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Dog Breed Differences in Visual Communication with Humans

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Domestic dogs (Canis familiaris) have developed a close relationship with humans through the process of domestication. In human-dog interactions, eye contact is a key element of relationship initiation and maintenance. Previous studies have suggested that canine ability to produce human-directed communicative signals is influenced by domestication history, from wolves to dogs, as well as by recent breed selection for particular working purposes. To test the genetic basis for such abilities in purebred dogs, we examined gazing behavior towards humans using two types of behavioral experiments: the ‘visual contact task’ and the ‘unsolvable task’. A total of 125 dogs participated in the study. Based on the genetic relatedness among breeds subjects were classified into five breed groups: Ancient, Herding, Hunting, Retriever-Mastiff and Working). We found that it took longer time for Ancient breeds to make an eye-contact with humans, and that they gazed at humans for shorter periods of time than any other breed group in the unsolvable situation. Our findings suggest that spontaneous gaze behavior towards humans is associated with genetic similarity to wolves rather than with recent selective pressure to create particular working breeds.
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RESEARCH ARTICLE
Dog Breed Differences in Visual
Communication with Humans
Akitsugu Konno
1,2,3
*, Teresa Romero
1,2
, Miho Inoue-Murayama
3
, Atsuko Saito
2
,
Toshikazu Hasegawa
2
1Japan Society for the Promotion of Science, Kojimachi 5-3-1, Chiyoda, Tokyo, Japan, 2Department of
Cognitive and Behavioral Science, The University of Tokyo, Komaba 3-8-1, Meguro, Tokyo, Japan,
3Wildlife Research Center, Kyoto University, Tanaka Sekiden cho 2–24, Sakyo, Kyoto, Japan
*akitsugukonno@gmail.com
Abstract
Domestic dogs (Canis familiaris) have developed a close relationship with humans through
the process of domestication. In human-dog interactions, eye contact is a key element of
relationship initiation and maintenance. Previous studies have suggested that canine ability
to produce human-directed communicative signals is influenced by domestication history,
from wolves to dogs, as well as by recent breed selection for particular working purposes.
To test the genetic basis for such abilities in purebred dogs, we examined gazing behavior
towards humans using two types of behavioral experiments: the ‘visual contact task’ and
the ‘unsolvable task’. A total of 125 dogs participated in the study. Based on the genetic
relatedness among breeds subjects were classified into five breed groups: Ancient, Herd-
ing, Hunting, Retriever-Mastiff and Working). We found that it took longer time for Ancient
breeds to make an eye-contact with humans, and that they gazed at humans for shorter
periods of time than any other breed group in the unsolvable situation. Our findings suggest
that spontaneous gaze behavior towards humans is associated with genetic similarity to
wolves rather than with recent selective pressure to create particular working breeds.
Introduction
Domestic dogs (Canis familiaris) have been living close to humans (Homo sapiens) for at least
15,000 to 50,000 years, a relationship that probably came about through multiple domestica-
tion events [15]. Dogs are currently thought to be one of the best models for understanding
cognitive skills in cross-species communication [69], and a number of studies have focused
on the ability of dogs to comprehend and respond to various types of human communicative
signals (e.g., [6,8,10,11]). For instance, it is known that dogs are able to processmany types of
human gestures including pointing, bowing, nodding, head turning and gazing as cues for find-
ing the location of hidden food [11].
It has been suggested that the skills required by dogs to interact with humans were acquired
through the process of domestication (e.g., [8,12]). Comparative studies of dogs and their clos-
est living relative, the wolf (Canis lups), have shown that hand-reared wolves are less responsive
to human social cues and less prone to showing human-directed gaze signals than domestic
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 1 / 14
a11111
OPEN ACCESS
Citation: Konno A, Romero T, Inoue-Murayama M,
Saito A, Hasegawa T (2016) Dog Breed Differences
in Visual Communication with Humans. PLoS ONE
11(10): e0164760. doi:10.1371/journal.
pone.0164760
Editor: Juliane Kaminski, University of Portsmouth,
UNITED KINGDOM
Received: October 28, 2013
Accepted: October 1, 2016
Published: October 13, 2016
Copyright: ©2016 Konno 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: This research was supported by the
MEXT with a Grant-in-aid for Challenging
Exploratory Research (No. 23650132, to T.H.), and
for Scientific Research on Innovative Areas ’The
Evolutionary Origin and Neural Basis of the
Empathetic Systems’ (No. 25118005 to M.M., No.
25118003 to T.H.) and by the JSPS Research
Fellowships for Foreign Researchers to T.R. (No.
P10311) and for Young Scientists to A.K. (No.
213762 and 243684).
Competing Interests: The authors have declared
that no competing interests exist.
dogs [9,1316]. Studies of captive silver foxes (Vulpes vulpes) also offer an insight into behav-
ioral modification in domesticated canids: fox strains selected for tameness are more sensitive
to human pointing gestures than non-selected individuals [1719]. These findings suggest that
an early divergence from wolves, possibly by artificial selection for tameness, may have had a
significant impact on modern dog’s communicative abilities [8].
However, modern dog’s behavior has been modifiednot only during the early stages of
domestication, but also during a later periodof breed creation [8,20]. Most modern purebred
dogs were established in Europe through an intensive selective breeding process for preferred
behavioral/phenotypictraits about 200 to 500 years ago. At present, the current number of
breeds worldwide has reached almost 400 [2125]. It is important to note that a subgroup of
modern purebred dogs,referred toas ‘Ancient’, ‘Primitive, or ‘Basal’ breeds, have experienced
lower selective pressure. In general, these breeds have kept a high genetic diversity and possess
similar genetic components to wolves due to their earlier isolation [1,21,22,26,27]. Besides this
important characteristic, Ancient breeds have not always been included in studies examining
the evolution of dog communicative skills (but see [2830]). To evaluate the impact of artificial
selection on dog behavior, the diversity of modern purebred dogs, including Ancient breeds,
should be considered.
Examining dog breed differences in behavior could shed light on the acquisition process of
their extraordinary abilities to communicate with humans. Thus, one could hypothesize that if
dog communicative skills developed during the period of the early split betweenwolves and
dogs, then more wolf-like dog breeds (i.e., Ancient breeds) may be less skilled at communicat-
ing with humans [30,31]. This ‘wolf remnant’ hypothesis has been supported by results from
recent studies of two wild dog breeds belonging to the Ancient group (i.e., dingo and New
Guinea singing dog). For instance, while dingoes are able to follow several human gestures in
order to locate hidden food, including tapping, pointing and standing behind the container,
they fail to respond to human gaze cues [31]. Since other breeds are generally successful in
using human gaze signals, Ancient breed performance appears to lie somewhere between that
of wolves and other dogs [30,31]. This suggests that a dog’s ability to comprehend human ges-
tures is associated with genetic closeness to wolves.
An alternative hypothesis for the source of modern dogs’ behavior holds that intensive
selective pressure for particular working purposes has significantly changed their ability to
communicate and interact with humans [28,30]. A recent study has shown that breeds selected
to work in close cooperation with humans (e.g., Shepherds and Huskies) are more effective in
using human pointing gestures than breeds not selected to work with humans (e.g., Basenji and
Toy Poodle) [30]. The authors emphasized that working breeds outperform non-working ones
in this regard independently of being genetically wolf-like. Furthermore, breeds selected to
work in close cooperation and in visual contact with humans (e.g., sheepdogs and gun dogs)
have been proven to be more skilled at reading human pointing gestures than other working
breeds (e.g., hounds and earth dogs) [28]. These findings are in line with the ‘working purpose’
hypothesis, which states that breed selection for specific types of cooperative activity with
human partners has contributed a large degree to the communicative behavior of dogs.
Compared to the skills usedin responding to human-given cues, dogs ability to produce
communicative signals towards humans has received much less attention and only recently a
few studies have begun to focus on this topic. It has been shown that hand-reared wolves are
less inclined to show gaze signals towards humans in a problem-solving situation than domes-
tic dogs [16]. Based on this finding, Passalacqua et al. [29] examined the potential effect of
breed groups (Primitive, Hunting/Herding and Molossoid groups) on spontaneous gazing
behavior towards humans when the dog also faced a problem-solving situation. Contrary to
the authors’ prediction that Primitive breeds would be less prone to showing human-directed
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 2 / 14
gazing behavior (i.e., the ‘wolf remnant’ hypothesis), Primitive and Molossoid groups showed
similar gazing behavior while both groups were outranked by Hunting/Herding breeds. On the
other hand, studies evaluating gaze responses in a direct human-to-dog feeding interaction
(with food in sight but out of reach)found significantbreed differencesin human-directed gaz-
ing behavior (e.g., [32][33]). For instance, in one study, Retrievers (a hunting breed specialized
in retrieving prey) spontaneously gazed at humans for longer periods of time than German
Shepherds (a herdingor livestockprotecting breed) or Poodles (a companion breed) [34].
Although these results seem to support the ‘working purpose’ hypothesis, the limited number
of breeds and workingtypes included in these studies does not allow any firm conclusion to be
drawn.
In summary, previous data from studies on breed differences in communicative behavior
provides partial support for both the ‘wolf remnant and the ‘working purpose’ hypotheses, and
hence it is not clear whether genetic similarity to wolves or to working types has a greater influ-
ence on modern dogs’ abilities to communicate with humans. Given that spontaneous gazing
at humans can facilitate the initiation and maintenance of dog-human communication and
bonding [16,32,33,35], further research examining how the domestication process has contrib-
uted to modern dog’s use of gazing behavior towards human is warranted.
The aim of the present study was to estimate the influence of selectivepressures on the abil-
ity of dogs to spontaneously produce communicative signals such as eye contact and gazing
towards humans. In particular, we predict that if the genetic remnant of wolves has a signifi-
cant influence on modern dog’s behavior then Ancient breeds would show less human-directed
gazing behavior than other purebred dogs. In contrast, if selection for some specificworking
purposes had a significant influence in the development of dog communicative abilities, then
particular working breed groups would display a greater capacity for human-directed gazing
behavior. Although dog’s genetic similarity with wolves and its selection history for working
purposes has been closely intertwined, the recently published data on the genetic clustering of
dog breeds brings a tentative solution to estimate indirect impact of genetic factors on dog’s
behavior [21].
To advance the current scarcity of data on the production of communicative signals by
dogs, the present study aims to address some of the methodological issues of previous studies.
Firstly, we tested a wide range of 26 pure breeds including major modern pure breeds as well as
ancient breeds. These breeds were further classified into broader breed groups (i.e., Ancient,
Herding, Hunting, Retriever-Mastiff and Working) that cluster genetically clusters according
to recent genomic analysis [21]. Grouping breeds in this way is important in order to estimate
the possible effect of selective pressures that may be shared by more than one breed, as well as
to compare inter-breed variation in ability to exchange communicative signals with humans.
Secondly, we used two different experimental paradigms to draw spontaneous gaze responses
towards humans when requesting out-of-reach food rewards: the ‘unsolvable task’ and the
‘visual contact task’. The use of multiple behavioral tasks allows us to examine whether each
breed group has a consistent behavioral pattern for sending communicative signals to humans
independently of the situation or task. Finally, for comparative purposes, we will also analyze
our data using the same breed classification used in the previous study that examined dogs’
communicative abilities in a relatively large number of breeds [29].
Materials and Methods
Ethical Statement
The current study was conducted in strict accordance with the ‘Guidelines for the Treatment of
Animals in Behavioural Research and Teaching’ by the Animal Behavior Society/Association
Dog Breed Differences in Human-Directed Gaze
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for the Study of Animal Behaviour, and was approved by the ethical committee at the Wildlife
Research Center, Kyoto University (WRC2010EC001). Dogs were recruited through advertise-
ments in veterinary clinics, trimming salons, local parks and breed specialists. Signed informed
consent for participation in this study was obtained from the owners.
Subjects
All subjects were purebred dogs living as companion animals at their owner’s home. Highly
trained dogs (i.e., dogs that engage in sport activity with their owners such as agility, disc, and
other games and/or dogs that have training experience for working purpose) were not included
in this study. A total of 125 adult dogs participated in this study. Subjects comprised 60 females
and 65 males from 26 different breeds. Five dogs (1 Border Collie,1 Doberman,1 Portuguese
Water Dog, and 2 Shiba Inu) were excluded from the analysis because they were not able to
complete the behavioral experiments: two dogs did not take the food rewards from the experi-
menter’s hand, and the other three never approached the apparatus used in one of the experi-
ments. As a result,120 dogs consistingof 57 females and 63 males with a mean age of 68.26
months (5.67 years old) were included in this study (Table 1).
Based on the recently published data on the genetic clustering of dog breeds [21], subjects
were classified into five breed groups: Ancient, Herding, Hound, Retriever-Mastiff and Work-
ing. The Ancient group consisted of five breeds with similar genetic components to gray wolves
[1,21,22], and that were originally from outsidecentral Europe (i.e., Middle-EastAsia, East
Table 1. Breed and breed group sample size (N), sex (F: female, M: male), and mean age (years) of dogs tested in the present study.
Breed Group Breed NSex Age
Ancient Afghan Hound 4 F = 2, M = 2 6.79
(N= 24) Akita Inu 8 F = 5, M = 3 3.47
Saluki 2 F = 2 2.50
Shiba Inu 5 F = 3, M = 2 6.83
Siberian Husky 5 F = 4, M = 1 6.53
Herding Border Collie 12 F = 3, M = 9 6.90
(N= 23) Welsh Corgi 10 F = 5, M = 5 8.50
Australian Shepherd 1 M 7.33
Hound Beagle 5 F = 3, M = 2 8.12
(N= 22) Borzoi 4 F = 3, M = 1 2.58
Dachshund 6 F = 3, M = 3 9.05
Irish Wolfhound 1 M 1.33
Italian Greyhound 6 F = 2, M = 4 6.13
Retriever-Mastiff Bernese Mountain Dog 5 F = 4, M = 1 5.08
(N= 24) Flat-coated Retriever 2 F = 2 4.42
Golden Retriever 6 F = 3, M = 3 5.51
Labrador Retriever 8 F = 6, M = 2 6.92
Mastiff 1 M 1.58
Newfoundland 1 M 1.00
Staffordshire 1 M 1.08
Working Doberman 5 F = 2, M = 3 6.35
(N= 27) German Shepherd 5 F = 3, M = 2 4.50
Standard Poodle 5 F = 2, M = 3 2.62
Toy Poodle 11 F = 2, M = 9 4.72
Portuguese Water Dog 1 F 2.83
doi:10.1371/journal.pone.0164760.t001
Dog Breed Differences in Human-Directed Gaze
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Asia or Siberia). The other four breed groups included 21 breeds originally from European
countries that differed in their primary use (i.e., working function) as well as genetic related-
ness [21].
Behavioral Experiments
To evaluate breed differences in producing visual signals, we tested the dog’s spontaneous gaze
at human faces using two experimental tasks: the visual contact task and the unsolvable task
(see S1 and S2 Movies). Small pieces of food (e.g., chipped beef) were used as rewards in both
tasks. To test the dog’s motivation for the reward, the experimenter offered the dog one piece
of food before and after each task, confirming that all dogs were highly attracted to the reward.
Each dog was tested separately in a familiar environment (e.g., in a room (N= 115) or garden
(N= 5) at the owner’s home) with no leash. In all cases, the test was carried out in a restricted
area of at least 2 square meters. To counterbalance the effectof order of task, half of the subjects
was given the visual contact task first, and the other half of the subjects was given the unsolv-
able task first. This counterbalancing procedure was conducted for each breed group. The
owner was present throughout the experimentalsession and was instructednot to give any
feedback to the dog for any of its responses. All experimental sessions were videotaped.
Visual Contact Task. The visual contact task used in this study is a modification of the
one used in Study 2 by Jakovcevic et al. [34]. The task consisted of two phases lasting 90 sec-
onds each. In the first warm-up phase, the experimentermoved around the test area while call-
ing the dog’s name and making physical contact with the dog in a friendly manner. The dog
was off leash and free to movingaround the testingarea. During thisphase, the subject received
at random intervals (mean 14.56 seconds) a total of four pieces of food directly from the hand
of the experimenter. Food rewards were placedin a container visible to the subject but out of
his/her reach. To focusthe dog’s attention towards the feeding place, the experimenterstood at
the exact same position, i.e., next to the food container, when giving the food rewards to the
subject. Importantly, during this warm-up phase, the experimenter avoided any eye contact
with the dog.
Right after the 90-second warm-up phase had elapsed, the test phase started. At this point,
the experimenter took one last piece of food and gave it to the dog while standing by the food
container. Immediately after that, the experimenter stopped moving and initiated eye contact
with the dog. The experimenterofferedcontinuous eye contact but the dog was able to move
freely and was not forced to make and/or maintain eye contact with the experimenter until the
end of the second phase. The dog’s gaze responses during the second phase were subjected to
analysis.
Unsolvable Task. The ‘unsolvable task’ [16] consisted of six consecutive ‘solvable trials
(i.e., the dog could reach the food reward) followed by a single ‘unsolvable trial. The experi-
mental apparatus comprised a 12 × 20 cm transparent plastic container and a 30 × 30 cm
wooden board. After calling the dog’s name, the experimenter set a piece of food at the center
of the wooden board and then put the plastic container over it. The bait of the apparatus was
visible to the dogs, but out of their reach (i.e., the experimenter held up the apparatus in front
of his/her face while baiting it, and prevented the dogs from touching the apparatus). The
experimenter then placedthe apparatus on the ground so that the subject was able to manipu-
late it and get the food reward by removing the container. During the solvable trials all dogs
learned how to get the food reward from the apparatus. After the sixth solvable trial, the experi-
menter presented to the dog one unsolvable trial in which the container was fixed to the
wooden board in such a way that the dog could not get the food anymore. During the unsolv-
able trial, both the experimenterand the owner stood quietly behindthe dog at a distance of
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 5 / 14
approximately 1.5 m, while the dog (off leash during the whole experimental session) was free
to move around the experimentalarea. The owner was instructed not to respond to any of the
dog behaviors except for eye contact. The dog’s behavior was recorded for 60 seconds after the
unsolvable trial was presented.
Analysis
The dog’s behavior in the two experiments was coded based on the subsequent video analysis.
Behavioral coding was made on the 0.3-second time scale by two independent observers naïve
to the purpose of the study.
For the visual contact task, we measured: (1) duration of the first gazing (i.e., time from the
moment the dog turned/liftedits head towards the experimenter for the first time until the
moment it turned its head away from him), and (2) total duration of gazing at the experimenter
during the 90-second test phase.
For the unsolvable task, we measured three behavioral variables: (1) latency to the first gaz-
ing (i.e., the time elapsed from the moment the unsolvable trial started to the moment the dog
turned/lifted its head for the first time back towards the experimenter or the owner), (2) total
duration of gazing at the person, and (3) total duration of physical contact with the apparatus
(i.e., the time the dog spent manipulating the apparatus including touching, scratching, push-
ing, sniffing and licking). To evaluate the general tendency of the dog’s gaze responses towards
humans, gazing at the experimenter and gazing at the owner were combined.
A subset of the videos (N= 30; 25.0%) was randomly selected and coded by an observer
naïve to the purpose of the study. Inter-observer reliability testing using Cohens Kappa indi-
cated a strong agreement between coders (visual contact task, first gazing duration: k= 0.691,
p<0.001; total gazing duration: k= 0.935, p<0.001; unsolvable task, latency to the first gaz-
ing: k= 0.760, p<0.001; total gazing duration: k= 0.862, p<0.001; total duration of apparatus
manipulation: k= 0.715, p<0.001).
To examine the effect of breed group on the dog’s gaze responses, we used generalized linear
models (GLM). The explanatory variables were breed group (Ancient, Herding, Hound,
Retriever-Mastiff or Working), age, their interaction, and sex, while the response variables
comprised each of the five behavioral variables. According to the distribution of the response
variables, we applied the negative binomial error structure with log link function for the five
behavioral variables. ‘Ancient’ and ‘female’ were entered as reference categories when con-
structing the parameter estimates (ß) using GLM. To test the fixed effect of each explanatory
variable, the likelihoodratio test with chi-square statistics was carried out (type III test). We
used the Steel-Dwass test as a supplementary post-hoc test. Effect of age was estimated by calcu-
lating Spearmans ρ or Pearsons r. Analyses were run on R version 2.15.2. (R foundation for
Statistical Computing).
Results
Visual Contact Task
During the test phase, all dogs except for one male Siberian Husky made eye contact with the
experimenter at least once. None of the explanatory variables (i.e., breed group, ß= -0.09 [vs.
Hound] to 0.60 [vs. Working]; age, ß= 0.00; breed group x age, ß= 0.00 [vs. Retrievers] to 0.01
[vs. Herding]; sex, ß= 0.04, P>0.05) have a significant effect on duration on first gaze (Tables
2and 3). We found a significant age-effect on the total duration of gazing behavior (ß= 0.01,
P= 0.047), with older dogs gazing for longer than younger ones (Spearmans ρ= 0.289,
P= 0.001) (Tables 2and 3). However, breed group (ß= 0.56 [vs. Retrievers] to 0.85 [vs.
Hound], P= 0.212), breed group x age interaction (ß= -0.01 [vs. Hound] to -0.00 [vs.
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 6 / 14
Working], P= 0.582), and dog’s sex (ß= -0.00, P= 0.215) did not have any significant effect on
total gazing duration (Tables 2and 3).
Unsolvable Task
During the unsolvabletrial, 4.2% of the subjects(two Akita Inu, one Border Collie, one Borzoi,
one Labrador Retriever and one Toy Poodle) never looked at the experimenter or the owner.
We found a significantdifference in thelatency to the first gazeaccordingto breed group (ß=
Table 2. Mean (in seconds) of the behavioral variables according to the different breed groups. Standard deviation is shown in parentheses.
Ancient Herding Hound Retriever Working
Visual contact task
The first gazing 6.98 11.70 10.74 9.49 14.90
(10.22) (12.81) (12.24) (8.76) (13.24)
Total gazing 34.16 54.59 46.35 47.20 50.79
(29.42) (18.23) (26.97) (21.56) (27.94)
Unsolvable task
Latency of the first gazing 29.90 18.96 17.41 12.52 14.86
(19.62) (15.55) (15.94) (12.02) (16.23)
Total gazing 4.28 12.80 13.59 17.12 14.90
(6.52) (8.48) (12.25) (13.35) (13.59)
Contact with apparatus 36.71 33.27 29.98 22.98 30.87
(19.50) (15.74) (17.87) (16.15) (18.64)
doi:10.1371/journal.pone.0164760.t002
Table 3. Results of the GLMs showing the effect of each explanatory variable (i.e., breed group, age, breed group x age, and sex) on dog’s com-
municative behaviors. Significant results (p<0.05) are shown in bold.
Response variables Explanatory variables df Deviance P
Visual contact task
The first gazing Breed group 4 2.13 0.712
Age 1 0.12 0.734
Breed group *Age 4 0.74 0.947
Sex 1 0.05 0.820
Total gazing Breed group 4 5.84 0.211
Age 1 3.94 0.047
Breed group *Age 4 2.85 0.582
Sex 1 1.54 0.215
Unsolvable task
Latency of the first gazing Breed group 4 21.42 <0.001
Age 1 0.57 0.449
Breed group *Age 4 8.89 0.064
Sex 1 0.38 0.538
Total gazing Breed group 4 12.42 0.014
Age 1 0.35 0.555
Breed group *Age 4 3.53 0.474
Sex 1 0.09 0.767
Contact with apparatus Breed group 4 1.66 0.798
Age 1 1.12 0.290
Breed group *Age 4 1.91 0.753
Sex 1 0.01 0.933
doi:10.1371/journal.pone.0164760.t003
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-0.64 [vs. Hound] to -1.49 [vs. Working], P= 0.000) with Ancient breeds gazing later than
Retrievers (Steel-Dwass test, P= 0.012) and Working breeds (Steel-Dwass test, P= 0.033)
(Tables 2and 3,Fig 1). Dog’s sex (ß= -0.10, P= 0.378), age (ß= -0.00, P= 0.449), and the inter-
action of age x breed group (ß= 0.00 [vs. Hound] to 0.01 [vs. Working], P= 0.064) did not
have any significant effecton the latency to the first gaze (Table 3).
For the total duration of gazing, we found a significanteffect of breed group (ß= 1.12 [vs.
Hound] to 1.85 [vs. Working], P= 0.015) with Ancient breeds gazing for shorter periods of
time than Herding (Steel-Dwass test, P= 0.002), Hound (Steel-Dwass test, P= 0.002), Retriev-
ers (Steel-Dwass test, P<0.001) and Working breeds (Steel-Dwass test, P= 0.011) (Tables 2
and 3,Fig 2). However, dog’s sex (ß= -0.05, P= 0.766), age (ß= 0.00, P= 0.555), and the inter-
action of age x breed group (ß= -0.01 [vs. Working] to -0.00 [vs. Hound], P= 0.474) did not
have any significant effect (Table 3).
Finally, the mean duration of physical contact with the apparatus was not affected by any of
the three explanatory variables included in the analysis (i.e., breed group, ß= -0.31 [vs. Retriev-
ers] to 0.03 [vs. Hound]; age, ß= 0.00; breed group x age, ß= -0.00 [vs. Hound] to 0.00 [vs.
Working]; sex, ß= 0.01, P>0.05, Tables 2and 3).
Fig 1. Mean latency (in seconds) to the dog’s first gazing behavior towards humans in the unsolvable task
according to dog breed groups. Box-plot depicts subject’s minimum and maximum (whiskers) excluding outliers
(blank circles), lower and upper quartiles (edge of the boxes), and medians (line across the box).
doi:10.1371/journal.pone.0164760.g001
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 8 / 14
Comparison with a previous study
We then followed the classification of Passalacqua et al. [29] and re-ran the analysis using only
the dog breeds that wereused in theirstudy (Primitive [Akita Inu, Shiba Inu, Siberian Husky]:
N= 19, Hunting/herding [Australian Shepherd, Beagle, Border Collie, Duchshund, Flat-coated
Retriever, GoldenRetriever, Labrador Retriever,]: N= 40, Molossoid [Bernese Mountain Dog,
Staffordshire, German Shepherd]: N= 11). Nevertheless, the results were in accordance with
our findings that Ancient breeds gazed at humans for a shorter period of time (see S1 Table.
Visual contact task: Steel-Dwass test, Total gaze duration: Primitive vs. Hunting/Herding,
P= 0.033, Primitive vs. Molossoid, P= 0.830, Hunting/Herding vs. Molossoid, P= 0.342;
Unsolvable task: Steel-Dwass test, Latency of the first gaze: Primitive vs. Hunting/Herding,
P= 0.008, Primitive vs. Molossoid, P= 0.044, Hunting/Herding vs. Molossoid, P= 0.949; Total
gaze duration: Primitive vs. Hunting/Herding, P<0.001, Primitive vs. Molossoid, P= 0.102,
Hunting/Herding vs. Molossoid, P= 0.702). Furthermore, in contrast to Passalacqua et al. [29],
there was no significant difference between Hunting/Herding and Molossoid breeds in any
communicative behavior in this additional analysis.
Fig 2. Mean total duration (in seconds) of dog’s gazing behavior towards humans in the unsolvable task
according to dog breed groups. Box-plot depicts subject’s minimum and maximum (whiskers) excluding outliers
(blank circles), lower and upper quartiles (edge of the boxes), and medians (line across the box).
doi:10.1371/journal.pone.0164760.g002
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 9 / 14
Discussion
To estimate the influence of selective breeding on modern dog’s ability to exchange visual com-
municative signals with humans, the present study examined potential breed group differences
in human-directed gazing behavior using two behavioral tasks. During the tests, almost all
dogs gazed spontaneously at humans suggesting that modern domestic dogs frequently send
visual signals to humans as communicative cues when seeking food rewards [16,36].
However, not all breeds were equally prone to using these social cues. We found that it took
longer for Ancient breed dogs to establish eye contact with humans, and that they gazed at
human faces for shorter periods of time than other breed groups in the unsolvable situation. It
could be argued that these inter-breed differences are merely the result of inter-individual dif-
ferences in motivation for seeking food rewards and/or the dog’s persistency to engage in a
problem-solving task [37,38]. However, this is unlikely since breed differences were not found
in the duration of physical manipulation of the apparatus during the unsolvable task, and all
dogs consumed the piece of food offered by the experimenter at the end of the experimental
sessions. Thus, these results suggest that the level of engagement in the unsolvable task did not
differ according to breed groups, but that Ancient breeds were particularly less prone to use
gaze signals with humans even though they are equally motivated to seek the reward.
To explore situation-dependency of behavioral patterns among the different breed groups,
we used multiple behavioral tasks. Results indicated that a statistically significant effect of
breed group was found only in the unsolvable situation. Thus, dog breed differences in human-
directed gazing behavior seem to vary depending on task or situation. In the visual contact task
humans gaze preceded dog’s gaze, and the dogs had only to keep eye-contact with humans for
begging for the reward. On the other hand, in the unsolvable task the dogs had to divert their
attention from the experimental apparatus and spontaneously produce gazing behavior–turn
back and look at the humans–in an attempt to send them communicative signals. The latter
could be considered more complex due to the involvement of a problem-solving component,
and the maintenance of the dogs gaze was lower than in the former (i.e.,the allocation of time
in human-directed gazingwas shorter in the unsolvabletask [20.96%] than in the visual con-
tact task [51.85%]; Steel-Dwass test, P<0.001). It is possible that, regardless of breed group
difference, dogs have commonly developed an ability to maintain eye-contact with humans in
response to human-given gaze, whereas dog’s ability for spontaneously producing gazing
behavior towards humans has been partially influenced by genetic factors associated with
breed clustering.
Previous studies using the ‘unsolvable task’ yielded similar results when analyzing species or
breed differences in the use of gaze signals towards humans. Miklósi et al. [16] found that
wolves showed a longer latency to the first gazing behavior, and a shorter duration of total gaz-
ing towards humans compared to domestic dogs. Passalacqua et al. [29] examined breed differ-
ence in human-directed gazing behavior and reported that Primitive breeds, which were
comparable to Ancient breeds used in this study, gazed at humans for shorter periods of time
than Hunting/Herding breeds, although the total duration of gazing behavior did not differ
between Primitive and Molossoid breed groups. Together with our results on Ancient breeds,
these findings support the ‘wolf-remnant’ hypothesis since both non-domesticated canine spe-
cies and Ancient dog breeds are less likely to produce spontaneous gaze signals towards
humans.
Recent genomic studies of modern purebred dogs have identified major breed clusters dis-
tinguishing dogs with similar genetic signatures to wolves (i.e., Ancient breeds) from those
under more recent intense artificialselection [21,22]. In the present study, we found a clear
behavioral distinction between Ancient breeds and other breed groups, which corresponds to a
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 10 / 14
larger genetic distance between them. Given that dogs of the Ancient breed group are diverse
in geographical origin, morphology and working purpose [1], it is likely that a genetic compo-
nent shared among those breeds (i.e.,genetic similaritywith wolves) may have a significant
impact on dog’s human-directed gazing behavior. Thus, that Ancient breeds engaged in less
gazing behavior suggests that a dog’s communicative ability to convey visual signals to humans
may be linked to their geneticsimilarity to wolves, providing furthersupport to the ‘wolf rem-
nant’ hypothesis.
The idea that canine behavior has been significantly altered by divergence between wolf-like
Ancient breeds and other modern primary breeds is also supported by several sources of pub-
lished data on the sensitivity of dogs to human-given social cues. Studies on wild dog breeds,
which have experiencedless of artificial selection,have shown that although dingoes and New
Guinea singing dogs are able to respond to human social cues they seem to be less sensitive
than other domestic dogs [30,31]. Therefore, it seems plausible that a dog’s predisposition for
communicating with humans has been enhanced by the artificial selection involved in the crea-
tion of modern European breeds [30,31].
However, other studies of breed differences have reported a greater influence of selective
breeding on a dogs social cognitiveskills involved in specific ‘cooperative’ work with humans
such as retrieving prey, hunting with human partners and herding or guarding sheep [28
30,34]. This ‘working purpose’ hypothesis is supported by the findings of the study by Passalac-
qua et al. [29] in which the Hunting/Herding group was found to look towards humans for lon-
ger times than the Primitive or the Molossoid breeds. In contrast, the current study showed no
clear differences within the different types of working groups (Herding, Hunting, Retriever-
Mastiff and Working). The discrepancy among the studies could be due to the different catego-
ries of breeds used in each study. Perhaps the inclusion of different breeds may have lead to the
discrepant results. For instance, the three mastiff-type breeds (Boxer, Bull Terrier, and Rottwei-
ler) that were included and classified as Molossoid breeds in Passalacqua et al. [29] were not
present in our study.
It is possible that the complicated breeding history of modern purebred dogs makes it hard
to detect any clear geneticor behavioral signature created duringthe selection process for par-
ticular working purposes. In fact, researchers are faced with the difficult challenge of estimating
a single original purpose along with the resulting selective force for each breed [20]. For
instance, the German Shepherd is thought to be originally bred for herding and guarding live-
stock but subsequently has also been used for search and rescue, as well as for police and mili-
tary roles [24,25]. Moreover, the current breeding of show dogs and companion dogs may be
also associated with modifying behavioral traits in purebred dogs, an idea that has recently
received support from a study on dog’s personalities [39]. If this is the case, then lineage differ-
ences within a single breed could also lead to behavioral differences. Since modern purebred
dogs have been established through various selective pressures at different points during their
breeding history, the domestication of dogs can be considered to be still in progress [20,39].
Further investigations focusing on a more detailed analysis of breeding processes is warranted
to elucidate the influence of a specific selective pressure on canine behavior. For instance, with
the further progress in canine genomic study, it would be important that future studies take
into account the actual genetic distance of each particular breed from the wolf.
Our results also show an effect of age on the use of visual signalstowards humans, which
may reflect the effect of a dog’s prior experiences on communication with humans. The present
study tested only adult dogs (more than 12 months old), with the assumption that their behav-
ior has already been fully formed by social experience through everyday interaction with their
human partners. We found that older dogs gazed for longer times at the experimenter in the
visual contact task. This result may be in line with previous findings showing that dog’s
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 11 / 14
performance is associated with living conditions and early experiences [4042]. For instance,
household dogs gaze at humans for longer than shelter-housed dogs in a similar visual contact
situation [41]. Moreover, while dog’s performance utilizing human gestural cues to locate hid-
den food appears at an early age and does not improve with developmental changes [15], dog’s
use of gazing behavior towards humans greatly improves with age [29]. Although all subjects
were household pet dogs that had not received any professional training, we cannot rule out
the possibility that differences in everyday interaction with their owners and/or previous expe-
rience in requesting help from humans could have accounted for part of the observed variabil-
ity. In fact, it is likely that the ability to interact with humans has been shaped by a complex
interaction between the breed’s inherited character and the individual dog’s experience during
ontogeny [7,29,43]. Further research should try to evaluate the degree to which prior experi-
ence in similar scenarios (e.g., how much they beg for food while their owners are eating) is rel-
evant, and incorporate that measure into the analyses.
In conclusion, the present study shows that dog breed difference in human-directed gazing
behavior between Ancient breeds and other breed groups is much larger than those among
non-Ancient purebred breeds. This pattern is particularly apparent in the unsolvable situation,
with Ancient breeds less prone to sending spontaneous gaze signals towards humans than
other European breeds. Our findings suggest that cross-specific communicative ability is
acquired during an earlier split between wolf-like Ancient breeds and other primary breeds,
although it might have been enhanced over the course of breed creation, which continues up to
the present day.
Supporting Information
S1 Movie. A video example of visual contact task.
(MP4)
S2 Movie. A video example of unsolvable task.
(MP4)
S1 Table. Results of the GLMs showing the effect of each explanatory variable (i.e., breed
group [Primitive, Hunting/Herding, Molossoid], sex, and age) on dog’s communicative
behaviors. Breed group are categorized according to Passalacqua et al. [29]. Significant results
(p<0.05) are shown in bold.
(DOCX)
Acknowledgments
We thank Jessie Cope and Kodai Kimura for their technical support, and the dogs as well as
their owners for their participation in the study.
Author Contributions
Conceptualization:AK TR MI-M AS TH.
Formal analysis: AK.
Funding acquisition: AK TR MI-M TH.
Investigation: AK TR.
Methodology: AK TR.
Project administration: MI-M TH.
Dog Breed Differences in Human-Directed Gaze
PLOS ONE | DOI:10.1371/journal.pone.0164760 October 13, 2016 12 / 14
Supervision: MI-M AS TH.
Writing – original draft: AK TR.
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Dog Breed Differences in Human-Directed Gaze
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Supplementary resource (1)

... The dogs' human-directed gazing behavior has been interpreted as a social problem-solving strategy, and as a request for help from the human [27,34,37,38]. This behavior shows individual and breed variation [39] and seems to also have a genetic component [40,41]. ...
... Two studies have reported that female dogs show more human-directed contactseeking behavior during an unsolvable problem compared to males [40,41]. However, one study failed to replicate these findings [39], and another study found no sex differences in human-directed gazing during a solvable problem [42]. In general, female dogs spend more time gazing at their owner or engaging in social interactions with people in various situations [43][44][45][46][47]. ...
... Our results showed that female dogs spent a significantly longer time behaving socially toward a human during the unsolvable task compared to males, which spent significantly longer attempting to solve the problem independently. Our results are consistent with those found in previous studies investigating dog behavior during an unsolvable task [40,41], although one study [39] did not replicate these findings. ...
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... In our study, herding dogs showed a much longer eye contact duration during UPT compared to the other breed groups, which is in line with Passalacqua et al. (2011). However, we found no difference between the ancient breed group and the solitary hunting breeds, indicating that not only relatedness to the wolf affects the eye contact-seeking behaviour as suggested by Konno et al. (2016), but also selection and function of the dog breed as suggested by Passalacqua et al. (2011). In Passalacqua et al. (2011) both herding dogs and retrieving breeds are grouped together as a Fig. 2 Mean duration (s ± 1SE) of a eye contact-seeking behaviour, b proximity, c physical contact, towards the owner and the stranger, and d interaction with the test apparatus, for ancient breed group, solitary hunting dogs and herding dogs *** p < 0.001, ** p < 0.01, * p < 0.05, (*) p < 0.1 hunting/herding group, which might give the impression that all hunting breeds are selected for human cooperation and show much human contact. ...
... In Passalacqua et al. (2011) both herding dogs and retrieving breeds are grouped together as a Fig. 2 Mean duration (s ± 1SE) of a eye contact-seeking behaviour, b proximity, c physical contact, towards the owner and the stranger, and d interaction with the test apparatus, for ancient breed group, solitary hunting dogs and herding dogs *** p < 0.001, ** p < 0.01, * p < 0.05, (*) p < 0.1 hunting/herding group, which might give the impression that all hunting breeds are selected for human cooperation and show much human contact. Our solitary hunting dogs gazed only short durations towards humans during the UPT, which is also different from the hounds in Konno et al. (2016) that found similar gazing durations for all breed groups except for the ancient breeds that gazed the least. In both studies the experimenter was training the dogs in solvable tasks before the task was made unsolvable. ...
... Even though we did not find any sex differences and, therefore, pooled the data, there might be a skewness that affects the results. However, in studies testing for possible sex differences in UPT, sex has been suggested to have little effect on the gazing behaviour (Konno et al. 2016;Passalacqua et al. 2011;Persson et al. 2015;Sommese et al. 2019;Topál et al. 1997) but note that female laboratory beagles show higher proximity to humans than male beagles (Persson et al. 2015). ...
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The communicating skills of dogs are well documented and especially their contact-seeking behaviours towards humans. The aim of this study was to use the unsolvable problem paradigm to investigate differences between breed groups in their contact-seeking behaviours towards their owner and a stranger. Twenty-four dogs of ancient breeds, 58 herding dogs, and 17 solitary hunting dogs were included in the study, and their behaviour when presented with an unsolvable problem task (UPT) was recorded for 3 min. All breed groups interacted with the test apparatus the same amount of time, but the herding dogs showed a longer gaze duration towards their owner compared to the other groups and they also preferred to interact with their owner instead of a stranger. Interestingly, the solitary hunting dogs were more in stranger proximity than the other groups, and they also showed a preference to make contact with a stranger instead of their owner. Hence, we found differences in contact-seeking behaviours, reflecting the dog–human relationship, between breed groups that might not only be related to their genetic similarity to wolves, but also due to the specific breeding history of the dogs.
... In studies on the communication and cognitive abilities of dogs in a social context, much more emphasis has been placed on the analysis of visual communication [43][44][45][46][47][48][49][50][51] than olfactory abilities [52]. We do not know exactly how strongly dogs base their orientation in the environment on olfactory cues, but we have a conviction about the enormous possibilities of perceiving a dog's sense of smell [53]. ...
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... Study 2 reported only certification status. Evidence suggests that dog breed explains some of the variability in human-canine bonding and communication (Konno et al., 2016) and is thus an important control variable. ...
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Evidence suggests that cognitive assessments can evoke feelings of stress for some children, potentially inhibiting cognitive performance and undermining the validity of results. Dogs have been found to be an unobtrusive form of social support for children in other settings, potentially offering a solution to this problem. The aim of this paper was to critically review the literature to explore what effect, if any, dogs may have on children’s performance on cognitive tests, and consider implications for clinical practice. To do so, five databases were systematically searched and returns were screened for eligibility. Studies were collectively described and then appraised using a common appraisal framework. Nine studies exploring the relationship between dogs and cognitive functioning in children (≤18 years) were identified in the literature search. All used an experimental methodology and were of good to fair quality. Together, results indicated that the presence of a dog could reduce stress and enhance cognitive performance across various domains, lending experimental evidence to support the idea that dogs may support children undergoing cognitive assessments. Further trials are now required to explore the generalizability of these associations to clinical settings and implications for test validity. Further implications for policy and practice are discussed.
... Cooperative working breeds, such as herding dogs, appear to have a higher propensity for human-directed gazing during unsolvable tasks than those bred for working independently (reviewed in Lazarowski et al. 2020). Furthermore, breeds considered as "primitive" or "wolf-like", such as the Czechoslovakian wolfdog, tend to gaze less at humans than other breed groups, including herding dogs, hounds, retrievers, and working breeds (Passalacqua et al. 2011;Konno et al. 2016;Maglieri et al. 2019;Sommese et al. 2019). Nonetheless, results have not been consistent across studies. ...
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Dogs are renowned for ‘looking back’ at humans when confronted with a problem, but it has been questioned whether this implies help-seeking or giving up. We tested 56 pet dogs from two breed groups (herding dogs and terriers) in a modified unsolvable task paradigm. One reward type (food or toy) was enclosed in a box, while the respective other reward was accessible. With both reward types, human-directed gazing in relation to the box was significantly positively correlated with interaction with the box, as long as an alternative was available. This suggests that both behaviours served to attain the unavailable reward and reflected individual motivation for the inaccessible vs the accessible reward. Furthermore, we varied whether the owner or the experimenter was responsible for handling the rewards. In the owner-responsible group, dogs rarely gazed at the experimenter. In the experimenter-responsible group, dogs preferentially directed box-related gazing (prior to or after looking at or interacting with the box) at the owner. Still, they gazed at the experimenter significantly longer than the owner-responsible group. Conversely, toy-related gazing was directed significantly more at the experimenter. Thus, dogs adjust their gazing behaviour according to the people’s responsibility and their current goal (help-seeking vs play). Gaze duration did not differ between herding dogs and terriers. We conclude that dogs use gazing at humans’ faces as a social problem-solving strategy, but not all gazing can be classified as such. Dogs’ human-directed gazing is influenced by the social relationships with the persons, situational associations, and context (unsolvable problem vs play).
... Many studies with some variation of methodologies (Mendes et al., 2021a) investigated factors affecting human-directed gazing. Older dogs seem to use it more often than pups (Passalacqua et al., 2011;Lazarowski et al., 2019); intensively stimulated agility and search and rescue dogs use it more than untrained dogs (Marshall-Pescini et al., 2009;D'Aniello et al., 2015), as well as dogs participating in animal-assisted interventions (Cavalli et al., 2019); breed groups seem to have an influence, with ancient breeds gazing at humans less than other groups (Konno et al., 2016). The attentional status of the audience also has an influence: dogs were shown to use more communicative behaviors when people are visually available for them (Marshall-Pescini et al., 2013;Savalli et al., 2016), and gazing can be quickly established and extinguished through associative learning (Barrera et al., 2011). ...
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Dogs are particularly skillful in communicating with humans, and growing evidence points towards the importance of both species intertwined evolutionary history and intense daily partnership. Gaze alternation is a communicative behavior used by dogs from a very young age and is affected by factors such as aging and experience. We analyzed how different degrees of daily human interaction affect dogs’ gazing behavior in the unsolvable task, where a desired food becomes inaccessible. Three groups with different degrees of daily exposure to humans were compared: pet dogs that live inside the house, pet dogs that live outside the house, and shelter dogs. We found no difference in latency to the first gaze, but pet dogs did show a higher proportion of individuals engaging in gaze alternation, a higher number of gaze alternations, and a longer duration of gaze than shelter dogs. Additionally, dogs living inside the house gazed more at the experimenter than dogs living outside. Overall, our results indicate a strong influence of experience over the development and use of these communicative behaviors in dogs, with groups that are closer to people in their daily lives being more willing to communicate with humans as a strategy to obtain a desired goal.
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One of the most well-studied differences between wolves and dogs is their ability to understand and communicate with humans. Here we review these studies and come to surprising conclusions. Overall, based on current knowledge, dog-wolf differences in communicative abilities with humans appear rather small and if existing at all, they are quantitative rather than qualitative in nature. Rather it seems that other traits, such as a propensity for conflict avoidance, proneness to ‘obey’, or persistence, may be responsible for some of the differences observed in the various tests. For example, while it seems that dog puppies are indeed better at following human pointing cues than wolves, wolf puppies do better in gaze following studies both with humans and conspecifics. As adults, both species can use both cues to some extent. One interpretation is that pointing cues might be perceived as imperative and dogs may just be more willing to follow human ‘commands’ from an early age, while wolves can learn to follow them with age probably as a result of positive experience (learning). The propensity to communicate with humans is also rather similar in wolves and dogs, if more basic differences such as their level of persistence in interacting with objects is taken into account. So for example, both wolves and dogs are equally successful in communicating to a naive human where a desired out-of-reach food item is located. Thus both species can communicate referentially with a human partner, and can also take the level of cooperativeness of the partner into account.
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The experiences that domestic dogs have with humans take many forms. We hypothesized that more experience with humans would lead to greater dependence on humans in problem-solving situations. We used the unsolvable task to compare persistence and gazing in dogs with differing degrees of experience with humans: 1) dogs living in a home for a year or more; 2) dogs living in a home for less than a year (including foster dogs); and 3) shelter dogs. Dogs first learned a solvable task; we then measured persistence as well as gazing at humans when the task was unsolvable. Dogs living in a home for a year or more gazed sooner and longer than shelter dogs. Formally trained dogs from breeders also gazed sooner than formally trained dogs from shelters. There were no differences in overall persistence among the three types of dog. However, shelter dogs spent more time biting the box and gazing at it than dogs in the home. Former shelter dogs, former strays, and dogs that had no formal training also spent more time biting the box. We conclude that ownership duration, background, and prior experiences with humans influence human-directed communication and persistence behaviors in dogs.
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Domestic dogs differ enormously in both their morphology and behavior. Numerous factors can influence the development and expression of canine behavior and, more generally, determine the success of the pet–owner relationship. This chapter considers the role of nature and nurture in shaping canine behavior. The influence of factors intrinsic to the animal is outlined, focusing on research that has explored the role of breed, sex, and cerebral lateralization in guiding canine behavior and cognitive functioning. The chapter goes on to consider the role of more extrinsic factors that can influence the development of dog behavior, discussing the contribution of early experience, source of acquisition, training techniques, and owner-related traits including personality and attachment style. The article points to the enormous amount of individual variation that exists between dogs and the myriad of factors that can work together to shape the behavior and functioning of the animal we see before us.
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Herding is done predominantly by breeds developed over centuries to millennia specifically for that purpose. Working-level herding breed dogs are intense, high-drive dogs that will work despite severe illness or pain, thereby masking clues that they are ailing or the nature of their problem. The handler should recognize subtle changes that might signal ill health, and veterinarians should take an active role in training handlers on essential skills. Herding dogs typically work entirely outdoors in rural to wilderness environments with continuous exposure to other domestic animals and wildlife and may be affected by trauma, toxin exposure, infectious diseases, and parasitic infections.
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Since the observations of O. Pfungst the use of human-provided cues by animals has been well-known in the behavioural sciences ("Clever Hans effect"). It has recently been shown that rhesus monkeys (Macaca mulatta) are unable to use the direction of gazing by the experimenter as a cue for finding food, although after some training they learned to respond to pointing by hand. Direction of gaze is used by chimpanzees, however. Dogs (Canis familiaris) are believed to be sensitive to human gestural communication but their ability has never been formally tested. In three experiments we examined whether dogs can respond to cues given by humans. We found that dogs are able to utilize pointing, bowing, nodding, head-turning and glancing gestures of humans as cues for finding hidden food. Dogs were also able to generalize from one person (owner) to another familiar person (experimenter) in using the same gestures as cues. Baseline trials were run to test the possibility that odour cues alone could be responsible for the dogs' performance. During training individual performance showed limited variability, probably because some dogs already "knew" some of the cues from their earlier experiences with humans. We suggest that the phenomenon of dogs responding to cues given by humans is better analysed as a case of interspecific communication than in terms of discrimination learning.
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The genetic bases of demographic changes and artificial selection underlying domestication are of great interest in evolutionary biology. Here we perform whole-genome sequencing of multiple grey wolves, Chinese indigenous dogs and dogs of diverse breeds. Demographic analysis show that the split between wolves and Chinese indigenous dogs occurred 32,000 years ago and that the subsequent bottlenecks were mild. Therefore, dogs may have been under human selection over a much longer time than previously concluded, based on molecular data, perhaps by initially scavenging with humans. Population genetic analysis identifies a list of genes under positive selection during domestication, which overlaps extensively with the corresponding list of positively selected genes in humans. Parallel evolution is most apparent in genes for digestion and metabolism, neurological process and cancer. Our study, for the first time, draws together humans and dogs in their recent genomic evolution.
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Here we report a high-quality draft genome sequence of the domestic dog (Canis familiaris), together with a dense map of single nucleotide polymorphisms (SNPs) across breeds. The dog is of particular interest because it provides important evolutionary information and because existing breeds show great phenotypic diversity for morphological, physiological and behavioural traits. We use sequence comparison with the primate and rodent lineages to shed light on the structure and evolution of genomes and genes. Notably, the majority of the most highly conserved non-coding sequences in mammalian genomes are clustered near a small subset of genes with important roles in development. Analysis of SNPs reveals long-range haplotypes across the entire dog genome, and defines the nature of genetic diversity within and across breeds. The current SNP map now makes it possible for genome-wide association studies to identify genes responsible for diseases and traits, with important consequences for human and companion animal health.
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Dogs show considerable variation in morphology, genetics and behaviour caused by long periods of artificial selection. This is evident in the large number of breeds we have today. Behavioural differences among breeds have often been regarded as remnants from past selection during the breeds’ origin. However, the selection in many breeds has, during the last decades, gone through great changes, which could have influenced breed-typical behaviour. In order to investigate this, breed differences were studied using data from a standardized behavioural test from 13,097 dogs of 31 breeds from the Swedish dog population. Based on the test results, breed scores were calculated for four behavioural traits: playfulness, curiosity/fearlessness, sociability and aggressiveness. These traits have previously been found to be stable and valid, and hence regarded as personality traits in the dog. The present results suggested large differences between breeds in all of the investigated traits, even though there were within-breed variations. No relationships between breed-characteristic behaviour and function in the breeds’ origins were found. Instead, there were correlations between breed scores and current use of the breeding stocks, which suggest that selection in the recent past has affected breed-typical behaviour. The breeds’ use in dog shows, the dominating use in general, was negatively correlated with all investigated traits, both in sires and in dams. In contrast, use in Working dog trials was positively correlated with playfulness and aggressiveness in sires. Thus, these results suggest that selection for dog show use is positively correlated with social and non-social fearfulness, and negatively with playfulness, curiosity in potentially threatening situations and aggressiveness, whereas selection for Working dog use is positively correlated with playfulness and aggressiveness. Furthermore, correlation analyses show that popular breeds have higher sociability and playfulness scores than less popular breeds, suggesting that a positive attitude towards strangers is an important characteristic of a functional pet dog and desirable by dog owners. This indicates that selection towards use in dog shows may be in conflict with pet dog selection. Furthermore, these results suggest that basic dimensions of dog behaviour can be changed when selection pressure changes, and that the domestication of the dog still is in progress. A standardized behavioural test, like the one used in this study, is suggested to be highly useful as a tool in dog breeding programs.
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At an experimental farm in Novosibirsk, Siberia, geneticists have been working for four decades to turn foxes into dogs. They are not trying to create the next pet craze. Instead, author Trut and her predecessors hope to explain why domesticated animals such as pigs, cattle and dogs are so different from their wild ancestors. Selective breeding alone cannot explain all the differences. Trut's mentor, the eminent Russian geneticist Dmitri Belyaev, thought that the answers lay in the process of domestication itself, which might have dramatically changed wolves' appearance and behavior even in the absence of selective breeding. To test his hypothesis, Belyaev and his successors at the Institute have been breeding another canine species, silver foxes, for a single trait: friendliness toward people. Although no one would mistake them for dogs, the Siberian foxes appear to be on the same overall evolutionary path—a route that other domesticated animals also may have followed while coming in from the wild.
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The traditional and relatively narrow-focused research on ape-human comparisons has recently been significantly extended by investigations of different clades of animals, including the domestic dog (Canis familiaris). Here, we provide a short overview of how the comparative investigation of canine social behaviour advances our understanding of the evolution of social skills and argue that a system-level approach to dog social cognition provides a broader view on the 'human-likeness' of canine social competence. We introduce the concept of evolutionary social competence as a collateral notion of developmental social competence. We argue that such an extended perspective on social competence provides a useful tool for conceptualising wolf-dog differences in socio-cognitive functioning, as well as for considering specific social skills not in isolation, but as a part of a system.