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The Social Dog. http://dx.doi.org/10.1016/B978-0-12-407818-5.00001-2
Copyright © 2014 Elsevier Inc. All rights reserved.
The Social Dog: History and
Evolution
Sarah Marshall-Pescini1,2,3 and Juliane Kaminski4
1Dipartimento di Fisiopatologia Medico-Chirurgica e dei Trapianti, Sezione di Neuroscienze,
Università degli Studi di Milano, Milan, Italy, 2Comparative Cognition, Messerli Research
Institute, University of Veterinary Medicine, University of Vienna, Vienna, Austria, 3Wolf Science
Centre, Ernstbrunn, Austria, 4Psychology Department, University of Portsmouth, Portsmouth, UK
1.1 WHERE DO DOGS’ SOCIALITY AND SOCIO-COGNITIVE
ABILITIES COME FROM? THE CANID STORY
The explosion of studies on dogs’ social behaviour and cognitive abilities since
the turn of the twenty-first century has been impressive (see Bensky et al., 2013,
for a comprehensive review), and the many hypotheses as to the causes behind
dog’s remarkable socio-cognitive abilities have engendered lively debates in
journals and at conferences. However, most debates revolve around the wolf–
dog comparison (the wolf being dog’s closest living relative), neglecting the fact
that the dog’s canine family is much larger and shows some unique and intrigu-
ing features that may well have played a role in allowing dogs’ emergence as our
favoured social companions. Hence, in the first part of this chapter, we intro-
duce dogs’ canine family, presenting some of these intriguing social features
and highlighting some of the characteristics that may have played a fundamen-
tal role in allowing the emergence of one species’ unique history with humans.
1.1.1 Introducing Dogs’ ‘Canine’ Family
The domestic dog belongs to the Canidae family, consisting of 35 related species
that diverged within the last ten million years (Wayne et al., 1997; Ostrander &
Wayne, 2005). In recent years, there has been considerable interest in the evolu-
tionary relationships between canids that has resulted in analyses based on both
morphological (Berta, 1987; Tedford et al., 1995; Lyras & Van Der Geer, 2003;
Zrzavý & Řičánková, 2004) and molecular data (Wayne et al., 1987; Wayne
et al., 1989), including, more recently, DNA sequencing (Wayne et al., 1997;
Bardeleben et al., 2005; Linblad-Toh et al., 2005; Wong et al., 2010). The devel-
opment of methodologies for the sequencing of DNA has allowed researchers to
Chapter 1
4SECTION | I Theoretical Aspects
reconstruct the dog’s family tree, with a certain amount of accuracy (although a
few grey areas still exist).
Taken together, current results converge in showing three major groupings
within the dog’s family: (1) the red fox–like canids, (2) South American canids,
and (3) wolf-like canids. Together, these three clades contain 93% of all living
canids. A separate lineage comprising the grey fox seems to be the most primi-
tive and suggests a North American origin of the living canids about ten million
years ago (Ostrander & Wayne, 2005; Bardeleben et al., 2005; Lindblad-Toh
et al., 2005; Graphodatsky et al., 2008) (see Figure 1-1).
When one looks more closely at the wolf-like canids, results place grey
wolves as the closest living ‘cousins’ of domestic dogs, followed by a close
affiliation with coyotes, golden jackals, and Ethiopian wolves. These phylo-
genetic relationships imply that the dog has several close relatives within its
genus, confirmed by results showing that all members of Canis can produce
fertile hybrids, and several species may have genomes that reflect hybridisation
in the wild (Wayne & Jenks, 1991; Gottelli et al., 1994; Roy et al., 1996; Adams
et al., 2003). Closest to the Canis group are the dhole and African wild dog (thus
completing the members of the wolf-like canids). Dhole and African wild dogs
do not, however, form a monophyletic group, and their exact relationship to the
Canis genus is still somewhat unclear (Bardeleben et al., 2005; Zhang & Chen,
2011). Finally, results from genetic analyses also appear to support an African
origin for the wolf-like canids because the two African jackals are the most basal
members of this clade (Lindblad-Toh et al., 2005).
1.1.2 Evolution of the Canid Brain: A Socially Driven
Phenomenon?
Studies on the evolution of canids show that this family separated from the other
mammals around 40 million years ago. Interestingly, a shift in canid encepha-
lisation and architectural reorganisation of the brain (i.e., expansion of the pro-
rean gyrus at the anterior end of the neocortex, general increase in the amount of
infolding of the frontal lobe, and expansion of the prefrontal cortex; Radinsky,
1969, 1973; Lyras & Van der Geer, 2003) appears to have occurred sometime
in the late Miocene or early Pliocene period, roughly coinciding also with a
sudden taxonomic diversification (Van Valkenburgh, 1991) and expansion of
global grasslands (Cerling et al., 1997). Based on these data, authors have put
forward a number of suggestions as to the possible causes driving these changes
in the brain.
According to some authors, they may simply have been a by-product of
a rapid taxonomic diversification in the new environment (Andersson, 2005);
however, considering the energetic expenditure of big brains, it would seem
more probable that such an expensive adaptation would be driven by some major
adaptive advantage. Work by Van Valkenburgh and colleagues puts forward the
possibility that, in fact, the onset of cooperative pack hunting (Van Valkenburgh
5
Chapter | 1 The Social Dog: History and Evolution
et al., 2003; Van Valkenburgh et al., 2004) may have driven this change. How-
ever, Finarelli’s (2008) analysis, taking into account a larger sample of both
extinct and living canids, suggests that encephalisation increased in the three
major living clades (wolf-like, fox-like, and South American canids) at the same
time, yet most of the smaller-bodied canids (except for the South American
bush dog) are not cooperative hunters. The trait that most canids share, however,
Arctic fox
Red fox
Cape fox
Blanford’s fox
Fennec fox
Raccoon dog
Short-eared fox
Maned wolf
Crab-eating fox
Bush dog
Black-backed jackal
Grey wolf
Bat-eared fox
Island fox
Grey fox
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
9–10
Myr
80
–
100
100 93
100
78
100
99
100
92
100
78
100
75
100
100
100
96
100
93
100
81
100
96
100
–
99
–
99
–
99
–
99
75
100
100
100
81
100
52
98
67
99
(4)
(9)
(2)
Kit fox
Corsac fox
Ruppell’s fox
Dog
Sechuran fox
Culpeo fox
Pampas fox
Chilla
Darwin’s fox
Hoary fox
Side-striped jackal
Golden jackal
Coyote
Ethiopian wolf
Dhole
African wild dog
Black bear
Giant panda
Northern elephant seal
Walrus
3–4
Myr
6–7.4
Myr
FIGURE 1-1 Branch colours identify the red fox–like clade (red), the South American clade
(green), the wolf-like clade (blue), and the grey and island fox clade (orange). (From Lindblad-Toh
et al., 2005.)
6SECTION | I Theoretical Aspects
is ‘monogamy’ (defined as a single male and single female mating exclusively
with each other over multiple reproductive cycles) and (to differing extents)
the cooperative rearing of the young. Hence, these authors suggest that it may
have been these traits driving encephalisation and that pack hunting would then
have emerged as a second-order adaptation, facilitated by, but not directly caus-
ally related to, the reorganisation of the canid brain. This hypothesis seems to
be plausible given another study showing that, among mammals and birds in
general, it is not the size of the social group that correlates with brain size (as
in primates), but instead it is species that live in pair-bonded social systems that
have the largest brains (when phylogeny and a range of life history and ecologi-
cal variables are partialled out; Shultz & Dunbar, 2007; Dunbar, 2009).
1.1.3 The Sociality of Canids’ Mating System: Pair Bonding
and Cooperative Pup Rearing
Taken as a whole, the dog’s canine family is one of the most fascinating
amongst carnivores. As a start, they are the most widespread, with at least one
species inhabiting every continent except Antarctica (although dogs, of course,
live there as well), and some spread over entire continents (Sillero-Zubiri et al.,
2004). Perhaps more interestingly for the purpose of this book, canids have a
number of interesting social adaptations, starting from their mating system.
Most species in this family are monogamous, a rare trait amongst mammals,
but a potentially characteristic trait for canids (Kleiman, 1977, 2011). However,
there is considerable interspecific variation in mating systems among canids,
and polygamy, polyandry, and monogamy have been documented (Bekoff et al.,
1981; Moehlman, 1989; Geffen et al., 1996; Carmicheal et al., 2007): for exam-
ple, red foxes, Arctic foxes, and coyotes appear to adopt a largely monogamous
strategy (Sillero-Zubiri et al., 2004; Hennessy et al., 2012; but see Carmicheal
et al., 2007), whereas a recent study using genetic analyses to determine parent-
hood across multiple populations of African wild dogs found that there was,
in fact, a greater than previously reported incidence of reproductive sharing in
that both beta females and males (and not just the dominant pair as previously
thought) played a significant role in producing young (Spiering et al., 2010),
suggesting a more promiscuous strategy in this species.
Canids are also unique in that intraspecific variation in mating systems may
be as great as interspecific variation (Moehlman, 1989); for example, swift
foxes, Arctic foxes, and urban red foxes may all live either in monogamous
pairs or polygamous groups depending on their ecological context (Baker et al.,
2004; Kamler et al., 2004; Carmicheal et al., 2007; and see Geffen et al., 1996
for a comprehensive review of canid social flexibility). Indeed, it appears that
the choice between a monogamous or polygamous strategy may even change
within the same population, most probably in relation to food availability (red
foxes: von Shantz, 1984; Zabel & Taggart, 1989). Such flexibility is not con-
fined to the fox-like canids; indeed, Ethiopian wolves show a similar level of
7
Chapter | 1 The Social Dog: History and Evolution
flexibility depending on ecological factors affecting food availability (Sillero-
Zubiri et al., 1996; Marino et al., 2012).
Alongside pair bonding, canids also show a variety of parental care strate-
gies. In some species, mostly the female appears to care for the young—the
most common strategy in mammals (e.g., bat-eared foxes and swift foxes: Kam-
ler et al., 2004; Poessel & Gese, 2013); however, in others, male provisioning
of both pups and lactating females occurs (e.g., black-backed jackals, red foxes,
coyotes: Moehlman, 1989; Zabel & Taggart, 1989; Gese, 1998); and in yet oth-
ers, both breeding individuals and their older offspring (that delay dispersal:
Emlen, 1991) are involved in pup rearing (e.g., grey wolves, African wild dogs,
dhole: Fritts & Mech, 1981; Malcolm & Marten, 1982; Creel & Creel, 2002;
Sillero-Zubiri et al., 2004; Venkataraman & Johnsingh, 2004). In fact, coop-
erative breeding, involving also the non-breeding pack members and including
‘helping behaviour’ such as den-site attendance; provisioning (including regur-
gitation); play; and grooming are perhaps among the defining characteristics of
a number of canid species (Macdonald, 1979; Moehlman, 1986; Mech et al.,
1999; Packard, 2003).
Such helping behaviour has been shown to have an adaptive value in a num-
ber of cooperative breeding species (banded mongoose: Hodge, 2005; meerkats:
Russell et al., 2007), although evidence in the canid family has been harder to
obtain (Gusset & MacDonald, 2010; but see Wright, 2006, for paternal invest-
ment on pup rearing success in bat-eared foxes and helper effect in red wolves;
Sparkman et al., 2011). However, sociality in many canid species is not just
apparent in pup rearing but emerges strongly also in relation to hunting and
territorial defence.
1.1.4 The Sociality of Canids’ Hunting and Defence Strategies
Canid hunting strategies vary widely, ranging from species that feed largely
solitarily on fish and insects, like the short-eared dog (Sillero-Zubiri et al.,
2004), to hypercarnivore species that hunt in packs, such as the African hunt-
ing dog, bush dog, wolf, and dhole (Venkataraman et al., 1995; Creel & Creel,
2002; Mech & Boitani, 2003; Sillero-Zubiri et al., 2004). Hunting techniques
are intimately linked with sociality levels in canids, because species that hunt
cooperatively are also described as the most social. Indeed, a number of authors
have suggested that pack hunting may be the major force behind canid social-
ity (Alexander, 1974; Pulliam & Caraco, 1984; Clark & Mangel, 1986). Group
hunting, in theory, may allow the capture of larger prey. However, the cause and
effect of such an argument may be difficult to tease apart: do some canid species
live in larger groups because in so doing they can hunt larger prey, or does the
availability of predominantly larger prey ‘oblige them’ to live in groups? In a
chapter reviewing the topic, MacDonald et al. (2004) suggest that at present the
evidence cannot tease these two alternatives apart, although novel methods of
modelling hunting success seem to suggest that, at least in African wild dogs,
8SECTION | I Theoretical Aspects
considering multiple factors such as energetic expenditure, frequency of hunts,
and pup guarding (so reduced participation due to helper role), the optimum
hunting party is a group of 10–15 animals, but when groups become larger,
costs to hunting increase, no longer providing a viable alternative (Creel &
Creel, 1995; Courchamp et al., 2002; Creel & Creel, 2002; MacDonald et al.,
2004). In wolves, based on recent data looking at multiple packs differing in
size and composition, groups larger than 4 individuals appear to have a signifi-
cantly reduced hunting success due to an increase in free-riders (individuals that
are present during the hunt but, in fact, avoid the riskier parts of the process,
such as attacking and killing of the prey; MacNulty et al., 2012). Interestingly,
it is the non-breeders of the pack (that have no offspring) that tend to become
free-riders, which appears to be consistent with reports of the breeding pair
being responsible for leading group hunts.
Within the hunting routine, however, the capture of the prey is only one of a
suite of actions required for a successful outcome (see Bailey et al., 2013, for an
in-depth review of group hunting strategies). Indeed, another important aspect
that has emerged in the evaluation of the benefits of numbers in foraging strate-
gies is the presence of scavengers. In wolves, it appears that in the absence of
scavengers, hunting in pairs is more productive than in large groups; however,
when ravens are put in the equation, the optimal group size increases (Vuce-
tich et al., 2004). Indeed, protection of prey from both intra- and interspecific
competitors appears to be a major factor that may tip the balance in favour of
group hunting, not just in wolves, but also for dholes driving tigers away from
kills and African wild dogs defending prey from hyaenas (Malcolm & Marten,
1982; Creel & Creel, 1995; Carbone et al., 1997; Carbone et al., 2005). Taken
together, although the jury is out as to whether the effect of group size on hunt-
ing success per se is enough to promote the formation and maintenance of large
groups in canids, it is undoubtedly the case that in many species, hunting is
likely to be a social affair, whether it is in dyads or larger parties.
Similarly, territorial defence is also in many cases a group activity, where
numbers seem to count. Thus, for example, in coyotes, domestic dogs, red
and Arctic foxes, as well as Ethiopian wolves and African wild dogs, clashes
between packs always result in the larger chasing off the smaller (coyotes:
Wells & Bekoff, 1982; domestic dogs: Bonanni et al., 2011; red foxes: Voigt &
MacDonald, 1984; Arctic foxes: Frommolt et al., 2003; Ethiopian wolf: Sillero-
Zubiri et al., 2004; African wild dog: Creel & Creel, 1998).
1.1.5 Why Wolves?
Based on genetic, morphological, and behavioural data, it is clear that the
domestic dog’s closest living relative is the grey wolf (Canis lupus); hence, the
comparative approach between wolves and dogs has naturally been the focus
of most studies (see following sections). However, one of the most intriguing
questions (yet to be addressed) is why, amongst canids, it was indeed the wolf
9
Chapter | 1 The Social Dog: History and Evolution
(and not, say, the dhole) that underwent the profound changes required for the
domestication process to occur. The Siberian farm fox experiment explained in
more detail in Section 1.2.2 clearly shows the potential for a process somewhat
similar in another canid species.
Indeed, archaeological evidence as well as a number of reports from vari-
ous sources suggest that in South America, where the arrival of domestic dogs
occurred relatively late, a number of wild canids were at least ‘tamed’ and kept
in close contact with humans (see Stahl, 2012, 2013, for exhaustive reviews of
the evidence). Hamilton-Smith (1839), for example, reported maned wolves
and other canids being kept by indigenous people and accompanying them in
hunting expeditions, and reported on interbreeding between endemic canids and
domestic dogs, which eventually replaced them as the preferred human compan-
ion. The species most often reported are the crab-eating fox, the bush dog, and,
to a lesser degree, the maned wolf (Stahl, 2013). More recently, in an exhaus-
tive report of all the status and known facts of all canid species, Sillero-Zubiri
et al. (2004) report of a number of South American canids, showing very docile
behaviour towards humans (e.g., short-eared dog) or that have historically been
kept as pets by indigenous populations (e.g., crab-eating foxes and bush dogs).
Taming is not the same process as domestication, in that whereas the former
involves the raising of a wild animal with human contact, the latter involves a
process of genetic selection, which ultimately results in an animal that is sub-
stantially different from its ancestor. Nevertheless, taken together, these dif-
ferent lines of research suggest that there may be specific canid (and not just
wolfish) characteristics that rendered this family particularly well suited (pli-
able) for one of its species to have undergone the domestication process. Given
the review regarding their sociality, both in terms of their reproductive strategy
and in relation to hunting and territorial defence; potentially their ‘monogamy’
in terms of their ability to establish a long-term relationship with one individual;
and their inter- and, perhaps even more importantly, their intraspecific flexibil-
ity in social organisation, these are perhaps the traits that allowed one particular
species to start associating with human beings, over time becoming our most
cherished companion. However, what characteristics may further set wolves
apart, or if wolves were simply in the right place at the right time, remains an
open question.
Unfortunately, at present, the social behaviour of many species is still rela-
tively poorly understood, with some of even the more basic information missing
for many species (see Macdonald & Sillero-Zubiri, 2004a, and Sillero-Zubiri
et al., 2004, for the most recent comprehensive and complementary reviews).
As has been pointed out by other authors in this book, most studies on canids
have focused on the socio-behavioural ecology of the species (e.g., prey–
predator relationship, ranging activities, territorial defense), whereas relatively
little data are available regarding their social behaviour in terms of, for exam-
ple, social organisation, affiliative relationships, coalition/alliance formation,
group/ fission–fusion dynamics, intergroup dynamics, etc. This area of research
10 SECTION | I Theoretical Aspects
remains largely unexplored, both with wild and captive populations of canids;
hence, it is not possible to identify whether, compared to other canids, wolves
may have specific characteristics particularly suited for the establishment of
a relationship with humans. Yet, whether by lucky coincidence or because of
some special trait in this species, it was indeed wolves that met humans, so we
now turn to when, where, and how this meeting took place.
1.2 WHERE DO DOGS’ SOCIALITY AND SOCIO-COGNITIVE
ABILITIES COME FROM? THE DOG–HUMAN STORY
There is no doubt that dogs are a very successful species. Wherever there are
men, there are dogs, be it the Inuits’ dogs in the Arctic regions or the Saluki in
the Arabic deserts. Dogs are everywhere. It is the only carnivore species that,
even though it has the potential to significantly harm (even kill) a human being,
we allow to exist in close proximity. Humans allow dogs in their households,
share their lives with dogs, and, in some cultures, accept dogs as part of their
families. One reason humans can do so is that domestication has changed dogs
so drastically that they can not only cope with the human lifestyle, but may in
fact have specifically adapted to it (see Chapters 2 and 11 of this book). As is
outlined further in the following sections, and in other chapters in this book,
selection pressure during domestication may have shaped dogs’ behaviour and
even their cognitive skills such that the latter are in some respects functionally
equivalent to human behaviour and human social skills (see Chapter 11). How-
ever, one of the intriguing questions that fascinates researchers and is spurring
a growing amount of research is when, where, and how humans and wolves/
dogs met. In the following sections, we outline the various answers to the when,
where, and how questions, drawing both from the archaeological evidence and
genetic studies conducted in the field, showing that although we may never have
an answer to the how question, data emerging from these fields can help tease
apart the plausibility of what would otherwise remain ‘just so’ stories.
We then move on to briefly outline the different hypotheses that have been
formulated as to what aspects of dogs’ social behaviour and cognition (both
towards conspecifics and humans) may have changed in the course of domes-
tication. We conclude the chapter by highlighting where further research is
needed to allow us to tease apart the competing hypotheses on how dogs became
man’s best friend.
1.2.1 When and Where Did Dogs and Humans Meet?
Looking at the history of the relationship between dogs and men, we know that
dogs are the first species humans domesticated. While canid remains were found
together with human remains dated at over 100,000 years BP (e.g., Olsen, 1985),
these remains were still wolf-like and showed no clear signs of domestication.
Morphological features used in archaeology to identify signs of domestication
11
Chapter | 1 The Social Dog: History and Evolution
in a prehistoric canid skull are the shortening of the facial region and reduc-
tion in tooth size, which leads to crowding of teeth (Olsen, 1985; Dayan, 1994;
Clutton-Brock, 1995). Morey (1994) states that the best indication of domestica-
tion taking place is a morphological pattern of mandibular and maxillary (snout)
reduction accompanied by a lesser reduction of tooth size.
The fact that wolf and human remains were found together over quite a time
span and at several locations is seen as an indicator that humans and wolves
overlapped and shared a similar habitat for quite some time during the Pleisto-
cene age (e.g., Nowak, 2003; Mech & Boitani, 2003). So even though humans
and wolves must have met on many occasions for thousands of years, archaeo-
logical evidence suggests clear signs of domestication on canid skulls found
near humans only quite late in the Pleistocene. One of the most important of
these findings was that of the Natufian site of Mallaha, Israel (Davis & Valla,
1978; Clutton-Brock, 1995). The site is dated as ≈12,000 BP and therefore falls
into the late Pleistocene (see also Tchernov & Valla, 1997, for evidence that
other canid remains found at Natufian sites show clear signs of domestication).
The Natufian people were thought to have been hunter-gatherers but with sta-
ble settlements, foraging for a wide variety of foods to then settle down to be
what people believe were the earliest farmers in history (Bar-Yosef, 1998). The
importance of dogs to the Natufian people not only becomes apparent in the
joint burials of dogs and men (Morey & Wiant, 1992; Tchernov & Valla, 1997),
which could be seen as evidence that dogs had a similar status as people (Losey
et al., 2011), but also becomes evident from the fact that jewellery excavated at
Natufian sites included one figurine that had an owl’s head at one and a dog’s
head at the other end (Bar-Yosef, 1998). So this supports the idea that dogs
and people were not just sharing the same habitat, but that there was a change
in humans’ perception and ideology towards dogs (maybe animals in general).
In the late Pleistocene and the beginning of the Holocene age, humans started
to settle. In many areas, agriculture now started to replace the more hunter-
gatherer–like culture. The near east is seen as the region in which agriculture
first developed ≈10,000 BP, but from there agriculture spread around the world
and to most corners of the globe (Richerson et al., 2001). There are several rea-
sons agriculture started then, climate change being one of them, as agriculture
would have been impossible in the glacial times of the Pleistocene (Richerson
et al., 2001). The beginning of agriculture not only marks an important change
in how humans organised their lives and the start of a rapid growth of the human
population, but also is clearly the starting point for the domestication of differ-
ent plant and animal species. So apart from dogs, we see goats being the first
ungulate to be domesticated ≈10,000 years ago (e.g., Zeder & Hesse, 2000) and
the domestication of pigs and cows (Loftus et al., 1994; Giuffra et al., 2000).
Because human settlement and agriculture during the end of the Pleistocene
and beginning of the Holocene is seemingly so closely connected to the first
findings of dog specimens, it is not surprising that earlier hypotheses about the
domestication of dogs developed a scenario in which human settlement played
12 SECTION | I Theoretical Aspects
a major role (e.g., Zeuner et al., 1967; Zimen, 1992; Clutton-Brock, 1995).
Researchers speculated that wolves probably approached human settlements,
maybe even continuously lived around human settlements, living from human
waste and leftovers. The hypothesis is that during this process humans either
actively selected nice and friendly wolf puppies to be their companions (Zimen,
1992) or that this was more like a process of self-domestication in the absence
of any intentional selection (Zeuner et al., 1967; Clutton-Brock, 1995; for a
review, see Hare et al., 2012).
1.2.2 How Did Wolves Become Dogs? The Self-Domestication
Hypothesis
The central argument of the self-domestication hypothesis is that the first stage
of the domestication of wolves was based on a selection against aggression or
fear. This was not intentional, meaning that humans did not actively pick certain
individuals based on their perception of them being less aggressive, but rather
wolf individuals that were less aggressive or less fearful had a selection advan-
tage (Zeuner, 1967; Hare et al., 2012). The reason that they might have had a
selection advantage could be that being less aggressive and less fearful towards
humans gave them the opportunity to live in closer proximity to them, hence the
opportunity to exploit new and potentially more reliable food sources (Zeuner,
1967). One series of studies that shows how strongly a selection against aggres-
sion and fear can affect a species’ behaviour and morphology is the famous
silver fox farm experiments carried out in Siberia.
This experimental study was started by Russian evolutionary biologist
Dmitri Belyaev. In this long-term study, researchers simulated selection pres-
sures during domestication by selecting a group of silver foxes for tameness
and against aggression towards humans. Foxes were divided in different groups
based on how they reacted towards the hand of a human reaching into their cage.
While the ones that behaved aggressively (or fearfully) against the hand were
selected to be in the non-domesticated group (Class III), the ones that stayed
calm and showed no signs of aggression towards the hand were moved to the
‘intermediate’ (Class II) group, and the ones that showed clear signs of friendli-
ness towards the humans (like approaching the hand, licking the hand, etc.) were
moved to the ‘domesticated’ (Class I) group (Trut et al., 2009). Interestingly,
after several generations of selection based on levels of tameness being the only
selection criterion, the Class I foxes showed clear signs of paedomorphic fea-
tures and ‘dog-like’ behaviour, such as whining, tail wagging, exhibiting signs
of clear submission towards humans, approaching humans, etc. (Trut et al.,
2004; Trut et al., 2009). There were also changes in morphology including, for
example, floppy ears and curly tails compared to the non-selected foxes (Trut
et al., 2009). These experiments therefore support the hypothesis that selection
against aggression or fear towards humans can lead to behavioural and mor-
phological changes in a canid species, and create something like a ‘proto-dog’,
13
Chapter | 1 The Social Dog: History and Evolution
which researchers have suggested to be the type of dog that was created by this
first wave of domestication (Zeuner, 1967; Coppinger & Coppinger, 2001; Hare
& Tomasello, 2005).
1.2.3 The Recent Genetic Revolution
Recently, the view that dog domestication started in the late Pleistocene and
early Holocene period has been seriously challenged by both archaeological
evidence and studies tracing the genetic origins of the domestic dog. Two main
findings suggest the story of domestication may change completely. First, a
number of skulls, showing clear signs of differentiation through domestication,
were found in the Goyet Cave in Belgium and the Altai Mountains in Russia
(Ovodov et al., 2011). A recent detailed analysis of these skulls dates them as
>30,000 years old (Germonpré et al., 2009; Druzhkova et al., 2013), making
them the oldest remains currently available. The dating of the skulls to 30,000
years is also supported by the second major line of research, which is based
on the comparison of DNA collected from these specimens (the Goyet skull
and the Altai skull) to that of modern dog breeds, modern wolves, and prehis-
toric wolf specimens. Thalmann et al. (2013) collected partial mitochondrial
genomes from prehistoric canids, modern wolves of Eurasian and American
origin, and modern dogs. The data suggest three things. First, it shows that the
30,000-year-old skulls are indeed dogs, not wolves (see also Druzhkova et al.,
2013; Ovodov et al., 2013). Second, it suggests a European origin of the dog, as
there was a strong association of the sequences from modern dogs with ancient
European specimens and with European wolves, but no association of modern
wolf sequences from the Middle East or East Asia with modern dogs (Thalman
et al., 2013); and last, it suggests that the wolf species, which was dogs’ ances-
tor, was more likely from a now-extinct branch than from a modern wolf species
still in existence today. Recent evidence presented by Freedmann et al. (2014)
suggests a very similar story. They compared the DNA from three different
grey wolves, chosen from Europe, the Middle East, and East/South Asia, which
represent the regions where domestication is hypothesised to have taken place
(see Savolainen et al., 2002, and Wang et al., 2013, for support of the hypoth-
esis that dogs originated in the Middle East and East Asia; and Thalmann et al.,
2013, for support of a European origin) to basenji DNA and dingo DNA and
used a golden jackal as an outgroup. Their data suggest that after dogs separated
from wolves, wolves went through a sharp bottleneck during which the number
of wolf lineages was significantly reduced. This might support the view also
brought up by Thalmann et al. (2013) that dogs’ ancestor is now extinct and not
represented by any of the modern wolf species.
If, as suggested by recent evidence, dogs were domesticated 30,000 years
ago, the story behind how wolves became dogs changes entirely. At that time,
humans were still hunter-gatherers, long before humans settled down and long
before agriculture started (as explained previously, agriculture together with
14 SECTION | I Theoretical Aspects
human settlement started ≈12,000 years ago [Larsen, 1995]). So a likely sce-
nario, then, would be that wolves probably followed humans during hunting and
were scavenging their share of the meat or simply fed on the leftovers (Thal-
mann et al., 2013). In this context, it is interesting that there is evidence of signs
of gnawing damage to ancient bones from larger mammals of the Pleistocene
period, which were found near human remains (Haynes, 1983). Haynes (1983)
compared these traces on the ancient bones to traces that modern wolves would
leave on bones from larger mammals and found that they were highly compa-
rable. This suggests that the marks on the ancient bones were also left from
wolves or at least some larger canid species (potentially proto-dogs). This there-
fore would support the hypothesis that wolves (or proto-dogs) basically were
around humans while they were hunting for larger mammals. There is even
some speculation that dogs played a role in the massive extinction of Megafauna
(e.g., mammoths) roaming earth during that period, for example, by transmit-
ting diseases to the mammals of areas that did not previously have dogs (see,
e.g., Fiedel, 2005) or because they increased humans’ hunting success so sig-
nificantly during the Pleistocene period. This, however, is purely speculative.
Yet, undoubtedly, for this type of relationship to have lasted over time, and
developed to the extent that it did, it must have brought substantial advantages to
both species, and likely these advantages were related to food intake. An inter-
esting study was conducted on the hunting success of today’s humans on moose,
in relation to the group size of the hunting party and the presence/absence of
dogs (Ruusila & Pesonen, 2004). Results clearly showed that the presence of
dogs increased hunting success, especially in human parties of fewer than ten
individuals, and where moose density was lower. Indeed, the role of dogs was
mostly to halt the prey, allowing one hunter to shoot down the animal down, and
the other hunters to be strategically placed to cut off the animal’s escape route.
It is therefore quite likely that a similar pattern occurred also in the past.
In the northern hemisphere, large ungulates such as moose were likely one of
the main food sources for both humans and wolves; however, rather than enter
in competition, what may have happened is that wolves and humans were able
to take advantage of each other’s specific skills. The hypothesis is that while
humans in those times already had the necessary tools (e.g., spears) to success-
fully kill large prey (Grayson & Meltzer, 2002), wolves would have been much
faster and more skilled at tracking and immobilising the prey, as indeed dogs
are today. The possibility is therefore that humans may have learned to follow
wolves to their selected prey and, with their more advanced technology, would
have succeeded in more rapidly finishing off the large animals after the wolves
had immobilised them. Assuming that then, as now, the presence of wolves/
proto-dogs increased hunting success, it would explain why our ancestors were
willing to share their spoils with the wolves/proto-dogs they hunted next to.
So while the timing of events changes the picture of dog domestication quite
a lot, the self-domestication hypothesis could still explain this first wave of
domestication. Both species—humans and wolves—were hunting for the same
15
Chapter | 1 The Social Dog: History and Evolution
prey. Both species possibly benefitted from hunting ‘together’ (i.e., alongside
each other). Maybe both species picked up on certain signs coming from the
other, indicating when prey was around and a hunt was imminent. Both species
probably followed each other’s routes in the expectation to find prey, though
here it is more likely that humans followed wolves, given that wolves’ ability to
detect prey were most likely much more advanced back then, as they are today.
Once prey was detected and the hunting started, the much faster wolves were
likely with the prey long before humans arrived and maybe started to attack, or
surround and immobilise, the prey while humans arrived later to finish the kill
with tools. The question is what may have happened next. Most likely, wolves
were not eager to let go of the prey after they had started the attack. So it could
be that in order to obtain it, the humans would have had to chase the wolves
away (not unlike how hyaenas react to African wild dogs at prey sites) or vice
versa. It is interesting to note that data so far suggest that hunting in packs
for a number of canid species is advantageous because it allows them to keep
scavengers away, rather than because it allows larger prey to be taken down
(see Section 1.1.4 earlier). Hence, success at holding on to the prey may have
depended on numerical factors in both species. However, humans may at some
point have recognised the benefit of these hunting ‘allies’ and chose to share the
spoils by cutting off pieces of the prey for the wolves (perhaps those parts which
humans have more trouble with, e.g., bones), not unlike a modern human–dog
hunting scenario. Following this scenario, it may be that the initial relationship
was one based on a mixture of reciprocal scavenging/scrounging of each other’s
prey, where on occasions, both species contributed to the actual killing, slowly
consolidating the advantages of following each other on the same hunts.
In this scenario, the self-domestication hypothesis can still easily explain the
first wave of domestication. A change of temperament due to self-domestication
would still mean a selection advantage in that wolf individuals that were less fear-
ful and aggressive around humans were probably the ones that were more likely
to join these hunting scenarios and probably also to benefit from scavenging and
leftovers. Most likely another wave of domestication occurred later, when humans
had settled and established agriculture. That changes during times of agriculture
actually put additional selection pressures on dogs is supported by recent work,
which suggests that dogs have adapted specifically to the starch-rich diet typical
for modern human agricultural societies (Axelsson et al., 2013). One can only
speculate as to what extent and how these additional selection pressures to cope
with life in close proximity to humans in times of agriculture also affected dogs’
behaviour.
Some authors, however, go one step further and argue for a co-evolution
of dogs and humans (e.g., Schleidt & Shalter, 2003). A co-evolution of two
species would mean that not only did both species co-exist (and evolve inde-
pendently while living next to each other), but that one species affected the
other’s evolutionary path and vice versa, e.g., the arms race of two species
that are in a predator–prey relationship. So if we consider the scenario of
16 SECTION | I Theoretical Aspects
a co-evolution of dogs and humans, we would have to show evidence that
being with dogs imposed a selection pressure on humans, which resulted in
a new trait emerging, and show that dogs acquired novel adaptions as a con-
sequence to life with humans. Miklósi and Szabo (2012) use a nice example
to explain what kind of evidence we would be looking for, using human com-
munication. We know that in modern times humans mostly guide dogs through
gestures. So one could speculate, very hypothetically of course, that humans
who used this kind of communication had a selective advantage because they
were more successful in guiding their dogs during hunting and hence were
more successful hunters, received more meat, and had more offspring. The
‘gestural communication’ trait therefore would have established quickly in the
human population, leading to humans regularly and frequently using point-
ing gestures in their communication—a trait that is seen to be unique to our
species (Tomasello, 2008). This scenario, however, is pure fiction, just an
example meant to illustrate the kind of process that would have had to occur
to justify the use of the term ‘co-evolution’ to refer to the dog–human evolu-
tionary relationship. As of yet, we, however, see no evidence of any trait being
established in the human population as a direct consequence of being with
dogs. We therefore think, similarly to Miklósi and Szabo (2012), that using
the term ‘co-evolution’ is rather misleading. In fact, at present, what is certain
is that the two species, wolves and humans, co-existed and evolved in paral-
lel for a long time, but at a certain point the co-existence led to advantages
that were significant enough for both species to continue seeking/maintaining
such proximity. Indeed, viewed in this light, the term ‘symbiotic mutualism’,
which indicates both species’ benefitting from living in this kind of relation-
ship, would be more appropriate (Coppinger & Coppinger, 2001; Reid, 2009).
1.2.4 Effects of Domestication on Social Behaviour
and Cognition
One crucial question, especially for a book like this one, is to what extent domes-
tication affected dogs’ behaviour and more specifically dogs’ social behaviour.
Clearly, domestication affected dogs’ morphology in ways paralleled by other
domesticated species (e.g., goats). Compared to wolves, dogs, for example,
have a reduced cranial capacity, have smaller canines, and also show a great
variety of fur pigmentation. Dogs also show a variety of paedomorphic features
in their morphology (e.g., large eyes, short nose; see Wayne, 1986), and some
speculate that they may also show paedomorphic features in their behaviour
(e.g., more play behaviour in dogs than wolves; Topál et al., 2005; see also
Bekoff, 1974, and Chapter 4 of this book). One selection pressure that has been
suggested to be crucial for the evolution of paedomorphic features is the selec-
tion against aggression (Trut et al., 2009), although, in fact, whether dogs are
indeed less aggressive than wolves, particularly in their intraspecific interaction,
has been questioned (Fedderson-Peterson, 2007; and see Chapter 2 of this book
17
Chapter | 1 The Social Dog: History and Evolution
for an in-depth discussion of this issue). Nonetheless, regardless of how specific
paedomorphic features emerged in dogs, a recent study by Waller et al. (2013)
suggests that they may indeed give dogs a selection advantage, because of the
preference humans show for these characteristics. In this study, the research-
ers used dog selection from a shelter as a proxy to study which features most
affected humans’ choices. Interestingly, dogs that produced a facial movement
(inner eyebrow raise) that made the dogs’ eyes look larger were selected from
the shelter quicker than dogs that did not produce that same facial movement as
often. Other behaviours such as tail wagging had no effect on selection. Results
from this study therefore suggest that humans (most likely unintentionally)
select along their preferences for paedomorphic features in dogs’ behaviour
(Waller et al., 2013).
Undoubtedly, domestication has had various repercussions on dogs’ social-
ity and cognition both in terms of their behaviour towards humans (see Chapter
2 and preceding section), and, equally interestingly, also in terms of dogs’ intra-
specific social organisation and behaviour (Chapters 2 and 3).
In terms of how domestication may have affected dogs’ social behaviour,
there is evidence that dogs, if living in conditions under which they are able to
form social groups with conspecifics, form stable, hierarchical groups, with a
social structure most likely resembling that of free-living wolves (see Chapter
3). Nonetheless, a number of differences in the intraspecific social behaviour/
organisation of wolves and dogs have been suggested by various authors, the
most prominent being dogs’ lack of pair bonding as the primary mating strategy
(Lord et al., 2013; Cafazzo et al., submitted); differences in parental care invest-
ment, with a reduced involvement of fathers and other pack members in litter
raising in dogs (Pal, 2005; Lord et al., 2013); a decreased reliance on coopera-
tive hunting strategies in dogs (Boitani & Ciucci, 1995; Boitani et al., 2007) and
less stability or reliance on the social group (Boitani & Ciucci, 1995; Coppinger
& Coppinger, 2001); a reduced/altered presence of a hierarchical organisation
within dog social groups (Boitani & Ciucci, 1995; Boitani et al., 2007); and
an increased tolerance (reduced aggressiveness) towards conspecifics in dogs
(Frank & Frank, 1982; Miklósi, 2007; Hare et al., 2012), but also the opposite,
that is, a decreased tolerance (or heightened aggression) towards conspecifics
in dogs and consequent decrease in cooperation (Fedderson-Peterson, 2007)
(see Chapters 2 and 3 for a discussion of most of these issues).
As can be deduced from the conflicting hypotheses being presented, to date,
firm conclusions on the effect of domestication on intraspecific social behav-
iour are impossible to draw. Indeed, this area of research has noticeably lagged
behind, probably due to the fact that although an estimated 83% of dogs world-
wide are thought to live largely free of direct human influence (Lord et al.,
2013), studying these populations is substantially harder than analysing the
behaviour of owned (pet) dogs, and perhaps because being human, we are more
interested in how dogs may have adapted to life with us, rather than the potential
effects of these adaptations to their behaviour towards each other.
18 SECTION | I Theoretical Aspects
Indeed, more has emerged as regards the potential effect of domestication
on dogs’ social behaviour towards humans. When dogs live with humans, they
do show behaviours that we do not seem to find in wolves raised in similar con-
ditions. Evidence that the bond between dogs and humans might be ‘special’
comes from research showing that dogs develop levels of attachment to humans
that might be comparable to the attachment of children to their parents (see
Chapter 6; see also Chapter 8) and which have not been found in wolves raised
in a similar way to dogs (Topál et al., 2005). Furthermore, in a number of stud-
ies, similarly raised wolves were slower or more reluctant to establish eye con-
tact with a human partner (Gácsi et al., 2005; Virányi et al., 2008; Gácsi et al.,
2009), and appeared to be less likely to adapt their behaviour in accordance with
a human’s change in attitude from threatening to friendly (Gácsi et al., 2013).
However, the latter study was conducted with pet dogs, rather than dogs raised
and living in the same manner as the tested wolves; hence, it is not clear whether
dogs being better attuned to the human partners’ behavioural changes was due
to experience or indeed an effect of the domestication process. Indeed, studies
comparing identically raised wolves and dogs show that the former accept the
humans they were raised with as social partners, inasmuch as they readily use
them as a source of information (e.g., following their gaze; Range & Virányi,
2011) and learn from them in various tasks (Range & Virányi, 2013, 2014).
Although, given the relative shyness wolves exhibit towards human strangers
compared to the ready friendliness of dogs, it may be that extending (or gener-
alising) the relationship of social partnerships to humans in general may be less
likely to occur in wolves. A recent study has nicely shown how oxytocin may
be involved in the establishment of the human–dog partnership both towards
the owner and towards strangers (Kis et al., 2014); hence, this may also provide
important implications as to the potential genetic underpinnings of the selective
changes from wolves to dogs in their sociality towards humans.
The strongest evidence to date, however, as regards to how the selection
pressures during domestication may have affected dogs’ social cognition comes
from research showing that dogs seem to have extraordinary skills in understand-
ing human forms of communication (for a review, see Kaminski & Nitzschner,
2013; see also Chapter 11). Dogs seem to stand out in the animal kingdom in
how sensitive they are to human communication. One hypothesis that has been
put forward is the domestication hypothesis, which suggests that through selec-
tion pressures during domestication, dogs evolved special social cognitive skills
that are in some domains functionally equivalent to that of humans (Hare et al.,
2002; Miklósi et al., 2003; see also Chapter 2 in this book for a discussion).
The hypothesis that selection pressures during domestication might have
affected dogs’ skills when it comes to the sensitivity to human communica-
tion is supported by several facts. First, dogs outperform other species when it
comes to their understanding of cooperative communicative signals (e.g., the
human pointing gesture). Dogs even outperform humans’ closest living rela-
tives, the chimpanzees, in how well they respond to these gestures (Hare et al.,
19
Chapter | 1 The Social Dog: History and Evolution
2002; Bräuer et al., 2006; Kirchhoffer et al., 2012). Dogs also outperform their
own closest living relative, the wolf, when it comes to reading subtle com-
municative cues and without receiving any special training (Hare et al., 2002;
Miklósi et al., 2003; Virányi et al., 2008; but see Udell et al., 2008, and Hare
et al., 2010, for a recent discussion). Finally, dog puppies, from an early age
on and again without receiving any major training, already follow human ges-
tures, suggesting that major learning during ontogeny cannot account for dogs’
behaviour in this domain (Riedel et al., 2008; Virányi et al., 2008). So while
the evidence is accumulating that selection during domestication seems to have
affected dogs’ skills in this domain, several hypotheses exist for how and to
what extent this may have occurred. As this is very much the topic of the chap-
ter by Viranyi and Range (Chapter 2), we do not go into much detail here and
rather simply summarise the hypotheses as falling into four main categories:
(1) the category that would predict generally advanced social cognitive skills in
dogs compared to other species (including wolves) (Hare & Tomasello, 2005);
(2) the category that would predict different (maybe more advanced) social
cognitive skills in some areas of dog social cognition as a special adaptation to
life with humans (Gasci et al., 2009; Kaminski & Nitzschner, 2013; Miklósi &
Topál, 2013); (3) the category which predicts that dogs’ social cognitive skills
are shared with wolves (and potentially other canids), and dogs’ uniqueness lies
in their capacity/willingness to direct these more easily towards human social
partners (see Chapter 2); and (4) the last category, which predicts no true differ-
ences between dogs’ cognitive skills and that of their closest living relative the
wolf, even when directed towards humans (e.g., Udell et al., 2008). It should be
noted, however, that researchers in this last category also do not categorically
rule out the effects of domestication on dogs, but rather they attribute possible
differences between the species on environmental influences and differences
in the development of dogs and wolves. Despite differing predictions, what is
interesting to note is that all hypotheses recognise some impact of domestica-
tion on dog’s behaviour and cognition; hence, what is rather being debated is
more specifically which behaviour and/or mechanisms may have been affected
and how such effects may have been brought about (e.g., specific changes in
genetic, epigenetic aspects of the two species). Unfortunately, currently, a
number of problems do not allow us to draw firm conclusions as regards the
validity of the suggested hypotheses.
One important point emerging from various studies is the need for more
comparable or standardised methodologies. Thus, for example, the hypothesis
put forward by Udell et al. (2010) is mainly based on one study in which
Udell et al. (2008) compared the behaviour of hand-raised (and specially
trained) wolves with that of normal pet dogs and former street dogs. The study
showed that, in fact, the hand-raised wolves outperformed the former street
dogs, suggesting that ontogeny might have affected the individuals more
than any selection during domestication. However, there is a major differ-
ence between this study compared to all other former studies looking at dogs’
20 SECTION | I Theoretical Aspects
(and wolves’) understanding of the human pointing gesture. The paradigm
that most researchers use is the so-called objects choice paradigm (Anderson
et al., 1995). In this paradigm, the animal is presented with two (ore more)
containers, one of which contains a piece of food that was hidden outside the
animal’s view. So, in the absence of any direct information about the loca-
tion of the food, the animal is then presented with some social information,
e.g., a pointing gesture indicating where the food is hidden. After the animal
receives that information, it is encouraged to make a choice between the pre-
sented containers. A correct choice would be counted as a choice in which
the animal follows the gesture and therefore finds the food, and consequently,
an incorrect choice would be any choice for the container the human did not
point to and hence did not contain the reward. Udell et al. (2008), however,
also counted trials in which subjects refused to make any choice as incorrect
choices. This means that any trial in which a subject was maybe too shy or
not motivated at all to participate was treated identically to trials during which
subjects chose the incorrect location, hence the location the human had not
pointed towards. A re-analysis of the data excluding trials during which sub-
jects did not make any choice changed the picture completely, suggesting that
the influence of ontogeny was not at all as strong as the authors had suggested
(Hare et al., 2010).
A second fundamental issue is the need for comparable subject populations
when testing wolves and dogs (see also Chapter 2) and the complementary need
for more diverse populations of pet dogs and captive/wild wolves to be included
in the subject pool.
The first aspect is crucial because a number of studies advocating dogs’
superior understanding of human communicative skills were based on results
comparing wolves that, although raised by humans during their first few months
of life, were then allowed to live in a captive-like setting with frequent but not
intensive human contact. The dogs in these studies, however, came from a pet
dog population, living in human homes and therefore with a far more intensive
everyday experience of human communication (e.g., Topál et al., 2009; Gácsi
et al., 2013). Similarly problematic, although from the opposite perspective, the
wolves that participated in the study by Udell et al. (2008) were not only hand-
raised by humans, but also received specific and rigorous training in order to
interact with humans. One training method used was the so-called clicker train-
ing. The wolves were rewarded with the sound of a clicker upon performing cor-
rectly. That this might have influenced the wolves’ behaviour to quite an extent
is illustrated by a study by Pongrácz et al. (2013), which showed that clicker
training (as performed on the wolves tested by Udell et al., 2008) strongly
and positively influenced dogs’ response to human gestures. Considering the
wolves’ performance on these tasks was compared to dogs with no such training
experience, it is perhaps not surprising that they performed on average better
than dogs. Hence, in both of these cases, the differing effects of experience on
the two species cannot be ruled out, making any claims to results referring to
21
Chapter | 1 The Social Dog: History and Evolution
‘domestication effects’ highly problematic. Indeed, where identically raised and
kept wolves and dogs have been tested, results have shown substantially smaller
differences than expected (Range & Virányi, 2013).
Widening the subject pool for both species is equally important, for a
number of reasons. First, today’s wolves are many generations away from the
shared wolf–dog ancestor; hence, a certain amount of caution appears to be
necessary when concluding that domestication is directly responsible for all
the potential differences observed between these two species. Indeed, consid-
ering the history of heavy persecution of wolves, it is quite probable that their
current shyness towards human beings may have been indirectly selected for
by the extermination of the ‘bolder’ wolves that did not keep well away from
human establishments. This inadvertent selection for shyer wolves may have
resulted in a suite of other by-products being passed on across generations as
‘covariants’ to shyness. Although it is reasonable to assume that the change
from common ancestor to today’s wolves may have been less rapid or dramatic
than that of dogs, we cannot assume that wolves as a species have remained
unchanged since their divergence from the wolf–dog ancestor. Indeed, this
seems to be supported by evidence of a serious genetic bottleneck and con-
sequent loss of genetic variability occurring in grey wolf populations both in
Europe and North America (Leonard et al., 2005; Sastre et al., 2011). In fact,
if the extermination of wolf populations by humans has resulted in the survival
of the shyer animals, it may be that differences between today’s wolves and
dogs are the result of opposite selection pressures, one for increased shyness
and the other for an increased tolerance/affiliation towards humans. Further-
more, there is growing evidence from genetic studies that dogs may have, in
fact, derived from a now-extinct subspecies (Thalman et al., 2013). Consider-
ing the above, it seems all the more important to broaden the focus of studies
to include as many subspecies of wolves as possible. Although this may be
difficult as regards experimental studies, a comparison between subspecies on
their intraspecific social behaviour may already shed light on the potential
variability within this species.
The second aspect worth considering in support of widening the subject
pool is that although a lot more is known about the social behaviour of grey
wolves than of many other canid species, the number of populations studied
(both in the wild and in captivity) is, in fact, relatively small, and given the
high intraspecific variability displayed by many canids depending on ecologi-
cal factors (Macdonald & Sillero-Zubiri, 2004b; Macdonald et al., 2004), it is
quite probable that with more populations being studied, a greater social flex-
ibility will emerge amongst wolf populations. The exact same argument is even
more applicable to free-ranging and feral dogs, where even fewer studies are
available (see Chapter 3 for a more in-depth discussion of this point). Hence,
for example, current conclusions on the potential differences between the intra-
specific social behaviour of these two species will need to be re-assessed once
a larger dataset on both species (in the wild and captivity) becomes available.
22 SECTION | I Theoretical Aspects
A similar argument applies also to cognition studies, where to be able to get at
questions relating to the relative importance of experience versus ‘domestica-
tion’, it would be overly important to include a variety of study populations,
particularly those with a reduced experience of humans (e.g., free-ranging dogs
with more or less human experience).
A third issue needing attention is that in the context of many of the socio-
cognitive abilities under examination, a comparison needs to be made not just
with wolves but also with other canids and other social mammals. A nice exam-
ple, in historical terms, is that of the study of dogs’ understanding of human
attentional states. As mentioned previously, dogs’ potentially extraordinary
abilities first emerged as regards their understanding of human communicative
gestures, where dogs appear to be outstanding in the animal kingdom (Hare
et al., 2002); however, it later emerged that dogs are also very sensitive to
humans’ attentional states (e.g., Call et al., 2003) in that they seem to under-
stand when a human is watching them and will avoid stealing food when the
human has her eyes open versus closed or her back turned towards them (Call
et al., 2003; Schwab & Huber, 2006; for a review, see Chapter 10 of this book).
Based on this evidence, claims were made that this seemingly sophisticated
understanding of a human’s attentional state might also be the result of pro-
cesses occurring during domestication, leading to hypothesise that not only
have dogs evolved specialised skills in one area (sensitivity to gestures) but
that they have evolved generally more sophisticated skills in all areas of social
cognition (Hare & Tomasello, 2005).
However, a later study found that dogs’ understanding of attentional states
was also displayed in conspecific social interaction, since in a detailed analysis
of dogs at play, Horowitz (2009) showed that not only did the signallers take
into account the receiver’s attentional state prior to emitting a particular signal,
but they also flexibility-adjusted the combination and strength of the signals in
accordance with their audiences’ state of attention. Hence, based on this evi-
dence, it would seem that either dogs’ ability to read human attentional states
was an extension to their ability to read their conspecifics’ state of attention or
vice versa.
Studies on a wider range of species, however, eventually highlighted the
fact that many different social living mammals understand when others are or
are not attentive and, in many cases, not just conspecifcs but humans as well
(see Rosati & Hare, 2009; and Kaminski & Nitzschner, 2013, for a review).
So the current evidence suggests that, in fact, this ability is widespread in
the animal kingdom and must be underpinned by an urgent evolutionary
function (see Emery, 2000). Hence, studies including a wider range of spe-
cies show that at least in the case of dogs’ comprehension of attentional
states, their performance is far from unique, calling into question claims
that domestication has somehow allowed dogs to evolve a more ‘human-
like set of socio-cognitive skills’. Indeed, later evidence also showed that
wolves (like many other social mammals tested) behave very similarly in
23
Chapter | 1 The Social Dog: History and Evolution
tests looking at their comprehension of human attentional states (see Udell
et al., 2011, for evidence of this).
A final issue is that there appears to be an urgent need for better integra-
tion between studies focusing on intraspecific and interspecific social skills to
allow questions regarding the effects of domestication to be addressed. As an
example, it has been suggested that the unique adaptation of dogs within the
human social environment is their understanding of communicative gestures as
‘referential’ (see Chapter 11 of this book). Indeed, as summarised previously,
this idea is supported by data showing dogs’ superior skills, as compared to
wolves and also various primate species, at understanding human communi-
cative cues such as pointing; however, only one study (based on a very small
sample) has also addressed whether dogs may see other dogs’ behaviour as ref-
erential (Hare et al., 1999). In this study, the authors compared whether dogs use
cues from conspecifics indicating the location of the hidden food equally well
as they use human cues. Results showed that, indeed, dogs were able to find
food in an object choice setting equally successfully regardless of the species
communicating with them (i.e., human pointing, dog head turning, etc.; Hare
et al., 1999). If wolves are also found to understand their conspecifics’ gestures
(e.g., the head turn) as referential, the uniqueness of dogs’ ability may lie in
their capacity to easily generalise their conspecific skills to humans, rather than
any new ability having emerged following the domestication process. A nice
example of a more integrated approach to this specific topic is given in Chapter
9, where dogs’ social learning abilities have been assessed both with conspecif-
ics and humans, allowing a more comprehensive picture to emerge. However,
until more integration between conspecific and interspecific studies is carried
out in a more systematic way, the relative merits of the different hypotheses are
difficult to assess.
1.3 CONCLUSIONS AND BOOK OVERVIEW
As we hope we have been able to suggest in the current chapter, dogs’ sociality
and their potentially ‘special’ socio-cognitive skills likely emerge both from
the specific characteristics of their canid ancestry (e.g., a reliance on ‘the pack’
in many contexts, their willingness to form life-long bonds, and a remarkable
social flexibility) and the unique event of having encountered and started living
alongside humans.
Because we think that both dogs’ intraspecific canid skills and their meeting
with humans played a crucial role in shaping the companion we have today, the
chapters of this book focus as much as possible on dogs’ social behaviour and
cognitive skills towards other dogs as well as humans. In the case of cognition,
because so little has been done within an ‘intraspecific’ framework, the empha-
sis cannot but be more on humans.
Hence, following this introductory chapter, and given the importance held
by the different domestication hypotheses in spurring further research, Virányi
24 SECTION | I Theoretical Aspects
and Range (in Chapter 2) outline the major theories, highlighting the impor-
tance of ‘older’ studies comparing wolves and dogs, and emphasising the need
for these to be taken into account when developing new hypotheses.
Together, we hope these first two chapters set the theoretical framework in
which many of the following issues addressed by each author can be read. The
remaining chapters of the book are organised in two major areas: (1) studies
focusing on dogs’ social behaviour directed towards other dogs and humans;
and (2) studies focusing on dogs’ social cognition.
The dogs’ social behaviour in their conspecific setting is first addressed in
Chapter 3 by Bonanni and Cafazzo, who review the theories regarding the effects
of domestication on dogs’ social structure and organisation and give a compre-
hensive overview of their studies on a population of free-ranging dogs living in
the outskirts of Rome, integrating their own results with those of other research-
ers. In the subsequent chapter (Chapter 4), Smuts presents a number of results
from studies on the social behaviour and social organisation of pet dogs frequent-
ing a ‘dog day care centre’ and hones in on play as one of the only affiliative
behaviours currently being studied in dogs. Taken together, these chapters appear
to highlight the variability and flexibility of dogs’ social behaviours and clearly
show that many more studies are needed in this field of research to allow us to
better comprehend the variables affecting dogs’ intraspecific social behaviour.
Taylor and colleagues, in Chapter 5, nicely bridge the gap between conspe-
cific and interspecific studies, by presenting an overview of studies on dogs’
acoustic communication, both in relation to other dogs and to humans. Indeed,
a comparison with the wolf communication system leads the authors to suggest
that a number of vocal adaptations in dogs may indeed be in response to their
increased need to communicate with us.
In Chapter 7, Miklósi and colleagues give an in-depth and critical overview
of studies on dog personality, highlighting exciting new research on the genetic
underpinnings of personality traits and presenting the wide range of implications
of dog personality amongst others for the establishment of the dog–human bond
and dog welfare issues. Following on from this chapter, the dog–human bond is
focused on more specifically by both Prato-Previde and Valsecchi (Chapter 6) and
Mills and colleagues (Chapter 8). In the former chapter, the authors give a compre-
hensive overview of studies on ‘attachment’, starting from a historical introduction
of this concept and following on with studies looking at different dog popula-
tions and discussing what the origins of the dog–human attachment bond may be.
The latter chapter shows how behaviours considered problematic by owners may
indeed arise from expectations established in the social relationship between our
two species, or misrepresentation of species-specific behaviours. As in any social
relationship, a number of elements may ‘go wrong’, and the current chapter has
important implications both from the theoretical and applied perspective.
The final five chapters of the book (Chapters 9 to 13) focus on major areas
being investigated under the umbrella term ‘social cognition’. In the first
25
Chapter | 1 The Social Dog: History and Evolution
chapter of this section (Chapter 9), Pongrácz, gives a critical overview of stud-
ies conducted investigating social learning in dogs, setting these studies in the
context of the wider research being carried out on social learning in animals. As
mentioned previously, this area of research nicely integrates both conspecific
and interspecific studies on the same question, setting a potential blueprint for
the future.
In the subsequent chapter (Chapter 10), Bräuer tackles this difficult question:
Do dogs understand humans as mental agents? Drawing on numerous studies
looking at how dogs relate to humans in different contexts, Bräuer presents
interesting results in the field of dog social cognition research. By comparing
results to those with other species, the author sets dogs in a wider context, con-
cluding that although dogs may have ‘special talents’ in understanding humans’
communicative intent, they might not ‘read’ humans as fully intentional agents,
as humans do one another.
In Chapter 11, Topál and colleagues expand on dogs’ ‘special talent’, pre-
senting an in-depth overview of the studies carried out on dog–human com-
munication, contrasting these with results from wolf studies and drawing the
parallel but also highlighting the differences between infant–adult and dog–
adult communication. Together, these chapters cover some of the major topics
being discussed in the field.
In the final two chapters (Chapters 12 and 13), some of the more innovative
aspects of the dog cognition research are presented. In Chapter 12, Burman
gives a critical overview of studies on dogs’ ‘cognitive bias’, setting these in
the context of similar studies in other species and highlighting the potential
implications for animal welfare. Whereas in the final chapter, Siniscalchi and
Quaranta present results from their studies on dog brain lateralisation, showing
how this may link to dogs’ emotions, cognition, and communication, and be
used as a tool in assessing dog welfare.
The study of dog social behaviour and cognition is relatively young; hence,
it not surprising that, in many areas, authors mention the need for more stud-
ies. Because it is our hope that this book will spur the next generation of dog
researchers to continue applying their talents to this field, we explicitly asked all
authors to include further directions in the field, highlighting which, according
to their expertise, are the major questions still needing an answer. We hope this
will inspire readers to ‘go find’ these answers.
ACKNOWLEDGEMENTS
The writing of this chapter and editing of the entire volume were done whilst being supported
by grants from the University of Milan and funding from the European Research Council
under the European Union’s Seventh Framework Programme (FP/ 2007-2013)/ERC Grant
Agreement n. [311870] to Sarah Marshall-Pescini. We wish to thank Simona Cafazzo for
constructive discussions and useful comments on parts of this manuscript.
26 SECTION | I Theoretical Aspects
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