nottingham, United Kingdom

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-6303-7458

3. Julie Duboscq

   CNRS-MNHN-Université Paris Cité, Paris, France

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

4. Alexander Mielke

   School of Biological and Behavioural Sciences, Queen Mary University of London, London, United Kingdom

   Contribution

   Software, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

5. Claire Pérez

   Department of Psychology, Centre for Comparative and Evolutionary Psychology, University of Portsmouth, Portsmouth, United Kingdom

   Contribution

   Data curation, Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

6. Peter R Clark

   1. Department of Psychology, Centre for Comparative and Evolutionary Psychology, University of Portsmouth, Portsmouth, United Kingdom
   2. School of Psychology, University of Lincoln, Lincoln, United Kingdom

   Contribution

   Data curation, Investigation, Writing - review and editing

   Competing interests

   No competing interests declared

7. Jérôme Micheletta

   Department of Psychology, Centre for Comparative and Evolutionary Psychology, University of Portsmouth, Portsmouth, United Kingdom

   Contribution

   Conceptualization, Supervision, Funding acquisition, Methodology, Project administration, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-4480-6781

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