-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
Psychological, clinical and neurobiological
findings endorse that empathic abilities are
more developed in women than in men. Because
there is growing evidence that yawn contagion is
an empathy-based phenomenon, we expect that the
female bias in the empathic abilities reflects
on a gender skew in the responsiveness to
others' yawns. We verified this assumption by
applying a linear model on a dataset gathered
during a 5 year period of naturalistic
observations on humans. Gender, age and social
bond were included in the analysis as fixed
factors. The social bond and the receiver's
gender remained in the best model.
The rates of contagion were significantly
lower between acquaintances than between friends
and family members, and significantly higher in
women than in men. These results not only
confirm that yawn contagion is sensitive to
social closeness, but also that the phenomenon
is affected by the same gender bias affecting
empathy. The sex skew, also found in other
non-human species, fits with the female social
roles which are likely to require higher
empathic abilities (e.g. parental care, group
cohesion maintenance, social mediation). The
fact that female influence in social dynamics
also relies on face-to-face emotional exchange
raises concerns on the negative repercussions of
having women's facial expressions forcibly
concealed.
1. Introduction
Empathy is defined as the ability to
understand and share the internal states of
others [1]. This ability is vital to
engage in successful relationships within
complex social networks and, consequently, to
increase individual fitness [2].
Possibly, because women are hard-wired for
maternity and parental care, they have been
classically considered as more empathic than men
(for an extensive review, see [3]).
Psychological studies indeed report that women
score higher than men on different self-reported
measures of empathy in childhood [4],
adolescence [5,6] and adulthood
[7-9] with differences growing with age
during the puberty period
[5,10-13].
The higher empathic capacity of women is
also strongly suggested by neurobiological
studies focusing on the mirror neuron system.
Through the recruitment of this system, an
observer can preconsciously activate shared
emotional representations during the perception
of an action or of a facial expression of others
[14-16]. This activation response, known
as perception-action mechanism [14], is
a basic requirement of empathy because it allows
individuals to automatically experience others'
affective states [3,14,17].
Empathy is considered to be the result of
the interactions between mirror neuron areas and
emotional-processing brain centres
[3,18]. Through a study of functional
magnetic resonance imaging, Schulte-Rüther
et al. [19] found that women activated
more than men the inferior frontal cortex when
asked to focus on either their own feelings or
the feelings of another person while seeing
facial emotional expressions. Such brain area
was found to include mirror neurons, as it had
been previously hypothesized
[20,21].
Moreover, within the same brain area
(inferior frontal gyrus, pars opercularis) women
seem to possess larger grey matter volume
compared with men, with the larger grey matter
volume being also coupled with higher
self-reported scores in the emotional empathic
propensity [22]. One of the outputs of
the perception-action coupling involving the
mirror neuron system is facial mimicry which, in
turn, is positively associated with empathy
[23,24].
Measures of facial electromyography revealed
greater facial muscle reactivity in women,
compared with men, when exposed to facial
expressions of anger and happiness
[25,26]. Additionally, women rely more
than men on facial feedback for recognizing
facial expressions [27]. Hence, it is
not surprising that one behavioural
manifestation of empathy is facial mimicry,
including contagious yawning
[3,28,29].
Yawning is an involuntary sequence of mouth
opening, deep inspiration, brief apnoea and slow
expiration. In humans, yawns last on average 6s,
and the individual yawn duration and frequency
remains remarkably stable over weeks
[30]. Yawning is an interesting topic
for neurobehavioural research owing to its
implications in several neuroendocrine and
physiological activities including sleep-awake
rhythms, thermoregulation, vigilance and
consequently, in the diagnostic of related
disorders (for an extensive review, see
Walusinski [31]).
Possibly because of its strict association
with hormones and physiology, yawning
performance can vary as a function of the degree
of sexual dimorphism (sexual dimorphism
hypothesis, [32]). For example, in
rhesus macaques, yawning rates are strictly
linked to testosterone levels, thus being more
frequent in males than in females [33],
the same occurs in geladas [34]. In
humans, Schino & Aureli [35] noted
that such androgen-driven dimorphism is not
present, with men and women yawning equally
often. Yawning is contagious in that it can be
triggered by others' yawns [30].
A wide range of sensory modes are vectors of
contagious yawning in humans, ranging from
hearing [36], seeing [30,37],
reading about [30] or even thinking
about yawning [30]. Moreover, yawn
contagion in humans can be affected by different
variables, such as the time of the day
[38], age [39] or familiarity
between subjects [40].
As a physiological response, yawn contagion
is expected to be sensitive to the interaction
between individual, environmental and social
factors. Despite few controversial results
[39], there is growing evidence that
yawn contagion is an empathy-based phenomenon.
Contagious yawning recruits different neuronal
networks involved in empathic processing,
including the inferior frontal gyrus and other
mirror neuron areas [36,41-45].
Although some aspects of empathy may appear
earlier than others [46], contagious
yawning follows a similar ontogenetic trajectory
as empathy. It increases with age starting at
4-5 years [47,48] when the ability to
identify others' emotions is being acquired
[2,49,50] and declines with old age
[39] when empathic abilities also
decline [51]. Contagion is significantly
less likely in subjects suffering from empathy
disorders, such as autism and psychopathy
[52-55]. Contagious yawning follows an
empathy gradient (sensu [14]) being more
frequent in response to kin, then friends, then
acquaintances, and lastly strangers
[40].
Previous reports indicate that not all
individuals are susceptible to others' yawns.
Approximately 40-60% of healthy humans were
never observed yawning in response to a yawn
stimulus under laboratory conditions
[28,30,37]. Moreover, susceptibility to
others' yawns appears to be stable under
different experimental contexts, and yawn
susceptibility is not significantly different
between men and women [39]. In their
naturalistic study on yawn contagion, Norscia
& Palagi [40] considered all the
potential responders, which also included
subjects showing no contagion.
The authors found that the probability to
contagiously yawn was affected by social bond
more than by any other tested variable,
including gender. Therefore, social modulation
more than individual features appeared to affect
the probability to respond to others' yawns
under natural settings. Yet, within the
susceptible population, the level of yawn
contagion may also vary according to different
individual features. If yawn contagion is an
empathy-based phenomenon, then we expect social
bond to be confirmed as a variable that
significantly affects yawn contagion frequencies
(prediction 1a). Moreover, if women are more
empathic than men, then we also expect that in
the susceptible population women are infected at
higher rates by others' yawns compared with men
(prediction 1b). We verified these assumptions
through an ethological, naturalistic approach
based on a 5 year period (2010-2015) of direct
observation on humans.
4. Discussion
Our results show that in the individuals
that are susceptible to yawn contagion, the
rates of yawn responses are affected by both the
social bond linking trigger and responder and by
responder's gender. In particular, yawn
contagion rates were significantly lower between
acquaintances than between friends and family
members (prediction 1a confirmed; figure 1) and
women responded at higher rates than men
(prediction 1b confirmed; figure 2) even though
men and women have not been found to differ in
their rates of spontaneous yawning
([35]; this study).
The former result is consistent with
previous findings by Norscia & Palagi
[40], who reported that in natural
conditions the occurrence and frequency of yawn
contagion correlated with the level of social
closeness. The relationship quality
(acquaintances, friends and kin) significantly
explains the variation of yawn contagion in
humans, either considering all the potential
responders [40] or susceptible subjects
only (present study). The increase of yawn
contagion rates along with social attachment
supports the hypothesis that this phenomenon has
an empathic basis. In fact, one outcome of the
perception- action model [14] is that
the more compatible and socially tied two
subjects are, the easier interpartner
identification is [59]. Yawn contagion
is socially modulated also in non-human
primates. Chimpanzees (Pan troglodytes)
contagiously yawn more in response to in-group
compared with out-group members [60]. In
bonobos (Pan paniscus), yawn contagion peaks
among closely bonded individuals, which are
those who exchange more affinitive contacts
[61]. A comparative study analysed the
variation in yawn contagion in humans and
bonobos and showed that its rates were affected
by the social bond more than by the species,
thus highlighting the salience of
interindividual attachment to yawn contagion
[57]. The relationship between yawn
contagion and social bond is not limited to
humans, bonobos and chimpanzees that share a
close common ancestor (about 5-7 Myr ago)
[62]. In geladas (Theropithecus gelada),
yawning is especially contagious between
socially close individuals [63], thus
suggesting that yawn infectiousness may be an
empathy-based phenomenon also in monkeys. This
is in line with the bottom-up perspective
proposed by de Waal & Ferrari [64],
who posit that a cognitive continuity bridges
non-human to human primates.
Although at variable frequencies, yawn
contagion has been also described between dogs,
wolves and between dogs and humans
[65-70], O'Hara & Reeve [71]
found no association between yawn response and
the familiarity of the human models. Later Silva
et al. [67] and Romero et al.
[68] found that adult dogs yawned more
in response to familiar than unfamiliar yawners,
regardless of the sensory modality through which
the animals perceived the stimulus (hearing or
seeing). Therefore, there is evidence that yawn
contagion between humans and dogs underlies some
empathic abilities. In wolves, yawn contagion
between conspecifics was also associated with
the social closeness of group members
[70]. Hence, in canids, familiarity or
social bond can positively affect the frequency
of yawning responses, suggesting that the
susceptibility of yawn contagion might correlate
with the level of emotional proximity
[68,70]. The available data on social
primates and canids are silent on whether the
association between yawn contagion and emotional
closeness found in these two mammalian taxa may
have a common origin (homology) or be the
outcome of convergent evolution related to
social living (analogy). Whatever the case,
empathy may be adaptive in highly cooperative
and cognitively demanding social systems. In
fact, empathy favours prosocial behaviour and
dyadic closeness [3,72]. Through
transitive emotional transmission [73],
interindividual attachment can spread within the
social network and increase group cohesion and
cooperation.
The completely new finding of this study is
that under natural conditions the women from our
population sample contagiously yawned at
significantly higher rates than men (figure 2).
This result further supports the empathic ground
of yawn contagion, in the light of the existing
psychological, clinical and neurobiological
evidence in favour of higher empathic abilities
of women compared with men
[4-9,19,22,25,26,74]. A recent study on
humans found no relationship between empathic
abilities or gender and yawn contagion. Yet,
this study was conducted in laboratory
conditions on a population including an enriched
cohort of university students (mean age = 32.0
± 15.7 s.d., range = 18-83 years) and was
based on yawn video stimuli, self-reported
contagion and self-reported scores for empathy
[39]. It is not possible to make direct
comparisons with our study, which is based on a
different target population (with no prevalence
of a specific cohort; mean age = 41.7 ±
11.3 s.d., range = 16-72 years), direct
observations of people in their natural
settings, not aware of being under study and
responding to real stimuli. Moreover, we used
the social linkage as a proxy for empathy at
dyadic level, because although the empathic
sensitivity can vary from one subject to
another, the individual expression of empathy is
strongly affected by the emotional bond shared
by the subjects [14].
The literature examining sex differences in
empathy-based behaviours is scarce but still
suggests that&emdash;compared with
males&emdash;females are more sensitive to
others' emotions and more inclined to behave
prosocially [3]. For example, compared
with males, female rats showed greater
sensitivity to other's pain (measured via an
increase of writhing; [75]) and were
more likely to release a trapped cagemate
[76]. In chimpanzees, female bystanders
were more likely to console-distressed
individuals [77] and in lowland
gorillas, immature females offered more
frequently consolatory contact than males
[78]. The presence of a female skew in
the phenomenon of yawn contagion was detected in
different non- human mammals and can be
interpreted in the light of the role of females
according to species-specific social dynamics.
Romero et al. [70] found that female
wolves showed a shorter reaction time than males
when observing yawns of close associates,
suggesting that females are more responsive to
emotional, social stimuli. This may be possibly
related to the fact that wolf family packs
possess a division-of- labour system in which
the female predominates primarily in such
activities as defence and pup care [79]
requiring the ability to quickly detect the
emotional state of the offspring (e.g. distress,
danger) and react accordingly.
In bonobos, Demuru & Palagi [61]
found that group members would respond more
likely to a female than to a male model. Also in
this case, the role of females is crucial to
interpret the result. In bonobos, adult females
represent the relational and decisional nucleus
of the society [80-84], thus playing a
key role in affecting the emotional states of
others [61,85].
In geladas, Palagi et al. [63] found
a stronger and more specific matching of yawn
types in female-female compared with female-male
dyads. In this species, females form coalitions
and long-term relationships, support each other
in infant rearing and remain together,
regardless of whether a dominant male is present
or not [86-88]. According to these
authors, the role of gelada females in cementing
the group may rely on their capacity of being
emotionally tuned to one another. The empathy
gender bias suggested by yawn contagion provides
biological and ethological support to some
sociology studies that are revisiting the role
of women in the mediation of social conflicts.
For example, women as peace negotiators seem to
be more generous and egalitarian than men in
that they expect and ask for less. The
propensity to fairness makes women potentially
more successful to resolve disputes when equity
is crucial to reach stable agreements, as it
occurs in international conflicts involving
disadvantaged parties [89,90]. Empathy
enhances parental care, interindividual
communication and group living, by motivating
prosocial behaviours and favouring the
development of moral reasoning [72]. The
higher empathic abilities of women compared with
men, also revealed by the gender bias in yawn
contagion, may have social repercussions. The
ability to preconsciously decode and replicate
the emotions of others, e.g. via yawn contagion
and facial mimicry, may allow women to respond
with more appropriate behaviours toward others
and to be more successful in forming enduring
alliances [3,91]. What happens when
women's social influence is reduced by forcibly
preventing them from decoding facial expressions
or auditory signals to connect with others
?
References
1. de Waal FBM. 2012 Empathy in primates and
other mammals. In Empathy&emdash;from bench to
bedside (ed. J Decety), pp. 87-106. Cambridge,
MA: The MIT Press.
2. Singer T. 2006 The neuronal basis and
ontogeny of empathy and mind reading: review of
literature and implications for future research.
Neurosci. Biobehav. Rev. 30, 855-863.
3. Christov-Moore L, Simpson EA,
Coudé G, Grigaityte K, Iacoboni M,
Ferrari PF. 2014 Empathy: gender e ects in brain
and behavior. Neurosci. Biobehav. Rev. 46,
604-627.
4. Auyeung B, Wheelwright S, Allison C,
Atkinson M, Samarawickrema N, Baron-Cohen S.
2009 The children's empathy quotient and
systemizing quotient: sex di erences in typical
development and in autism spectrum conditions.
J. Autism Dev. Disord. 39, 1509-1521.
5. Mestre MV, Samper P, Frías MD, Tur
AM. 2009 Are women more empathetic than men? A
longitudinal study in adolescence. Span. J.
Psychol. 12, 76-83.
6. Davis MH, Franzoi SL. 1991 Stability and
change in adolescent self-consciousness and
empathy. J. Res. Pers. 25, 70-87
7. Baron-Cohen S, Wheelwright S. 2004 The
empathy quotient: an investigation of adults
with Asperger syndrome or high functioning
autism, and normal sex di erences. J. Autism
Dev. Disord. 34, 163-175.
8. Rueckert L, Branch B, Doan T. 2011 Are
gender di erences in empathy due to di erences
in emotional reactivity? Psychology 2, 574.
9. Berg K et al. 2015 Standardized patient
assessment of medical student empathy: ethnicity
and gender e ects in a multi-institutional
study. Acad. Med. 90, 105-111.
10. Eisenberg N, Fabes RA, Schaller M,
Miller PA. 1989 Sympathy and personal distress:
development, gender di erences, and
interrelations of indexes. New Dir. Child
Adolesc. Dev. 44, 107-126.
11. Van Tilburg MAL, Unterberg ML,
Vingerhoets AJJM. 2002 Crying during
adolescence: the role of gender, menarche, and
empathy. Br. J. Dev. Psychol. 20, 7 7-87.
12. Lam CB, Solmeyer AR, McHale SM. 2012
Sibling relationships and empathy across the
transition to adolescence. J. Youth Adolesc. 41,
1657-1670.
13. Michalska KJ, Kinzler KD, Decety J. 2013
Age-related sex di erences in explicit measures
of empathy do not predict brain responses across
childhood and adolescence. Dev. Cogn. Neurosci.
3, 22-32.
14. Preston SD, de Waal FBM. 2002 Empathy:
its ultimate and proximate bases. Behav. Brain
Sci. 25, 1-71.
15. Gallese V. 2003 The manifold nature of
interpersonal relations: the quest for a common
mechanism. Phil. Trans. R. Soc. Lond. B 358,
517-528.
16. Gallese V, Keysers C, Rizzolatti G. 2004
A unifying view of the basis of social
cognition. Trends Cogn. Sci. 8, 396-403.
17. Iacoboni M. 2009 Imitation, empathy, and
mirror neurons. Annu. Rev. Psychol. 60,
653-670.
18. Carr L, Iacoboni M, Dubeau MC, Mazziotta
JC, Lenzi GL. 2003 Neural mechanisms of empathy
in humans: a relay from neural systems for
imitation to limbic areas. Proc. Natl Acad. Sci.
USA 100, 5497-5502.
19. Schulte-Rüther M, Markowitsch HJ,
Shah NJ, Fink GR, Piefke M. 2008 Gender
differences in brain networks supporting
empathy. Neuroimage 42, 393-403.
20. Rizzolatti G, Craighero L. 2005 Mirror
neuron: a neurological approach to empathy. In
Neurobiology of human values (eds JP Changeux,
AR Damasio, W Singer, Y Christen), pp. 107-124.
Berlin, Germany: Springer.
21. Kilner JM, Neal A, Weiskopf N, Friston
KJ, Frith CD. 2009 Evidence of mirror neurons in
human inferior frontal gyrus. J. Neurosci. 29,
10 153-10 159.
22. Cheng Y, Chou KH, Decety J, Chen IY,
Hung D, Tzeng OJL, Lin CP. 2009 Sex di erences
in the neuroanatomy of human mirror-neuron
system: a voxel-based morphometric
investigation. Neuroscience 159, 713-720.
23. Dimberg U, Andréasson P, Thunberg
M. 2011 Emotional empathy and facial reactions
to facial expressions. J. Psychophysiol. 25,
26-31.
24. Dimberg U, Thunberg M. 2012 Empathy,
emotional contagion, and rapid facial reactions
to angry and happy facial expressions. PsyCh. J.
1, 118-127.
25. Dimberg U, Lundquist LO. 1990 Gender di
erences in facial reactions to facial
expressions. Biol. Psychol. 30, 151-159.
26. Lundquist LO. 1995 Facial EMG reactions
to facial expressions: a case of facial
emotional contagion? Scand. J. Psychol. 36,
130-141.
27. Stel M, van Knippenberg A. 2008 The role
of facial mimicry in the recognition of a ect.
Psychol. Sci. 19, 984-985.
28. Platek SM, Critton SR, Myers TE, Gallup
GG. 2003 Contagious yawning: the role of
self-awareness and mental state attribution.
Cogn. Brain Res. 17, 223-227.
29. Campbell MW, Carter JD, Proctor D,
Eisenberg ML, de Waal FBM. 2009 Computer
animations stimulate contagious yawning in
chimpanzees. Proc. R. Soc. B 276,
4255-4259.
30. Provine RR. 1986 Yawning as a
stereotyped action pattern and releasing
stimulus. Ethology 72, 448-455.
31. Walusinski O (ed.). 2010 The mystery of
yawning in physiology and disease. Frontiers of
neurology and neuroscience. Basel, Switzerland:
S. Karger AG.
32. Zannella A, Norscia I, Stanyon R, Palagi
E. 2015 Testing yawning hypotheses in wild
populations of two strepsirrhine species:
Propithecus verreauxi and Lemur catta. Am. J.
Primatol. 77, 1207-1215.
33. Phoenix CH, Chambers KC. 1986 Threshold
for behavioral response to testosterone in old
castrated male rhesus macaques. Biol. Reprod.
35, 918-926.
34. Leone A, Ferrari PF, Palagi E. 2014 Di
erent yawns, di erent functions? Testing social
hypotheses on spontaneous yawning in
Theropithecus gelada. Sci. Rep. 4, 4010
35. Schino GE, Aureli F. 1989 Do men yawn
more than women? Ethol. Sociobiol. 10,
375-378.
36. Arnott SR, Singhal A, Goodale MA. 2009
An investigation of auditory contagious yawning.
Cogn. A ect. Behav. Neurosci. 9, 335-342.
37. Provine RR. 1989 Faces as releasers of
contagious yawning: an approach to face
detection using normal human subjects. Bull.
Psychonom. Soc. 27, 211-214.
38. Giganti F, Zilli I. 2011 The daily time
course of contagious and spontaneous yawning
among humans. J. Ethol. 29, 215-219.
39. Bartholomew AJ, Cirulli ET. 2014
Individual variation in contagious yawning
susceptibility is highly stable and largely
unexplained by empathy or other known factors.
PLoS ONE 9, e91773.
40. Norscia I, Palagi E. 2011 Yawn contagion
and empathy in Homo sapiens. PLoS ONE 6,
e28472.
41. Platek SM, Mohamed FB, Gallup Jr GG.
2005 Contagious yawning and the brain. Cogn.
Brain Res. 23, 448-452.
42. Schürmann M, Hesse MD, Stephan KE,
Saarela M, Zilles K, Hari R, Fink GR. 2005
Yearning to yawn: the neural basis of contagious
yawning. Neuroimage 24, 1260-1264.
43. Nahab FB, Hattori N, Saad ZS, Hallett M.
2009 Contagious yawning and the frontal lobe: an
fMRI study. Hum. Brain
44. Cooper NR, Puzzo I, Pawley AD,
Bowes-Mulligan RA, Kirkpatrick EV, Antoniou PA,
Kennett S. 2012 Bridging a yawning chasm: EEG
investigations into the debate concerning the
role of the human mirror neuron system in
contagious yawning. Cogn. A ect. Behav.
Neurosci. 12, 393-405.
45. Haker H, Kawohl W, Herwig U,
Rössler W. 2013 Mirror neuron activity
during contagious yawning: an fMRI study. Brain
Imaging Behav. 7, 28-34.
(doi:10.1007/s11682-012-9189-9) possible
expression of empathy. Proc. Natl Acad. Sci. USA
106, 19 262-19 267.
46. de Waal FBM, Ferrari PF. 2010 Towards a
bottom-up perspective on animal and human
cognition. Trends Cogn. Sci. 14, 201-207.
46. Roth-Hanania R, Davidov M, Zahn-Waxler
C. 2011 Empathy development from 8 to 16 months:
early signs of concern for others. Inf. Behav.
Dev. 34, 003) 447-458.
47. Anderson JR, Meno P. 2003 Psychological
in uences on yawning in children. Curr. Psychol.
Lett. 11, connection 12 Jan 2016. See
http://cpl.revues.org/390.
48. Millen A, Anderson JR. 2011 Neither
infants nor toddlers catch yawns from their
mothers. Biol. Lett. 7, 440-442.
49. Wiggers M, van Lieshout FM. 1985
Development of recognition of emotions:
children's reliance on situational and facial
expressive cues. Dev. Psychol. 21, 338-349.
50. Saxe R, Carey S, Kanwisher N. 2004
Understanding other minds: linking developmental
psychology and functional neuroimaging. Annu.
Rev. Psychol. 55, 87-124.
51. Chen YC, Chen CC, Decety J, Cheng Y.
2014 Aging is associated with changes in the
neural circuits underlying empathy. Neurobiol.
Aging 35, 827-836.
52. Senju A, Maeda M, Kikuchi Y, Hasegawa T,
Tojo Y, Osanai H. 2007 Absence of contagious
yawning in children with autism spectrum
disorder. Biol. Lett. 3, 706-708.
53. Helt MS, Eigsti IM, Snyder PJ, Fein DA.
2010 Contagious yawning in autistic and typical
development. Child Dev. 81, 1620-1631.
54. Giganti F, Esposito Ziello M. 2009
Contagious and spontaneous yawning in autistic
and typically developing children. Curr.
Psychol. Lett. Behav. Brain Cogn. 25, 1-11.
55. Rundle BK, Vaughn VR, Stanford MS. 2015
Contagious yawning and psychopathy. Pers. Indiv.
Di er. 86, 33-37.
56. Provine RR. 2005 Yawning. Am. Sci. 93,
532-539.
57. Palagi E, Norscia I, Demuru E. 2014 Yawn
contagion in humans and bonobos: emotional a
nity matters more than species. Peer J. 2,
e519
58. Kaufman AB, Rosenthal R. 2009 Can you
believe my eyes? The importance of
inter-observer reliability statistics in
observations of animal behaviour. Anim. Behav.
78, 1487-1491. (doi:10.1016/j.anbehav.2009.
09.014)
59. de Waal FBM. 2008 Putting the altruism
back into altruism: the evolution of empathy.
Annu. Rev. Psychol. 59, 279-300.
(doi:10.1146/annurev.psych.
59.103006.093625)
60. Campbell MW, de Waal FBM. 2011
Ingroup-outgroup bias in contagious yawning by
chimpanzees supports link to empathy. PLoS ONE
6, e18283.
(doi:10.1371/journal.pone.0018283)
61. Demuru E, Palagi E. 2012 In bonobos yawn
contagion is higher among kin and friends. PLoS
ONE 7, e49613.
(doi:10.1371/journal.pone.0049613)
62. Fleagle JG. 2013 Primate adaptation and
evolution. 3rd edn. New York, NY: Academic
Press.
63. 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
65. Joly-Mascheroni RM, Senju A, Shepherd
AJ. 2008 Dogs catch human yawns. Biol. Lett. 4,
446-448.
66. Harr AL, Gilbert VR, Phillips KA. 2009
Do dogs (Canis familiaris) show contagious
yawning? Anim. Cogn. 12, 833-837.
67. Silva K, Bessa J, de Sousa L. 2012
Auditory contagious yawning in domestic dogs
(Canis familiaris): rst evidence for social
modulation. Anim. Cogn. 15, 721-724.
68. Romero T, Konno A, Hasegawa T. 2013
Familiarity bias and physiological responses in
contagious yawning by dogs support link to
empathy. PLoS ONE 8, e71365.
69. Madsen EA, Persson T. 2013 Contagious
yawning in domestic dog puppies (Canis lupus
familiaris): the e ect of ontogeny and emotional
closeness on low-level imitation in dogs. Anim.
Cogn. 16, 233-240.
70. Romero T, Ito M, Saito A, Hasegawa T.
2014 Social modulation of contagious yawning in
wolves. PLoS ONE 9, e10596
71. O'Hara SJ, Reeve AV. 2011 A test of the
yawning contagion and emotional connectedness
hypothesis in dogs, Canis familiaris. Anim.
Behav. 81, 335-340.
72. Decety J. 2011 The neuroevolution of
empathy. Ann. N.Y. Acad. Sci. 1231, 35-45.
73. Dezecache G, Conty L, Chadwick M, Philip
L, Soussignan R, Sperber D, Grèzes J.
2013 Evidence for unintentional emotional
contagion beyond dyads. PLoS ONE 8, e67371.
74. Stanyon R, Bigoni F. 2014 Sexual
selection and the evolution of behavior,
morphology, neuroanatomy and genes in humans and
other primates. Neurosci. Biobehav. Rev 46,
579-590
75. Langford DJ, Crager SE, Shehzad Z, Smith
SB, Sotocinal SG, Levenstadt JS, Chanda ML,
Levitin DJ, Mogil JS. 2006 Social modulation of
pain as evidence for empathy in mice. Science
312, 1967-1970.
76. Bartal IBA, Decety J, Mason P. 2011
Empathy and pro-social behavior in rats. Science
334, 1427-1430.
77. Romero T, Castellanos MA, de Waal FBM.
2010 Consolation as possible expression of
sympathetic concern among chimpanzees. Proc.
Natl Acad. Sci. USA 107, 12 110-12 115.
78. Cordoni G, Palagi E, Tarli SB. 2006
Reconciliation and consolation in captive
western gorillas. Int. J. Primatol. 27,
1365-1382.
79. Mech LD. 1999 Alpha status, dominance,
and division of labor in wolf packs. Can. J.
Zool. 77, 1196-1203.
80. Furuichi T. 2011 Female contributions to
the peaceful nature of bonobo society. Evol.
Anthropol. 20, 131-142.
81. Parish AR. 1994 Sex and food control in
the 'uncommon chimpanzee': how bonobo females
overcome a phylogenetic legacy of male
dominance. Ethol. Sociobiol. 15, 157-179.
82. Vervaecke H, De Vries H, Elsacker LV.
2000 Dominance and its behavioral measures in a
captive group of bonobos (Pan paniscus). Int. J.
Primatol. 21, 47-68.
83. Palagi E, Paoli T. 2007 Play in adult
bonobos (Pan paniscus): modality and potential
meaning. Am. J. Phys. Anthropol. 134,
219-225.
84. Paoli T, Palagi E, Borgognini-Tarli SM.
2006 Reevaluation of dominance hierarchy in
bonobos (Pan paniscus). Am. J. Phys. Anthropol.
130, 116-122.
85. Furuichi T, Idani GI, Ihobe H, Hashimoto
C, Tashiro Y, Sakamaki T, Mulavwa MN, Yangozene
K, Kuroda S. 2012 Long-term studies on wild
bonobos at Wamba, Luo Scienti c Reserve, DR
Congo: towards the understanding of female life
history in a male-philopatric species. In
Long-term eld studies of primates (eds PM
Kappeler, DP Watts), pp. 413-433. Heidelberg,
Germany: Springer.
86. Bramblett CA. 1970 Coalitions among
gelada baboons. Primates 11, 327-333.
87. Dunbar RIM. 1983 Structure of gelada
baboon reproductive units II. Social
relationship between reproductive females. Anim.
Behav. 31, 556-564. (
88. Mori A, Belay G, Iwamoto T. 2003 Changes
in unit structures and infanticide observed in
Arsi geladas. Primates 44, 217-223.
89. Eckel C, De Oliveira A, Grossman PJ.
2008 Gender and negotiation in the small: are
women (perceived to be) more cooperative than
men? Negotiation J. 24, 429-445.
90. Klein RS. 2012 The role of women in
mediation and con ict resolution: lessons for UN
Security Council Resolution 1325. Wash. &
Lee J. Civil Rts. Soc. Just. 18, 27 7-313.
91. Korb S, Malsert J, Rochas V, Rihs TA,
Rieger SW, Schwab S, Niedenthal PM, Grandjean D.
2015 Gender di erences in the neural network of
facial mimicry of smiles: an rTMS study. Cortex
70, 101-114.
There
is no difference in contagious yawning between
men and women
In their commentary, Gallup & Massen
[1] criticize the fact that we did not
consider 'more than a dozen' previous
publications which did not report gender
differences in human contagious yawning. We
thank the authors for pointing out this issue
and for giving us the possibility to provide a
brief explanation on some aspects that are not
as obvious as we thought.
Our investigation was ethological and our
framework was centred on behavioural studies
also on non-human primates and other mammals. We
therefore selected the articles that were
relevant to our comparative and evolutionary
approach. Gallup & Massen [1] state
that the gender difference in yawn contagion
detected in our study is a false positive and
that the null effect is real. Unfortunately, the
sample that they used to make this assumption
(17 negative cases and one positive case) is
incorrect and, consequently, so is their
conclusion. The possibility to find a phenomenon
relies on whether the sample and the methodology
used are suitable to detect it. To retain the
metaphor used by Gallup & Massen
[1], you can flip a coin as many times
as you want and never find what you expect if
what you expect is to get a six. You should
change the approach and roll a dice,
instead.
The results presented in the article by
Palagi et al. [2] were based on
naturalistic observations (and not on videos as
it is said in table 1 of the commentary
[1]) and the database also included
bonobos, in which the sex of the trigger and not
the sex of the responder tended to influence
yawn contagion rates [3]. Therefore, it
could not be used to evaluate which variables
affect yawn contagion rates in humans only. Four
of the articles mentioned in their commentary
must be excluded from the sample, because they
were focused on sexually immature subjects and
on the difference between autistic versus
non-autistic children [4-7], whereas our
study was focused on non-pathological adults.
Children are not suitable to test for gender
differences because the power of empathy and
yawn contagion is strongly influenced by age
[8]. One further article cannot be
included because the gender of the potential
responder was not considered at all [9],
and another one has to be excluded because it
investigated yawn contagion and psychopathy
[10]. In seven articles, the
experimental subjects were either aware of the
purpose of the study and/or a control condition
was missing (the rate of spontaneous yawning)
[11-17]. Adopting a blind
procedure&emdash;with the experimental subjects
not knowing the purpose of the study&emdash;is
crucial when dealing with yawn contagion because
simply thinking about yawning can elicit yawns
[18]. Knowing the baseline level of
spontaneous yawns is also pivotal to properly
measure the real differences between the rate of
spontaneous and infected yawns.
Four of the articles mentioned in Gallup
& Massen's commentary [1] used
static images as stimulus to elicit a motor
pattern [12,14-16], and six were based
on self-reports and not on objective
observations (as the authors specify in table 1
of their commentary) [12-17]. The
commentary's authors state that there is no a
priori reason to believe that different methods
and measurements would alter the expression of
yawns in men versus women consistently in one
direction. The literature, however, does not
support this statement. Static images of facial
expressions lack the dynamic complexity of
naturalistic social-emotional interactions and,
therefore, have limited external validity
[19,20]. There is evidence that static
and dynamic images have a different effect on
men and women, with the latter showing an
increase of the perception of the emotional
intensity when exposed to both happy and angry
dynamic facial stimuli [21]. As for the
validity of self-reporting methods, a
significant gender bias has been demonstrated in
a wide variety of studies focusing on many
different contexts [22-24]. Petrides
& Furnham [25], for example,
demonstrated gender differences in measured and
self-estimated emotional intelligence with men
showing higher correlations between measured and
self-estimated scores, whereas women
underestimated their emotional reactions and
skills. Hence, there are solid reasons to
believe that different methods and measurements
can alter the expression of yawns in men versus
women because the existence of
methodology-related gender biases has already
been highlighted in previous studies focusing on
the expression of emotional states. If we
exclude the articles that cannot be used for
comparisons for the above-mentioned reasons
(self-reported scores, static images, no proper
control and non-blind procedures), only two
articles of the initial pseudo-sample remain.
These two studies considered humans in their
natural conditions: one [26] was carried
out on all individuals to find out what factors
influenced the presence and frequency of yawn
contagion and the other [27] considered
only the susceptible population to detect if
other factors could affect the rate of yawn
contagion when yawn contagion occurs. Based on
the real available sample, and the related
probability, it cannot be stated that our result
is a false positive.
2. Comparative versus comparable
studies
As regards non-human animals, the
commentary's authors criticize the fact that we
did not cite all the literature taking into
account possible sex effects in yawn contagion.
This is not correct. We cited the literature
that was relevant to support and understand our
results. Very briefly, we excluded articles
dealing with (i) birds [28] because the
framework of our study connects yawn contagion
with the mirror neuron system and the mammalian
brain, (ii) stressed dogs showing no yawn
contagion [29], (iii) animals exposed to
videos of humans or avatars [30,31] and
(iv) sexually immature subjects
[32].
The work by Massen et al. [33]
deserves a specific comment as it supports our
general idea that yawn contagion is also
influenced by the role that individuals play in
their society. Chimpanzees form male-bonded
societies. Hence, it is not surprising that yawn
contagion may be higher in response to males,
because the relationship with males can be the
most meaningful to the group members. As we
summarize in Norscia & Palagi [34],
there is growing evidence that the social status
affects the degree of emotional involvement of
individuals and their interest in what others
may feel [35,36]. However, we believe
that this study should be replicated without
using slow motion videos because, as said above,
mimicry responses are influenced by the quality
of motor patterns. Moreover, the authors failed
to demonstrate that the yawning response of
chimpanzees was elicited by the video stimulus
and not by other group mates yawning nearby.
This bias raises serious concerns on how to
interpret the final results.
The other works mentioned by Gallup &
Massen [1] were considered when and if
appropriate. As we specify in our article,
Campbell & de Waal [37] found that
only the social bond influenced yawn contagion
rates in chimpanzees, which is similar to what
we found in humans in our previous article
[26]. The same applies to the study on
dogs by Romero et al. [38], which is
cited in our article. The importance of social
bond in influencing yawn contagion can be so
strong as to dampen the effect of any other
factor if we consider the whole population (both
susceptible and non-susceptible subjects).
The commentary's authors also state that
'the findings supporting a female bias in
non-humans do not actually describe a female
bias that is comparable to what Norscia and
co-authors [27] report for humans'.
However, we did not state that the other works
of non-human animals described the exact same
bias that we found. We stated that several other
works had found a female skew (not the same
skew) in yawn contagion and then we interpreted
the different skews in the light of the role
that females have in their groups 'according to
species-specific social dynamics' ([27],
p. 6). Finding exactly the same bias would go
against our own framework, which links possible
biases in yawn contagion to social dynamics. If
the social dynamics are different, so should be
the biases.
3.When the sample is not simple
The commentary's authors confirm that at
least within our restricted sample women are
more likely to yawn contagiously. And we still
claim this. Within the susceptible subjects
included in our study, women contagiously yawned
more than men. In some of the studies cited in
the commentary, some concerns could be raised
about the possibility to generalize the results
when the analyses are restricted to a certain
cohort of individuals (e.g. undergraduate
students), uprooted from their context (e.g.
laboratory condition) and exposed to unreal
stimuli (static images or slow motion videos;
e.g. [11,16]).
In our case, Gallup & Massen [1]
question how we selected the sample for the
analysis, only leaving 34.5% of the original
dataset. We indicated the size of the original
dataset to precisely show that contrary to
laboratory-controlled conditions, in natural
settings it is necessary to gather an enormous
quantity of behavioural bouts to obtain a
sufficient amount of data suitable for analyses.
This is a common situation in observational
studies, not only in humans, but also in
non-human animals.
It is true that in our 2016 study, we 'did
not assess whether there was a difference in
contagious yawning frequency in the total sample
of men and women'. Indeed, as Gallup &
Massen [1] also note, we had already
demonstrated in 2011 that in the susceptible and
non-susceptible population there is no
difference between men and women in the yawn
contagion frequency [26]. As a further
step, we wanted to verify whether within the
population in which the phenomenon of yawn
contagion is present, different factors other
than social bonding would affect the rates of
the yawning response. We confirmed that the
social bond is a key factor but also that gender
can make the difference in how much a subject
responds to another one within the 'yawning
dyad'. Gallup & Massen [1] also
criticize our choice of considering only the
subjects exposed to at least three stimuli
(yawns) but we strenuously defend this approach.
In a natural setting, with confounding auditory
and visual stimuli, we must be reasonably sure
that the study stimulus is detected. This
approach mirrors laboratory experimental
procedures in which the yawning pattern is
repeated several times in a single video to make
sure that the stimulus is perceived by the
observer.
In sum, the sample of articles on human
contagious yawning that Gallup & Massen used
to conclude that our result is a false positive
is incorrect, because the cited articles cannot
be reliably compared with our study. The
comparative studies considering non-human
animals were used to discuss why it is
reasonable to interpret the different types of
biases in contagious yawning in the light of the
role that the individuals play in their social
groups. Finally, not to replicate previously
published results, we focused on the subjects
that showed yawn contagion and we made sure that
the eliciting stimulus was perceived. In our
study, we found that women produce slightly more
yawns than men (moderate effect size) and that
gender plays a statistically significant role in
susceptible people, with women showing a higher
level of yawn contagion than men. We are
confident that future studies will confirm our
results.
