Paedomorphic Facial Expressions Give Dogs a Selective Advantage

Abstract

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

Full text

Paedomorphic Facial Expressions Give Dogs a Selective
Advantage
Bridget M. Waller
1
*, Kate Peirce
1
,Ca
´tia C. Caeiro
1
, Linda Scheider
2
, Anne M. Burrows
3,4
, Sandra McCune
5
,
Juliane Kaminski
1
1Centre for Comparative and Evolutionary Psychology, University of Portsmouth, Portsmouth, Hampshire, United Kingdom, 2Department of Psychology, Freie Universita
¨t
Berlin, Berlin, Germany, 3Department of Physical Therapy, Duquesne University, Pittsburgh, United States of America, 4Department of Anthropology, University of
Pittsburgh, Pittsburgh, United States of America, 5WALTHAMH, Centre for Pet Nutrition, Leicestershire, United Kingdom
Abstract
How wolves were first domesticated is unknown. One hypothesis suggests that wolves underwent a process of self-
domestication by tolerating human presence and taking advantage of scavenging possibilities. The puppy-like physical and
behavioural traits seen in dogs are thought to have evolved later, as a byproduct of selection against aggression. Using
speed of selection from rehoming shelters as a proxy for artificial selection, we tested whether paedomorphic features give
dogs a selective advantage in their current environment. Dogs who exhibited facial expressions that enhance their neonatal
appearance were preferentially selected by humans. Thus, early domestication of wolves may have occurred not only as
wolf populations became tamer, but also as they exploited human preferences for paedomorphic characteristics. These
findings, therefore, add to our understanding of early dog domestication as a complex co-evolutionary process.
Citation: Waller BM, Peirce K, Caeiro CC, Scheider L, Burrows AM, et al. (2013) Paedomorphic Facial Expressions Give Dogs a Selective Advantage. PLoS ONE 8(12):
e82686. doi:10.1371/journal.pone.0082686
Editor: Claire Wade, University of Sydney, Australia
Received July 8, 2013; Accepted October 27, 2013; Published December 26, 2013
Copyright: ß2013 Waller et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The study was funded by a WALTHAM Foundation Research Grant to BMW, JK and AB. The funder had some input during study design, but did not
influence study findings, interpretation of results or writing of the manuscript. The funder had some input during study design, but did not influence study
findings, interpretation of results or writing of the manuscript.
Competing Interests: The authors declare that author SM is an employee (Research Manager) of WALTHAM, a division of Mars Inc. All other authors have
declared that no competing interests exist. This does not alter their adherence to all the PLOS ONE policies on sharing data and materials.
* E-mail: bridget.waller@port.ac.uk
Introduction
Wolves were domesticated early in the history of human
civilization [1], and have since evolved into dogs whose lives are
now inextricably linked to those of humans. The initial steps that
led to wolves becoming domesticated, however, is unknown. One
hypothesis suggests that wolves underwent a process of self-
domestication as tamer individuals took advantage of opportuni-
ties to scavenge from human settlements during the agricultural
revolution [2]. In support of this theory is recent evidence that
domestic dogs exhibit genetic mutations to a starch-rich diet [3].
During domestication, dogs have departed from wolves on various
other behavioral and physical dimensions [2,4,5], one of the most
striking being paedomorphism. In many ways dogs appear more
like wolf puppies than wolf adults. These features are thought to
have evolved as a byproduct of the domestication process, and
arose accidently when aggression was actively selected against
[6,7], for a detailed review see [8].
Paedomorphic features, however, could have evolved much
earlier in response to human preferences. Domestic cats have
developed modified purr vocalizations that appear to solicit
increased care from human hosts by mimicking human infant
cries [9], and which may have increased tolerance of cats in
human environments during domestication. Likewise, the
shorter snout and wider cranium of the dog give the dog face
a more puppy like appearance (although there is variation
between breeds) which may have evolved as the well
documented human preference for paedomorphic facial char-
acteristics [10] was exploited. Paedomorphic facial features can
be further enhanced through use of upper face facial muscle
contractions that lift the brow to increase the apparent height
and overall size of the orbital cavity (i.e. the apparent size of the
eyes: figure 1). Large eyes relative to the rest of the face are a
prominent feature in human infants and are associated with
perceived cuteness of and motivation to invest in human infants
by human adults [10,11]. Toys (teddy bears) that display this
trait are also preferred [12,13]. Infantile facial features are
similarly preferred in pet dogs and cats [14], and manipulation
of infant-like facial traits increases perceived cuteness [15].
However, in all of these studies humans are making forced
choices in experimental conditions. In addition, demonstrating
visual preference does not necessarily mean that these animals
are (or have been) selected preferentially. To demonstrate
whether these human preferences translate into differential
investment we need to examine which dog characteristics incur
a current selective advantage. Current fitness is not necessarily
indicative of past selection of course, but it is a common
assumption in behavioural ecology and evolutionary anthropol-
ogy.
Juvenile traits other than face may have also been subject to
selection, of course. Tail wagging and other submissive behaviours
are more common in wolf puppies than adult wolves but persist in
the adult dog [5], and are more often human directed [16]. Such
behaviours, however, are not human-like or even universally
mammalian, so it is unlikely that they would be as salient as the
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face (to humans), which is widely understood to be an attention
grabbing stimulus in both humans and other animals.
Dog facial expressions have been described in classic studies
[17], but as the facial muscles of social mammals (including
humans) can exhibit great subtlety of movement, standardised
methods for facial movement measurement are needed to make
accurate observations within and between species. Scientists must
use validated, anatomically based systems for recording facial
expression. First, facial expressions are processed as whole units in
an automatic, streamlined manner which makes it difficult to see
the detail accurately [18]. Second, human observers tend to
categorise facial expressions in terms of emotion, which can affect
how comparisons between species are made [19]. The Facial
Action Coding System (FACS: [20]) is an anatomically based
facial expression coding system used in humans to counter these
problems, which identifies observable facial changes associated
with underlying muscle movement. Recently, the system has been
successfully modified for use with chimpanzees [21], rhesus
macaques [22], hylobatids [23] and orangutans [24]. The systems
are objective, reliable and standardised, and allow subtle
movements to be identified and quantified.
In the current study we used shelter dog rehoming as a proxy
for dogs’ selection over time. We tested whether humans (when
adopting dogs from a shelter) actively select for dogs, which appear
more juvenile in the face as a result of facial muscle contraction.
AU101 (inner brow raiser) raises the medial portion of the brow
increasing the apparent size of the eyes in relation to the face, and
as such enhances one of the features of the face associated with
infants. Subtle facial muscle movements were recorded using an
anatomically based facial muscle coding system (DogFACS). We
examined whether frequent use of these movements (AU101:
inner brow raiser) was associated with selection by humans using
real world shelter dog adoption speed as a proxy for human
selection over evolutionary time.
Materials and Methods
Ethics Statement
This study was carried out in strict accordance with the
recommendations in the ASAB/ABS guidelines for the use of
animals in research and was approved by the University of
Portsmouth Animal Ethics Committee.
Development of DogFACS
Footage from 28 privately owned dogs of varying breeds
(approximately 8–10 hours) from the Max Planck Institute for
Evolutionary Anthropology DogLab was the primary source for
DogFACS development. In addition, we sourced approximately
100 clips from www.youtube.com (permission granted from the
copyright holder of each clip) and used ad hoc footage from 86
dogs at four dog shelters (Portsmouth City Dog Kennels; Wood
Green, The Animal’s Charity in Cambridge; The Dog’s Trust,
West London, Harefield and RSPCA Southridge Animal Centre,
London). Each facial movement was documented by appearance
changes, minimal criteria for identification and comparison to
other species, in line with FACS terminology (Table 1). The
muscular basis of each facial movement was verified in light of
dissection of a face from a specimen of a domestic dog (AMB) as
well as previously published dissections [25]. The manual is freely
available and requires certification to use (www.dogfacs.com).
Shelter Dog Data Collection
The study used a correlational design using data from a one-
shot, timed observation. Dogs were observed at the same four re-
homing shelters (above). The modal breed group (bull breeds,
which includes all breeds derived from the molasser breed,
Staffordshire Bull Terriers, Mastiffs and mixed bull breeds: as
classified by the shelter staff using criteria from the UK Kennel
Club) was chosen for analysis to minimise the variance associated
with breed differences, and totalled 29 dogs. Each dog was filmed
Figure 1. Example of facial movement AU101 (inner brow raiser) in a domestic dog (Rhodesian Ridgeback, not a subject in the
study), increasing the height and overall size of the orbital cavity (eye): A) neutral on right side of face, B) AU101 on right side of
face.
doi:10.1371/journal.pone.0082686.g001
Paedomorphic Facial Expressions in Dogs
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for a 2 min period (focal sampling) during controlled first contact
with the experimenter. The experimenter approached the subject’s
kennel room and stood in front of the room with a neutral stance
and holding out one hand. Each 2 min video sample (from each
dog subject) was coded using DogFACS to record the frequency of
facial movements (full DogFACS coding), duration of tail wagging
and time spent at the front of the kennel in close proximity to the
experimenter. The number of days between becoming available
for re-homing and leaving the shelter was recorded. Reliability
assessment was conducted on the behavioural coding (DogFACS
AUs and other behaviours: Table 2) for 30% of the sample (8 dogs)
using Wexler’s Agreement (Ekman et al., 2002):
Table 1. Comparison of action units (AUs) and the underlying facial muscles in humans [20] and dogs.
Action Units Facial Musculature
Humans Dogs Humans Dogs
Upper Face
1Inner brow raiser 101 Inner brow raiser Frontalis (medial) Frontalis is present but it does not seem
to raise the brow region. Levator anguli
occuli medialis raises the inner brow
region.
2Outer brow raiser Not observed Frontalis (lateral) (As above)
4Brow lowerer Not observed Procerus, corrugator supercilii,
depressor supercilii
Not present
5Upper lid raiser Not observed Levator palpebrae superioris Not described
6Cheek raiser Observed only with 143 and 145 Orbicularis occuli Present
7Lid tightener Not observed (As above) (As above)
43 Eye closure 143 Eye closure Relaxation of levator palpebrae
superioris
Orbicularis occuli
45 Blink 145 Blink (As above) (As above)
Lower Face
9Nose wrinkler 109+110 Nose wrinkler and upper lip
raiser - nose wrinkler hard to code
independently
Levator labii superioris
alaeque nasi
Levator nasolabialis, caninus, levator
labii maxillaris
10 Upper lip raiser 110 Upper lip raiser Levator labii superioris (As above)
11 Nasiolabial furrow deepener Not observed Zygomaticus minor Not present
12 Lip corner puller 12 Lip corner puller Zygomaticus major Zygomaticus
13 Sharp lip puller Not observed Caninus Present
14 Dimpler Not observed Buccinator Present
15 Lip corner depressor Not observed Depressor anguli oris Not present
16 Lower lip depressor 116 Lower lip depressor Depressor labii inferioris Platysma
17 Chin raiser Not observed Mentalis Present
18 Lip pucker 118 Lip pucker Incisivii labii (superioris and
inferioris), orbicularis oris
Only orbicularis oris present
20 Lip stretcher Not observed Risorius Not present
22 Lip funneler Not observed Orbicularis oris Present
23 Lip tightener Not observed Platysma Present
24 Lip presser Not observed Orbicularis oris Present
25 Lips part 25 Lips part Orbicularis oris, depressor labii
inferioris, levator labii superioris
Orbicularis oris, caninus, levator labii
maxillaris, levator nasolabialis, platysma
26 Jaw drop 26 Jaw drop Non-mimetic muscles: masseter, temporalis, pterygoid and digastricus
27 Mouth stretch 27 Mouth stretch (As above)
Action Units Facial Musculature
Humans Dogs Humans Dogs
Miscellaneous Action Units
8Lips towards each other Not observed Orbicularis oris Present
21 Neck tightener Not observed Platysma Present
38 Nostril dilator Observed during sniff (AD40) Nasalis Not present
39 Nostril compressor (As above) (As above) (As above)
doi:10.1371/journal.pone.0082686.t001
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2(#AUs on which Coder 1 and Coder 2 agreed)
total #of AUs scored by the two coders
Proximity and tail wagging were treated as categorical variables
by using number of bouts instead of overall duration for the
reliability and agreement was also assessed using Wexler’s
Agreement.
Table 2. Wexler’s agreement calculations for the behavioural
coding.
Behaviour Agreement
EAD101 (ears forward) 0.69
EAD102 (ears adductor) 0.79
EAD103 (ears flattener) 0.73
EAD104 (ears rotator) 0.83
AU101 (inner brow raiser) 0.78
AD19 (tongue show) 0.71
AD137 (nose wipe) 0.86
AU25 (lips parted) 0.91
AU26 (jaw drop) 0.88
Proximity 1.00
Tail wagging 0.76
doi:10.1371/journal.pone.0082686.t002
Figure 2. Relationship between frequency of AU101 and days before re-homing in the dog shelter. Curved line shows the power
estimation.
doi:10.1371/journal.pone.0082686.g002
Table 3. Relationship between behaviours exhibited during
the 2 min observation period and the number of days before
re-homing.
Behaviour Days before re-homing
Spearman’s rho p value
#AU101 (inner brow raise) 2.501 .008
#AU19 (tongue show) .070 .729
#AD137 (nose wipe) .339 .083
#AU25 (lips parted) .262 .187
#AU26 (jaw drop) .268 .176
#EAD101 (ears forward) 2.331 .091
#EAD102 (ears adductor) 2.236 .236
#EAD103 (ears flattener) 2.187 .349
#EAD104 (ears rotator) 2.005 .981
Tail wagging duration .424 .027
Time at front of kennel 2.393 .042
Age (months)
1
.153 .474
1
N = 24 as age was unavailable for some dogs.
doi:10.1371/journal.pone.0082686.t003
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Results
Two dogs were removed as their time before re-homing was
greater than the upper quartile by more than 1.5 IQR (82+87
days), and thus were perceived to be outliers (and their long
stay most likely due to unusual factors). Our final sample
included 27 dogs for analysis (Age range = 7–96 months,
M= 29.46 months). Nonparametric correlations (as the depen-
dent variable was not normally distributed) were used to explore
the relationships between the behavioural variables and the
number of days before re-homing (Table 3). AU101 and time at
the front of the kennel were the only variables significantly
negatively correlated with days before re-homing, indicating that
dogs that produced more of these behaviours were re-homed
quicker. Tail wagging was positively correlated indicating that
dogs that tail wagged more were re-homed slower. Note,
however, that if Bonferroni corrections were applied, no
variables would be deemed significant so these exploratory
findings should be taken with caution. Visual inspection of
scatter plots and curve estimation were used to explore the
relationships further. Time spent at the front of the kennel and
tail wagging had very weak or no linear or curvilinear
relationships with the dependent variable. AU101 had a
significant power curve relationship with the dependent variable
and the model explained a significant proportion of the variance
in re-homing speed (R
2
= 0.39, F(1,25) = 15.63, p,0.005), see
Figure 2. From the regression equation (y = 114.12x
20.515
, see
Table 4) we can predict that a dog that produces five AU101
during the 2 min observation will stay in the shelter for 49.83
days on average, but if it produces 10 AU101, this would be
reduced to 34.88 days, and if it produces 15, this would be
reduced to 28.31 days. As there is a negative power relationship
the slope becomes less steep as AU101 increases, and so the
benefit (in terms of re-homing) in producing AU101 reduces
with increasing AU101.
Discussion
Domestic dogs who produced a high frequency of facial
movement to raise the inner brow (AU101) were adopted more
quickly from re-homing shelters. As AU101 enhances a key
feature of paedomorphism (eye size and height: [10]) this
suggests that dogs have evolved to manipulate the human
preference for paedomorphic features using the face. This is the
first empirical evidence that paedomorphism plays a key role in
humans’ current selection of dogs, and the first time that actual
investment has been used as an indicator of preference. If the
selection process in the shelter context emulates past selection
during domestic dog evolution, this preference may have also
been at work during early dog domestication.
Interestingly, tail wagging and close proximity to the human
were not strongly associated with speed of selection by adopters,
despite being factors that are commonly believed to indicate a
friendly temperament. In fact, higher durations of tail wagging
resulted in a longer period before re-homing. This finding
further supports the growing evidence that indirect manipulation
of human sensory preferences (particularly a preference for
juvenile facial characteristics) has been a particularly powerful
selective force in domestication [2,9], even more so than
genuine indicators of temperament. Importantly, it is highly
possible that these facial expressions do not correlate with
suitability as a pet, but, like superficial morphological traits, are
still preferred over more relevant behavioural traits [26].
In humans, the equivalent facial movement to AU101 is
AU1(inner brow raiser), which features heavily in human
sadness expressions [20]. It is possible, therefore, that human
adopters were responding not to paedomorphism, but instead to
perceived sadness in the dogs looking for adoption. However, it
is also possible that the human sadness expression is itself
derived from paedomorphism, and that sadness is attributed to
this specific facial movement because it enhances paedomorphism
and thus perceived vulnerability. Another possibility is that
humans are responding to the increase in white sclera exposed
in the dogs as the orbital cavity is stretched through AU101
action. Visibile sclera is a largely unique human trait [27]
(which likely contributes to our extensive gaze following abilities)
and people are more likely to cooperate or behave altruistically
when exposed to cues of being watched [28,29]. It is unclear,
however, whether it is the sclera specifically or simply the
presence of eyes per se which has such a powerful affect on
human behavior and attention, and so this is more a
complimentary hypotheses as opposed to an alternative.
Our real world data show that domestic dogs who exhibit
paedomorphic characteristics are preferentially and actively
selected by humans as pets from rehoming shelters. This
therefore supports the hypothesis that paedomorphic character-
istics in domestic dogs arose as a result of indirect selection by
humans rather than only being a by-product of selection against
aggression. Whether our findings are transferable to other
contexts, such as breeding, is unknown, and it is possible that
modern breeding practices put emphasis on such specific
morphological and behavioural traits that this effect is obscured.
However, given that recent evidence leans towards early wolf
domestication arising from tolerance of their presence rather
than direct selection per se [2,3], adoption from shelters might
be a more appropriate proxy than modern breeding. We can
therefore speculate that early domestication of wolves may have
occurred not only as wolf populations became tamer [2,3], but
also as they exploited human preferences for paedomorphic
characteristics.
Supporting Information
Raw Data S1 The raw data.
(SAV)
Acknowledgments
We would like to thank the following for access to their shelter dogs:
Portsmouth City Dog Kennels; Wood Green, The Animal’s Charity in
Cambridge; The Dog’s Trust, West London, Harefield and RSPCA
Southridge Animal Centre, London. We thank Jamie Whitehouse for
reliability coding. We also thank Alison Colyer (Statistics Team,
WALTHAMH) and Ed Morrison for helpful comments on the statistics,
and two anonymous reviewers for constructive help revising the
manuscript.
Table 4. Regression statistics (power curve fit) between
AU101 and the number of days before re-homing, showing
unstandardised co-efficients (B) and the associated standard
error (SE B), standardised co-efficients (b) and significance
values (P).
BSEBbP
(Constant) 114.12 30.26
AU101 2.52 .13 2.62 .001
doi:10.1371/journal.pone.0082686.t004
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Author Contributions
Conceived and designed the experiments: BMW AMB JK. Performed the
experiments: KP CCC LS. Analyzed the data: BMW. Contributed
reagents/materials/analysis tools: AMB. Wrote the paper: BMW JK.
Assisted with study design: SM.
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