Breeding of tomorrow’s chickens to improve well-being1
H.-W. Cheng2
Livestock Behavior Research Unit, USDA-Agricultural Research Service, West Lafayette, IN 47907
ABSTRACT Chickens, as well as other animals, have
the ability to change their behavior (behavioral plasticity) and physiology (physiological plasticity) based on
the costs and benefits to fit their environment (adaptation). Through natural selection, the population preserves and accumulates traits that are beneficial and
rejects those that are detrimental in their prevailing
environments. The surviving populations are able to
contribute more genes associated with beneficial traits
for increased fitness to subsequent generations. Natural
selection is slow but constant; working over multiple
generations, the changes to the population often appear silent or undetectable at a given point in history.
Chickens were domesticated from the wild red jungle
fowl. The principle of domestication of chickens, as well
as other farm animals, by humans is similar to that
of natural selection: selecting the best animals with
the highest survivability and reproducibility (artificial
selection). Compared with natural selection, the process of artificial selection is motivated by human needs
and acts more rapidly with more visible results over a
short time period. This process has been further accelerated following the development of current breeding programs and the emergence of specialized breeding
companies. A laying hen, for example, produces more
than 300 hundred eggs a year, whereas a jungle fowl
lays 4 to 6 eggs in a year. During the domestication
process, chickens retained their capability to adapt to
their housing environments, which is usually achieved
by genetic changes occurring with each subsequent generation. Genes control the behavioral, physiological, immunological, and psychological responses of animals to
stressors, including environmental stimulations. With
advances in understanding of genetic mediation of animal physiology and behavior and the discovery of the
genome sequences of many species, animal production
breeding programs can be improved in both speed and
efficiency. Modern chicken breeding programs have the
potential to be operated successfully in the breeding
of tomorrow’s chickens with high production efficiency
and optimal welfare, resulting from resistance to stress,
disease, or both.
Key words: adaptation, selection, farm animal, chicken, well-being
2010 Poultry Science 89:805–813
doi:10.3382/ps.2009-00361
THE ABILITY OF ANIMALS’ ADAPTATION
ior to fit a particular environment through adaptation
(Crespi and Denver, 2005). How well animals adapt to
their environment affects their reproductive success,
survival capability, and degree of well-being.
Adaptation, in a physiological context, is the basic
phenomena encompassing various biological processes
that ensure an organism becomes better suited to its
current environment (plasticity). In an evolutionary
context, adaptation refers to changes in the characteristics of populations or species resulting from natural
selection. The apparent degree of adaptation could be
significantly different among species and among individuals within a species based on their genetic make-up
(hereditary); however, adaptation is a universal reaction
of all living organisms. In general, adaptation can be
classified as evolutionary adaptation (heritable changes over generations), individual adaptation (changes
within an individual during its lifetime), and cultural
adaptation (passing on individual changes to others in
the group). In fact, there are overlaps between the different adaptations in animals to meet the requirements
Change is defined as becoming different or modification. Change is the rule (i.e., our world is constantly
changing). In nature, the changing environment puts
selection pressure on all living things including animals
for survival and reproduction (natural selection). In
artificial or man-made environments (domestication),
farm animals including chickens also constantly change
to meet human needs (artificial selection). In fact, under selection pressure (natural selection, artificial selection, or both), an animal or species has the ability to
alter its development, growth, physiology, and behav©2010 Poultry Science Association Inc.
Received July 17, 2009.
Accepted August 16, 2009.
1 Presented as part of the Keynote Symposium: Tomorrow’s Poultry: Genomics, Physiology, and Well-Being at the Poultry Science Association’s annual meeting in Raleigh, North Carolina, July 20–23,
2009.
2 Corresponding author: [email protected]
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Cheng
of their given environment. Commonly, animal populations are genetically modified in response to environmental challenge to shape their unique characteristics
in an adaptive manner (Brommer, 2000; Horton, 2005).
The genetically associated adaptation can be observed
in changes in the physical, physiological, and behavioral expression (i.e., associations of molecular markerbiological traits; Gilbert, 2001; Nijhout, 2003; Crespi
and Denver, 2005; Soller et al., 2006). The ability of
animals to express plasticity at genetic and physiological characteristics provides a foundation for the breeding of tomorrow’s chickens to improve well-being and,
at the same time, to meet human needs.
MECHANISMS OF ADAPTATION
OF ANIMALS
Genetic Plasticity
Genes are sensitive to environmental change. Adaptation of animals can occur through modification of
their chromatin structure, such as change of the gene
sequence through genetic drift, mutation, and recombination (Soller et al., 2006). Genetic changes in a population of animals, as a function of selection pressure,
lead to sustained differences in phenotypes (phenotypic
plasticity). Each phenotype, with changed gene expression, will have uniquely observable biological characteristics (Price et al., 2003; Price, 2006). For example,
natural variations in stress response in rats influence
gene expression and stress response in their offspring
(i.e., some of them adapt to stimulations better than
others; McGowan et al., 2008). Genetic improvement
of farm animals including chickens has been done
through selecting varieties under the production conditions (phenotypes based on human needs). The better
flitted animals were selected to breed (specific alleles)
and, consequently, to pass on favorable characteristics
(genes) to their offspring. Genetic diversity in chickens
(Soller et al., 2006) and their different expressions in response to various stimuli, such as social stress and temperature (cold and hot stress), have been reported previously (Craig and Muir, 1996a,b; Hester et al., 1996;
Cheng and Muir, 2005). Understanding the mechanisms
underlying genetic plasticity and expression as well as
their association with biological traits will provide new
strategies for breeding tomorrow’s chickens to improve
their well-being.
Physiological Plasticity
Physiological plasticity refers to changes in the biological processes of an animal in response to environmental stimuli. It permits the animal to adapt to a
particular environment for successful survival or reproduction, or both. In animals, physiological changes
could act at multiple levels, such as within the endocrine, metabolic, and nervous systems. Among these
systems, the nervous system plays an important role in
animal adaptation to a given environment.
In the central nervous system, neurons receive, identify, integrate, and interpret incoming sensory stimuli
from the internal and external environments of the
body, then produce electrochemical impulses that are
transmitted to the effectors organs of the body (muscles and glands) to initiate appropriate responses to
the stimuli (adaptation). The responses aim to satisfy
physiological drives of an organism, such as survival,
experience of positive or avoidance of negative emotions, and learning to improve performance. In response
to changes in the environment, neurons have the ability
to change cellular characteristics and functions (neuroplasticity).
Neuroplasticity refers to the ability of the brain to
respond and adapt functionally and structurally (such
as synaptic plasticity; i.e., activity-dependent modification of the strength of synaptic transmission) to a
given environmental challenge, which in turn adjusts
subsequent movement, thoughts, feelings, and behavior (Kasper and McEwen, 2008; Pittenger and Duman,
2008; Calabrese et al., 2009; Maleszka et al., 2009).
There is evidence that suggests that the central nuclei
of avians, at least in part, are morphofunctional homologous to the mammalian nuclei, such as the hypothalamus (Watkins, 1975), nucleus taeniae (homolog to the
amygdala of mammals; Thompson et al., 1998; Soma
et al., 1999), and Raphe nucleus (Challet et al., 1996),
and exert a similar capability for plasticity in response
to environmental stimulations (Lowndes and Stewart,
1994; Tramontin and Brenowitz, 2000; Meitzen et al.,
2009; Wissman and Brenowitz, 2009).
The mechanisms underlying alterations in neuroplasticity are believed to relate to changes in neurotransmitters, hormones, and growth factors (Kasper and
McEwen, 2008). Neurotransmitters are regulated by
neuronal activity that is affected by changes in the morphological and physiological properties of the central
nervous system neurons. Changes in the neurotransmitter system, including alterations in biosynthesis, densities of receptors, and gene expression, have been used
as indicators of central neuronal plasticity in response
to stimulations, including domestication, in mammals
(Popova et al., 1997; Ferris et al., 1999). These changes
functionally help the animal to adapt to its environment and are reflected as changes in behaviors. There
is evidence in birds, as in mammals, that neurotransmitter systems exert similar functions in controlling
behavioral adaptation (Barrett et al., 1994). Previous
studies have shown that there are similar distributions
of neurotransmitter receptors, including dopaminergic
and serotonergic receptors, in avians as those found in
mammals (Richfield et al., 1987; Walker et al., 1991).
Different genotypic or phenotypic, or both, characteristics are associated with specific neurotransmitter systems (Popova et al., 1997; Siegel et al., 1999) and several neurotransmitters, such as serotonin (5-HT) and
KEYNOTE SYMPOSIUM
dopamine (DA), that control stress response and behavioral styles have been reported in animals including
chickens (Bell and Hobson, 1994; Popova et al., 1997;
Weiger, 1997; Cheng and Muir, 2005, 2007).
Behavioral Plasticity
Behavioral plasticity is defined by changes in the
way that individuals respond and interact to a given
environment (such as searching for food, mating, vocalization, and migration). Behavior of animals is controlled by both internal and external factors. Behavioral traits evolve as a function of other phenotypic
and morphological traits, such as neural and endocrine
factors (Hetts, 1991; Mehiborn and Rehkamper, 2009).
For example, in the chickens, behaviors such as fear,
feather pecking, and aggression can be reduced through
selecting productivity or longevity, or both, in a group
selection paradigm (Muir, 1996, 2003, 2005; Bolhuis et
al., 2009).
There are variations in behavioral phenotypes within
a species and within an individual over time. Behavioral
traits have a strong hereditable component in much the
same way as physiological characteristics [i.e., inherited
patterns of behavior of individuals (innate behavior
traits) can be modified in accordance with the habitat
on an individual]. In addition, behavior of an animal is
also determined by its memory and ability to learn new
behaviors. Both instinct and learning affect inherited
patterns in behavior.
Ability to Learn
Animals can learn new behaviors by trial and error.
Wild animals live in a natural environment and possess both inborn behavior patterns (species-specialized)
and learned behaviors from life experiences (individual-specialized) to survive and to produce successful
offspring in competitive environments. Similarly, farm
animals including chickens have the ability to learn new
behaviors, which affects their ability to adapt to given
environments (Martin et al., 2000; Gibbs et al., 2008).
Change of spine and dendrite morphology (synaptic
plasticity) as well as the strength of synaptic transmission (long-term potentiation) in the limbic system, especially in the hippocampus, has been found in animals
following memory tasks (Martin et al., 2000). Ali et al.
(2009) reported that a single exposure to an enriched
environment for 1 h stimulates the activation of discrete neuronal populations in the mouse brain. Within
the populations, animals’ memory and ability to learn
are influenced by both heritable and nonheritable factors.
Physical Plasticity
Physical plasticity is the type of change in an animal
affecting its actual structure (structural adaptation).
It exhibits as changes of physical features of an ani-
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mal, such as beak shape and body covering in birds, by
which the animal can live in a particular environment
and in a particular way. For example, in 1977, Peter
and Rosemary Grant documented that during drought,
finches can change their physical characteristics, increased body size and beak length, to meet drought-associated environmental demands (Grant, 1986). Honey
bees can adjust their body development in response
to their social environment (i.e., body development is
slowed down in response to an isolated environment;
Maleszka et al., 2009).
Taken together, animals including chickens have the
ability to adapt to better fit their surrounding environments through functional and physical plasticity.
However, the genetic-based varieties in plasticity have
been found among the individuals of a population and
species in response to natural selection, artificial selection, or both.
NATURAL SELECTION IN ANIMALS
Individuals of a population or populations can be
changed by their environment through natural selection. Natural selection is defined as that “selection due
to ongoing selection else effects of a past environment,”
(i.e., an evolutionary process that leads to differential
survival and reproductive success among individuals
or groups; Wikipedia, 2009). Competing species have
to constantly adapt to their environment to maintain
their relative standing. Natural populations carry an
immense amount of genetic variability (Dobzhansky,
1981). Some individuals within a population, with favorable phenotypes for a particular environment, are
better suited to survive and to have more offspring than
others, passing their genetic material, including the genetic variants that code for those favorable phenotypes,
on to the next generation through natural selection.
Darwin (1859) was the first to recognize that natural
selection causes the phenotypic diversity of evolution in
natural populations. In nature, selection acts to provide
animals with the ability to display the best behavior
(flexible behavioral programs, also called behavioral
plasticity) and physiology (flexible energy programs,
also called physiological plasticity) based on the costs
and benefits of each, with the largest net benefit under different conditions of life being selected for at any
given point in history (Krebs and Davies, 1991; Arnold,
2004; Hendry, 2005; Arnold and Burke, 2006).
Natural selection randomly applies selection pressure
(the blind force) on the individuals of a population or
species. Selection pressures pull in different directions,
phenotype as a whole, and the adaptation results in
an elegant compromise. Competing species have to
constantly adapt to maintain their relative standing.
However, in nature, not all individuals and species of
animals have equal capability to adapt to their environments or modify their behavioral and physiological
characteristics in response to environmental challenges.
Most animals die before becoming sexually mature. Only
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Cheng
Table 1. Selection-induced alterations in the productivity and
survivability in laying hens
KGB line1
Trait
Mortality (%)
Longevity (d)
Egg number, per hen
Egg mass, per hen (g/d)
Egg weight (g)
1.3b
363b
295b
48b
59.4a
±
±
±
±
±
0.1
0.4
11
2
0.6
MBB line1
8.6a
193a
108a
17a
58.9a
±
±
±
±
±
0.5
21
12
1.8
0.8
a,bMeans within a row with different superscripts differ significantly
(P < 0.05).
1The KGB (kind gentle birds) and MBB (mean bad birds) lines were
selected from high and low productivity and survivability resulting from
cannibalism and flightiness (Cheng and Muir, 2005).
the individuals and populations with greatest adaptive
capability survive to pass on their genetic material to
future generations, and subsequent generations become
better adapted to the environments. Diversification of
populations is achieved through natural selection, beneficial traits in a given environment are acquired and
maintained (in terms of survival and reproductive),
whereas those detrimental in the same environment
are rejected (Hendry, 2005). The process (phenotypic
plasticity) is evidenced in almost every group of plant
and animal (Via and Lande, 1985). However, it may
take multiple generations before the changes are great
enough to be observed.
Farm animals including chickens were domesticated
from wild animals thousands of years ago to meet a
variety of human needs, such as meat, milk, and skin
from beef-dairy cattle; meat and skin from pigs; and
meat and eggs from chickens (Andersson, 2001). Animals have to adapt to their artificial environment for
survival during the process of domestication. Adaptation in farm animals can be viewed as a continuing domestication process and a developmental phenomenon.
DOMESTICATION OF FARM ANIMALS
INCLUDING CHICKENS
Changes in physical, physiological, and behavioral
characteristics occur far more rapidly through domestication. Domestication is a cumulative process that occurs over multiple generations. During domestication,
the selected populations of animals adapt to humans
and to their captive environments by integrated changes
in their genes, behaviors, physiology, and psychology to
ensure the animals achieve superior inheritable plasticity. Chickens, for example, were domesticated from the
wild red jungle fowl at least 5,000 yr ago (Fumihito et
al., 1994) and are a very productive food source of both
meat and eggs. The commercial laying hen produces
more than 300 eggs a year; in contrast, their ancestral
parent species, the jungle fowl, lays 4 to 6 eggs per year
(Natural Encounters Inc., 2006).
During domestication, animals are housed in environments under protection by human beings, resulting in morphological and physiological changes in the
animals, which could greatly shift their priorities and
interests from those of their wild counterparts (Boessneck, 1985). Domesticated chickens, as an example, are
provided with food, water, and protection and are artificially selected for specific traits, such as meat or egg
production. This paradigm results in survival strategies that are likely to be different compared with those
from their wild ancestral breeds for which food is scare
and predation pressure is high (Gustaffson et al., 1999;
Andersson et al., 2000). The outcomes of domestication may increase the fitness of farm animals because
Halverson (2003) indicated that domestication is not
only improvement of the productive performance but
also of the quality of life of farmed animals. The natural
environments may not be suitable for domestic farm
animals because they are modified or designed, or both,
differently by artificial selection (domestication) as well
as natural selection to function in certain ways to adapt
to their surrounding environments (Broom, 1991; Rollin, 1992, 1993, 1995).
The outcomes during domestication could lead to improvement of the welfare of animals by increasing fitness
for the given environments. Alternately, these adaptive
changes may carry a risk of leading to poor welfare by
decreasing fitness resulting in distress. The effects of
these changes on welfare should be determined from
well-designed functional and motivational analyses of
the natural behaviors of farm animals and the capability of their adaptability to their housing environments.
Artificial Selection
The changes in individuals in a population during
domestication can be further enhanced by human intervention through artificial selection (phenotypic evolution; Yamasaki et al., 2007). Artificial selection is the
traditional way to bring about genetic improvements in
farm animals [i.e., the animals with variations better
fitted to the production conditions are chosen to breed
for passing on favorable characteristics (specific genes)
to their offspring (Gomez-Raya et al., 2002)]. The principle of artificial selection of animals including chickens
by humans is similar to that of natural selection: selecting the best animals with the highest survivability and
reproducibility. Domesticated animals are spectacular
departures from their original native partners, in terms
of behavioral, physical, or physiological characteristics,
Table 2. Selection-induced alterations in the adrenal systems
Lines1
KGB
MBB
Adrenal glands (index)2
72 ±
58 ±
4a
5b
Corticosterone (ng/mL)
1.87 ± 0.19
1.49 ± 0.21
a,bMeans within a column with different superscripts differ significantly (n = 12, P < 0.05).
1The KGB (kind gentle birds) and MBB (mean bad birds) lines were
selected for high and low productivity and survivability resulting from
cannibalism and flightiness (Cheng and Muir, 2005).
2Adrenal weight index = the absolute adrenal gland weight/BW ×
100.
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Figure 1. Annual percentage of mortality of the commercial (Dekalb XL), control, and KGB (kind gentle birds) lines. Compared with
birds from the Dekalb XL line and control line, selected KGB birds
had the lowest mortality (Cheng and Muir, 2005).
or all of these characteristics. As Darwin (1859) indicated, artificial selection and the production of domesticated animals was a powerful analogy for the action
of natural selection, and any given species is being genetically molded through selection (nature, artificial, or
both) into a composite of individuals whose anatomy,
physiology, and behavior are optimally suited for living
and reproducing in a given environment. However, the
outcomes of artificial selection are much faster and visible than those of natural selection. In some cases, its
effects can be seen within one generation or just a few
more (Bolhuis et al., 2009).
Changing animals (modifying their genes) to accommodate their housing systems has become an important
tool in breeding farm animals. Humans are constantly
changing the selection pressures on domesticated farm
animals, with the aim of achieving the best economic outcome, and evaluating whether populations and
species of selected animals are able to adapt accordingly. Animal breeding is a slow process; however, a
combination of strong selection and a high degree of
heritability can change the relative abundance of genes
in a population up to 10% per generation (Wikibooks,
2009). Repeated, selective breeding events will alter the
proportion of different genes over time; selected genes
associated with desired characteristics will become
overrepresented.
Historically, animal welfare, such as expression of desirable behavioral and physiological traits, was not con-
sidered in the traditional breeding programs (Hester,
2005). Artificial selection of most livestock species had
been motivated by traits related to efficiency and quality of production such as BW, egg production, feed
efficiency, and egg quality, but this was often at the expense of animal welfare (Stricklin, 2001). The extreme
selection for one trait (productivity) could affect other
traits, causing negative effects on animal welfare. For
example, in laying hens, there are several consequences of selection that have ignored animal welfare: 1) if
productivity is correlated with competitive capability,
then the effect of selection for production is to increase
competition; 2) increased competition has the effect of
lowering productivity of other animals such as subordinates that are in direct contention, thus resulting in reduced (or negative) gains for productivity (as a group);
and 3) genotype-genotype interactions (competition)
invalidate the traditional best linear unbiased prediction animal model and negate many advantages of this
technology and could in fact make it a liability. For
instance, through more than 20 yr of selection, egg production has increased significantly in the commercial
Dekalb XL birds, whereas mortality due to aggression
and cannibalism in non-beak-trimmed birds has also
increased about 10-fold (Muir, 1996).
Broiler chickens, selected for meat production, grow
too rapidly (more than 2.5 to 3 kg within 5 to 6 wk)
to be supported by their legs and heart, resulting in
lameness or ascites, or both. Similar to the findings
in poultry, selection for the Rex hair color in rabbits
has resulted in disturbance of metabolic and endocrine
functions that increase mortality and susceptibility to
specific diseases (Muntzing, 1959). These findings support our hypothesis that an animal is a wholeorganism.
Selection for phenotypic characteristics associated with
production will affect other traits that regulate their
domestic behavioral and physiological adaptabilities to
the current intensive housing environments. The results
further provide evidence that when selection acts on a
single trait, it can simultaneously act to move 2 or more
traits that are linked by pleiotropy (i.e., physical linkage or adjacent to one another on the chromosome and
behave as if they are one gene; Sinervo, 1997; Stricklin,
2001; Bijma et al., 2007a,b).
In chickens, artificial selection has acted on the genetic variability (specific alleles) of the populations
to produce food for humans, such as egg production
or meat production, causing genetic changes that result in visible structural alterations and the changes
Table 3. Selection-induced alterations in blood concentrations of catecholamines and serotonin in laying hens
Lines1
KGB
MBB
a,bMeans
Dopamine (ng/mL)
0.59 ±
2.42 ±
0.08a
0.76b
Epinephrine (ng/mL)
0.30 ±
0.59 ±
0.06a
0.13b
Norepinephrine (ng/mL)
EP:NE2 (%)
Serotonin (ng/mL)
0.86 ± 0.12
0.84 ± 0.13
34.0a
72.5b
11.8 ± 0.07a
14.3 ± 0.06b
within a column with different superscript differ significantly (P < 0.01).
KGB (kind gentle birds) and MBB (mean bad birds) lines were selected from high and low productivity and survivability resulting from cannibalism and flightiness (Cheng and Muir, 2005).
2EP = epinephrine; NE = norepinephrine.
1The
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Cheng
Table 4. Selection-induced alterations in the differential leukocyte counts in laying hens
Line1
KGB
MBB
Heterophils (H)
10.7 ±
20.4 ±
1.1b
1.8a
Lymphocytes (L)
83.4 ±
72.3 ±
H:L ratio (×100)
1.3a
1.8b
Monocytes
13.0b
29.4a
2.6 ± 0.4
2.1 ± 0.4
Eosinophils
1.7 ±
3.8 ±
0.2b
0.4a
Basophils
1.6 ± 1.1
1.4 ± 0.2
a,bMeans
within a column with no common superscript differ significantly (P < 0.01).
KGB (kind gentle birds) and MBB (mean bad birds) lines were selected for high and low productivity and survivability resulting from cannibalism and flightiness. (Cheng and Muir, 2005).
1The
in associated physiological activities. However, these
changes could be positive or negative to chicken wellbeing. Selection pressure should be carefully balanced
across multiple traits, especially in the context of their
housing environments, such as battery cages, furnished
cages, barn system, and free-range, as well as group size
and density.
Group Selection in Laying Hens
Breeding of tomorrow’s chickens to improve well-being requires enhancing the adaptability of the animals
to their surrounding environments. It is a complex interaction between genes and the social environment.
Social interactions can substantially increase heritable
variance in trait values (Bijma et al., 2007b; Bergsma
et al., 2008; Ellen et al., 2008). In laying hens, for example, social effects contribute to approximately half of
the heritable variance in mortality due to cannibalism
(Ellen et al., 2008). Functional integrations between behavior, physiology, and morphology may create suites
of traits in animals that are simultaneously acted upon
by selection. Based on those findings, we developed a
selection program named group selection (Craig and
Muir, 1996a,b; Muir, 1996, 1997, 2003, 2005). In group
selection, effort is focused on assessing how individuals
survive and reproduce in a group. The advantage of
the program is that it allows selection on production
traits but takes into account competitive interactions
in a group setting. The program focuses on gene(s), environment, and genetic-environmental interactions, by
which it turns “survival of the fittest” with emphasis
on the individuals to “survival of the adequate” with
emphasis on the group, by which antisocial behaviors
are overcome.
In the studies, a synthetic line of White Leghorns was
used in the selection program. A commercial Dekalb XL
line was one of the resources used to establish the line
(unselected control line) from which the selected kinder
gentler line was established. During the selection, each
sire family was housed as a group in a multiple-bird
cage and selected or rejected as a group based on the
production performance and longevity. Birds were not
beak-trimmed and lights were maintained at high intensity so as to allow expression of variation for aggression, feather pecking, and cannibalism. Through the
selection, 2 divergent chicken lines, KGB (kind gentle
birds) with high group productivity and survivability
and MBB (mean bad birds) with low group productivity and survivability, were developed (Table 1, Figure
1; Muir, 1996; Cheng and Muir, 2005). Use of these 2
diversely selected strains as animal models has shown
that selection for high and low group productivity and
longevity with alterations in cannibalism and flightiness
affected the regulations of the neuroendocrine system
of selected birds. Corticosterone (Table 2) and monoamines, such as 5-HT, DA, epinephrine, norepinephrine
(Table 3), and immune parameters (Table 4, 5, Figure
2; Cheng and Muir, 2005), were differently regulated
following group selection pressure. Compared with
the reverse selected birds (MBB), KGB birds selected for more productivity and longevity showed higher
domestic behaviors, (low cannibalism and flightiness)
and positive alterations in the neuroendocrine system
(lower blood concentrations of 5-HT, DA, and epinephrine and higher levels of plasma corticosterone). These
alterations are likely associated with their superior coping ability when confronted with a novel environment
or a greater resistance to stressors (Hester et al., 1996).
The functional interactions between behavior, physiology, and morphology may create suites of traits for different coping capabilities to their environments. The
unique homeostatic characteristics of each selected line
may provide a neurobiological basis for investigating
effects of genetic factors on physiological functions of
biogenic amines involved in productivity and longevity related to domestic behaviors. Results from these
studies have shown that productivity can be increased
while at the same time well-being improved. The method has been verified in poultry breeding applications
Table 5. Selection-induced alterations in the subpopulations of T cells in the hens
Group1
KGB
MBB
a,bMeans
CD4+ cells (% positive)
33.0 ± 2.1
29.3 ± 3.3
CD8+ cells (% positive)
18.2 ±
25.8 ±
1.8b
1.5a
CD4+:CD8+ (ratio)
γδ cells (% positive)
1.9a
1.1b
16.1 ± 2.1
12.2 ± 2.8
within a column with no common superscript differ significantly (P < 0.01).
KGB (kind gentle birds) and MBB (mean bad birds) lines were selected for high and low productivity and survivability resulting from cannibalism and flightiness (Cheng and Muir, 2005).
1The
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Figure 2. A) Separated proteins on the gels were stained with Coomassie Blue. B) Separated proteins on the gels were detected by the Western
blot analysis plus enhanced chemiluminescence. Lane 1 = prestained broad range molecular weight marker; lane 2 = commercial chicken IgG;
lanes 3 to 5 = samples from KGB (kind gentle birds) hens; lanes 6 to 8 = samples from MBB (mean bad birds) hens. The band from samples
was identical with the band prepared with commercial chicken IgG, and size of IgG was identified approximately at 67 kDa (arrow) (Cheng and
Muir, 2005).
and has resulted in dramatic improvements in survivability, productivity, and welfare (Ellen et al., 2008).
Similar selection programs, targeting desirable traits,
have been practiced in pigs (Crawley et al., 2005) and
cattle (Moioli et al., 2004).
GENETIC ENGINEERING IN POULTRY
The genetic makeup of farm animals, including that
of chickens, has been changed by selective breeding for
desirable production, behavior, and other biological
traits (phenotypes) since domestication. Genetic selection is an important breeding tool that can be used
for improving the coping capability of an animal to
a particular production environment and for increasing economic benefits. The progress made in breeding
and biotechnology has brought new life to the attempts
of research and industry to improve animal well-being
through modification of behavioral and physiological
characters of animals. Over the course of the past 2 decades, researchers have evidenced the potential for alternative methods of selection to increase both productivity and animal well-being. Such methods will benefit
both the producers and the animals.
Over the past 5 decades, specialized companies have
emerged to develop high-yielding breeds of broiler chickens, laying hens, pigs, and dairy and beef cattle using
various modern technologies in addition to traditional
methods of animal breeding, such as artificial insemination, embryo transfer, and cloning. Recently, with
the discovery of the map of genomics, including whole
genome sequences (International Chicken Genome Sequencing Consortium, 2004a) and a high-density SNP
map (International Chicken Polymorphism Map Consortium, 2004b) in chickens, the characterization of
avian biodiversity can be established more rapidly and
efficiently. Breeding programs will be improved greatly
by identification of candidate genes (molecular markers) related to desirable physical or behavioral characteristics (biological traits), that is, marker-trait associations (functional genomics), as well as transgenics and
RNA interference. Selection on genes, as opposed to
phenotype, promises to be more accurate, efficient, and
economically beneficial even before production traits
are measured (Burt, 2005; Harpending and Cochran,
2006; Cogburn et al., 2007; Womack, 2007; Laible,
2009). Such selection has been and will continue to be
very successful in breeding chickens, as well as other
farm animals, with high production efficiency and optimal welfare.
In conclusion, numerous studies in various farm animals including chickens have demonstrated that animals can adapt to their environments by changing their
behavioral and biological characteristics including genetic sequence. The heritable traits that are beneficial
to individuals of a population in a particular environment can be passed on to future generations. In addition, the discovery of genomic sequences is an essential
step toward identifying genetic markers of adaptation
of animals. Advanced genetic technologies provide a
new opportunity for genetic improvement of animals,
which will speed up breeding programs for successfully
breeding tomorrow’s animals including chickens with
high production efficiency and optimal welfare, resulting from resistance to stress, disease, or both.
REFERENCES
Ali, A. E., Y. M. Wilson, and M. Murphy. 2009. A single exposure
to an enriched environment stimulates the activation of discrete
neuronal populations in the brain of the fos-tau-lacZ mouse.
Neurobiol. Learn. Mem. 92:381–390.
Andersson, L. 2001. Genetic dissection of phenotypic diversity in
farm animals. Nat. Rev. Genet. 2:130–138.
Andersson, M., P. Jensen, and E. Nordin. 2000. Domestication effects on foraging strategies in fowl (Gallus gallus). Appl. Anim.
Behav. Sci. 70:99–114.
Arnold, M. L. 2004. Natural hybridization and the evolution of
domesticated, pest and disease organisms. Mol. Ecol. 13:997–
1007.
Arnold, M. L., and J. M. Burke. 2006. Natural hybridization. Pages
399–413 in Evolutionary Genetics: Concepts and Case Studies.
C. W. Fox and J. B. Wolf, ed. Oxford University Press, Oxford,
UK.
Barrett, J. E., L. Zhang, S. Gleeson, and E. H. Gamble. 1994. Anxiolytic and antidepressant mechanisms of 5-HT1A drugs in the
812
Cheng
pigeon: Contributions from behavioral studies. Neurosci. Biobehav. Rev. 18:73–83.
Bell, R., and H. Hobson. 1994. 5-HT1A receptor influences on rodent social and agonistic behavior: A review and empirical study.
Neurosci. Biobehav. Rev. 18:325–338.
Bergsma, R., E. Kanis, E. F. Knol, and P. Bijma. 2008. The contribution of social effects to heritable variation in finishing traits of
domestic pigs (Sus scrofa). Genetics 178:1559–1570.
Bijma, P., W. M. Muir, E. D. Ellen, J. B. Wolf, and J. A. M. Van
Arendonk. 2007a. Multiple selection 2: Estimating the genetic
parameters determining inheritance and response to selection.
Genetics 175:289–299.
Bijma, P., W. M. Muir, and J. A. M. Van Arendonk. 2007b. Multiple
selection 1: Quantitative genetics of inheritance and response to
selection. Genetics 175:277–289.
Boessneck, J. 1985. Domestication and its sequelae. Tierarztl. Prax.
13:479–497.
Bolhuis, J. E., E. D. Ellen, C. G. Van Reenen, J. De Groot, J. Ten
Napel, R. Koopmanschap, G. De Vries-Reilingh, K. A. Uitdehaag, B. Kemp, and T. B. Rodenburg. 2009. Effects of genetic
group selection against mortality on behaviour and peripheral
serotonin in domestic laying hens with trimmed and intact beaks.
Physiol. Behav. 97:470–475.
Brommer, J. E. 2000. The evolution of fitness in life-history theory.
Biol. Rev. Camb. Philos. Soc. 75:377–404.
Broom, D. M. 1991. Animal welfare: Concepts and measurement. J.
Anim. Sci. 69:4167–4175.
Burt, D. W. 2005. Chicken genome: Current status and future opportunities. Genome Res. 15:1692–1698.
Calabrese, F., R. Molteni, G. Racagni, and M. A. Riva. 2009. Neuronal plasticity: A link between stress and mood disorders. Psychoneuroendocrinology doi:10.1016/j.psyneuen.2009.05.014
Challet, E., D. Miceli, J. Pierre, J. Reperant, G. Masicotte, M.
Herbin, and N. P. Vesselkin. 1996. Distribution of serotonin-immunoreactivity in the brain of the pigeon (Columba livia). Anat.
Embryol. (Berl.) 193:209–227.
Cheng, H. W., and W. M. Muir. 2005. The effects of genetic selection for survivability and productivity on chicken physiological
homeostasis. World’s Poult. Sci. J. 61:383–397.
Cheng, H. W., and W. M. Muir. 2007. Mechanisms of aggression
and production in chickens: Genetic variations in the functions
of serotonin, catecholamine, and corticosterone. World’s Poult.
Sci. J. 63:233–254.
Cogburn, L. A., T. E. Porter, M. J. Duclos, J. Simon, S. C. Burgess,
J. J. Zhu, H. H. Cheng, J. B. Dodgson, and J. Burnside. 2007.
Functional genomics of the chicken—A model organism. Poult
Sci. 86:2059–2094.
Craig, J. V., and W. M. Muir. 1996a. Group selection for adaptation
to multiple-hen cages: Beak-related mortality, feathering, and
body weight responses. Poult. Sci. 75:294–302.
Craig, J. V., and W. M. Muir. 1996b. Group selection for adaptation to multiple-hen cages: Behavioral responses. Poult. Sci.
75:1145–1155.
Crawley, A. M., B. Mallard, and B. N. Wilkie. 2005. Genetic selection for high and low immune response in pigs: Effects on immunoglobulin isotype expression. Vet. Immunol. Immunopathol.
108:71–76.
Crespi, E. J., and R. J. Denver. 2005. Ancient origins of human developmental plasticity. Am. J. Hum. Biol. 17:44–54.
Darwin, C. 1859. On the origin of species by means of natural selection or the preservation of favored races in the struggle for life.
John Murray, London, UK.
Dobzhansky, T. 1981. Dobzhansky’s Gentics of Natural Populations.
R. C. Lewontin, J. A. Moore, W. B. Provine, and B. Wallace.
Columbia University Press, Irvington, NY.
Ellen, E. D., J. Visscher, J. A. M. van Arendonk, and P. Bijma.
2008. Survival of laying hens: Genetic parameters for direct
and associative effects in three purebred layer lines. Poult. Sci.
87:233–239.
Ferris, C. F., T. Stolberg, and Y. Delville. 1999. Serotonin regulation
of aggressive behavior in male golden hamsters (Mesocricetus auratus). Behav. Neurosci. 113:804–815.
Fumihito, A., T. Miyake, S. Sumi, M. Takada, S. Ohno, and N.
Kondo. 1994. One subspecies of the red junglefowl (Gallus gallus
gallus) suffices as the matriarchic ancestor of all domestic breeds.
Proc. Natl. Acad. Sci. USA 91:12505–12509.
Gibbs, M. E., A. N. Johnston, R. Mileusnic, and S. F. Crowe. 2008.
A comparison of protocols for passive and discriminative avoidance learning tasks in the domestic chick. Brain Res. Bull.
76:198–207.
Gilbert, S. F. 2001. Ecological developmental biology: Developmental biology meets the real world. Dev. Biol. 233:1–12.
Gomez-Raya, L., H. G. Olsen, F. Lingaas, H. Klungland, D. I. Vage,
I. Olsaker, S. B. Talle, M. Aasland, and S. Lien. 2002. The use
of genetic markers to measure genomic response to selection in
livestock. Genetics 162:1381–1388.
Grant, P. R. 1986. Ecology and Evolution of Darwin’s Finches.
Princeton University Press, Princeton, NJ.
Gustafsson, M., P. Jensen, F. de Jonge, and T. Schuurman. 1999.
Domestication effects on foraging strategies in pigs (Sus scrofa).
Appl. Anim. Behav. Sci. 62:305–317.
Halverson, M. 2003. Animal well-being issue: Where economics of
intensive production and welfare conflict. Pages 42–45 in Sharing Costs of Changes in Food Animal Production: Producers,
Consumers, Society and the Environment. One in a Series of
Educational Programs Presented by the Future Trends in Animal
Agriculture. R. Reynnells, ed. USDA, Washington, DC.
Harpending, H., and G. Cochran. 2006. Genetic diversity and genetic burden in humans. Infect. Genet. Evol. 6:154–162.
Harris, D. L., and S. Newman. 1994. Breeding for profit: Synergism between genetic improvement and livestock production (a
review). J. Anim. Sci. 72:2178–2200.
Hendry, A. P. 2005. The power of nature selection. Nature 433:694–
695.
Hester, P. Y. 2005. Impact of science and management on the welfare of egg laying strains of hens. Poult. Sci. 84:687–696.
Hester, P. Y., W. M. Muir, J. V. Craig, and J. L. Albright. 1996.
Group selection for adaptation to multiple-hen cages: Hematology and adrenal function. Poult. Sci. 75:1295–1307.
Hetts, S. 1991. Psychologic well-being: Conceptual issue, behavioral
measures, and implications for dogs. Vet. Clin. North Am. Small
Anim. Pract. 21:369–387.
Horton, T. H. 2005. Fetal origins of developmental plasticity: Animal models of induced life history variation. Am. J. Hum. Biol.
17:34–43.
International Chicken Genome Sequencing Consortium. 2004a. Sequence and comparative analysis of the chicken genome provide
unique perspectives on vertebrate evolution. Nature 432:695–716.
PubMed
International Chicken Polymorphism Map Consortium. 2004b. A genetic variation map for chicken with 2.8 million single-nucleotide
polymorphisms. Nature 409:860–921.
Kasper, S., and B. S. McEwen. 2008. Neurobiological and clinical
effects of the antidepressant tianeptine. CNS Drugs 22:15–26.
Krebs, J. R., and D. B. Davies. 1991. Behavioural Ecology: An Evolutionary Approach. Blackwell Scientific Publications, Oxford,
UK.
Laible, G. 2009. Enhancing livestock through genetic engineering—
Recent advances and future prospects. Comp. Immunol. Microbiol. 32:123–137.
Lowndes, M., and M. G. Stewart. 1994. Dendritic spine density in
the lobus parolfactorius of the domestic chick is increased 24 h
after one-trial passive avoidance training. Brain Res. 654:129–
136.
Maleszka, J., A. B. Barron, P. G. Helliwell, and R. Maleszka. 2009.
Effect of age, behaviour and social environment on honey bee
brain plasticity. J. Comp. Physiol. A Neuroethol. Sens. Neural.
Behav. Physiol. 195:733–740.
Martin, S. J., P. D. Grimwood, and R. G. Morris. 2000. Synaptic
plasticity and memory: An evaluation of the hypothesis. Annu.
Rev. Neurosci. 23:649–711.
McGowan, P. O., M. J. Meaney, and M. Szyf. 2008. Diet and the
epigenetic (re)programming of phenotypic differences in behavior. Brain Res. 1237:12–24.
Mehiborn, J., and G. Rehkamper. 2009. Neurobiology of the homing
pigeon—A review. Naturwissenschaften 96:10111025, .
Meitzen, J., A. L. Weaver, E. A. Brenowitz, and D. J. Perkel. 2009.
Plastic and stable electrophysiological properties of adult avian
KEYNOTE SYMPOSIUM
forebrain song-control neurons across changing breeding conditions. J. Neurosci. 29:6558–6567.
Moioli, B., F. Napolitano, and G. Catillo. 2004. Genetic diversity
between Piedmontese, Maremmana, and Podolica cattle breeds.
J. Hered. 95:250–256.
Muir, W. M. 1996. Group selection for adaptation to multiplehen cages: Selection program and direct responses. Poult. Sci.
75:447–458.
Muir, W. M. 1997. Genetic selection—Strategies for the future.
Poult. Sci. 76:1066–1070.
Muir, W. M. 2003. Indirect selection for improvement of animal wellbeing. Pages 247–256 in Poultry Breeding and Biotechnology. W.
M. Muir and S. Aggrey, ed. CABI Press, Cambridge MA.
Muir, W. M. 2005. Incorporation of competitive effects in forest tree
or animal breeding programs. Genetics 170:1247–1259.
Muntzing, A. 1959. Darwin’s views on variation under domestication in the light of present-day knowledge. Proc. Am. Philos.
Soc. 103:190–220.
Natural Encounters Inc. 2006. Burmese Red Junglefowl (Gallus
gallus).
hhttp://www.naturalencounters.com/othersB.
html#BrolgaCrane Accessed July 10, 2009.
Nijhout, H. F. 2003. Development and evolution of adaptive polyphenisms. Evol. Dev. 5:9–18.
Pittenger, C., and R. S. Duman. 2008. Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology 33:88–109.
Popova, N. K., A. V. Kulikov, D. F. Avgustinovich, N. N. Voitenko,
and L. N. And Trut. 1997. Effect of domestication of the silver
fox on the main enzymes of serotonin metabolism and serotonin
receptor. Genetika 33:370–374.
Price, T. D. 2006. Phenotypic plasticity, sexual selection and the
evolution of colour patterns. J. Exp. Biol. 209:2368–2376.
Price, T. D., A. Ovarnstrom, and D. E. Irwin. 2003. The role of
phenotypic plasticity in driving genetic evolution. Proc. Biol.
Sci. 270:1433–1440.
Richfield, E. K., A. B. Young, and J. B. Penney. 1987. Comparative distribution of dopamine D-1 and D-2 receptors in the basal
ganglia of turtles, pigeons, rats, cats, and monkeys. J. Comp.
Neurol. 262:446–463.
Rollin, B. E. 1992. Animal Rights and Human Morality. Rev. ed.
Prometheus Books, Buffalo, NY.
Rollin, B. E. 1993. Animal welfare, science and value. J. Agric.
Environ. Ethics 6(Suppl. 2):44–50.
Rollin, B. E. 1995. Farm Animal Welfare: Social, Bioethical, and
Research Issues. Iowa State University Press, Ames.
Siegel, A., T. A. Roeling, T. R. Gregg, and M. R. Kruk. 1999. Neuropharmacology of brain-stimulation-evoked aggression. Neurosci. Biobehav. Rev. 23:359–389.
813
Sinervo, B. 1997. Introduction to natural and sexual selection: 3. Adaptation and selection. http://bio.research.ucsc.edu/~barrylab/
classes/animal_behavior/SELECT.HTM Accessed July 10,
2009.
Soller, M., S. Weigend, M. N. Romanov, J. C. Dekkers, and S. J.
Lamont. 2006. Strategies to assess structural variation in the
chicken genome and its associations with biodiversity and biological performance. Poult. Sci. 85:2061–2078.
Soma, K. K., R. K. Bindra, J. Gee, J. C. Wingfield, and B. A.
Schlinger. 1999. Androgen-metabolizing enzymes show regionspecific changes across the breeding season in the brain of a wild
songbird. J. Neurobiol. 41:176–188.
Stricklin, W. R. 2001. Genetic bases of animal welfare. Pages 313–
324 in Animal Welfare Considerations in Livestock Housing Systems. Proceedings of the International Symposium. Agricultural
University of Wroctaw, Szklarska Poreba, Poland.
Thompson, R. R., J. L. Goodson, M. G. Ruscio, and E. AdkinsRegan. 1998. Role of the archistriatal nucleus taeniae in the
sexual behavior of male Japanese quail (Cotunix japonica): A
comparison of function with the medial nucleus of the amygdala
in mammals. Brain Behav. Evol. 51:215–229.
Tramontin, A. D., and E. A. Brenowitz. 2000. Seasonal plasticity in
the adult brain. Trends Neurosci. 23:251–258.
Via, S., and R. Lande. 1985. Genotype-environmental interaction
and the evolution of phenotypic plasticity. Evolution 39:505–
522.
Walker, E. A., T. Yamamoto, P. J. Hollingsworth, C. B. Smith, and
J. H. Woods. 1991. Discriminative-stimulus effects of quipazine
and l-5-hydroxytryptophan in relation to serotonin binding sites
in the pigeon. J. Pharmacol. Exp. Ther. 259:772–782.
Watkins, W. B. 1975. Immunocytochemical identification of neurophysin-secreting neurons in the hypothalamo-neurohypophysial
system of some non-mammalian vertebrates Cell Tissue Res.
162:511–521.
Weiger, W. A. 1997. Serotonergic modulation of behaviour: A phylogenetic overview. Biol. Rev. Camb. Philos. Soc. 72:61–95.
Wikibooks. 2009. Animal Behavior/Evolution. http://en.wikibooks.
org/wiki/Animal_Behavior/Evolution Accessed July 10, 2009.
Wikipedia. 2009. Natural selection. http://en.wikipedia.org/wiki/
Natural_selection Accessed July 10, 2009.
Wissman, A. M., and E. A. Brenowitz. 2009. The role of neurotrophins in the seasonal-like growth of the avian song control system. J. Neurosci. 29:6461–6471.
Womack, J. E. 2007. Advances in livestock genomics: Opening the
barn door. Genome Res. 15:1699–1705.
Yamasaki, M., S. I. Wright, and M. D. McMullen. 2007. Genomic
screening for artificial selection during domestication and improvement in Maize. Ann. Bot. (Lond.) 100:967–973.