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mystery of yawning 

 

 

 

 

mise à jour du
2 avril 2017
J Comp Psychol.
2017
Yawning and Social Styles:
Different Functions in Tolerant and Despotic Macaques(Macaca tonkeana and Macaca fuscata)
 Zannella A, Stanyon R, Palagi E.

Chat-logomini

Abstract
 
Yawning is a multifunctional behavior with a role in social communication. In Old World monkeys, the "tension yawn" is often used as a threat, allowing individuals to completely expose their canines.
 
To explore the role of this phenomenon, the authors selected 2 closely related species-Japanese macaques (Macaca fuscata) and Tonkean macaques (M. tonkeana)-which differ primarily in terms of their tolerance levels. Japanese macaques are classified as despotic; Tonkean macaques are classified as tolerant. Both species live in multimale-multifemale societies, show a high level of sexual dimorphism, and have comparable yawning repertoires that include displaying a covered teeth yawn and an uncovered gums yawn.
 
They found comparable baseline frequencies of the 2 yawning types and a similar distribution of these behaviors according to sex (males yawned more frequently than females). This morphological homogeneity permitted us to evaluate potential differences in the meaning of yawning as a function of social tension, aggressive contexts, and dominance hierarchy. Divergent social styles determine a functional dichotomy in the use of the covered teeth yawn and the uncovered gums yawn. The covered teeth yawn is not susceptible to social and environmental stimuli and seems to be a form of yawning mostly linked to the physiology of the sleep-wake cycle.
 
However, the uncovered gums yawn is modulated according to different social contexts, and its use could be favored by natural selection, especially in tolerant species, which apparently require more elaborate forms of social communication.
-Demuru E, Palagi E. In Bonobos Yawn Contagion Is Higher among Kin and Friends. PLoS One. 2012; 7(11): e49613
-Leone A, Mignini M, Mancini G, Palagi E. Aggression does not increase friendly contacts among bystanders in geladas (Theropithecus gelada) Primates. 2010;51(4):299-305
-Leone A, Ferrari PF, Palagi E. Different yawns, different functions? Testing social hypotheses on spontaneous yawning in Theropithecus gelada. Scientific Reports 2014;4;4010
-Norscia I, Palagi E. Yawn Contagion and Empathy in Homo sapiens. PLoS ONE. 2011;6(12): e28472
-Norscia I, Demuru E, Palagi E. She more than he: gender bias supports the empathic nature of yawn contagion in Homo sapiens. R. Soc. open sci. 2016:3:150459. http://dx.doi.org/10.1098/rsos.150459
-Palagi E, Leone A, Mancini G, Ferrari PF. Contagious yawning in gelada baboons as a possible expression of empathy. Proc Natl Acad Sci USA. 2009;106(46):19262-19267
-Palagi E, Norscia I, Demuru E. Yawn contagion in humans and bonobos: emotional affinity matters more than species PeerJ 2:e519
-Zannella A, Stanyon R, Palagi E. Yawning and Social Styles: Different Functions in Tolerant and Despotic Macaques (Macaca tonkeana and Macaca fuscata). J Comp Psychol. 2017
-Zannella A, Norscia I, Stanyon R, Palagi E. Testing Yawning Hypotheses in Wild Populations of Two Strepsirrhine Species: Propithecus Verreauxi and Lemur Catta. Am J Primatol. 2015;77(11):1207-1215
 

 

Yawning is a widespread behavior documented in most vertebrate species (Deputte, 1994), and it is easily recognizable due to its plesiomorphic nature (an ancient character shared by several taxa; Provine, 1996). A yawn is characterized by a deep inspiration, followed by a lengthy, forceful expiration with simultaneous contraction of many skeletal muscle groups (Darwin, 1872). Recently, authors have focused on the neurology and physiology of yawning. Some possible explanations have been suggested for this behavior, including respiration, circulation, arousal, brain oxygenation, thermoregulation, and the sleep&endash;wake cycle (Gallup, 2014; Giganti & Zilli, 2011; Matikainen & Elo, 2008; Provine, 1996). Moreover, the neurological complexity of yawning is implied because it also appears to be driven by social complexity (Campbell & De Waal, 2011; Guggisberg, Mathis, Schnider, & Hess, 2010; Provine, 1997). Primates have the largest and most variable yawning repertoire among mammals, most likely due to their neurological, social, and morphological complexity (Gallup, Church, & Pelegrino, 2016).
 
In sexually dimorphic primate species, males typically have larger canines than females and also yawn more frequently (Altmann, 1967). "Threat yawns" allow males to show their weapons (i.e., long canine teeth) during both intragroup ranking competition and intergroup territorial defense (Macaca nigra, Hadidian, 1980; M. fascicularis, Deputte, 1994; Troisi, Aureli, Schino, Rinaldi, & de Angelis, 1990; Theropithecus gelada, Leone, Ferrari, & Palagi, 2014). Altmann (1967) suggested that adolescent baboons learn to appropriately direct threat yawns toward conspecifics. Thus, yawns can acquire a communicative function to regulate social relationships, even if yawns are not always under voluntary control. Anderson and Wunderlich (1988) attempted to demonstrate that food reinforcement led to a certain degree of "voluntary" control of yawning in M. tonkeana males. Covered and uncovered tooth yawns in chimpanzees may indicate either some degree of voluntary control or a different arousal in the activation of facial movements (Vick & Paukner, 2010). However, it is clear that yawns can be modulated according to context, thus acquiring different meanings (Vick & Paukner, 2010). T. gelada displays three different morphologies of yawning, and only the uncovered gum yawns (the most intense version of the motor pattern) are displayed during tense, agonistic situations (Leone et al., 2014). Yawning can also be triggered by environmental and social stressors (Liang, Grace, Tompkins, & Anderson, 2015; Schino, Maestripieri, Scucchi, & Turillazzi, 1990). For this reason, yawning can also be categorized as a displacement behavioral pattern similar to scratching (a well-known index of anxiety in primates; Troisi, 2002). Moreover, yawning response latency can be environmentally modulated. It was shown that under laboratory conditions, perturbing stimuli (e.g., electric shocks) caused an increase in yawning frequency after an interval of 20 to 40 min (Miller, Gallup, Vogel, Vicario, & Clark, 2012; Moyaho & Valencia, 2002). In the wild, perturbing stimuli (i.e., predatory attacks and intragroup aggression) may provoke a faster yawning response (Zannella, Norscia, Stanyon, & Palagi, 2015).
 
The social role of yawning is effectively demonstrated by its infective nature as reported in both human and nonhuman animals (Campbell & De Waal, 2011; Demuru & Palagi, 2012; Norscia, Demuru, & Palagi, 2016; Palagi, Leone, Mancini, & Ferrari, 2009; Romero, Konno, & Hasegawa, 2013). In humans, contagious yawning is easily triggered by seeing, hearing, reading, or simply thinking about another individual yawning (Norscia & Palagi, 2011; Provine, 2005). Yawn contagion increases with the level of bonding between individuals (Palagi, Norscia, & Demuru, 2014), suggesting a link between yawning and social variables. These data suggest that yawning is a multifunctional behavior whose meaning can vary according to social contexts. Primates, due to their large social variability both within and between species, provide promising models to explore the multifaceted phenomena of social yawning.
 
To investigate the social modulation of yawning, we selected M. fuscata (Japanese macaques) and M. tonkeana (Tonkean macaques), two closely related species (Delson, 1980; Eudey, 1981; Hoelzer & Melnick, 1996) with comparable levels of sexual dimorphism. Both species present two variant displays of yawning: covered teeth (teeth remain covered also in the correspondence of the acme phase) and uncovered gums (teeth and gums exposed along with the duration of the acme phase). The species belonging to the genus Macaca can be arranged along a gradient of social style ranging from more intolerant (despotic, Grade 1) to more tolerant (egalitarian, Grade 4; Matsumura, 1998; Thierry, 2000). These differences in social styles influence a wide range of behaviors, including aggressive and affiliative patterns, dominance relationships, and nepotism (Aureli, Das, & Veenema, 1997; De Waal & Luttrell, 1989; Petit, Abegg, & Thierry, 1997; Thierry, 1985). Despotic species such as Japanese macaques with low levels of social tolerance have a strong, kin-centric power asymmetry between dominants and subordinates (Aureli et al., 1997; Kurland, 1977; Kutsukake & Castles, 2001). In contrast, egalitarian species, such as Tonkean macaques, have relationships that are only moderately influenced by social ranking and kinship. The repertoire of formal submissive patterns is reduced and the proportion of friendly interactions is high even among unrelated subjects (Butovskaya, 2004; Butovskaya & Kozintsev, 1996; Preuschoft & van Hooff, 1995).
 
The tolerance degree of a given species relates to how the control over resources is distributed in social communities (Flack & De Waal, 2004; Vehrencamp, 1983), which has a strong impact on their communicative repertoire (social intelligence hypothesis; Whiten & van Schaik, 2007). In tolerant societies, interactions among group members are characterized by high variability independently from rank differences and kinship (Butovskaya, 2004; Freeberg, Dunbar, & Ord, 2012). The high degree of freedom characterizing these species creates a high level of uncertainty arising from such interactions (Butovskaya, 2004; Flack & De Waal, 2004). For this reason, in tolerant social systems, individuals must rely on greater and more sophisticated communicative skills in comparison to despotic species (Flack & De Waal, 2004; Maestripieri, 1995; Preuschoft, Paul, & Kuester, 1998; Scopa & Palagi, 2016; Whiten & van Schaik, 2007).
 
If yawning is linked, at least in part, to species-specific communicative abilities, we expect that, in tolerant societies, yawning can acquire different functions according to its different morphologies.
 
Discussion
Due to their social complexity and variability, the species of the genus Macaca are excellent models to study the multifunctional nature of social yawning. Japanese and Tonkean macaques share a common yawning repertoire&emdash; both species showed covered teeth and uncovered gum yawns. This morphological homogeneity permitted us to evaluate potential differences in the meaning of yawning depending on different levels of tolerance. The Japanese macaque had a steeper dominance hierarchy when compared to the Tonkean macaque. We also found that both species showed similar baseline frequencies of yawning, with males displaying the uncovered gum yawn more frequently than females. Even though the two study groups had different sample sizes, all these findings suggest that they were still suitable for an accurate comparison (see also Ciani, Dall'Olio, Stanyon, & Palagi, 2012). Our findings support the dimorphism hypothesis. In all primate species in which yawning frequency significantly differs between sexes, males always yawn more than females (Altmann, 1967; Bertrand, 1969; Dixson, 2015; Goy & Resko, 1972; Hadidian, 1980; Hall & DeVore, 1965; Leone et al., 2014; Redican, 1975; Troisi et al., 1990). This difference is related to the sexual dimorphism in canine size: The larger size of canines may make male yawns a more effective intimidating signal. This hypothesis is strengthened by the fact that primate species, which do not show sexual dimorphism in canine size, have no gender difference in the baseline frequency of yawning (Lemur catta and Propithecus verreauxi, Zannella et al., 2015; Pan paniscus, Demuru & Palagi, 2012; Pan troglodytes, Vick & Paukner, 2010; Homo sapiens, Norscia et al., 2016; Schino & Aureli, 1989).
 
A functional dichotomy in the use of this display became clear when we compared different yawning morphologies in our two study species. No statistical difference was found in the frequencies of covered teeth yawns. However, the two species strongly differed in the performance of uncovered gum yawns, with Tonkean macaques exhibiting the highest frequencies of this behavior, which was mainly performed during highly tense situations such as feeding (the around-food condition). Covered teeth yawns were more frequent in the relaxed condition.
 
No differences were found between these two yawn types in Japanese macaques. The presence of a functional dichotomy in the use of yawning morphologies in the tolerant species but not in the despotic species supports the communicative redundancy hypothesis, which predicts that tolerant species will tend to show a larger communicative repertoire (Dobson, 2012; Freeberg et al., 2012; Maestripieri, 1995; Scopa & Palagi, 2016). Interindividual tolerance makes the outcome of most interactions unpredictable due to the limited influence of rank (despotism) and kinship (nepotism) in shaping social relationships (Butovskaya, 2004; Freeberg et al., 2012). This uncertainty favors a greater and more sophisticated communicative repertoire to reduce the risk of misunderstanding (Flack & De Waal, 2004; Maestripieri, 1995; Preuschoft et al., 1998; Scopa & Palagi, 2016; Whiten & van Schaik, 2007). The more evident the signal, the clearer the message.
 
The uncovered gum yawn is also elicited by anxious stimuli (Baker & Aureli, 1997; Hadidian, 1980; Leone et al., 2014; Liang et al., 2015; Miller et al., 2012; Moyaho & Valencia, 2002; Schino et al., 1990; Vick & Paukner, 2010; Zannella et al., 2015). However, the extent to which anxiety is experienced by subjects strictly depends on social organization and subjects' levels of tolerance. Uncovered gum yawns and scratching frequencies were higher in subordinates than in dominants in M. fuscata but not in M. tonkeana. This result is in agreement with the resource inequity hypothesis, which predicts that in despotic societies, dominants will limit low-ranking subjects' access to resources by attacking and intimidating them. The result is that subordinates experience higher levels of anxiety (Sapolsky, 2005). In contrast, egalitarian societies have more equal resource distribution, and anxiety is not directly linked to low-ranking status (Sapolsky, 2005). However, in tolerant species, at least at an immediate level, the linkage between yawning and anxiety is not totally absent. To investigate whether yawning was a short-term anxiety-based display, we compared the frequency of yawning in the postconflict and matchcontrol conditions. We never recorded the covered teeth variant after displays of aggression in either species. As predicted by the uncertainty relationship hypothesis, uncovered gum yawns, as for scratching, were significantly higher after an aggressive event only in Tonkean macaques compared to the control condition. In this species, the unpredictability due to the high risk of renewed aggression is elevated. Moreover, immediately after agonistic events involving subjects who share strong bonds, the anxiety response can be even higher because the good relationship between aggressor and victim is at risk (Aureli & Schaffner, 2002; Kutsukake & Castles, 2001). The agonistic events are apparently one of the potential variables affecting uncovered gum yawns and scratching, which are good indicators of short-term anxiety, at least in tolerant species.
 
Our study highlights the substantial stability of covered teeth yawns as a function of (a) social tension conditions (no differences between the around-food and relaxed conditions), (b) aggressive contexts (no differences between the postconflict and matchcontrol observations), and (c) dominance hierarchy (no correlation as a function of ranking position; see Figure 4). Therefore, the covered teeth yawn is a form of yawning that appears not to be susceptible to social and environmental stimuli, although future research should investigate the possible relation between covered teeth yawns and endogenous and physiological changes (e.g., the sleep&endash;wake cycle transition). However, the uncovered gum yawn is a more evident form of yawning (canines are completely visible) whose performance seems to be highly sensitive to all of the aforementioned variables (see Figure 4). This plasticity indicates that the uncovered gum yawn is most likely modulated according to differences in social contexts.
 
It is possible that the communicative function of yawning could be favored by natural selection, especially in tolerant species, which need to elaborate more complex forms of social communication. Research on yawning could be advanced by further comparative studies in a wider range of primate societies varying in social styles, systems, and the degree of canine dimorphism (see Figure 5). In particular, for full comprehension of the social functions of yawning, future studies should focus on its variability by taking into account not only frequency but also other factors such as morphology, duration, and contagious nature.