animal domestication and behaviour - s u · animal domestication and behaviour with focus on the...
TRANSCRIPT
Animal domestication
and behaviour
With focus on the domestication of
the dog (Canis familiaris)
DOKTORANDUPPSTATS
Christina Hansen, PhD student
Stockholm University
2
TABLE OF CONTENTS
Part I
1. Abstract 3
2. Introduction to domestication 4
3. Selection for tameness – the farm fox experiment 6
4. Cause and effect of domestication 11
1. Neuro-‐endocrine causation of the domesticated phenotype 13
1. Thyorid horomone metabolism 14
2. Glucocorticoids 15
Part II
5. Domestication of the dog 18
1. The ancestral origin of the domestic dog 18
2. When was the dog domesticated? 19
3. The geographical origin of the domestic dog 20
4. How was the dog domesticated? 22
6. Conclusion 27
7. References 28
3
1. ABSTRACT
Part I of the paper is an overview of the domestication process. Man started domesticating livestock
animals around the time when the society structure gradually changed from hunter-‐gatherers to
agriculture about 10,000 years ago. Domestication is an evolutionary process driven by natural,
conscious and un-‐conscious selection in which a population of animals gradually adapts to life in
captivity. Some animals are naturally more equipped for a live as domesticated animals, and the
domesticated species are largely biased towards ungulates and birds. Domestication is strongly driven
by selection for desirable behavioural traits such as tameness and decreased aggression. A long-‐term
study beginning in the Soviet Union in the late 1950’s showed how quickly some degree of
domestication could be obtained by selectively breeding for tameness in a population of farm foxes.
With the behavioural changes brought about in the study dramatic morphological changes followed as
well; changes that are characteristic across various domesticated species. These changes are as a
syndrome referred to the domesticated phenotype. The underlying mechanisms for these changes are
found in alterations of the physiology, especially in the neuro-‐endocrine system.
Part II of the paper evolves around the domestication of the dog. The domestication of the dog
remains a popular and quite controversial subject. The dog was domesticated from the grey wolf at
least 15,000 years ago, but both fossil findings and molecular analyses points in the direction that the
dog is in fact much older than that. Using arguments based on genetic analyses there is an on-‐going
discussion if the domestic dog originated from Southern East Asia or from Europe/the Middle East.
The question remains unanswered. As do the question of how the dog was domesticated. The
individual-‐based selection theory suggests that the domestication of the dog started with taming and
breeding of individual wolves, whereas the population-‐based selection theory suggests that the
wolves them-‐selves started the domestication process by gradually increasing the acceptance of
humans. With little conclusive evidence on the subject as a whole, this part of the paper gives an
overview of the different perspectives of the domestication of the dog.
4
2. INTRODUCTION TO DOMESTICATION
It has proven problematic to obtain general consensus about the definition of domestication
(Crockford, 2002; Gentry et al., 2004; Driscoll et al., 2009; Morey, 2010; Zeder, 2012). A probable
explanation for this discrepancy is the difficulties in understanding the various intermediate stages in
the continuum framed by the two extremes observable for us today; the wild ancestor and its truly
domesticated derivative. Domestication is not necessarily the only alternative to a wild existence, and
the concept could be looked upon as a gradual process with little or no absolute values when we try
to quantify the degree of domestication in an animal originated from a wild ancestor (Gentry et al.,
2004; Dobney & Larson, 2006; Driscoll et al., 2009). However, domestication in a broader perspective
can be described as an on-‐going evolutionary process that happens through a combination of genetic
and environmental induced developmental changes occurring over generations through natural,
conscious and unconscious selection. By this process a population of animals gradually becomes
adapted to man and to the captive environment he provides(Price, 2002; Gentry et al., 2004; Morey,
2010; Zeder, 2012).
Gentry et al. (2004) states four main characteristics that collectively describes the most developed
form of a domesticated animal: 1) Breeding should be under human control, 2) the domesticated
animal should be of use to humans by providing some sort of product or service, 3) the animal should
display a behaviour that can be classified as “tame”, and 4) the animal has been selected away from its
original wild type. Isaac (via Crockford, 2002) stated a very similar description of a truly domesticated
animal already back in 1970, and adds a fifth point to the above; that the animal’s survival should
depend on humans, whether voluntarily or not. However, far from all domesticated animals actually
possess all these features, and we might find ourselves struggling with placing particular animals
and/or species in strictly wild or strictly domesticated categories (Gentry et al., 2004).
Part I
5
Animals possessing certain behavioural and physical traits are considered more suited for
domestication than others, and can be described as being “pre-‐adapted” to become domesticated
(Price, 2002; Drsicoll et al., 2009; Zeder, 2012. The level of pre-‐adaptation is determined by the capacity
of individual animals of a given species to adapt to a captive environment. Thus parameters such as
social organization, reproductive behaviour, dietary needs, habitat requirements and response to
humans are all factors in determining a species potential for domestication (Diamond, 2002; Price,
2002; Driscoll et al., 2009; Zeder, 2012). Species displaying a natural behaviour resembling the
behaviour expected and possible in captivity is considered to posses the largest degree of pre-‐
adaptation. Pre-‐adaptational traits in the natural range of a species’ ecology are primarily traits that
make it easier for humans to in-‐cooperate themselves in the life of the animals by taking leadership
and controlling and manipulating reproductive behaviour and food sources (Diamond, 2002; Zeder,
2012). Thus species with large gregarious and social group structure are more pre-‐adapted than
territorial species living in family groups, and species with promiscuous and/or polygamous mating
systems are more pre-‐adapted than species with a monogamous mating system. Furthermore, species
with a more flexible ecology, such as a generalist and omnivores are more flexible in their adaptation
to captivity than species with highly specialized dietary preferences (Price, 2002; Zeder, 2012). The
majority of domesticated species are to a large (Cameron-‐Beaumont et al., 2002; Diamond, 2002; Price,
2002; Driscoll et al., 2009) extent biased towards ungulates and gallinaceous birds, which strongly
indicates that pre-‐adaptation for domestication was present in the wild phenotype of these species.
This suggests that pre-‐adaptation varies with species’ and that different orders of animals might not
possess the same capacity for domestication (Diamond, 2002; Price, 2002; Cameron-‐Beaumont et al.,
2002; Jensen, 2005; Driscoll et al., 2009).
When agriculture (and thereby the domestication of plants) emerged about 10,000 years ago
(Diamond, 2002; Price, 2002), it is believed that the initial domestication of the larger ungulate species,
including cattle, directly followed this process (Diamond, 2002; Price, 2002). Pigs (Sus scrofa) are
believed to have been domesticated 9,000 years ago (Jansen et al., 2002; Price, 2002), and rabbits
6
(Oryctolagus cuniculus) 2,500 years ago (Price, 2002). When horses (Equus caballus) were
domesticated remains somewhat inconclusive; authors speculate in a timespan from almost 12,000
years ago (Bruford et al., 2003) to 6,000 years ago (Vila, 2001; Price, 2002). The discrepancy on the
subject has lead to the proposal that horses were domesticated numerous times with various
geographical origins (Bruford et al., 2003).
Tameness can be defined as a behavioural phenotype in which an individual displays some degree of
decreased aggression towards, and increased acceptance of, humans. Individuals displaying tameness
are also likely to show of motivation to approach and/or initiate contact with humans (Trut, 2001;
Price, 2002; Albert et al., 2008). Some wild animals can display various degrees of tameness and vice
versa some domestic animals may display decreased tameness (Diamond, 2002; Driscoll et al., 2009).
Tameness should be separated from tameability; the capacity for an animal or species to be tamed.
Tameability is believed to be a heritable trait and could thereby be a part of the genetic heritage of
domestication. Hence, some species and individuals are expected to be more tameable than others,
which is in accordance with the pre-‐adaptational theory (Diamond, 2002; Price, 2002; Driscoll et al.,
2009). Taming on the other hand, is a learning process in which an individual throughout its lifespan
reduces its avoidance behaviour and aggression directed at humans and increases its willingness to
approach humans (Price, 2002). Domestication and taming are two very different concepts and
processes, and one does not necessarily result in the other (Diamond, 2002; Price, 2002). Taming of an
individual is brought about by a conditioned behavioural modification (Belyaev et al., 1985; Spady &
Ostrander, 2007; Trut, 1999), whereas domestication is a heritable permanent genetic alteration of
species and/or breeds (Price, 2002).
3. SELECTION FOR TAMENESS -‐ THE FARM-‐FOX EXPERIMENT
In 1959 the Russian geneticist Dimitri K. Belyaev (1917-‐1985) initiated a long-‐term study to investigate
the genetics behind the evolutionary process of domestication (Belyaev et al., 1985; Trut, 1999; Spady
7
and Ostrander, 2007). The study was based on the hypothesis that the striking similarity we see across
a broad spectrum of domesticated species today, is brought about as by-‐products of selection for
behaviour (Trut, 1999; Trut et al., 2004;2009; Morey, 2010). Belyaev believed, that the methodical
selection for behavioural traits alone could explain the general domesticated phenotype, and he was
especially interested in the process in which dogs were domesticated from wolf ancestors (Trut,
1999). Thus, he began his study at The Institute of Cytology and Genetics in Novosirbirsk, Siberia – a
study that should become quite remarkable and important in our understanding of the domestication
process (Trut et al., 2009; Morey, 2010).
The study species was silver foxes (Vulpes vulpes), bred as farmed foxes for their fur. The main
hypothesis of the study was based on Belyaev’s own observations that while the foxes were generally
strongly aggressive and fearful towards their human caretakers and handlers, a small fraction of them
displayed a decreased level of aggression and fear (Morey, 2010). This led Belyaev to suggest that
behavioural variation could be the primarily causation and driving force of variation among
domesticates in general (Trut et al., 2009). To investigate whether his theories were accurate, Balyaev
created a strain of foxes selectively bred strictly and solely on the trait tameness and compared them
to an unselected strain. The founder population of the tame fox strain consisted of 100 females and 30
males carefully selected from various fur-‐farm populations (Trut, 1999; Trut et al., 2004; Spady and
Ostrander, 2007). The foxes were chosen based only on observational evaluations of their degree of
tameness, as an experimenter approached and opened their cage. Where wild-‐type foxes displayed
aggressive and/or avoidance behaviour towards humans, about 10% of the farm-‐fox population (more
females than males) reviewed for selection displayed a lowered, or in some cases non-‐present, wild-‐
type response (Fig. 1) -‐ those were the foxes chosen for the founder population (Trut et al., 2009;
Morey, 2010).
8
For every generation following these founder foxes, only the tamest individuals were allowed to
breed. Pups were raised with their mothers until approximately two months of age and then moved to
a different cage with their littermates. Here the pups would stay, until they where put in separate
cages at three months of age (Trut et al., 2004). To assess the level of tameness in individual foxes, the
behavioural testing began already when pups were one month old; here they were offered food by
hand-‐feeding while the experimenter attempted to stroke them. Each pup was submitted to this test
twice; once in a social context when in an enclosure with littermates and once in a solitary context in a
cage. This test was repeated once a month until the pups were six or seven months old. Reaching
sexual maturation at approximately six to eight months of age, the foxes were categorized according
to three classes based on the degree of tameness (Trut, 1999; Spady and Ostrander, 2007):
Class III: Foxes in this class displayed the least tame behaviour; they displayed both fearful and
aggressive behaviour, by attempting to flee from or bite the handler when stroked or
handled. However, by accepting hand-‐feeding these foxes were still considered tamer than
the most docile farm-‐bred foxes.
Class II: Foxes in this class accepted to be handled and stroked without displaying aggressive or
fearful behaviour, but they did not show initiative to approach the handler and they showed
no friendly disposition towards the handler.
Fig. 1. On the left, a fox displaying the wild phenotype, being stressed, scared and aggressive when humans approach the cage. On the right, displaying an altered phenotype, being curious and friendly to human contact. From Trut et al., 2009.
9
Class I: Foxes in this class showed clear friendliness towards the handler by wagging their tails and
whining when approached. They readily accepted hand-‐feeding, stroking and handling.
Class IE: This class was not part of the original set-‐up, but was added in the sixth generation of strict
selective breeding for tameness as a domesticated-‐elite class. Those foxes actively sought the
attention from handlers even when not approached, and would whimper and wag their tails
to induce human contact. They would lick and sniff experimenters once contact was initiated.
The amount of foxes qualifying for breeding in each generation were under strict control, and only 3%
of the males and 8-‐10% of the females in the highest tameness-‐classes were used as parents for the
next generation, creating an extreme selection pressure for tameness (Trut et al., 2004; 2009).
Generation six was the first generation containing elite individuals (EI); out of 213 offspring going
through the behavioural test procedure only 4 individuals were classified as belonging to class EI. This
translates to 1.8% of the tested population. In the 10th generation 66 out of 370 individuals tested were
elite animals, increasing the elite percentage to 17.8%. In generation 20, 1438 individuals qualified for
behavioural testing, of those 503, or 35%, were elite animals. In the 30th generation 1641 individuals
were tested, of those 804 or 49% were elite animals. The elite percentage reached 71.2% in generation
42, where 642 out of 902 individuals tested were elite animals (Mignon-‐Grasteau et al., 2005; Trut et
al., 2009). The changes in tameness over generations are illustrated in table 1.
Table 1 (from Trut et al., 2004): The proportion of individuals belonging to Class IE in different generations
during selective breeding for tameness.
Year Generation No. of offspring
tested
No. of elite
individuals Elite percentage
1965 F6 213 4 1.8
1970 F10 370 66 17.8
1980 F20 1438 503 35.0
1990 F30 1641 804 49.0
2002 F42 902 642 71.2
10
Impressive as these results are, tame foxes with wagging tails and a dog-‐like friendliness towards
humans were not the only outcome of the farm-‐fox experiment. Jensen (2002) describes various
general traits characteristic for the “domesticated phenotype”, which apart from generally reduced
body size and altered reproductive behaviour, includes additional morphological and physiological
alterations. A very characteristic external morphological feature seen in the domesticated phenotype
is the alteration of coat and plumage colours. Depigmentation resulting in varying shapes and degrees
of white patchy colouration is thus seen in a wide range of domesticated animals, such as rabbits
(Oryctolagus cunticulus), pigs (Sus scrofa domesticus), cows (Bos taurus), horses (Equus caballus) and
dogs (Canis familiaris) (Jensen, 2002; Trut et al. 2009). This typical white colour pattern seen in
domesticates might be explained by relaxed selection pressures on predator-‐avoidance (Mignon-‐
Grasteau et al., 2005). Other external morphological traits that are repeated across domesticated
species are features such as curly tails and floppy ears (Trut et al., 2009). The general occurrence of
phenotypically similarities across a wide range of species seems unlikely to have its origin in separate
mutations of structural homologous genes, but rather to be a result of the altered selection pressures
brought about by domestication. Darwin speculated about this very hypothesis in Origin of Species
(1859), and many after him did as well – including Belyaev (Trut, 1999; Trut et al., 2004; Spady &
Ostrander, 2007; Trut et al., 2009; Morey, 2010).
As it turned out, it would seem that Belyaev had been astonishingly correct in his initial hypothesis
(Spady and Ostrander, 2007), that the morphological similarities seen across a wide range of
domesticated species could be explained as by-‐products, or correlated traits, for selection on
tameness alone. Thus, Belyaev and his team did not only see behavioural alterations in the study
population, they also saw striking changes in morphology, all of which were very much in accordance
with the domesticated phenotype as described above. After only 8 to 10 generations colour
alterations started to appear in the study population (Trut, 1998; 1999; Trut et al., 2004). Molting in
brown and yellow colours started deviating from the standard silver grey coat of the foxes and
11
characteristic localized depigmentation, often located on the face in shape of a star (piebaldness)
started to occur. Piebaldness is widely spread in domestic animals, and is claimed to be one of the first
changes appearing in domesticated populations across species (Trut, 1998; 1999). As an example, pale
and spotted coat colourings have been reported to occur in the very early stages of dog
domestication at least 3,000 years BC (Hemmer, 1990; Trut et al., 2004). After a few more generations
of selection for tameness, floppy ears and curly tails starting to appear in the study population, and
after 15 to 20 generations some of the foxes would display shortened tails, shortened legs and
attenuated skull morphology, such as widened skulls, shorter snouts and disproportionate jaws (Fig.
2) (Trut, 1999).
4. CAUSE AND EFFECT OF DOMESTICATION
Domestication is to a large extent driven by conscious selection for desirable traits, which in turn
might lead to unconscious selection for correlated traits, as elegantly illustrated in the farm-‐fox study;
thus the domesticated phenotype likely contains various traits that were not intended, at least not to
begin with (Trut, 1999; Trut et al., 2004; Spady & Ostrander, 2007; Trut et al., 2009; Morey, 2010).
Fig. 2. A few examples of the morphological changes that followed the selection only for tameness in the farm fox project. Top left: two fox kits of which one has visible floppy ears. Top right: a fox with a remarkable short tail. Middle right: a fox with curly tail. Bottom right: fox kits with distinct and dog-‐like white pigmentation. Bottom middle: a fox with distinct white pigmentation exhibiting dog-‐like play behaviour. Bottom left: a young fox displaying an extreme degree of tameness towards its handler (Trut, 1999; Byrne, 2005; Trut et al., 2009).
12
Genes control phenotypic variance, and thus when we select for traits, we are selecting for certain
genes or the alteration of the expression of certain genes (Jensen, 2006).
Increased brain size has been linked with refinement of sensory organs, motor skills and behavioural
flexibility (Diamond, 2002; Sol et al., 2008), and it seems reasonable to assume that these are essential
elements for wild animals to survive. Domesticates in fact do show an overall decrease in relative brain
size when compared to their similar sized wild relatives: pigs (Sus scrofa) 36%, turkeys (Meleagris
gallopavo) 30%, dogs (Canis familiaris) 29%, sheep (Ovis aries) 24%, horses (Equus caballus) 14% and rats
(Rattus norvegicus) 8% (Kruska, 1988; Clutton-‐Brock, 1992; Kruska, 1996; Diamond, 2002; Price, 2002;
Jensen, 2002; Zeder, 2012;). The brain is a very costly organ to develop and maintain, and in a captive
environment, where survival is no longer a daily struggle, it makes good sense that the selective
pressure on brain size eventually became relaxed (Diamond, 2002; Byrne & Corp, 2004; Sol et al.,
2008). As increased relative brain size has been linked to enhanced cognitive function (Byrne & Corp,
2004; Sol et al., 2005), and it naturally raises the question if domesticates then have impaired cognitive
functionality compared to their wild counterparts. However, a smaller relative brain size is not
necessarily the same as a lowered level of cognition (Cooper et al., 2003). Cognition is a broad
category implicating various forms of behavioural capacity, and for instance the social form of
cognition has been shown to be linked the complexity and size of a specific part of the brain, the
neocortex, and not the total size of the brain (Kruska, 1988; Cooper et al., 2003; Sol et al., 2005;
Dunbar & Bever, 2010). Furthermore, it has been suggested that domestic animals might outperform
their wild relatives in learning tests; while wild (but tamed) individuals do have larger relative brains
than domesticated conspecifics, they have also maintained an enhanced sensory system, which will
make them more perceptual to external stimuli. Therefore wild individuals could be expected to have
a general higher baseline level of vigilance, which might divert their focus from the learning task in a
test situation (Kruska, 1988).
13
Many authors have led our attention to the phenomenon “domesticated phenotype” (Clutton-‐Brock,
1992; Trut, 1999; 1998; Crockford, 2002; Price, 2002; Jensen, 2002; Driscoll et al., 2009). Adding to these
morphological changes described in the farm-‐fox study, a general reduction in body size is seen when
comparing domesticates with their wild relatives (Tchernov & Horwitz, 1991; Price, 2002; Jensen, 2002;
Jensen, 2006). Shortening and altered proportions of the skull and legs are also considered to be
changes related to domestication (Clutton-‐Brock, 1992; Jensen, 2006). Reproductive biology
represents another distinct difference, when comparing wild living ancestral species with their
domesticated relatives; in general we see earlier sexual maturation, lowered generation time,
increased reproductive rates and larger litter sizes in domesticated animals (Belyaev et al., 1985;
Tchernov & Horwitz, 1991; Künzl & Sachser, 1999; Price, 2002; Jensen, 2006).
It might seem to be an overwhelming task to connect all these alterations and preferences through
cause and effect, but it remains clear that behaviour and attenuation capacity of behaviour remains
key in animal domestication; when we select for tameness as a behavioural trait, we unconsciously
select for the mechanisms and correlated traits associated with tameness as a behavioural trait. Thus
the intense artificial selection pressures induced upon domesticated animals are for the vast majority
primarily driven by desirable behavioural attributes (such as decreased fear of humans, lowered
aggression, trainability etc.) and secondary with physiological and morphological preferences (Zeder,
2012). But what are we actually selecting upon if we select for behavioural traits – just as Belyaev did
on the farm-‐foxes? If behaviour is the effect, then what is the cause?
4.1 Neuro-‐endocrine causation of the domesticated phenotype
One of the most fundamental effects of domestication is the alteration of the neuro-‐endocrine
system, in turn influencing various physical and behavioural traits in domesticated animals. Thus
domesticates express an attenuated hormonal profile due to alterations of activity in different
secretion systems (Crockford, 2002; Dobney & Larson, 2006).
14
4.1.1 Thyorid hormone metabolism
The morphological, physiological and behavioural changes we see from wild type to domesticate are
for the vast majority traits that are under the influence of thyroid metabolism (Crockford, 2002).
Indications have been found that several traits associated with domestication to a great extent
resemble symptoms for hypothyroidism. Thyroid hormone metabolism plays a crucial role in physical
and cognitive development, both in the embryonic and postnatal state, and have been stated to be
key to domestication through its profound effect on ontogeny in animals (Crockford, 2002; Dobney &
Larson, 2006). In a comparative study on lab rats and wild rats, it was found that domesticated rats
had significantly smaller thyroid glands compared to wild rats. Furthermore, the decreased gland size,
and thus decreased secretion levels, in domesticated rats also reduced flight behaviour when
compared to their wild counterparts (Dobney & Larson, 2006). Another very interesting study on the
effects of thyroid hormones in rats showed how thyroid hormones affect growth and development;
rat embryos were manipulated so that they became hypo-‐thyroidic while still in the womb and again at
the age of 18 days after birth, and compared with non-‐manipulated rats. Hypo-‐thyroidic rats displayed
significant morphological differences from non-‐mainpulated rats, including smaller overall size,
shorter muzzle and floppy ears (Crockford, 2002). Those features are all considered to be traits
included in the “domesticated phenotype” as described above (Jensen, 2002; Trut et al., 2009; Hare et
al., 2012), and these traits also represents the phenomenon of paedomorphism (Crockford, 2002;
Dobney & Larson, 2006). Paedomorphism is the retention of juvenile physiological, morphological and
behavioural characteristics into adult life, and is believed to represent another typical sign of
domestication (Clutton-‐Brock, 1992; Morey, 1994; Goodwin et al., 1997; Crockford, 2002; Cooper et al.,
2003; Driscoll et al., 2009; Hare et al., 2012). It has been suggested that paedomorphism might be the
result of conscious selection for docility, which would equal selection of animals displaying slower
reaction patterns to external stimuli and thus lowered and naive perception of their surroundings
(Clutton-‐Brock, 1992).
15
Using the thyroid metabolism as an example, one can hypothesize how genetic changes actually
induce the alterations we see from wild to domesticated phenotype. The thyroid hormone
metabolism plays a crucial part in the ontogeny, and the regulation of the hormones is so delicate that
even minor alterations might cause profound changes in physiological and behavioural profiles
(Crockford, 2002). Still, though the thyroid-‐controlled ontogeny in wild and captive animals do differ,
the hormonal metabolism still functions in domesticated animals; domesticates just exhibit a
significant lowered thyroid secretion, which is still sufficient to produce the various physiological and
cognitive changes that we see in domesticated animals. An alteration of the functional parts of these
genes therefore seems less likely. Based on this, it is tempting to assume that the differences in
thyroid synthesis between wild and domesticated animals should be found in differences in
components involved in gene expression. This means that domestication potentially could be the
result of the alteration of the non-‐coding part of only a small number of regulatory genes that have
their effect on early development resulting in increased taming capacity (Crockford, 2002; Dobney &
Larson, 2006).
4.1.2 Glucocorticoids
The hypothalamus remains a key component in adjusting neuro-‐endocrine responses according to
altered environmental scenarios. As domesticates must be considered to live in a less extreme and a
less changeable environment when compared to their wild ancestors, it seems reasonable to suggest
that this has changed the selection pressure in domesticates. This in turn could hold part of the
explanation for the altered neuro-‐endocrine gene expression in domesticates (Saetre et al., 2004).
Lowered levels of glucocorticoids have been established in various species when comparing
individuals displaying tame and non-‐tame behaviour. A study on mink, with two strains selected for
“fearfulness” and “confidentiality” respectively, showed that though the individuals of the two strains
had the same capacity to secrete cortisol, fearful mink exhibited significantly higher plasma levels than
the confident mink in a adrenocorticotropic hormone challenge test (Price, 2002). Similar results have
16
been found in silver foxes (Vuples vulpes) methodically bred for tame or non-‐tame behaviour for
generations (Trut et al., 2004). In a study where 15 animals from generation 35-‐40 from the tame
population were compared with 15 animals from the 25th to 30th generation from the non-‐tame
population, plasma levels of ATCH and cortisol were measured and compared in a handling situation.
Results showed that foxes bred for tame behaviour displayed a significantly lowered level of plasma
ATCH and cortisol when compared to the non-‐tame population (Gulevich et al., 2004). Furthermore,
domesticates also show attenuated activity of hypothalamic-‐pituitary-‐adrenal (HPA) responses;
animals exhibiting tameness have higher plasma concentrations of serotonin, which manifests in
lowered aggression (Popova et al., 1991; Trut et al., 2004; Trut et al., 2009; Hare et al., 2012).
The established interaction between glucocorticoids and neurotransmitters only emphasizes the
influence the alterations of these hormonal systems have on behaviour and in turn domestication
(Price, 2002). It seems reasonable to assume that attenuated plasma hormonal levels of mothers in
domesticated species will have an effect on offspring already in the prenatal state (Francis, 1999).
However, indications that postnatal maternal behaviour might also affect the expression of hormonal
responses to stress in offspring have been found (Francis, 1999; Price, 2002). Mothers will differ in
their frequency and quality on displayed maternal behaviour, and variation in maternal behaviour has
been indicated to be individually stable across litters/offspring and furthermore to correlate to the
future maternal behaviour in daughters (Fairbanks, 1989; Meaney, 2001). A study on domestic rats
(Rattus norvegicus) showed an inverse relationship between the frequency of maternal behaviour and
the offsprings’ HPA-‐mediated response to stressful situations in later life. But this relationship also
applied to the quality of maternal behaviour given to the offspring when they were young; mothers
primarily assuming a sitting position with their backs arched and the hind legs to the side when
nursing her pups, raised offspring with a lowered HPA-‐mediated response later in life than mothers
primarily nursing their pups lying down. An arched back posture when nursing provide the pups with
17
more flexibility in terms of nipple switching etc., and is thus considered to be a higher quality of
nursing than when the mothers lie down (Meaney, 2001).
Another study illustrating how alterations of hormonal profiles changes the behaviour of
domesticated animals, was done by comparing domestic guinea pigs (Cavia pocellus) with their wild
ancestor the cavy (Cavia aperea) (Künzl & Sachser, 1999). Seven groups of adult domestic guinea pigs
and five groups of adult wild cavies were used in this study. Each group consisted of three un-‐related
individuals; one male and two females. The behaviour of the animals was recorded daily throughout a
two-‐week period. Furthermore, during the two-‐week study period, males were subjected to a novel
arena test and blood samples were taken before, during and after the test for hormonal analyses.
Results showed that the domestic guinea pigs and the wild cavies showed the same behavioural
repertoire, but the wild cavies showed significantly more aggressive behaviour compared to the
domestic guinea pigs, and the domestic guinea pigs showed significantly more socio-‐positive
behaviour than the wild cavies. Wild cavy males and domestic guinea pig males had the same baseline
level of serum concentrations of cortisol, but in the novel arena test, the wild cavies showed a
significantly increased stress response compared to the domestic guinea pigs. Furthermore, domestic
guinea pig males displayed significantly higher levels of courtship behaviour and serum testosterone
concentrations than the wild cavy males. These results are in accordance with the general consensus
that domestication leads to lowered aggression, lowered stress responses and increased reproductive
behaviour(Belyaev et al., 1985; Tchernov & Horwitz, 1991; Jensen, 2006; Künzl & Sachser, 1999; Price,
2002; Zeder, 2012).
18
5. DOMESTICATION OF THE DOG
As elaborated below, the domestication of the dog turns out to be quite a unique event. In spite of the
obvious lack of the pre-‐adaptational traits suggested for most potential (livestock) domestic
animals(Cameron-‐Beaumont et al., 2002; Diamond, 2002; Price, 2002; Jensen, 2002; Driscoll et al.,
2009), the dog remains the only large carnivore, and the only member of the Canidae family, to ever
be domesticated(Clutton-‐Brock, 1995; Wayne & vonHoldt, 2012).
5.1 The ancestral origin of the domestic dog
The origin of the domestic dog has been a subject of great discussion through time. Given the extreme
diversity seen in domestic dogs many scientists, including Darwin (1859), have speculated whether the
species had its origin in one or multiple wild ancestral species( Scott & Fuller, 1965; Clutton-‐Brock,
1995; Klütsch & Savolainen, 2001; Galibertet al., 2011). Shared haplotypes and successful intra-‐breeding
events among various species in the canid family and domestic dogs might suggest that serveral of the
38 present canid species (Clutton-‐Brock, 1995) have contributed to the genetic basis of the domestic
dog, and thus portrays a more complex ancestry than just a single species origin. Especially the jackal
has been a popular candidate when speculating about possible ancestors (Clutton-‐Brock, 1995; Vila &
Wayne, 1999; Dobney & Larson, 2006; Galibert et al., 2011). However, based on morphological,
phylogenetic, behavioural, and in particular molecular genetic analyses, there is now a general
consensus that the grey wolf (Canis lupus) is the unique ancestor of the domestic dog (Morey, 1994;
Vila & Wayne, 1999; Klütsch & Savolainen, 2001; Wayne & Vila, 2001; Savolainen et al., 2002; Cooper et
al., 2003; Driscoll et al., 2009; Galibert et al., 2011). Still, many researchers are hypothesizing that
multiple wolf populations and/or backcrossing events after initial domestication of the dog can explain
the extreme diversity we see in the more than 400 dog breeds we have today (Vila et al., 1997; Galibert
et al., 2011). However, a large proportion of the substantial in-‐between breed variation could be
produced by a relatively modest number of mutations. Taking into account how many possible
combinations only a few handfuls of mutations can actually produce, this might be enough to explain
Part II
19
the large variety we see within the domestic dog as a species (Scott & Fuller, 1965; Sutter et al., 2007;
Parker et al., 2009; Wayne & vonHoldt, 2012). For example, the morphological phenotype
chondrodysplasia, which we see as the short-‐limbs in dog breeds such as dachshunds and corgies,
derived from the same mutation (Parker et al., 2009; Wayne & vonHoldt, 2012). This is remarkable as
the 19 dog breeds displaying chondrodysplasia were developed in several independent geographical
locations for various purposes, and genomics analyses of their populations’ structure reveals that they
in fact do not share a recent common ancestor (Parker et al., 2009). Adding to that, large variation
among wolves, both between populations but also within one pack, could also support that the
potential for profound within-‐species variation might have been latent from the very beginning of
domestication of the dog (Scott & Fuller, 1965).
5.2 When was the dog domesticated?
The dog was by far the first animal to be domesticated (Klütsch & Savolainen, 2001; Driscoll et al.,
2009; Galibert et al., 2011; Larson et al., 2012). Archaeological findings of dog remains buried with
humans date back to the Stone Age some 15,000 years ago (Morey, 1994; Driscoll et al., 2009; Larson
et al., 2012), but recent evidence obtained from genome-‐sequencing suggest that domestication of
the dog might be more than twice as old dating back to 32,000 years ago (Wang et al., 2013). The
finding of even older dog-‐like remains in Belgium, suggests an incipient dog from as early as 36,000
years ago (Ovodov et al., 2011). Several authors even mention that the dog could have been
domesticated more than 100,000 years ago based on mtDNA control region sequencing showing that
the monophyletic clade representing the domestic dog diverged from the wolf at that time (Vila et al.,
1997; Diamond, 2002; Dobney & Larson, 2006;). The mismatch between the age of the domestic dog
obviously poses some problems. Some claim that using archaeological records in determining the
“when” and where” in the earliest dog domestication has its clear weak points (Klütsch & Savolainen,
2001). Remains are often incomplete and vary greatly in frequency and quality with geography. For
instance, soil acidity in certain areas has a potentially large effect on the quality of excavated bones.
20
Furthermore, determining if early fossil findings are wolf or a dog remains can prove very difficult. For
instance, when are skull proportions different enough for us to separate between ancestral wolf and
early domestic dog (Scott & Fuller, 1965; Morey, 1994; Klütsch & Savolainen, 2001; Wayne & Vila, 2001)?
Ovodov et al. (2011) object to this, by emphasizing that morphological evidence of the gradual
characteristic changes making a wolf into a dog remains the single most reliable criterion to tell the
two relatives apart. Still, even though some find it questionable whether early archaeological findings
are actually wolves or an early stage of domestic dogs, a lot of these fossil remains are found with or
in close proximity to human fossil settlements and/or remains. This suggests that early humans and
wolves, or maybe early dogs, were living close enough together to share the same territories, thus
indicating a potential preliminary domestication processes was already in effect (Galibert et al., 2011).
5.3 The geographical origin of the domestic dog
With the ancestral heritage settled, the geographical origin of the domestic dog remains quite
controversial when discussing the evolution of the species. There is a profound discrepancy regarding
this subject, and the lines seem to be drawn rather hard between the scientists who believe that
Southern East Asia is the geographical origin of the domestic dog (Klütsch & Savolainen, 2001;
Savolainen et al., 2002; Pang et al., 2009; Ding et al., 2012), and the scientists who lead our attention to
Europe and the Middle East (Verginelli, 2005; vonHoldt et al., 2010; Galibert et al., 2011; Wayne &
vonHoldt, 2012) as the possible cradles of the species. As no final conclusions have been found at this
time, a point to address in this discussion is the methods used for analysing genetic material to reach
consensus on the geographical origin of the domestic dog. The advocates for a Southern East Asia
origin of the domestic dog (Klütsch & Savolainen, 2001; Savolainen et al., 2002; Pang et al., 2009)
mainly base their conclusions on genetic analysis obtained from mtDNA. There is an obvious bias
challenge in this set up, as mtDNA is solely maternally inherited. Therefore, mtDNA analyses might be
an inadequate estimator of which individuals actually contributed to domestication, and furthermore,
it will be very problematic to pick up on backcrossing events, which must be considered to be a very
21
likely event in the early stages of dog domestication (Miklósi, 2007). Furthermore, the markers used in
mtDNA analyses are only approximately 15,000 base pairs long. Thus, conclusions based on this form
of mtDNA can possibly be considered diluted and less strong (Vila et al., 2005). However, recent
evidence using a 14,437 bp Y-‐chromosome DNA sequence sampled in 151 dogs around the world shows
a similar pattern as obtained using the mtDNA sequencing and thus supports the belief that the dog
originated from Southern east Asia (Ding et al., 2012).
The researchers arguing Europe and the Middle East to be the possible geographic origins of domestic
dogs mainly use nuclearDNA for their analyses (Wayne & vonHoldt, 2012). NuclearDNA markers have
the advantage of 1) being considerably larger, and 2) not being restricted by maternal inheritance,
which could lead to the assumption that they would give a more nuanced and precise result. However,
too increase the complexity in the discussion further, some authors suggesting a Middle Eastern or
European origin actually do use mtDNA analyses to reach their conclusions (Verginelli, 2005). Either
way, the scientists favouring an European and/or Middle Eastern origin are to a large extent supported
by archaeological evidence (Galibert et al., 2011; Ovodov et al., 2011).
While this seemingly never-‐ending discussion continues, one have the opportunity to wonder if the
scenario of one shared origin of domesticated dogs in fact seems a bit naïve. It seems unlikely that
domestication of dogs was a unique event, taking place in a single isolated location in the world, and
much more likely that domestication arose from various geographical locations simultaneously (Byrne,
2005). This is supported by the fact that archaeological evidence tells us that humans and wolves co-‐
existed in multiple geographic regions during the late Pleistocene( Vila et al., 1997; Dobney & Larson,
2006;). Furthermore, the two earliest dogs known were found in Belgium and Siberia. They are
estimated to be 36,000 and 33,000 years old respectively, and the very early dating held together with
the large geographical separation profoundly points in the direction of a simultaneous and multi-‐
regional origin to the domestic dog (Ovodov et al., 2011).
22
5.4 How was the dog domesticated?
The quite over-‐whelming accumulation of controversies of “when” and “where” in domestication of
the dog leads us to “how” -‐ which turns out to be just as debated. However, based primarily on
archaeological evidence, there is a general agreement (for now) that the dog was domesticated at
least 15,000 years ago during the Mesolithic period, were humans lived in nomadic hunter-‐gatherer
societies with a geographical overlap with wolf populations (Coppinger & Coppinger, 2001; Price, 2002;
Miklósi, 2007; Driscoll et al., 2009; Morey, 2010;). Various theories on how dogs became domesticated
have been proposed. They are all based on a variety of selection hypotheses, and are more or less
convincing in their outlines of how wolves transformed into the domesticated dog. The two most
popular theories involve 1) individual-‐based selection and 2) population-‐based selection (Miklósi, 2007;
Morey, 2010).
Humans from the time of initial stages of dog domestication would be co-‐existing with, and
encounter, wolves on a regular basis (Clutton-‐Brock, 1995; Miklósi, 2007; Morey, 2010). The main
argument in the individual-‐based selection theory is that humans initially did not see wolves as possible
hunting companions and guard dogs, but simply as a clothing-‐ and food source. Pups in a den are very
vulnerable and it is thus hypothesized that humans took wolf pups straight from their dens for
consumption purposes (Clutton-‐Brock, 1995). Just as Balyaev found it in his initial process of choosing
individuals for the founder population of the farm fox study (Trut et al., 2009; Morey, 2010), some of
these pups would likely have displayed a more docile and tame behaviour than others, and those pups
might have been spared and kept within the human settlement and socialized. As the usefulness of
these animals for other purposes than food probably became more and more evident, individuals
continuously displaying desirable features in behaviour and temperament likely became subjects for
selective breeding over multiple generations and the wild wolf gradually and very slowly turned into
the domestic dog (Clutton-‐Brock, 1995; Miklósi, 2007). Advocates of this theory points to the fact that
we see wide behavioural spans and distinctions among pups of wild canids, and that some individuals
23
should be more suitable for domestication than others; i.e. the capacity for taming varies in a litter of
wild pups and some pups are more tame than others. In other words, they are in a rough
interpretation of the concept “pre-‐adapted for domestication” (Price, 2002; Miklósi, 2007; Morey,
2010). The existence of stabile and individual behavioural differences have been shown in a wide
range of species from hermit crabs (Dardanus calidus) to swift foxes (Vulpes velox) (Bremner-‐Harrison
et al., 2004; Sih et al., 2004; Svartberg et al., 2005; Briffa et al., 2008; Sinn et al., 2008; Wolf & Weissing,
2012), but most studies on the subject have been conducted on adult individuals. Studies on such
features in juvenile individuals are sparse, and indications that individual behavioural traits are more
plastic in juvenile individuals when compared to adult individuals have been found (Sinn et al., 2008).
However, studies on wolf pups suggest that individual behavioural differences do become stabile in
the juvenile stage (Mac Donald & Ginsburg, 1981; MacDonald, 1983). In one study (MacDonald, 1983), a
litter of five male wolf pups were raised with their mother in captivity for the first four weeks of their
life. At four weeks of age, the pups were taken from their mother and group housed. The pups
underwent extensive behavioural testing already from 17 days of age. When the pups reached 44 days
of age a cyclic schedule consisting of five periods of no testing and five periods with testing were
introduced. Non-‐testing periods lasted approximately two weeks each, and here the litter was broken
up and pups were in turn housed paired or in isolation. Testing periods were approximately one week
long, in which pups were housed as a litter. Throughout the test periods, various test types were used
to test stability in individual behavioural traits; novel object tests together as a litter and as individuals,
unfamiliar person tests and a bone competition test. The results showed that already from day 30
there was a clear pattern of which pup would repeatedly claim the bone in the bone competition test,
and from day 44 a stabile individual boldness score in the novel object tests throughout the litter was
evident. The conclusion of the study was that early variability in the form of stabile individual
behavioural differences was present in this litter of wolf puppies; individual behavioural patterns
became stabile already around day 44 of age and showed very little variance hereafter. Furthermore,
the study suggests, due to the cyclic discontinued environmental setting for the pups during the
24
study, that environmental continuity is not a necessity for the development of stabile individual
behavioural differences. In another study (Mac Donald & Ginsburg, 1981), wolf pups were raised under
various restricted conditions, and still displayed clear individual behavioural differences, which the
authors even determined to be exaggerated at an early stage due to the restricted upbringing. These
studies supports the argument used by those in favour of the individual-‐based selection theory;
namely that early individual behavioural differences in wolf pups, might have led to the very first
selection initiatives on the way to creating the domestic dog.
The population-‐based theory suggests, that human settlements created a new niche for wolves in
terms of an easy food supply in discarded food and other waste. Less timid wolves successfully
exploited this new niche by living as scavengers, gradually tolerating a closer proximity to humans by
displaying an increasingly lowered flight-‐distance. In time, these animals gained a selective advantage
over the wolves not exploiting the new found resource (Coppinger & Coppinger, 2001; Price, 2002;
Miklósi, 2007; Driscoll et al., 2009; Morey, 2010;). This phenomenon is described as proto-‐
domestication; a natural speciation process in which wild animals themselves found populations
consisting of descendants with modified phenotypes (Crockford, 2002; Galibert et al., 2011). The result
is “primitive natural domesticates” which show higher levels of pre-‐adaption to domestication than
un-‐modified conspecifics. Other authors refer to this process as self-‐domestication (Hare, 2002). The
proto-‐domestication would then be followed up with conscious artificial selection for desirable traits,
once humans realized the gain in domesticating dogs (Coppinger & Coppinger, 2001; Price, 2002;
Driscoll et al., 2009;).
Coppinger & Coppinger (2001) argues that the individual-‐based selection theory requires that our
human ancestors either understood the usefulness of dogs and/or desired them as pets. The question
is, according to Coppinger & Coppinger, whether Mesolithic people had the knowledge to engage in
the ambitious process that directional selection is; how could they? They had no references.
25
Furthermore, the authors emphasize that dog-‐like variation is not present in wild wolf populations
today and thus assumedly was not present in the Mesolithic period either. With the lack of variation,
how could they select for it? Even if our ancestors indeed did see a potential in taming wild wolves
through even the slightest variation in the population, the authors find it highly questionable that they
had the pre-‐disposition to meticulously select for these vague differences generation after generation.
And wolves presumably do not make good pets. Even with extensive socialization, hand-‐reared wolf
pups have been shown to have significantly lower attachment to their human caregivers when
compared to dog pups reared under the same conditions (Topál et al., 2005). Indications have been
found that the socialization period in wolf pups is both shorter and more rigid than in dog pups, and
missing the window of opportunity in terms of socialization in wolf pups seems to be more or less
irreversible (Trut et al., 2004; Topál et al., 2005). Furthermore, wolves are hard to contain and hard to
train (R. Coppinger & Coppinger, 2001). However, authors (Hope, 1994; R. Coppinger & Coppinger,
2001) do point to the fact, that in the juvenile stage, both pure-‐breed wolves and wolf-‐dog hybrids
display a playful and pleasant behaviour towards humans if socialized correctly. However, the idyllic
picture undergoes a very radical change once sexual maturity sets in in these animals at about 2 years
of age; they fulfil their genetic disposition and become the pack-‐oriented, wide-‐ranging and highly
territorial predators they really are. In the case of wolf-‐hybrids, the clash of dog and wolf behavioural
features can prove especially problematic; while the hybrid displays an increased level of tameness
towards humans its predatory instincts remains relatively intact (Price, 2002). Estimates from the
Humane Society in the United States, paints the sinister picture of 80-‐90% of ownerships of wolf-‐dog
hybrids ending in failure before the hybrid reaches the age of 3 years. The outcome is often fatal to the
hybrid, being abandoned or euthanized (Hope, 1994).
With the above in mind, one can only wonder if keeping wolves would be desirable to our forefathers,
or if the attempt to tame single wild individuals would have proven successful (R. Coppinger &
Coppinger, 2001; Price, 2002). Belyaevs legendary study ( Trut, 1998; Trut, 1999; Trut et al., 2004; Trut
26
et al., 2009;) arguably provides support for the individual-‐based selection theory, given that our
ancestors only bred individuals displaying pre-‐adaptation traits for domestication. Belyaev selectively
bred silver foxes solely on the trait “tameness”, which resulted in foxes with dog-‐like features such as
wagging tails, floppy ears and altered coat colours in only 4-‐10 generations. So, individual-‐based
selection can be done with surprisingly fast results. But applying this to the individual-‐based selection
theory raises the obvious question of how individual wolves displaying tameness were successfully
kept and contained throughout sexual maturity and later reproductive stages. Miklosi (2007) argues
that the selective breeding of wolves was not the first stage in domestication of the dog, but occurred
once initial domestication had taken place as a selection for breeds with different morphological and
behavioural pre-‐dispositions. But then we are still left with a missing piece in the puzzle: how did initial
domestication take place?
The self-‐domestication process in the population-‐based selection theory might explain initial
domestication. Some critics of this theory believe that domestication only took place in a few
geographical locations, and raise the question whether it thus seem likely that multiple places where
humans and wolves lived together only resulted in a handful of origins to domestication of the dog.
Another objection to the population-‐based selection theory is that in a hunter-‐gatherer society
enough food waste was not produced to sustain a larger group of scavenging wolves. They would
need to hunt as a supplement, thereby losing their selective advantage of switching to a strict
scavenger diet (Miklósi, 2007). Ovodov et al. (2011) suggest what could be an important fact, and
possible explanation, for the great controversy of the geographical origin of the domestication dog;
domestication depended on several concurrent conditions to be fulfilled, and it thus seems likely the
process would have failed on numerous occasions before it was complete. The authors are strong
supporters of the theory of multiple origins of the domestic dog brought about by self-‐domestication.
However, they also emphasize that certain aspects of human activity, such as hunting techniques,
food surplus and a rather permanent settlement in an otherwise nomadic time period, all were
27
criterias to initiate the self-‐domestication process. If dog domestication indeed was a process
dependent on multiple factors, and the ideal conditions in fact were present, they might only have
existed for a short time, not producing anything but modified wolves with some dog-‐like
characteristics. Adding to this, Crockford (in Morey, 2010) acknowledge that proto-‐domestication
probably happened on multiple occasions, thus supporting the theory that domestication was
initiated serveral times by wild living wolves themselves through self-‐domestication, but the process
often failed in these early stages.
At the end of the day, these two very different domestication theories do have some common ground;
they both boil down to the fact some wolves were more tolerant towards humans than others. Why
was that? Suggestive answers leads us back to the big wheel of alterations of the neuro-‐endorcine
system (Crockford, 2002): the sympathetic adrenal gland function is controlled by adrenergic
receptors and adrenergic receptors are in turn under strong influence of thyroid hormone levels. Thus
thyroid hormones are directly controlling the stress response in animals. Animals (wild and domestic)
display variation in thyroid metabolism both on interspecific and intraspecific levels, which means that
there will be variations in stress responses across populations and species. This could be a plausible
explanation; both entire populations and single wolves displaying a higher stress-‐tolerance would be
better adapted to the novel environment human settlements created. This in turn could have created
a population of proto-‐domesticated animals that later were subject for artificial selection (Morey,
2010). In connection to the earlier paragraph on the proven neuro-‐endocrine changes in domesticated
animals, this theory makes a rather convincing argument. Thus wolves displaying attenuated thyroid
hormone profiles might have founded the domestic dog (Crockford, 2002)
6. CONCLUSION
The domestication process started a cascade of events that gradually changed wild animals in to
animals that we could use for food, transportation, recreation and company. The desirable behaviour
we consciously select for in our domesticated animals originates in basic changes in neuro-‐endocrine
28
pathways, which has lead to further alterations of morphology and physiology. The fascinating study
started by Belyaev back in the 1950’s illustrates the domestication process and all the changes it brings
with it, by only selective for one single behavioural trait. This emphasizes how important a role
behaviour must have played in the animals founding domesticated populations, and how these valued
behaviours were recognized by our forefathers thousands of years ago.
There are still many unanswered questions about the domestication process, and particular in the
domestication of the dog. The seemingly unlikely event of successfully domesticating a large carnivore
as the wolf also happened to be the very first event of domestication, and the subject fascinates many
scientists. As our methods for tracking such events back in time improve, we get a little closer to
answering the questions we so vividly discuss about how, when and where the dog was domesticated.
It might seem more likely that we eventually will learn the answer about the geographical origin of the
dog, and with it how old the dogs is a species, than how the dog was domesticated. While Belyaev has
provided us with the evidence for a possible rapid domestication process by selecting for tameness
alone, the initial process remains puzzling and very hard to answer. With the event of domestication of
the dog lies 15,000 or more years back in time obtaining clues of how this process started are difficult
to obtain. However, increasing our knowledge and understanding of the behavioural differences
between wolves and dogs might be a start.
7. REFERENCES
Albert, F. W., Shchepina, O., Winter, C., Römpler, H., Teupser, D., Palme, R., et al. (2008). Phenotypic differences in behavior,
physiology and neurochemistry between rats selected for tameness and for defensive aggression towards humans. Hormones and Behavior, 53(3), 413–421.
Belyaev, D. K., Plyusnina, I. Z., & Trut, L. N. (1985). Domestication in the silver fox (Vulpes fulvus Desm): Changes in
physiological boundaries of the sensitive period of primary socialization. Applied Animal Behaviour Science, 13, 359-‐370. Bremner-‐Harrison, S., Prodohl, P. A., & Elwood, R. W. (2004). Behavioural trait assessment as a release criterion: boldness
predicts early death in a reintroduction programme of captive-‐bred swift fox (Vulpes velox). Animal Conservation, 7(3), 313-‐320.
Briffa, M., Rundle, S. D., & Fryer, A. (2008). Comparing the strength of behavioural plasticity and consistency across
situations: animal personalities in the hermit crab Pagurus bernhardus. Proceedings, the Royal Society, Biological Sciences, 275(1640), 1305-‐1311.
Bruford, M. W., Bradley, D. G., & Luikart, G. (2003). DNA markers reveal the complexity of livestock domestication. Nature
Reviews. Genetics, 4(11), 900–910. Byrne, R. W. (2005). Animal Evolution: Foxy Friends. Current Biology, 15(3), 86-‐87. Byrne, R. W., & Corp, N. (2004). Neocortex size predicts deception rate in primates. Proceedings of the Royal Society of
London B: Biological Sciences, 271(1549), 1693–1699.
29
Cameron-‐Beaumont, C., Lowe, S. E., & Bradshaw, J. W. S. (2002). Evidence suggesting preadaptation to domestication throughout the small Felidae. Biological Journal of the Linnean Society, 75(3), 361–366.
Clutton-‐Brock, J. (1992). The process of domestication. Mammal Review, 22(2), 79–85. Clutton-‐Brock, J. (1995). The Domestic Dog: Its Evolution, Behaviour and Interactions with People. The Domestic Dog: Its
Evolution, chapter 2. Cambridge University Press. Cooper, J. J., Ashton, C., Bishop, S., West, R., Mills, D. S., & Young, R. J. (2003). Clever hounds: social cognition in the
domestic dog (Canis familiaris). Applied Animal Behaviour Science, 81(3), 229–244. Coppinger, R., & Coppinger, L. (2001). Dogs: A New Understanding of Canine Origin, Behavior & Evolution. University of
Chicago Press, 2nd edition. Crockford, S. J. (2002). Animal domestication and heterochronic speciation. Human Evolution Through Developmental Change,
chapter 6. The Johns Hopkins University Press. Darwin C. (1859). The origin of species. London: Murray
Diamond, J. (2002). Evolution, consequences and future of plant and animal domestication. Nature, 418(6898), 700–707. Ding, Z.-‐L., Oskarsson, M., Ardalan, A., Angleby, H., Dahlgren, L.-‐G., Tepeli, C., et al. (2012). Origins of domestic dog in
southern East Asia is supported by analysis of Y-‐chromosome DNA. Heredity, 108(5), 507–514. Dobney, K., & Larson, G. (2006). Genetics and animal domestication: new windows on an elusive process. Journal of Zoology
(269), 261-‐271. Driscoll, C. A., Macdonald, D. W., & O'Brien, S. J. (2009). From wild animals to domestic pets, an evolutionary view of
domestication. Pnas, 106(1), 9971–9978. Dunbar, R. I. M., & Bever, J. (2010). Neocortex Size Predicts Group Size in Carnivores and Some Insectivores. Ethology, 104(8),
695–708. Fairbanks, L. A. (1989). Early experience and cross-‐generational continuity of mother-‐infant contact in vervet monkeys.
Developmental Psychobiology, 22(7), 669–681. Francis, D. (1999). Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat.
Science, 286(5442), 1155–1158. Galibert, F., Quignon, P., Hitte, C., & André, C. (2011). Toward understanding dog evolutionary and domestication history.
Comptes Rendus Biologies, 334(3), 190–196. Gentry, A., Clutton-‐Brock, J., & Groves, C. P. (2004). The naming of wild animal species and their domestic derivatives. Journal
of Archaeological Science (31), 645-‐651 . Giuffra, E., Kijas, J. M. H., Amarger, V., Carlborg, Ö., Jeon, J. T., & Andersson, L. (2000). The origin of the domestic pig:
independent domestication and subsequent introgression. Genetics (154), 1785-‐1791. Goodwin, D., Bradshaw, J. W. S., & Wickens, S. M. (1997). Paedomorphosis affects agonistic visual signals of domestic dogs.
Animal Welfare Information Center Newsletter (USA), 53, 297–304. Gulevich, R. G., Oskina, I. N., Shikhevich, S. G., Fedorova, E. V., & Trut, L. N. (2004). Effect of selection for behavior on
pituitary–adrenal axis and proopiomelanocortin gene expression in silver foxes (Vulpes vulpes). Physiology and Behavior, 82(2-‐3), 513–518.
Hare, B. (2002). The Domestication of Social Cognition in Dogs. Science, 298(5598), 1634–1636. Hare, B., Wobber, V., & Wrangham, R. (2012). The self-‐domestication hypothesis: evolution of bonobo psychology is due to
selection against aggression. Animal Welfare Information Center Newsletter (USA), 83(3), 573–585. Hemmer, H. (1990). Domestication: The Decline of Environmental Appreciation. Cambridge University Press; 2 edition. Hope J. (1994). Wolves and wolf hybrids as pets are big business but a bad idea, Smithsonian, Volume 25:3
30
Jansen, T., Forster, P., Levine, M. A., Oelke, H., Hurles, M., Renfrew, C., et al. (2002). Mitochondrial DNA and the origins of
the domestic horse. Proceedings of the National Academy of Sciences, 99(16), 10905–10910. Jensen, P. (2002). The ethology of domestic animals -‐ an introductory text. CABI Publishing. Jensen, P. (2006). Domestication—From behaviour to genes and back again. Applied Animal Behaviour Science, 97(1), 3–15. Klütsch, C. F., & Savolainen, P. (2001). Geographical Origin of the Domestic Dog. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd: Chichester.
Kruska, D. (1988). Mammalian Domestication and its Effect on Brain Structure and Behavior (pp. 211–250). Berlin, Heidelberg: Springer Berlin Heidelberg.
Kruska, D. (1996). The effect of domestication on brain size and composition in the mink ( Mustela vison). Journal of Zoology,
239(4), 645–661. Künzl, C., & Sachser, N. (1999). The Behavioral Endocrinology of Domestication: A Comparison between the Domestic Guinea
Pig (Cavia apereaf.porcellus) and Its Wild Ancestor, the Cavy (Cavia aperea). Hormones and Behavior (35), 28-‐37. Larson, G., Karlsson, E. K., Perri, A., Webster, M. T., Ho, S. Y. W., Peters, J., et al. (2012). Rethinking dog domestication by
integrating genetics, archeology, and biogeography. Proceedings of the National Academy of Sciences, 109(23), 8878–8883.
Mac Donald, K. B., & Ginsburg, B. E. (1981). Induction of normal prepubertal behaviour in wolves with restricted rearing.
Behavioral and Neural Biology, 33, 133–162. MacDonald, K. (1983). Stability of individual differences in behavior in a litter of wolf cubs (Canis lupus). Journal of
Comparative Psychology, 97(2), 99–106. Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across
generations. Annual Review of Neuroscience, 24, 1161–1192. Mignon-‐Grasteau, S., Boissy, A., Bouix, J., Faure, J.-‐M., Fisher, A. D., Hinch, G. N., et al. (2005). Genetics of adaptation and
domestication in livestock. Livestock Production Science, 93(1), 3–14. Miklósi, Á. (2007). Dog Behaviour, Evolution, and Cognition. Oxford University Press Inc. Morey, D. (2010). Dogs: Domestication and the Development of a Social Bond. Cambridge University Press. Morey, D. F. (1994). The early evolution of the domestic dog. American Scientist, 82(4), 336–347. Ovodov, N. D., Crockford, S. J., Kuzmin, Y. V., Higham, T. F. G., Hodgins, G. W. L., & van der Plicht, J. (2011). A 33,000-‐year-‐old
incipient dog from the Altai Mountains of Siberia: evidence of the earliest domestication disrupted by the Last Glacial Maximum. PLoS ONE, 6(7), e22821.
Pang, J.-‐F., Kluetsch, C., Zou, X.-‐J., Zhang, A.-‐B., Luo, L.-‐Y., Angleby, H., et al. (2009). mtDNA data indicate a single origin for
dogs south of Yangtze River, less than 16,300 years ago, from numerous wolves. Molecular Biology and Evolution, 26(12), 2849–2864.
Parker, H. G., vonHoldt, B. M., Quignon, P., Margulies, E. H., Shao, S., Mosher, D. S., et al. (2009). An expressed fgf4
retrogene is associated with breed-‐defining chondrodysplasia in domestic dogs. Science, 325(5943), 995–998. Popova, N. K., Voitenko, N. N., Kulikov, A. V., & Avgustinovich, D. F. (1991). Evidence for the involvement of central serotonin
in mechanism of domestication of silver foxes. Pharmacology, Biochemistry, and Behavior, 40(4), 751–756. Price, E. O. (2002). Animal domestication and behaviour. CABI Publishing, CAB Int., 1–307. Saetre, P., Lindberg, J., Leonard, J. A., Olsson, K., Pettersson, U., Ellegren, H., et al. (2004). From wild wolf to domestic dog:
gene expression changes in the brain. Molecular Brain Research, 126(2), 198–206. Savolainen, P., Zhang, Y.-‐P., Luo, J., Lundeberg, J., & Leitner, T. (2002). Genetic evidence for an East Asian origin of domestic
dogs. Science, 298(5598), 1610–1613.
31
Scott, J. P., & Fuller, J. L. (1965). Genetics and the social behavior of the dog -‐ the classic study. University of Chicago Press. Sih, A., Bell, A., & Johnson, J. C. (2004). Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology &
Evolution, 19(7), 372–378. Sinn, D. L., Gosling, S. D., & Moltschaniwskyj, N. A. (2008). Development of shy/bold behaviour in squid: context-‐specific
phenotypes associated with developmental plasticity. Animal Behaviour (75), 433-‐442. Sol, D., Bacher, S., Reader, S. M., & Lefebvre, L. (2008). Brain size predicts the success of mammal species introduced into
novel environments. The American Naturalist, 172 Suppl 1, 63–71. Sol, D., Duncan, R. P., Blackburn, T. M., Cassey, P., & Lefebvre, L. (2005). Big brains, enhanced cognition, and response of
birds to novel environments. Pnas, 102, 5460–5465. Spady, T. C., & Ostrander, E. A. (2007). Canid genomics: mapping genes for behavior in the silver fox. Genome Research, 17(3),
259–263. Sutter, N. B., Bustamante, C. D., Chase, K., Gray, M. M., Zhao, K., Zhu, L., et al. (2007). A single IGF1 allele is a major
determinant of small size in dogs. Science, 316(5821), 112–115. Svartberg, K., Tapper, I., Temrin, H., Radesäter, T., & Thorman, S. (2005). Consistency of personality traits in dogs. Animal
Behaviour), 69(2), 283–291. Tchernov, E., & Horwitz, L. K. (1991). Body size diminution under domestication: Unconscious selection in primeval
domesticates. Journal of Anthropological Archaeology, 10, 54-‐75. Topál, J., Gácsi, M., Miklósi, Á., Virányi, Z., Kubinyi, E., & Csányi, V. (2005). Attachment to humans: a comparative study on
hand-‐reared wolves and differently socialized dog puppies. Animal Behaviour, 70(6), 1367–1375. Trut, L. (1999). Early Canid Domestication: The Farm-‐Fox Experiment. American Scientist, 87(2), 160-‐165. Trut, L. N. (1998). The evolutionary concept of destabilizing selection: status quo. Journal of Animal Breeding and Genetics, 115,
415-‐431 Trut, L. N. (2001). Experimental studies of early canid domestication. The Genetics of the Dog, chapter 2. CABI Publishing. Trut, L. N., Plyusnina, I. Z., & Oskina, I. N. (2004). An Experiment on Fox Domestication and Debatable Issues of Evolution of
the Dog. Russian Journal of Genetics, 40(6), 644–655. Trut, L., Oskina, I., & Kharlamova, A. (2009). Animal evolution during domestication: the domesticated fox as a model.
Bioessays, 31(3), 349–360. Verginelli, F. (2005). Mitochondrial DNA from Prehistoric Canids Highlights Relationships Between Dogs and South-‐East
European Wolves. Molecular Biology and Evolution, 22(12), 2541–2551. Vila, C. (2001). Widespread Origins of Domestic Horse Lineages. Science, 291(5503), 474–477. Vila, C., & Wayne, R. K. (1999). Hybridization between Wolves and Dogs. Conservation Biology, 13(1), 195–198. Vila, C., Savolainen, P., Maldonado, J. E., Amorim, I. R., Rice, J. E., Honeycutt, R. L., et al. (1997). Multiple and ancient origins
of the domestic dog. Science, 276(5319), 1687–1689. Vila, C., Seddon, J., & Ellegren, H. (2005). Genes of domestic mammals augmented by backcrossing with wild ancestors.
Trends in Genetics, 21(4), 214–218. vonHoldt, B. M., Pollinger, J. P., Lohmueller, K. E., Han, E., Parker, H. G., Quignon, P., et al. (2010). Genome-‐wide SNP and
haplotype analyses reveal a rich history underlying dog domestication. Nature, 464(7290), 898–902. Wang, G.-‐D., Zhai, W., Yang, H.-‐C., Fan, R.-‐X., Cao, X., Zhong, L., et al. (2013). The genomics of selection in dogs and the
parallel evolution between dogs and humans. Nature Communications, 4, 1860. Wayne, R. K., & Vila, C. (2001). Phylogeny and origin of the domestic dog. The Genetics of the Dog, chapter 1. CABI Publishing.
32
Wayne, R. K., & vonHoldt, B. M. (2012). Evolutionary genomics of dog domestication. Mammalian Genome, 23(1-‐2), 3–18. Wolf, M., & Weissing, F. J. (2012). Animal personalities: consequences for ecology and evolution. Trends in Ecology &
Evolution, 27(8), 452–461. Zeder MA. (2012). Pathways leading to domestication. Chp 9 in Biodiversity in Agricultre: Domestication, Evolution and Sustainability. Edited by Gepts P, Famula TR, Bettinger RL, Brush SB, Damania AB, McGuire PE, Qualset CO.Cambridge University Press.