Jensen,_P._2006[1]

Domestication—From behaviour

to genes and back again§

Per Jensen *

IFM-Biology, Linkoping University, SE-58183 Linkoping, Sweden

Available online 18 January 2006

Abstract

During domestication, animals have adapted with respect to behaviour and an array of

other traits. This tends to give rise to a specific domestication phenotype, involving similar

changes in colour, size, physiology and behaviour among different species. Hence, domestication

offers a model for understanding the genetic mechanisms involved in the trade-off between

behaviour and other traits in response to selection. We compared the behaviour and other

phenotypic traits of junglefowl and white leghorn layers, selected for egg production (and

indirectly for growth). To examine the genetic mechanisms underlying the domestication-related

differences, we carried out a genome scan for quantitative trait loci (QTLs) affecting behaviour

and production traits in F2-birds of a junglefowl � white leghorn intercross. Several significant

or suggestive QTLs for different production traits were located and some of these coincided

with QTLs for behaviour, suggesting that QTLs with pleiotropic effects (or closely linked QTLs)

may be important for the development of domestication phenotypes. Two genes and their

causative mutations for plumage colouration have been identified, and one of these has a

strong effect on the risk of being a victim of feather pecking, a detrimental behaviour disorder. It

is likely that fast and large evolutionary changes in many traits simultaneously may be caused

by mutations in regulatory genes, causing differences in gene expression orchestration.

Modern genomics paired with analysis of behaviour may offer a route for understanding the

www.elsevier.com/locate/applanim

Applied Animal Behaviour Science 97 (2006) 3–15

§ This paper is part of the special issue entitled International Society for Applied Ethology Special Issue—A

Selection of Papers from the 38th International Congress of the ISAE, Helsinki, Finland, August 2004, Guest

Edited by Victoria Sandilands and Carol Petherick.

* Tel.: +46 13 281298.

E-mail address: [email protected].

0168-1591/$ – see front matter # 2005 Elsevier B.V. All rights reserved.

doi:10.1016/j.applanim.2005.11.015

relation between behaviour and production and predicting possible side-effects of breeding

programs.

# 2005 Elsevier B.V. All rights reserved.

Keywords: Domestication; Gene; Genomics; Poultry; Chicken; QTL

1. Introduction: genes and behaviour

Let’s not mince matters: genes control behaviour, and this insight is one of the great

achievements of ethology. Of course, every biologist is well aware that a statement like

this will have to be expressed carefully to be generally true, for example, by saying that

a certain part of the phenotypic variation in behaviour is attributable to variation in

genotype (Alcock, 2001). However, it is quite clear that a particular behaviour

expression will never be possible unless there is a particular genetically determined

development of sensory organs, neurosystems and muscular systems. Hence, whether

we want to subscribe to the rather definite statement above will largely depend on what

we understand by ‘‘behaviour’’ and ‘‘genetic control’’ (Baker et al., 2001). For the

present discussion, I will use the term behaviour to include both the actual pattern of

muscle contractions forming a specific behaviour, and the level and intensity with

which it is expressed in a given situation. Genetic control will include all genetic

specifications of developmental pathways necessary for the expression of a particular

behaviour.

Embarrassingly enough, science has very little knowledge about how such control is

executed. Genes code for proteins, and modern genomics have excellent tools to

understand the genetic code on the level of proteins. Modern ethology likewise has

excellent tools for measuring and quantifying behaviour, but the link from DNA to

observable behaviour is – except for a few, rather simple cases – obscured by the seemingly

inaccessible complexity. Nevertheless, understanding the links is necessary if we want to

make real progress in understanding how behaviour is shaped by evolution, since natural

selection acts on the phenotype, but selects alleles for the next generation. The branch of

science involved in dissecting the molecular mechanisms involved in genetic control of

behaviour could be termed ‘‘behaviour genomics’’.

2. Domestication—a model for evolution

As already realised by Darwin, domestication offers a beautiful model for studying

phenomena like this. According to Price (1997), three processes are central to

domestication. Firstly, there is a relaxation of certain natural selection factors, such as

predation and starvation. Secondly, there is an intensified selection of traits preferred by

humans. Thirdly, there is natural selection under captivity, leading to adaptation. Side-

effects of selection, such as those outlined above, constitute a separate process, which also

needs attention when investigating domestication effects.

P. Jensen / Applied Animal Behaviour Science 97 (2006) 3–154

There is limited experimental research on the evolution of different traits, including

behaviour, during domestication. However, there is sufficient evidence based on

comparative studies of domestic stocks and their wild ancestors, to identify a number

of typical domestication changes, which can be summarized under the concept of ‘‘the

domesticated phenotype’’. This includes the following aspects:

(1) External morphological changes such as altered fur and plumage colours (mainly an

increased frequency of white and spotted colour morphs), changes in body size and

growth pattern, and changes in relative size of different body parts (including

brachycephaly, the shortening of skulls, and chondrodystrophy, the shortening of legs)

(Clutton-Brock, 1999).

(2) Internal morphological changes, such as an overall decrease in brain size, and modified

relative sizes of other internal organs, for example intestines (Jackson and Diamond,

1996; Kruska, 1996).

(3) Physiological changes, such as changes in endocrine responses and reproductive

cycles (Setchell, 1992; Kuenzl and Sachser, 1999).

(4) Developmental changes, such as earlier sexual maturity and changes in the length of

sensitive periods for socialisation (Belyaev et al., 1984).

(5) Behavioural changes, such as reduced fear, increased sociability, and reduced anti-

predator responses (Hedenskog, 1995; Johnsson et al., 1996; Price, 1997).

A typical domesticated phenotype of a species could therefore grossly be summarised

as differing from its wild ancestor in having a different plumage colour (probably being

white or spotted), being brachycephalic and chondrodystrophic, having a reduced brain

size and increased reproductive capabilities, developing faster and in a more flexible

manner, and being less fearful, more sociable and more risk-prone towards predators. This

is a trait complex, which tends to reoccur in many different domesticated species, and

therefore suggests that it may represent a general adaptation pattern to captivity and

domestication.

Interestingly, this complex of changes may develop rapidly, in only few generations, and

in concert, even though only one of the traits is selected for. Belyaev and co-workers

selected farm foxes only for reduced fearfulness towards humans, and found that the

frequency of animals showing this complex of adaptations, including morphological and

physiological changes, increased dramatically within 10–20 generations (Belyaev et al.,

1984; Vasilyeva, 1995). Observations such as this has led some researchers to suggest that

domestication phenotypes may be under control of few genes, perhaps regulating large

complexes of other genes affecting developmental and other traits (Stricklin, 2001).

Identifying such genes would be of prime importance for understanding the genetic

mechanisms involved in evolutionary change.

3. The genomic strategy

Genomics generally proceeds along a specific pathway of investigations in order to

identify genes involved in specific traits (Andersson, 2001), and determining its

P. Jensen / Applied Animal Behaviour Science 97 (2006) 3–15 5

mechanisms. First, we need animals which differ on the traits we are interested in—for

example growth rates, if we are interested in growth-related genes, or aggression if we are

interested in genes controlling aggressive behaviour. In such animals we may use

molecular methods to search for allelic differences which may help explaining the

phenotypic differences. Often, this may be facilitated by crossing parental animals of the

extreme phenotypes and looking at the inheritance patterns of the traits.

Once we have access to a suitable pedigree of animals with relevant variation in

interesting traits, unless we already have strong candidate genes, the genomic strategy

is to map the location of the genes we are looking for. Since behaviour is normally

inherited in a polygenic, additive manner, we are actually looking for many genes,

and we wish to estimate the contribution of each of the genes to the phenotypic

variation.

When the location of the genes is known, finding the actual gene and the mutations

causing the phenotypic variation can be done by utilising genome sequences and

bioinformatics tools. Most mapping methods will give a chromosome location which limits

the number of possible genes to perhaps a couple of hundred, so the actual gene

identification may be a rather time-consuming task.

Only when the gene is known with some certainty, we can start examining how the

mutations may cause the phenotypic variation we started out to examine. This process will

probably lead into proteomics and developmental biology. Applied to the case of

behavioural variation, the strategy of behaviour genomics will therefore lead us from

behaviour to genes and back again.

4. Chickens as model species

The first part of the strategy is to find a suitable animal material and pedigree. The

chicken has proved to be an excellent model animal for a number of reasons.

All poultry breeds are domesticated genotypes of the red junglefowl, Gallus gallus,

which live wild in south-east Asia, and it appears that domestication commenced at least

8000 years ago (Siegel et al., 1992; Yamashita et al., 1994). Junglefowl are readily

available, since they are kept in zoos throughout the world, and chickens exhibit among the

largest breed variability of all domestic animals, along with species such as dogs and

rabbits. For example, breeds are selected for appearance (show and hobby breeds),

aggression (fighting cocks), egg production (laying breeds), or rapid growth (broilers). This

makes the chicken an excellent model for genetic research, since crossings which produce

fertile offspring are possible between all breeds and their ancestors.

Birds have a definitive advantage over mammals such as rats and mice as behaviour

genetics models: their environments can be controlled from the point of egg laying (shortly

after fertilisation). By using artificial incubation and controlled rearing, environmental

variation can be controlled and reduced to a minimum, which means that genetic variation

will account for a larger proportion of the phenotypic variation in behaviour. Hence,

components of behaviour affected by genetic factors will be easier to detect in birds than in

mammals, where maternal effects during pregnancy and maternal care will add a large

portion of environmental variation which is different to control.


In addition, selection for production has been more intense in chickens than in any other

domestic species, and the production levels of modern poultry have therefore increased

dramatically. Production birds of today fall into two categories, the specialised laying hen,

selected for egg production, and the specialised broiler, selected for rapid growth.

However, even if the laying hen is not specifically selected for growth, it grows to about

double the size of junglefowl, and lays about ten times more eggs per year, which each is

more than double the size of those of junglefowls (Schutz, 2002). Some correlated side-

effects, both in health and behaviour, have been reported as a result of this (Braastad and

Katle, 1989; Rauw et al., 1998).

Last, but not least, the chicken genome recently became the first bird genome to be

sequenced (Consortium, 2004), which makes the species even more attractive as a model in

genomic studies.

5. Behavioural differences between laying hens and red junglefowl

In order to characterise the behavioural differences between the ancestor and a

selected model strain of laying hens, we compared their undisturbed behaviour in semi-

natural enclosures and in different controlled behaviour test situations (Schutz and

Jensen, 2001; Schutz et al., 2001). We found that mainly four aspects of behaviour

differed. Firstly, layers were generally less active, showing a reduced foraging and

exploratory behaviour. Secondly, they showed a less intense social behaviour, expressed

as a lower frequency of social interactions. Thirdly, they had a modified and less intense

antipredatory behaviour in tests where they were exposed to predator models, and

fourthly, there was a modified foraging strategy, where layers were less inclined to

explore unknown food sources. This is generally in line with the expectations from the

domestication phenotype theory, and would indicate a behavioural adaptation to

domestication in layers.

Phenotypic characterisations of these behavioural differences were then performed in a

number of different experiments involving junglefowl and laying hens which were

incubated, hatched and reared under identical conditions. In these experiments, we found

that junglefowl were generally more exploratory and appeared able to use the information

obtained by this exploration to adapt better to a sudden change in environmental conditions

(Lindqvist et al., 2002).

The social behaviour of the strains has also been further characterised. We found that the

type of behaviour patterns used by white leghorns in social interactions were very similar,

so no signal has been lost during domestication; however, junglefowl tend to display more

of the sexual and aggressive signals under identical conditions (Vaisanen et al., 2004).

Furthermore, we found indications that layers may have greater difficulty forming and

remembering social relationships (dominance–subordinance) than junglefowl, since the

aggression level after regrouping was generally higher in layers and persisted for a longer

time (Vaisanen et al., 2004). Again, the results indicate an adaptation to the domestication

environment on the part of laying hens, and signs of a negative effect on social adaptability.

The main phenotypical differences in behaviour and other traits between the laying hen

and its wild ancestor is summarised in Table 1.


6. QTL-analysis

The next step in the behaviour genomic strategy is to map the phenotypic differences to

specific loci. As already mentioned, behaviour as well as the other typical components of

the domestication phenotype (growth, physiology, etc.), are most likely polygenic and

show a quantitative inheritance pattern. Such traits have historically been very difficult to

map to specific loci, since mapping used to depend on analysing co-segregation of linked

loci with Mendelian inheritance, i.e. the offspring should fall into clear phenotypic

categories as a consequence of dominance patterns at single loci. However, the discovery of

molecular markers and the possibility of relatively simple analysis of these opened the

possibility for mapping so called quantitative loci, by means of analysing the inheritance of

neutral markers and measuring quantitative phenotypic traits in the same pedigree

(Andersson, 2001). This is referred to as quantitative trait locus analysis (QTL-analysis),

and a QTL is defined as a locus which contains alleles that differentially affect the

expression of a continuously distributed phenotypic trait. Finding a QTL for a trait is

therefore the first step towards identifying a gene affecting a phenotypic trait.

To start locating and identifying genes controlling the phenotypic differences between

junglefowl and layers, we performed a large scale QTL-analysis of different traits, including

morphological, physiological and behavioural ones. A QTL-analysis is commonly

performed by breeding a segregating population, for example an F2-intercross between

divergent lines, and then analysing the segregation of DNA-markers in this population. By

analysing the statistical association between DNA-markers and phenotypic traits, the control

of polygenic traits can be linked to specific chromosomal areas (Weller, 2001). The

junglefowl we used stemmed from zoo populations, and were obviously affected genetically


Table 1

Some important phenotypic differences in morphology, production traits, and behaviour between red junglefowl

and white leghorn layers; average values (data adopted from Schutz and Jensen, 1999; Lindqvist et al., 2002;

Schutz et al., 2002)

Phenotypic character Red junglefowl White leghorn

Adult body weight (g) Males: 1100, females: 800 Males: 2100, females: 1600

Age at start of

egglaying (week)

25 20

Egg size (g) 23 57

Egg mass produced

per week (g)

97 367

Plumage colour Wild-type White

Feeding behaviour Extensive, wide-ranging Intensive, local feeding

Explorative behaviour Frequent, wide-ranging

exploration

Less frequent, less wide-ranging

Anti-predator behaviour Vigilant, intensive reactions Less vigilant, less intensive reactions

General fearfulness Fearful to novel

stimuli and humans

Less fearful to novel stimuli and humans

Social behaviour Forms dominance relations fast,

frequent interactions

in stable groups

Forms dominance relations slower,

less frequent interactions in stable groups

For precise figures of behavioural differences, see the original publications.

and behaviourally by captivity (Hakansson and Jensen, 2005). However, they were

sufficiently different from domesticated breeds to suffice for our analysis.

We crossed one junglefowl male with four white leghorn females and intercrossed 36

F1-birds to obtain more than 1000 F2-animals. The parental male had a distinct genotype

on the DNA-markers, which allowed a powerful QTL-analysis. From 751 F2-

individuals, we obtained a full data matrix containing 101 DNA-markers (mostly

microsatellites), data on growth, egg production and feed consumption, and behavioural

data from an array of different tests, designed mainly to quantify aspects, which had been

characterised as major differences between the parental strains (as summarised in

Table 1).

Fig. 1 shows the general layout of the F2-intercross, together with a schematic layout of

how the QTL-analysis was performed.


Fig. 1. Schematic representation of the layout of the F2-intercross and the associated QTL-analysis. In the

parental chromosomes, indicated as vertical bars, two markers are denoted by M and N, with alleles 1 and 2,

respectively. The position of the QTL is indicated by Q, and in this example, the parentals are assumed to be fixated

for alternative alleles of Q, denoted 1 and 2. F1-animals in the middle row were all heterozygous on both marker

loci and QTLs. During gamete formation in the F1s, recombination gives rise to mosaic chromosomes in the F2-

generation, where the associations between marker alleles and QTL-alleles will depend on the distance between

them. In the bottom panel, some possible recombinations are shown. In F2, the parental origin of each marker can

be ascertained, and the regression between the probability of a specific marker genotype and the trait value

associated with the QTL can be calculated. When markers are evenly spaced on all chromosomes, a probability for

a particular locus to be associated with a particular trait (QTL) can therefore be obtained for all loci in the genome.

7. Coinciding QTLs for production and behaviour

We analysed for genome-wise significance and used Monte Carlo simulations to

ascertaing the critical p-values for the different traits (Carlborg et al., 2003). A number of

QTLs associated with growth and egg production were located. A surprising finding was

that a limited number of QTLs explained a large proportion of the difference in growth rate

between the junglefowl and the white leghorn—four QTLs explained 50% of the difference

in adult body weight of females and 80% of that of males (Kerje et al., 2003a). A QTL

analysis testing for epistasis revealed that epistatic interaction between genes played a

significant role for early growth but not for late growth (Carlborg et al., 2003). The two

most important growth QTLs were located on chromosome 1 (tentatively named Growth1

and Growth2). Growth1 was also found to be significantly related to egg production (mean

egg size), even after allometric corrections.

Both Growth1 and Growth2 were also related to different aspects of behaviour. In a

genome-wide scan, QTLs for tonic immobility duration and induction were located in the

same region as Growth1 and Growth2. Regression analysis of these two QTLs on various

behavioural variables showed significant effects on other fear-related behaviour as well,

such as latency to approach a novel object, activity in an open field and corticosterone

reaction in an open field (Schutz, 2002; Schutz et al., 2004) (Table 2).

It is possible that pleiotropic QTLs like these may have played a major role during

domestication, although a similar effect can be caused by closely linked QTLs. In

particular Growth1 is a potentially interesting locus to analyse further. Interestingly, no

other QTL analyses of growth performed on chickens have revealed this locus despite the

fact that it had the most prominent effect in our intercross with the red junglefowl (Kerje

et al., 2003a). Since all other studies have involved intercrosses between domestic breeds


Table 2

Position of genome-wide QTLs (chromosome number and position in centimorgans, cM) with behavioural effects,

and some of their pleiotropic effects, as mapped in an F2-intercross between red junglefowl and white leghorn

layers

Chromosome Position (cM) Behavioural trait affected Observed pleiotropic trait effects

1 67 Tonic immobility** Growth**, egg mass**

1 480 Tonic immobility* Growth**

1 467 Novel object reaction** Growth**

1 394 Headflick frequency* –

1 176 Restraint inactivity* –

3 272 Restraint defecation* –

6 51 Restraint activity* –

7 174 Foraging behaviour** –

11 0 Restraint reaction** –

13 14 Open field activity* –

26 32 Victim of feather-pecking** Plumage melanisation**

27 0 Sociality** –

Data adopted from Schutz et al. (2002, 2004), Carlborg et al. (2003), Kerje et al. (2003a,b, 2004) and Keeling et al.

(2004). For precise estimates of precision in positions and significance levels, see the original publications.* p < 0.2.

** p < 0.05.

(for example, crosses between broilers and layers), this suggests that the domestic alleles at

the Growth1 locus are fixed in domestic breeds, which in turn may be an indication that this

allele was selected early during domestication.

8. Gene localisation and animal welfare

Of course, localisation of a QTL is only the first step towards finding the actual genes

and mutations causing a phenotypic effect. Using homologies between other sequenced

genomes (for example mouse, rat and human) and the chicken genome, it has been possible

to identify and characterise some of the genes and their causative mutations in our animals.

This has enabled us to identify genes involved in plumage colouration variation in fowl. We

have identified a mutation in the melanocortin 1-receptor (MC1R) gene, which has a

significant effect on the phenotypic expression of black pigment (Kerje et al., 2003b).

Furthermore, we identified a causative mutation in the PMEL17 gene, which we could

show to be responsible for the well-known dominant white-phenotype: birds with the

mutation, which involves a nine base-pair insertion in one of the exons, causing a

dysfunction of the eumelanosomes, do not express any black pigment at all (although they

may express other pigments, such as red) (Kerje et al., 2004). Since plumage colour is a

significant element of the domestication phenotype, these results are potentially interesting

in their own right in understanding domestication biology.

One of the colour mutation genes was also found to have a profound effect on an

important welfare-related behaviour, namely feather pecking. This is one of the most

important welfare-related behavioural problems in modern egg production, where birds

peck at and pull out the feathers of other individuals in the same group (Fig. 2). We found

that feather pecking was common in junglefowl, and more common in females than in

males (Jensen et al., 2005). Examining both the performance of feather pecking and the


Fig. 2. The average feather pecking damage score of birds with pigmented plumage, compared to white birds

(where the white colour is caused by a mutation in the gene PMEL17). Data adopted from Keeling et al. (2004).

resulting plumage condition in all F2-birds, we found a significant QTL for plumage

condition, indicating the risk of being the victim of the behaviour (Keeling et al., 2004).

This QTL coincided perfectly with the PMEL17-locus, and homozygote for the wild

genotype were significantly more vulnerable to being victims, whereas heterozygote were

almost as protected from the behaviour as the homozygous mutant (both heterozygote and

homozygote mutants were largely white). Furthermore, the risk of being victimised

apparently increased when the wild-types were more common in a cohort.

Even though the full significance of these findings remains speculative, it is clear that

victim traits may influence the development of this detrimental behaviour, which have

many parallel cases in other domesticated species (for example, tail biting in fattening pigs

and wool eating in sheep). It may also suggest that lack of plumage pigmentation could be

an adaptive evolutionary response, which reduces the risk of being victim of feather

pecking in chickens, and thus help explaining the development of domesticated white

phenotypes in this species.

9. Beyond allelic variation: gene expression patterns

Traditionally, evolutionary biologists have thought in terms of Mendelian genetics,

where phenotypic variation is ascribed to mutations in specific alleles, and where the

inheritance patterns of these mutations hold the keys to evolution of a population. However,

it has become increasingly clear that allelic variations cannot explain the vast phenotypic

variation between organisms with rather similar genomes. For example, humans and

chimpanzees have DNA-sequences which are on average 98.8% similar, and it has so far

been very difficult to pinpoint specific mutations explaining the main differences between

the species (Paabo, 2003). Recently, scientists have therefore started to look deeper into

how and when genes are actually expressed in mRNA and proteins, and found striking

effects on behaviour (Hofmann, 2003). For example, in voles, experimentally changing the

expression level of one single gene (V1aR, encoding a vasopressin receptor) in the ventral

forebrain changed the behaviour of a normally promiscuous species into a pair-forming

animal (Lim et al., 2004). Hence, large phenotypical differences can be achieved without

large allelic differences.

The orchestration of gene expression during development may be an important part of

developmental biology and domestication (Saetre et al., 2004), and such patterns of

expression differences may be affected by mutations in regulatory genes (Andersson and

Georges, 2004). In such a scenario, a single nucleotide mutation may have huge effects on a

variety of phenotypic traits, and such mutations may therefore underlie the rapid and

complex phenotypic changes observed during domestication. Our findings, where we have

found one specific genomic region involved in many apparently unrelated phenotypes, may

lend support to this possibility. To analyse effects caused by changes in gene expression, we

have developed a cDNA chip containing over 13 000 expressed sequence tags (EST;

roughly corresponding to genes). In future research, we will therefore be able to analyse not

only allelic differences between domesticated and wild birds, but also the relative

expression of thousands of different genes in different tissues, such as the brain, at different

times.


10. Implications: breeding and animal welfare

Over the last decades, breeding for increased production has been the dominating goal

for animal agriculture. It has been estimated that average production levels have increased

by more than 85% since 1960, and parallel to that, many production-related diseases and

disorders have increased; for example, leg problems in fattening pigs, mastitis and

lameness in dairy cattle, and locomotory and circulatory problems in fast-growing broilers

(Rauw et al., 1998). Hence, breeding animals with a large emphasis on increasing

production may be associated with risks for animal welfare. To be able to maintain, and

even increase, production levels in farm animals in the future, without jeopardising

welfare, there is a need for increased biological knowledge about the mechanisms behind

side-effects on traits, which are not explicitly selected for. For example, increasing the

frequency of alleles which cause faster growth may at the same time cause a modification

in developmental, behavioural, physiological or immunological traits under the influence

of the same genes.

Behaviour is a central part of the mechanisms allowing animals to adapt to their social

and physical environments (for example, through learning and through forming social

systems). Therefore, selection side-effects on behaviour may have serious effects on the

welfare of animals. If genes that are under selection pressure during breeding for increased

production simultaneously affect behaviour, the adaptive capacity of the selected animals

may be affected.

11. Conclusions

Domestication involves a rapid and complex change of many different phenotypic

changes, which act in concert in a similar manner in many different species. We have

shown that, in chickens, an array of these changes are affected by few loci, and I suggest

that this may indicate that domestication changes can be caused by only few genes,

possibly with regulatory functions. In addition to increasing the understanding of genetic

control of behaviour, this may help us understand how animals adapt to selection pressures

induced by man during domestication.

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