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Chapter 3

Approaches to the Study

of Domestication

Before getting into the biological mechanisms associated with the process of
domestication, it is important to note how current knowledge of domestication has
been derived. This chapter introduces and discusses the four major approaches
that have been used to gain a better understanding of the domestication process:
(i) comparison of wild and domestic stocks (of a species); (ii) monitoring the
generation-by-generation changes in a population that has recently been brought
into captivity; (iii) searching for ‘domestication’ genes; and (iv) the study of
wild × domestic hybrids.

Comparing Wild and Domestic Stocks

The most commonly used approach in studying the domestication process is to
compare wild and domestic stocks of a given species (e.g. Price, 1973; Desforges
and Wood-Gush, 1976; Huck and Price, 1976; Boice, 1980; Price, 1980; Wong
et al., 1982). This approach assumes that the wild stock used is representative of
the wild ancestors of the domesticated population investigated, a requirement that
is difficult if not impossible to attain, even for our more recently domesticated
animals. First, the ancestral origin of many of our domesticated species is
uncertain (Zeuner, 1963; Hyams, 1972). For decades the common laboratory
mouse was believed to have been derived from wild M. musculus (Schwarz
and Schwarz, 1943). Then, Marshall (1981) argued that the morphology of
the laboratory mouse resembled M. domesticus more closely. Now, Blank et al.
(1986) have provided information suggesting that the common inbred strains
and substrains of laboratory mice have been derived from several Mus species
including M. musculus, M. castaneus, M. molossinus and M. domesticus. This conclusion
is based on a survey of protein and DNA polymorphism data suggesting extensive

©CAB International 2002. Animal Domestication and Behavior

(E.O. Price) 13

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14 Chapter 3

fixation of alleles from various loci in the above species. An additional dilemma
is that the wild counterparts of some of our common domesticated animals
have become extinct or are unavailable for scientific experimentation (Isaac,
1970). Even when ancestral populations are available, one cannot assume these
populations have remained static since the domestication process was initiated.
Selection of an experimental wild population may present an additional
problem. Because of geographical variation, no single population selected
for study may adequately represent the genetic diversity present in the species
(Mitchell et al., 1977; Berry, 1978; Van Oorschot et al., 1992). Leopold (1944)
reported differences in the escape patterns of certain populations of wild and
domestic turkey poults (M. gallopavo) in response to alarm calls. However, Hale
(1969) noted that differences among wild subspecies are even greater, leaving
open the question whether the differences observed by Leopold were due to
domestication. Garcia-Marin et al. (1991) found that only 3% of the total genetic
variation among hatchery stocks of brown trout (Salmo trutta) could be explained
by stock differences whereas 60% of the total genetic variation among wild trout
was due to differences between populations.
Once a suitable wild population is identified, capture bias may confound
efforts to obtain a representative cross-section of individuals from that population.
Baker et al. (2001) reported that free-living subordinate red foxes (Vulpes vulpes)
were trapped more frequently than dominant individuals. This concern is
especially important if wild-caught individuals rather than subsequent, captive-
reared generations are used for study.
A related problem lies in identifying a representative domestic population
(Box, 1973, p. 122). The many breeds or strains of our common domestic animals
and the geographical variation associated with most of these stocks re-emphasize
the problem of choosing representative populations for study. Boreman and Price
(1972) systematically hybridized four strains of domestic rats (R. norvegicus) to
produce a single, more representative domestic stock for study.
In addition, most comparisons of wild and domestic populations are con-
ducted on animals reared either in nature or captivity but not both environments.
If we assume that wild animals are best adapted to wild environments and domes-
tic animals are best adapted to domestic environments (Garcia-Marin et al., 1991),
such comparisons are likely to be skewed in favor of one of the test populations,
usually the domestic population since most domestication research is conducted in
the captive environment. Even when wild and domestic populations are reared
in both environments (Wecker, 1963; Price, 1969), the comparative approach
provides little or no information on how the traits actually develop or how rapidly
phenotypic changes occur during the domestication process. The comparative
approach only provides a description of differences between specific populations
of wild and domestic animals at a single point in time. Consequently, its major
usefulness is in generating hypotheses regarding the effects of domestication upon
behavior. Gross (1998) has summarized some of the genetic- and developmentally
based differences between farmed and wild Atlantic salmon (Salmo salar) (Table
3.1). This information is especially useful since many of the studies compared both

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Approaches to the Study of Domestication 15

Table 3.1. Some genetic and developmental differences between cultured

(farmed) and wild salmon. (From Gross, 1998.)

Genetic Developmental

Confirmed Suspected Confirmed Suspected

Increased growth No ejaculation Lower stamina Gut length

rate Reduced male Smaller eggs Diet preference
Increased age of courtship More eggs Stream
maturity Higher hatchery More fat knowledge
Increased weight survival Smaller rayed fins Body odor
Increased disease Higher temperature (parr and adult)
resistance tolerance Smaller heads on
Decreased stress Shallower depth parr
response preference Bulkier body on
Lower genetic Larger testes adult
diversity Juvenile color Distorted jaw on
Allele frequency Adult color adult
change Longer head on
Malic enzyme adult
allele change Longer adipose fin
Reduced predator on adult
response Smaller hearts in
Increased juvenile females
aggression Decreased juvenile
Increased tameness color
Lower survival in Decreased adult
wild color

stocks reared in either captive or wild environments. Studies comparing wild

animals reared in nature and their domesticated counterparts reared in captivity
(Diefenbach and Goldberg, 1990; Mesa, 1991) are necessarily confounded by
rearing environment.

The Longitudinal Approach

In contrast to the comparative approach just described, the longitudinal approach
to domestication research monitors phenotypic changes in a population of
animals over generations of breeding in captivity. With this information, one can
better estimate the rate at which phenotypic changes occur during domestication
under different regimens of breeding and husbandry. The problem of species
representativeness is less restrictive when using the longitudinal approach since
the emphasis is on how individual populations change over time (generations).

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16 Chapter 3

An example of the longitudinal approach is a study by King and Donaldson

(1929) and King (1939), who monitored changes in the growth rate and
reproductive success of a population of wild Norway rats (R. norvegicus) over the
first 25 generations in captivity. During this period, positive gains were noted for
body weight, percentage of mated pairs that produced offspring, number of litters
born and length of the reproductive lifespan. The investigators also reported that
the tendency to escape and the resistance to handling declined over generations,
although these responses were not quantified.
Connor (1975) also used the longitudinal approach in an attempt to re-enact
the domestication process in a population of wild house mice (M. musculus). Three
subpopulations of genetically wild mice were established: (i) a randomly bred wild
population maintained in standard laboratory cages; (ii) a randomly bred wild
population maintained in an enriched naturalistic environment (located in the
laboratory); and (iii) an inbred population of wild mice (brother/sister matings)
maintained in standard laboratory cages. In addition, Connor established three
populations of inbred domestic mice for comparative purposes. A battery of six
behavioral tests (19 variables that clearly differentiated wild and domestic mice)
was administered to the various populations over ten generations of breeding in
captivity. No behavioral differences were found between tenth-generation wild
mice reared in standard laboratory cages and wild mice maintained in the
naturalistic environment. Yet both of these stocks still differed significantly from
domestic mice. Inbreeding reduced intermale aggression and resistance to capture
by humans but failed to affect body weight, handling-elicited vocalizations,
investigation of intruders and escape from intruders. These results suggest that
ten generations of breeding in captivity is insufficient to produce the domestic
phenotype in this species, with or without systematic inbreeding.

The Search for ‘Domestication’ Genes

In addition to the comparative and longitudinal approaches to domestication
research, one may look for so-called ‘domestication genes’ in animal populations.
Keeler et al. (1968) and Keeler (1975) reported that tameness in captive red foxes
(V. vulpes) is linked in a correlated (pleiotropic) manner to alleles for pelage color-
ation. Avoidance of humans by captive foxes was inversely related to the number
of mutant coat-color alleles in the genotype. Keeler had much earlier (1942)
reported that docility in the domestic Norway rat (R. norvegicus) is associated with
the nonagouti (black) pelage-color allele. The nonagouti allele is masked by the
albino locus in this species (Robinson, 1965). Cottle and Price (1987) confirmed
Keeler’s hypothesis. They found that captive-reared wild-genotype Norway
rats homozygous for the recessive nonagouti allele, which confers black pelage
coloration, could be handled with greater ease than animals heterozygous or
homozygous for the agouti allele, whose pelage coloration is brown (Table 3.2).
Interestingly, the black and agouti subjects did not differ in three other tests that
clearly differentiate wild and domestic stocks of rats (open-field test, platform

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Approaches to the Study of Domestication 17

Table 3.2. Percentage of agouti (n = 62) and black (n = 28) Norway rats
exhibiting the behaviors listed on the first day of handling tests. (From Cottle
and Price, 1987.)

Behavior Agouti (AA) Black (aa)

Could be touched 64% 96%

Could be stroked 32% 89%
Attacked–attempted to bite 59% 25%
Jumped 91% 57%

jumping and response to a novel food). Hughes et al. (1981) also reported no differ-
ences between black and agouti wild Norway rats in open-field (novel arena)
behavior and activity-wheel running.
A decade later, Hayssen (1997) replicated the Cottle and Price (1987) study
with deermice (Peromyscus maniculatus) some 20 generations removed from the
wild. The results were very similar; nonagouti deermice were more touchable,
strokeable, catchable and less likely to attack the experimenter’s hand than the
agouti subjects. While nonagouti and agouti rats did not differ in the platform
jump measures, nonagouti deermice were less likely than agouti subjects to
jump off the platform. In addition, nonagouti mice spent significantly more
time grooming.
Biochemical studies with recombinant agouti protein (Lu et al., 1994; Willard
et al., 1995) indicate that agouti is an antagonist of melanocyte-stimulating
hormone (MSH) at its receptor on pigment cells and potentially at other melano-
cortin receptors in neural tissues. Melanocortins are potent neuromodulators with
diverse effects on mammalian behavior and physiology (e.g. O’Donohue and
Dorsa, 1982). Thus, the behavioral differences between agouti and nonagouti rats
and mice are probably related to the regulation and effects of MSH. In addition,
Hayssen et al. (1994) reported that agouti and nonagouti deermice differ in their
neural catecholamine profiles, especially in the mid- and hindbrain. Neural MSH
is located primarily in the hypothalamus, and pituitary MSH is regulated by
dopamine neurons (see Hayssen, 1997, for references). Interestingly, selection for
tameness (toward humans) in foxes, mink and rats is accompanied by changes in
brain biochemistry (see Chapter 14).
Although most behaviors are polygenic (i.e. influenced by many genes),
certain alleles have a relatively large impact on the development of certain
behavioral characters specific to domestic animals. The nonagouti allele in rats
and mice may be such a major ‘domestication’ gene. It is not surprising, then, that
over 70% of approximately 140 inbred mouse strains and over 80% of approx-
imately 50 inbred rat strains that have been characterized at the agouti locus are
homozygous for the nonagouti allele (Festing, 1979a,b, 1989; Staats, 1981, cited
in Hayssen, 1997).

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18 Chapter 3

Hybridization of Wild and Domestic Stocks

Hybridization of wild and domestic stocks has also been used to provide informa-
tion on behavioral development and the process of domestication (Leopold, 1944;
Boreman and Price, 1972; Rood, 1972; Smith, 1972; Cheng et al., 1979b). Mater-
nal effects can be assessed by comparing reciprocal hybrids with each other and
with the parental strains. Hybridization can also be used to provide information
on the mode of inheritance of the trait or traits in question, namely directional
dominance, over-dominance (heterosis) or intermediate inheritance (Bruell,
1967). Of course, the outcome of hybridization experiments may be affected by
the choice of parent stocks (i.e. representativeness) as in the comparative approach
to domestication research. In addition, hybridization offers no direct information
regarding the rate of phenotypic changes during the domestication process.
When wild and domestic stocks are interbred, the behavior of the hybrids
usually falls intermediate to the two parent populations. Price and Loomis (1973)
examined the behavior of wild and domestic Norway rats (R. norvegicus) and their
reciprocal hybrid crosses in response to being placed in a 122 × 30.5 × 28 cm
novel enclosure. Wild rats initiated activity in the enclosure more quickly, were
more active during the 5-min test and spent more time grooming than domestic
rats. Hybrids were intermediate (Table 3.3). Boreman and Price (1972) observed
the relative social dominance of wild, domestic and hybrid strains of Norway rats
(R. norvegicus) in mixed groups of 12 animals (four animals per strain) housed in
a 7.6 × 3.6 × 2.7 m room for 13 consecutive days. Domestic rats were dominant
to wild rats in both spontaneous and competitive interactions and hybrids were
intermediate (see p. 176 for data and additional explanation). These results are
not surprising, inasmuch as most behaviors are influenced by many genes acting
synergistically or in an additive manner. Intermediate inheritance is characteristic
of traits with an intermediate optimum; selection has removed dominant genes
from the gene pool (Bruell, 1967).
Price and Loomis (1971) found little support for a maternal effect in explain-
ing the differences between wild and domestic rats (R. norvegicus) in response to a

Table 3.3. Mean (± SE) behavioral responses of wild and domestic Norway
rats and their reciprocal hybrids when exposed for 5 min to a novel
122 × 30.5 × 28 cm enclosure. (From Price and Loomis, 1973.)

Straina

Behavior DD DW WD WW

Number of subjects 23 21 22 17
Latency to be active (s) 22.1 ± 3.0 8.7 ± 1.2 6.7 ± 0.9 5.2 ± 1.0
Total activity units 25.1 ± 6.8 32.4 ± 5.5 47.5 ± 6.5 63.6 ± 7.8
Time grooming (s) 25.4 ± 4.4 72.2 ± 10.6 65.1 ± 9.7 119.4 ± 25.5
aD, domestic; W, wild; first letter indicates maternal strain.

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Approaches to the Study of Domestication 19

novel environment. Conversely, Richardson et al. (1994) discovered a maternal

effect in comparing the basal metabolic rate (BMR) of wild and domestic house
mice (M. domesticus) and their reciprocal hybrids. Hybrid mice from wild dams had
significantly lower BMRs than hybrid mice from domestic dams, and both hybrid
groups had lower BMRs than pure laboratory mice (−23.1 and −11.2%, respec-
tively). First-generation laboratory reared wild mice also exhibited lower BMRs
than the domestic stock (−17.2%).
Cases where the hybrids score significantly higher (or lower) on a quantitative
scale than either parent stock (over-dominance) usually indicate that the parent
stocks have experienced a loss in vigor due to inbreeding (Bruell, 1967). Cheng
et al. (1979b) reported that a greater percentage of hybrid mallard ducklings (Anas
platyrhynchos) exhibited the ‘following’ (imprinting) response than did young from
pure wild or game-farm parent stocks. However, the hybrids exhibited an
intermediate level of arousal, which was believed to facilitate the expression of
following behavior. Wild ducklings were over-aroused and game-farm ducklings
were under-aroused for maximum following under the experimental conditions
employed.
Lickliter and Ness (1990) argued that our understanding of the domestication
process has been hampered by the lack of a coherent framework of theories and
concepts that can be empirically tested. Lickliter and Ness are correct in assuming
that a developmental systems approach to domestication research is likely to be
more productive than attempts to separate the relative contributions of genetic
and environmental factors. All behaviors develop through an interaction of genes
and environment, and studies comparing the effects of this interaction in nature
and captivity will contribute the most to our understanding of the domestication
process.

Conclusions
Of the four approaches to domestication research, the longitudinal approach
provides very useful information. By monitoring changes in populations of
animals over generations in captivity, the longitudinal approach can provide
information on the rate and magnitude of phenotypic changes over generations
without concern about stock or sample representativeness. Unfortunately,
longitudinal studies on domestication have been few and far between, and
the long-term nature of such work creates logistical problems that discourage
would-be researchers. The use of invertebrates with relatively short generation
intervals (e.g. Drosophila) would partially alleviate this problem if variables relevant
to the domestication process can be identified and effectively tracked over time.
The search for ‘domestication genes’ is intriguing but success is limited by
the polygenic nature of most behavioral traits. The one exception to date is
the research linking coat-color genes in mammals to brain biochemistry and
behaviors which facilitate domestication and ease of handling. Further work in

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20 Chapter 3

this area could provide a major contribution in explaining differences between

wild and domestic animals in their responses to people.
Of the four approaches, studies comparing wild and domestic populations of
a species are most common, primarily because such studies are relatively easy to
initiate once stocks of animals become available and investigations are typically
short term. The usefulness of comparative studies is limited by the perceived
representativeness of the animal stocks employed. It is difficult, if not impossible,
to find contemporary wild populations that match the wild ancestors of many of
our common domesticated species. Biological differences found between wild and
domestic stocks will to some degree apply only to the specific populations studied.
Hybridization studies can provide useful information on the inheritance of
traits important to domestication, but little more.

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