Genetics and the Behavior of Domestic Animals
(Chapter One)
Acedemic Press 1998
ISBN # 0-12295130-1
Department of
A
bright orange sun is setting on a prehistoric horizon. A lone hunter is on his
way home from a bad day at hunting. As he crosses the last ridge
before home. a quick movement in the rocks off
to his right catches his attention. Investigating, he discovers some wolf pups
hiding in a shallow den. He exclaims, "Wow ... cool!
The predator... in infant form."
After a quick scan of
the area for adult wolves, he cautiously approaches. The pups are all clearly
frightened and huddle close together as he kneels in front of the den . . . all
except one. The darkest colored pup shows no fear of
the man's approach. "Come here you little predator! Let me take a look at
you, he says. After a mutual bout of petting by the man and licking by the
wolf, the man suddenly has an idea. "If I take you home with me tonight,
maybe mom and the kids will forgive me for not catching dinner . . .
again."
The
opening paragraphs depict a hypothetical scenario of man first taming the wolf.
Although we have tried to make light of this event, the fact is that no one
knows exactly how or why this first encounter took place. The earliest archeological estimate indicates that it occurred in the
late Glacial period, approximately 14,000 years BC (Boessneck, 1985). Another scenario is that wolves
domesticated themselves. The presumption is that calm wolves with low levels of
fear were likely to scavenge near human settlements. Both Coppinger
and Smith (1983) and Zeuner (1963) suggest that wild
species which later became domesticants started out
as camp followers. Some wolves were believed to have scavenged near human
settlements or followed hunting parties; wild cattle supposedly invaded grain
fields, and wild cats may have invaded grainaries
while hunting for mice. However, the most recent evidence obtained by
sequencing mitochondrial DNA of 67 dog breeds and wolves from 27 localities
indicates that dogs may have diverged from wolves over 100,000 years ago (Vita et
al., 1997).
In any event, wolves
kept for companions had to be easy to handle and socialize to humans. Within a
few generations, early humans may have turned wolves into dogs by selecting and
breeding the tamest ones. Thousands of years ago, humans were not aware that behavior in animals was heritable. However, even today
people who raise dogs, horses, pigs, cattle, or chickens notice differences in
the behavior of the offspring. Some animals are
friendly and readily approach people, while others may be shy and nervous.
Price
(1984) defined domestication as a process by which a population of animals
becomes adapted to man and the captive environment by some combination of
genetic changes occurring over generations and environmentally induced
developmental events recurring during each generation:' In long-term selection
experiments designed to study the consequences of selection for the tame"
domesticated type of behavior, Belyaev
(1979) and Belyaev et al. (1981) studied foxes
reared for their fur. The red fox (Vulpes fulva) has been raised on seminatural
fur farms for over 100 years and was selected for fur traits and not behavioral traits. However, they demonstrate three distinctly
different characteristic responses to man. Thirty percent were extremely
aggressive toward man, 60% were either fearful or fearfully aggressive, and 10%
displayed a quiet exploratory reaction without either fear or aggression. The
objective of this experiment was to breed animals similar in behavior to the domestic dog. By selecting and breeding the
tamest individuals, 20 years later the experiment succeeded in turning wild
foxes into tame, border collie-like fox-dogs. The highly selected
"tame" population of (fox-dog) foxes actively sought human contact
and would whine and wag their tails when people approached (Belyaev
1979). This behavior was in sharp contrast to wild
foxes which showed extremely aggressive and fearful behavior
toward man. Keeler et al. (1970) described this behavior:
Vulpes fulva (the wild fox) is a bundle of jangled nerves. We
had observed that when first brought into captivity as an adult, the red fox
displays a number of symptoms that are in many ways similar to those observed
in psychosis. They resemble a wide variety of phobias, especially fear of open
spaces, movement, white objects, sounds, eyes or lenses, large objects, and
man, and they exhibit panic, anxiety, fear, apprehension and a deep trust of
the environment~ They are 1) catalepsy-like frozen positions, accompanied by
blank stares; 2) fear of sitting down; 3) withdrawal; 4) runaway flight
reactions; and 5) aggressiveness. Sometimes the strain of captivity makes them
deeply disturbed and confused, or may produce a depression- like state. Extreme
excitation and restlessness may also be observed in some individuals in
response to many changes in the physical environment. Most adult red foxes soon
after capture break off their canine teeth on the mesh of our expanded metal cage
in their attempts to escape. A newly captured fox is known to have torn at the
wooden door of his cage in a frenzy until he dropped
dead from exhaustion.
Although
the stress of domestication is great, Belyaev (1979)
and Belyaev et al. (1981) concluded that
selection for tameness was effective in spite of the many undesirable
characteristics associated with tameness. For example, the tame foxes shed
during the wrong season and developed black and white patterned fur, and
changes were found in their hormone profiles. This means that the monoestrus (once a year) cycle of reproduction was
disturbed and the animals would breed at any time of the year. Furthermore,
changes in behavior occurred simultaneously with
changes in tail position and ear shape, and the appearance of a white muzzle,
forehead blaze, and white shoulder hair. The white color
pattern on the head is similar to many domestic animals (Belyaev
1979) (Figs. 1.1 and 1.2). The most dog-like foxes had white spots and patterns
on their heads, drooping ears, and curled tails and looked more like dogs than
the foxes that avoided people. The behavioral and
morphological (appearance) changes were also correlated with corresponding
changes in the levels of gender hormones. The tame foxes had higher levels of
the neurotransmitter serotonin (Popova et al.,
1975). Serotonin is known to inhibit some kinds of aggression (Belyaev, 1979), and serotonin ~levels are increased in the
brains of people who take Prozac (fluoxetine).
The study of behavioral genetics can help explain why selection for calm
temperament was linked to physical and neurochemical
changes in Belyaev's foxes. Behavior
geneticists and animal scientists are interested in understanding effects on behavior due to genetic influences or those which are due
to environment and learning.
This
historical review is not intended to he comprehensive; our objective is to
discuss some of the early discoveries that are important for our current
understanding of animal behavior, with particular
emphasis on genetic influence on behavior in domestic
animals.
Early in the 17th
century, Descartes came to the conclusion "that the bodies of animals and
men act wholly like machines and move in accordance with purely mechanical
laws" (in Huxley 1874). After Descartes, others undertook the task of
explaining behavior as reactions to purely physical,
chemical, or mechanical events. For the next three centuries scientific thought
on behavior oscillated between a mechanistic view
that animals are '~automatons" moving through life without consciousness
or self-awareness and an opposing view that animals had thoughts and feelings
similar to those of humans.
In "On the Origin
of the Species" (1859),
Other scientists
realized the implications of
During
the middle of the 20th century', scientific thought again reverted to the
mechanical approach and behaviorism reigned
throughout
The first author
visited with Dr. Skinner at
However, a rat's behavior is very limited in a Skinner box. It's a world
with very little variation, and the rat has little opportunity to use its
natural behaviors. It simply learns to push a lever
to obtain food or prevent a shock. Skinnerian principles explain why a rat
behaves a certain way in the sterile confines of a 30 x 30-cm Plexiglas box,
but they don't reveal much about the behavior of a
rat in the local dump. Outside of the laboratory, a rat's behavior
is more complex.
Skinner's
influence on scientific thinking slowed a bit in 1961 following the publication
of ~The Misbehavior of Organisms" by Brelands and Brelands. This paper
described how Skinnerian behavioral principles
collided with instincts. The Brelands were trained
Skinnerian behaviorists who attempted to apply the
strict principles of operant conditioning to animals trained at fairs and
carnivals. Ten years before this classic paper, the Brelands
(1951) wrote, we are wholly affirmative and optimistic that principles derived
from the laboratory can be applied to the extensive control of animal behavior under non laboratory condition]' However, by 1961,
after training more than 6000 animals as diverse as reindeer, cockatoos,
raccoons, porpoises, and whales for exhibition in zoos, natural history
museums, department store displays, fair and trade convention exhibits, and
television, the Brelands wrote a second article
featured in the American Psychologist (1961), which stated, our backgrounds in behaviorism had not prepared us for the shock of some of
our failures."
One of the failures
occurred when the Brelands tried to teach chickens to
stand quietly on a platform for 10 to 12 seconds before they received a food
reward. The chickens would stand quietly on a platform in the beginning of
training; however, once they learned to associate the platform with a food
reward, half (50%) started scratching the platform, and another 25% developed
other behaviors, such as pecking the platform. The Brelands salvaged this disaster by developing a wholly
unplanned exhibit involving a chicken that turned on a juke box and danced.
They first trained the chickens to pull a rubber loop which turned on some
music. When the music started, the chickens would jump on the platform and
start scratching and pecking until the food reward was delivered. This exhibit
made use of the chicken's instinctive food-getting behavior.
The first author remembers as a teenager seeing a similar exhibit, at the
Arizona State Fair, of a piano-playing chicken in a little red barn. The hen
would peck the keys of a toy piano when a quarter was put in the slot and would
stop when the food came down the chute. This exhibit also worked because it was
similar to a Skinner box in the laboratory.
The Brelands
experienced another classic failure when they tried to teach raccoons to put
coins in a piggy bank. Because raccoons are adept at manipulating objects with
their hands, this task was initially easy. As training progressed, however, the
raccoons began to rub the coins before depositing them in the bank. This behavior was similar to the washing behavior
raccoons do as instinctive food-getting behavior. The
raccoons at first had difficulty letting go of the coin and would hold and rub
it. However, when the Brelands introduced a second
coin, the raccoons became almost impossible to train. Rubbing the coins
together 'in a most miserly fashion]' the raccoons got
worse and worse as time went on. The Brelands
concluded that the innate behaviors were suppressed
during the early stages of training and sometimes long into the training, but
as training progressed, instinctive food-getting behaviors
gradually replaced the conditioned behavior. The
animals were unable to override their instincts and thus a conflict between
conditioned and instinctive behaviors occurred.
While
Skinner and his fellow Americans were refining the principles of operant
conditioning on thousands of rats and mice, ethology
was being developed in
Understanding the
mechanisms and programming that result in innate behavioral
patterns and the motivations behind why animals behave the way they do is the
primary focus of ethologists. Konrad
Lorenz (1939, 1965, 1981) and Niko
Tinbergen (1948, 1951) cataloged
the behavior of many animals in their natural
environments. Together they developed the ethogram.
An ethogram is a complete listing of all the behaviors that an animal performs in its natural
environment. The ethogram includes both innate and
learned behaviors.
An interesting
contribution to ethology came from studies on
egg-rolling behavior in the greylag goose (Lorenz,
1965, 1981). He observed that when a brooding goose notices an egg outside her
nest, an innate instinctive program is triggered to retrieve it. The goose
fixates on the egg, rises to extend her neck and bill out over it, then gently rolls it back to the nest. This behavior is performed in a highly mechanical way If the egg is removed as the goose begins to extend her neck,
she still completes the pattern of rolling the nonexistent egg back to the
nest. Lorenz (1939) and Tinbergen (1948) termed this
a 'fixed action pattern." Remarkably, Tinbergen
also discovered that brooding geese can be stimulated to perform egg rolling on
such items as beer cans and baseballs. The fixed action pattern of rolling the
egg back to the nest can be triggered by anything outside the nest that even
marginally resembles an egg. Tinbergen realized that
geese possess a genetic-releasing mechanism for this fixed action pattern.
Lorenz and Tinbergen called the object that triggers
the release of a fixed action pattern "sign stimuli." When a mother
bird sees the gaping mouth of her young, it triggers the maternal feeding behavior and the mother feeds her young. The gaping mouth
is another example of sign stimuli that acts as a switch and turns on the
genetically determined program (Herrick, 1908; Tinbergen,
1951).
Ethologists also explained the innate
escape response of newly hatched goslings. When goslings are tested with a
cardboard silhouette in the shape of a hawk moving overhead, it triggers a
characteristic escape response. The goslings will crouch or run. However, when
the silhouette is reversed to look like a goose, there is no effect (Tinbergen, 1951). Several members of the research community
doubted the existence of such a hard-wired instinct because other scientists
failed to repeat these experiments (Hirsh et al., 1955). Recently Canty and Gould (1995) repeated the classic experiments and
explained why the other experiments failed. In the first place, goslings only
respond to the silhouette when they are under 7 days
old. Second, a large silhouette which casts a shadow must be used; third,
goslings respond to the perceived predator differently depending on the
circumstances. For example, birds tested alone try to run away from the hawk
silhouette and birds reared and tested in groups tend to crouch (Canty and Gould, 1995). Nevertheless, fear is likely to be
the basis of the response. Ducklings were shown to have higher heart rate
variability when they saw the hawk silhouette (Mueller and Parker, 1980).
Research by Balaban (1997) indicates that
species-specific vocalizations and head movements in chickens and quail are
controlled by distinct cell groups in the brain. To prove this, Balaban transplanted neural tube cells from developing
quail embryos into chicken embryos. Chickens hatched from the transplanted eggs
exhibited species-specific quail songs and bobbing head movements.
Do similar fixed action
patterns occur in mammals? Fentress (1973) conducted
an experiment on mice which clearly showed that animals have instinctive
species-specific behavior patterns which do not
require learning. Day-old baby mice were anesthetized and had a portion of
their front legs amputated. Enough of the leg remained that the mice could
easily walk. The operations were performed before the baby mice had fully
coordinated movements so there was no opportunity for learning. When the mice
became adults, they still performed the species-specific face-washing behavior; normal mice close their eye just prior to the
foreleg passing over the face, and in the amputees the eye still closed before
the nonexistent paw hit it. The amputees performed the face- washing routine as
if they still had their paws. Fentress (1973)
concluded that the experiment proved the existence of instincts in mammals.
Two
years after the Brelands article, Jerry Hirsh (1963)
at the
A basic principle to
remember is that animals with large, complex brains are less governed by innate
behavior patterns. For example, bird behavior is governed more by instinct than that of a dog,
whereas an insect would have more hard-wired behavior
patterns than that of a bird. This principle was clear to Yerkes
(1905) who wrote:
Certain
animals are markedly plastic or voluntary in their behavior,
others are as markedly fixed or instinctive. In the primates plasticity has
reached its highest known stage of development; in the insects fixity has
triumphed, instinctive action is predominant. The ant has apparently sacrificed
adapt-ability to the development of ability to react quickly, accurately and
uniformly in a certain way Roughly, animals might he separated into two
classes: those which are in high degree capable of immediate adaptation to
their conditions, and those that are apparently automatic since they depend
upon instinct tendencies to action instead of upon rapid adaptation.
Some behavior patterns are similar between different species,
and some are found only in a particular species. For example, the neural
programs that enable animals to walk are similar in most mammals (Melton,
1991). On the other hand, courtship rituals in birds are very species-specific
(Nottebohm, 1977). Some innate behavior
patterns are very rigid and experience has little effect on them; other
instinctive behaviors can be modified by learning and
experience. The flehmann, or lip curl response of a
bull when he smells a cow in estrus, and the
kneel-down (lordois) posture of a rat in estrus are examples of behaviors
that are rigid. Suckling of the mother by newborn mammals is another example of
a hard-wired behavioral system. Suckling behavior does not vary Newborn mammals suckle almost
anything put in their mouth.
An example of an innate
behavior that is affected by learning is burrowing behavior in rats. Boice (1977)
found that wild
Other behaviors are almost entirely learned. Some seagulls learn
to drop shellfish on rocks to break them open, while
others drop them on the road and let cars break them open (Grandin,
1995). Many animals ranging from apes to birds use tools to obtain food.
Innate behaviors used for finding food, such as grazing,
scavenging, or hunting, are more dependent on learning than behaviors
used to consume food. Mating behavior, nesting,
eating, and prey-killing behaviors tend to be
governed more by instinct (Gould, 1977). The greater dependence on learning to
find food makes animals in the wild more flexible and able to adapt to a
variety of environments. Behaviors used to kill or
consume food can be the same in any environment. Mayr
(1974) called these different behavioral systems
"open" or "closed" to the effects of experience. A lion
hunting her prey is an example of an open system. The hunting female lion
recognizes her prey from a distance and carefully stalks her approach. Herrick
(1910) wrote, "the details of the hunt vary every time she hunts;
therefore, no combination of simple reflex arcs laid down in the nervous system
will be adequate to meet the infinite variations of the requirements for
obtaining food:'
Some of
the interactions between genetics and experience have very complex effects on behavior. In birds, the chaffinch learns to sing its
species-specific song even when reared in a sound-proof box where it is unable
to hear other birds (Nottebohm, 1970, 1979). However,
when chaffinches are allowed to hear other birds sing, they develop a more
complex song. The basic pattern of canary song emerges even in the absence of conspecific (flock-mate) auditory models (Metfessel, 1935; Poulsen, 1959).
Young canaries imitate the song of adult canaries they can hear, and when
reared in groups they develop song patterns that they all share (Nottebohm, 1977). Many birds, such as the white crowned
sparrow chaffinch, and parrot, can develop local song dialects (Nottebohm et al., 1976). Sparrows are able to learn
songs by listening to recordings of songs with either pure tones or harmonic
overtones. Birds trained with harmonic overtones learned to sing songs with
harmonic overtones, but 1 year later, 85% of their songs reverted back to
innate pure tone patterns (Nowicki and Marler, 1988). Further experiments by Mundinger
(1995) attempted to determine the relative contribution of genetics and
learning in bird song. Inbred lines of roller and border canaries were used in
this study along with a hybrid cross of the two. The rollers were cross
fostered to border hens and vice versa to control for effects of maternal behavior. The roller and border males preferred to sing
innate song patterns instead of copying their tutors. The hybrids preferred to
learn some of both songs. Furthermore, canaries are capable of learning parts
of an alien song but have a definite preference for their own songs. Comparing
these animals to those in Brelands and Brelands (1961) exhibits, birds can be trained to sing a
different song, but genetically determined patterns have a strong tendency to
override learning. In reviewing all this literature, it became clear that
innate patterns in mammals can be overridden. Unfortunately the animals tend to
revert back to innate behavior patterns.
Novelty
is anything new or strange in an animal's environment. Novelty is a paradox
because it is both fear-provoking and attractive. Paradoxically it is most
fear-provoking and attractive to animals with a nervous, excitable temperament.
Skinner (1922) wrote that a flighty animal such as the pronghorn antelope will
approach a person lying on the ground waving a red flag. Einarsen
(1948) further observed that some wild animals will approach various large,
dangerous objects such as a power steam shovel. In more recent studies, Kruuk (1972) also observed attraction and reaction to
novelty in Thompson's gazelles in
Confronted
with sudden novelty, highly reactive animals are more likely to have a major
fear reaction. Examples of sudden novelty include being placed in a new cage,
transport in a strange vehicle, an unexpected loud noise, or being placed in an
open field. Using various experimental environments, Hennessy and Levine (1978)
found that rats show varying degrees of stress and stress hormone levels
proportional to the degree of novelty of the environment they are placed in; a
glass jar is totally novel in appearance compared to the lab cage to which the
animal was accustomed. Being placed in a glass jar was more stressful for rats
than a clean lab cage with no bedding.
Studies
of the reaction to novelty in farm animals have been conducted by Moberg and Wood (1982), Stephens and Toner (1975), and Dantzer and Mormede (1983). When
calves are placed in an open field test arena that is very dissimilar from
their home pen, they show the highest degrees of stress (Dantzer
and Mormede, 1983). Calves raised indoors were more
stressed by an outdoor arena and calves raised outdoors were more stressed by
an indoor arena. The second author is painfully familiar with similar responses
in horses. When horses are taken to the mountains for the first time, a
well-trained riding horse that is accustomed to many different show rings may
panic when it sees a butterfly or hears a twig snapping on a mountain trail.
In
mammals and birds, normal development of the brain and sense organs requires
novelty and varied sensory input. Nobel prize winning
research of Hubel and Wiesel
(1970) showed that the visual system is permanently damaged if kittens do not
receive varied visual input during development. When dogs are raised in barren
and nonstimulating environments they are also more
excitable (Walsh and Cummins, 1975; Melzak and Burns,
1965). Schultz (1965) stated, "when stimulus
variation is restricted central regulation of threshold sensitivities will
function to lower sensory thresholds." Krushinski
(1960) studied the influence of isolated conditions of rearing on the
development of passive defense reactions (fearful
aggression) in dogs and found that the expression of a well-marked fear
reaction depends on the genotype of the animal. Airedales and German shepherds
were reared under conditions of freedom (in homes) and in isolation (in
kennels). Krushinski (1960) found that the passive defense reaction developed more acutely and reached a
greater degree in the German shepherds kept in isolation compared to the
Airedales. In general, animals reared in isolation become more sensitive to
sensory stimulation because the nervous system attempts to readjust for the
previous lack of stimulation.
In an experiment with
chickens, Murphy (1977) found that chicks from a flighty genetic line were more
likely to panic when a novel ball was placed in their pen, but they were also
more attracted to a novel food than birds from a calm line. Cooper and Zubeck (1958), and Henderson (1968) found that rats bred to
be dull greatly improved in maze learning when housed in a cage with many
different objects; however, enriched environments had little effect on the rats
bred for high intelligence. Greenough and Juraska (1979) found that rearing rats in an environment
with many novel objects improves learning and resulted in increased growth of
dendrites, which are nerve endings in the brain.
Pigs raised in barren
concrete pens also seek stimulation (Grandin, 1989a,b; Wood-Gush and Vestergaard,
1991; Wood-Gush and Beilharz, 1983). Piglets allowed to choose between a familiar object and a novel object
prefer the novel object (Wood-Gush and Vestergaard,
1991). Pigs raised on concrete are strongly attracted to novel objects to chew
on and manipulate. The first author has observed that nervous, excitable hybrid
pigs often chew and bit vigorously on boots or coveralls. This behavior is less common in placid genetic lines of pigs.
Although hybrid pigs
are highly attracted to novelty, tossing a novel object into their pen will
initially cause a strong flight response. Compared to calm genetic lines,
nervous-hybrid pigs pile up and squeal more when startled. Pork producers
report that nervous, fast-growing, lean hybrid pigs also tail-bite other pigs
more often than calmer genetic lines Of pigs. jail biting occurs more often when pigs are housed on a
concrete slatted floor which provides no opportunity for rooting.
Strong attraction or
strong reaction to novelty has also been observed by the first author in
cattle. Cattle will approach and lick a piece of paper laying
on the ground when they can approach it voluntarily (Fig. 1.3). However, the
same piece of paper blowing in the wind may trigger a massive flight response.
Practical experience by both authors suggests that highly reactive horses are
more likely to engage in vices such as cribbing or stall weaving when housed in
stalls or runs where they receive little exercise. Denied variety and novelty
in their environments, highly reactive animals adapt poorly compared to animals
from calmer genetic lines (Price, 1984).
In summary, in both
wild and domestic animals novelty is both highly feared and necessary Novelty
is most desirable when animals can approach it slowly. Unfortunately, novelty
is also fear-provoking when animals are suddenly confronted with it.
In
animals as diverse as rats, chickens, cattle, pigs, and humans, genetic factors
influence differences in temperament (Murphey et
al., 1980b Kagan et al., 1988; Grandin, 1993b; Fordyce et al., 1988; Fujita et
al., 1994; Hemsworth et al., 1990; Broadhurst,
1975; Reese et al., 1983; Murphy, 1977; Tulloh,
1961; Blizard, 1971). Some individuals are wary and
fearful and others are calm and placid. Boissy (1995)
stated, fearfulness is a basic psychological characteristic of the individual
that predisposes it to perceive and react in a similar manner to a wide range
of potentially frightening events]' In all animals, genetic factors influence
reactions to situations which cause fear (Davis, 1992; Murphey
et al., 1980b; Kagan et al, 1988; Boissy and Bouissou, 1995);
therefore, temperament is partially determined by an individual animal's fear
response. Rogan and LeDoux (1996) suggest that fear
is the product of a neural system that evolved to detect danger and that it
causes an animal to make a response to protect itself. Plomin
and Daniels (1987) found a substantial genetic influence on shyness
(fearfulness) in human children. Shy behavior in
novel situations is considered a stable psychological characteristic of certain
individuals. Shyness is also suggested to be among the most heritable
dimensions of human temperament throughout the life span.
In an experiment
designed to control for maternal effects on temperament and emotionality, Broadhurst (1960) conducted cross-fostering experiments on Maudsley Reactive (MR) and Non Reactive (MNR) rats. These
lines of rats are genetically selected for high or low levels of emotional
reactivity The results showed that maternal effects were not great enough to
completely mask the temperament differences between the two lines (Broadhurst, 1960). Maternal effects can affect temperament,
but they are not great enough to completely change the temperament of a
cross-fostered animal which has a temperament that is very different from that
of the foster mother. In extensive review of the literature, Broadhurst (1975) examined the role of heredity in the
formation of behavior and found that differences in
temperament between rats persist when the animals are all raised in the same
environment.
One
method of testing fearfulness is the open field test (Hall, 1934). Sudden
placement of an animal in an open field test arena is used to measure
differences in fearfulness. Open field testing has shown differences in
fearfulness between different genetic lines of animals. The test arena floor is
usually marked in a grid to measure how much the animals walk around and
explore. Huck and Price (1975) showed that domestic rats are less fearful and will
walk round the open held more than wild rats. Price and Loomis (1973) explained
that some genetic strains of rats are less fearful and explore an open field
arena more than others. Eysenck and Broadhurst (1964) found that rodents with high emotional
reactivity are more fearful and explore the open field less compared to placid
genetic lines.
In their study of
genetic effects on behavior, Fuller and Thompson
(1978) found that "simply providing the same defined controlled
environment for each genetic group is not enough. Conditions must not only be
uniform for all groups, but also favorable to the
development of the behavior of interest." For
example, in wartime
Mahut (1958) demonstrated an example
of differences in fear responses between beagles and terriers. When frightened,
beagles freeze and terriers run around frantically In
domestic livestock, measuring fear reactions during restraint or in an open
field test has revealed differences in temperament both between breeds and
between individuals within a breed (Grandin, 1993a; Tulloh, 1961; Dantzer and Mormede, 1983; Murphey et al.,
1980b, 1981). The fearful, flighty animals become more agitated and struggle
more violently when restrained for vaccinations and other procedures (Fordyce et
al., 1988; Grandin, 1993a). Fear is likely to be
the main cause of agitation during restraint in cattle, horses, pigs, and
chickens. Genetic effects on behavior during
transport, handling, and restraint of these animals are further discussed in
Chapter 4.
In an
open field test, frightened rodents often stay close to the arena walls,
whereas frightened cattle may run around wildly and attempt to escape. Rodents
stay close to the walls because they naturally fear open spaces, whereas cattle
run around wildly because they fear separation from the herd. This is an
example of differences between species in their response to a similar fear-
provoking situation. Fear can be manifested in many different ways. For
example, a frightened animal may run around frantically and try to escape in
one situation, while in another situation the same animal may freeze or limit
its movement. Chickens often freeze when handled by humans. Jones (1984) called
this "tonic immobility." The chickens become so frightened that they
cannot move. Forceful capture of wild animals can sometimes inflict fatal heart
damage. Wildlife biologists call this capture myopathy
In summary, much is known about the complex phenomenon
of fear, but many questions still remain.
Genetics
influences the intensity of fear reactions. Genetic factors can also greatly
reduce or increase fear reaction in domestic animals (Price, 1984; Parsons,
1988; Flint et al., 1995). Research in humans has clearly revealed some
of the genetic mechanisms which govern the inheritance of anxiety (Lesch et al., 1996). LeDoux (1992) and Rogan and LeDoux (1996) state that all vertebrates can be
fear-conditioned.
Heart rate, blood
pressure, and respiration also change in animals when the flight or fight
response is activated (Manuck and Schaefer, 1978).
All these autonomic functions have neural circuits to the amygdala.
Fear can be measured in animals by recording changes in autonomic activity In humans, Manuck and Schaefer
(1978) found tremendous differences in cardiovascular reactivity in response to
stress, reflecting a stable genetic characteristic of individuals.
Fearfulness
and instinct can conflict. This principle was observed firsthand by the second
author during his experience raising Queensland Blue Heeler dogs. Annie's first
litter was a completely novel experience because she had never observed another
dog giving birth or nursing pups. She was clearly frightened when the first pup
was born and it was obvious that she did not know what the pup was; however, as
soon as she smelled it her maternal instinct took over and a constant
uncontrollable licking began. Two years later, Annie's daughter Kay had her
first litter. Kay was more fearful than her mother and her highly nervous
temperament overrode her innate licking program. When each pup was born Kay ran
wildly around the room and would not go near them. The second author had to
intervene and place the pups under Kay's nose; otherwise, they may have died.
Kay's nervous temperament and fearfulness were a stronger motivation than her
motherly instinct.
Raising
young animals in barren environments devoid of variety and sensory stimulation
will have an effect on development of the nervous system. It can cause an
animal to be more reactive and excitable when it becomes an adult. This is a
long-lasting, environmentally induced change in how the nervous system reacts
to various stimuli. Effects of deprivation during early development are also
relatively permanent. Melzak and Burns (1965) found
that puppies raised in barren kennels developed into hyperexcitable
adults. In one experiment the deprived dogs reacted with ~diffuse
excitement" and ran around a room more than control dogs raised in homes
by people. Presenting novel objects to the deprived dogs also resulted in
diffuse excitement." Furthermore, the EEGs of the kennel-raised dogs
remained abnormal even after they were removed from the kennel (Melzak and Burns, 1965). Simons and Land (1987) showed that
the somatosensory cortex in the brains of baby rats
will not develop normally if sensory input was eliminated by trimming their
whiskers. A lack of sensory input made the brain hypersensitive to stimulation.
The effects persisted even after the whiskers had grown back.
Development of
emotional reactivity of the nervous system begins during early gestation. Denenberg and Whimbey (1968)
showed that handling a pregnant rat can cause her offspring to be more
emotional and explore less in an Open field compared to control animals. This
experiment is significant because it shows that handling the pregnant mother
had the opposite effect on the behavior of the infant
pups. Handling and possibly stressing the pregnant mothers changed the hormonal
environment of the fetus which resulted in nervous
offspring. However, handling newborn rats by briefly picking them up and
setting them in a container reduced emotional reactivity when the rats became
adults (Denenberg and Whimbey
1968). The handled rats developed a calmer temperament.
The adrenal glands are
known to have an effect on behavior (Fuller and
Thompson, 1978). The inner portions of the adrenals secrete the hormones
adrenaline and noradrenaline, while the outer cortex
secretes the gender hormones androgens and oestrogens
(reproductive hormones), and various corticosteroids (stress hormones). Yeakel and Rhoades (1941) found that Hall's (1938)
emotional rats had larger adrenals and thyroids compared to the nonemotional rats. Richter (1952, 1954) found a decrease in
the size of the adrenal glands in
Adult
wild rats can be tamed and become accustomed to handling by people (Galef, 1970). This is strictly learned behavior.
Taming full-grown wild animals to become accustomed to handling by people will
not diminish their response to a sudden novel stimulus. This principle was
demonstrated by Grandin et al. (1994) in
training wild antelope at the Denver Zoo for low- stress blood testing. Nyala are African antelope with a hair-trigger flight
response used to escape from predators. During handling in zoos for veterinary
treatments, nyala are often highly stressed and
sometimes panic and injure themselves. Over a period of 3 months, Grandin et al. (1995) trained nyala
to enter a box and stand quietly for blood tests while being fed treats. Each
new step in the training had to be done slowly and carefully Ten days were
required to habituate the nyala to the sound of the
doors on the box being closed.
All the training and
petting by zoo keepers did not change the nyala's
response to a sudden, novel stimulus. When the nyala
saw repairman on the barn roof they suddenly reacted with a powerful fear
response and crashed into a fence. They had become accustomed to seeing people
standing at the perimeter of the exhibit, but people on the
roof was novel and very frightening. Sudden movements such as raising a
camera up for a picture also caused the nyala to
flee.
Wild
herding species show much stronger fear responses to sudden novelty compared to
domestic ruminants such as cattle and sheep. Domestic ruminants have attenuated
flight responses due to years of selective breeding (Price, 1984). Wild
ruminants will learn to adapt in captivity and associate people with food, but
when frightened by some novel stimulus they are more likely to panic and injure
themselves (Grandin, 1993b, 1997).This is especially
likely if they are prevented from fleeing by a fence or other barrier.
Principles for training and handling all herding animals are basically similar.
Training procedures used on flighty antelope or placid domestic sheep are the
same. The only difference is the amount of time required. Grandin
(1989c) demonstrated this by training placid
In summary, experience
can affect behavior in two basic ways: by
conventional learning or by changing nervous system reactivity Most importantly, environmental conditions (enriched versus
barren) have the greatest effect on the nervous systems of young animals.
Neoteny is the retention of the juvenile features in an adult animal.
Genetic factors influence the degree of neoteny in
individuals. Neoteny is manifested both behaviorally and physically In the
forward to "The Wild Canids" (Fox, 1975),
Conrad Lorenz adds a few of his observations on neoteny
and the problems of domestication:
The
problems of domestication have been an obsession with me for many years. On the
one hand I am convinced that man owes the life-long persistence of his
constitutive curiosity and explorative playfulness to a partial neoteny which is indubitably a consequence of domestication
In a curiously analogous manner does the domestic dog owe its permanent
attachment to its master to a behavioral neoteny that prevents it from ever wanting to be a pack
leader On the other hand, domestication is apt to cause an equally alarming
disintegration of valuable behavioral traits and an
equally alarming exaggeration of less desirable ones.
Infantile
characteristics in domestic animals are discussed by Price (1984), Lambooij and van Putten (1993), Coppinger and Coppinger (1993), Coppinger and Scheider (1993),
and Coppinger et al. (1987). The shortened
muzzle in dogs and pigs is an example. Domestic animals have been selected for
a juvenile head shape, shortened muzzles, and other features (Coppinger and Smith, 1983). Furthermore, retaining juvenile
traits makes animals more tractable and easy to handle. The physical changes
are also related to changes in behavior.
Genetic studies point
to the wolf as the ancestor of domestic dogs (Isaac, 1970). During
domestication, domestic dogs have retained many of the infant wolf behaviors. For example, wolf pups bark and yap a lot but
adult wolves rarely bark; domestic dogs bark a lot (Fox, 1975; Scott and
Fuller, 1965). Wolves have hard-wired instinctive behavior
patterns that determine dominance or submission in social relationships. In
domestic dogs, the ancestral social behavior patterns
of the wolf are fragmented and incomplete. Frank and Frank (1982) observed that
the rigid social behavior of the wolf has
disintegrated into "an assortment of independent behavioral
fragments." Malamutes raised with wolf pups fail to read the social behavior signals of the wolf pups. Further comparisons
found that the physical development of motor skills is slower in the malamute.
Goodwin et al. (1997) studied 10 different dog breeds which ranged from
German shepherds and Siberian huskies to bulldogs, cocker spaniels, and
terriers. They found that the breeds which retained the greatest repertoire of
wolf-like social behaviors were the breeds that
physically resembled wolves, such as German shepherds and huskies. Barnett et
al. (1979) and Price (1985) both conclude that experience can also cause an
animal to retain juvenile traits. Gould (1977) also considered the effects of neoteny and stated that neoteny
is determined by changes in a few genes that determine the timing of different
developmental stages.
Countless
examples of serious problems caused by continuous selection for a single trait
can be found in the medical literature (Steinberg et al., 1994; Dykman et al., 1969). People with experience in
animal husbandry know that overselection for single
traits can ruin animals. Good dog breeders know this. Sometimes traits that
appear to be unrelated are in fact linked. Wright (1922, 1978) demonstrated
this clearly by continuous selection for hair color
and hair patterns in inbred strains of guinea pigs. Depressed reproduction
resulted in all the strains. Furthermore, differences in temperament, body
conformation, and the size and shape of internal organs were found. Belyaev (1979) further showed that continuous selection for
a calm temperament in foxes resulted in negative effects on maternal behavior and neurological problems. The fox experiments
also found graded changes in many traits over several years of continuous
selection for tame behavior. Physiological and behavioral problems increased with each successive
generation. In fact, some of the tamest foxes developed abnormal maternal behavior and cannibalized their pups. Belyaev
et al. (1981) called this "destabilizing selection," in
contrast to "stabilizing selection" found in nature (Dobzhansky 1970; Gould, 1977).
There are also
countless examples in the veterinary medical literature of abnormal bone
structure and other physiological defects caused by overselecting
for appearance traits in dog breeds (Ott, 1996). The
abnormalities range from bulldogs with breathing problems to German shepherds
with hip problems. Scott and Fuller (1965) reported the negative effects of
continuous selection for a certain head shape in cocker spaniels:
In our
experiments we began with what were considered good breeding stocks, with a
fair number of champions in their ancestry. When we bred these animals to their
close relatives for even one or two generations, we uncovered serious defects
in every breed. . .Cocker spaniels are selected for a broad forehead with
prominent eyes and a pronounced "stop," or angle, between the nose
and forehead. When we examined the brains of some of these animals during
autopsy, we found that they showed a mild degree of hydroencephaly;
that is, in selecting for skull shape, the breeders accidentally selected for a
brain defect in some individuals. Besides all this, in most of our strains only
about 50 percent of the females were capable of rearing normal, healthy
litters, even under nearly ideal conditions of care.
Single-minded
selection for production traits such as rapid gain and leanness resulted in
pigs and cattle with more excitable temperaments (Grandin,
1994). Compared to the older genetic lines with more hack fat, observations by
the first author on thousands of pigs indicate that lean hybrids are more
excitable and difficult to drive through races. Lean hybrid pigs also have a
greater startle response. Separating a single animal from the group is more
difficult. Recent research conducted in our laboratory has shown that cattle
with an excitable temperament have lower weight gains and more meat quality
problems (Voisinet et al., 1997a,b). This research illustrates that selection away from a
very excitable temperament would be beneficial. However, overselection
for an excessively calm temperament could possibly result in some unknown
detrimental trait.
Casual
observations by the first author also indicate that the most excitable, flighty
pigs and cattle have a long, slender body with fine bones. Some of the lean
hybrid pigs have weak legs and a few of the normally brown-eyed pigs now have
blue eyes. Blue eyes are often associated with neurological problems (Bergsma
and Brown, 1971; Schaible, 1963). Furthermore, pigs
and cattle with large, bulging muscles often have a calmer temperament than
lean animals with less muscle definition. However, animals with the muscle
hypertrophy trait (double muscling) have a more excitable temperament (Holmes et
al., 1972). Double muscling is extreme abnormal muscling and it might have
the opposite effect on temperament compared to normal muscling.
Another example of
apparently unrelated traits being linked is deafness in dogs of the pointer
breed selected for nervousness (Kllen et al.,
1987, 1988). There appears to be a relationship between thermoregulation and
aggressiveness. Wild mice selected for aggressiveness used larger amounts of
cotton to build their nests than mice selected for low aggression (Sinyter et al., 1995). This effect occurred in both
laboratory and wild Strains of mice.
Researchers using
high-tech "knockout" gene procedures have been frustrated by the
complexity of genetic interactions. In this procedure, genes are knocked out in
a gene-targeting procedure whereby a gene is prevented from performing its
normal function. The knockout experiments have shown that blocking different
genes can have unexpected effects on behavior. In one
experiment, superaggressive mice were created when
genes involved with learning were inactivated (Chen et al., 1994). The
mutant mice had little or no fear and fought until they broke their backs. In
another experiment the knockout mutants demonstrated normal behavior
until they had pups, and failed to care for them (Brown et al., 1996).
In still another experiment, Konig et al.
(1996) disabled the gene that produces enkephalin (a
brain opioid substance) and found unexpected results.
Enkephalin is a substance normally involved in pain
perception; however, the mice that were deficient in this substance were very
nervous and anxious. They ran frantically around their cages in response to
noise. The bottom line conclusion from several different knockout experiments
is that changing one gene has unexpected effects on other systems. Traits are
linked, and it may be impossible to completely isolate single gene effects.
Researchers warn that one must be careful not to jump to a conclusion that they
have found an '~aggression gene" or a "maternal gene" or an
"anxiety gene." To use an engineering analogy, one would not conclude
that they had found the "picture center" in
a television set after they cut one circuit inside the set that ruined the
picture. Gerlai (1996) and
Twenty years ago behavioral geneticists concluded that the inheritance of behavior is complex. Fuller and Thompson (1978) concluded,
"It has been found repeatedly that no one genetic mechanism accounts
exclusively for a particular kind of behavtor.
Behavioral geneticists have discovered that it is impossible to completely
control variation in some traits. Gartner (1990) found that breeding
genetically similar inbred lines of rats failed to stop weight fluctuations.
Even under highly standardized laboratory conditions, body weights continued to
fiuctuate between animals. Pig breeders have also
observed that commercially bred hybrid lines of pigs do not gain weight at the
same rate. Random unknown factors affect variability even in genetically
identical animals. Factors in utero may be one cause;
the other causes are unknown. Darrel Tatum and his students at
Gartner (1990)
concluded that up to 90% of the cause of random variability cannot be explained
by differences in the animals' physical environment. In both mice and cattle,
random factors affected body weights. Gartner (1990) believes that the random
factors may have their influence either before or shortly after fertilization.
The interactions
between environmental and genetic factors are complex. Both an animals' genetic
makeup and its environment determine how it will behave. In subsequent chapters
in this book the interactions of genetics and environment will be discussed in
greater detail. Genetics has profound effects on an animal's behavior.
There
is a complex interaction between genetic and environmental factors which
determines how an animal will behave. The animal's temperament is influenced by
both genetics and learning. Another principle is that changes in one trait,
such as temperament, can have unexpected effects on other apparently unrelated
traits. Overselection for a single trait may result
in undesirable changes in other behavioral and
physical traits.
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