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Chapter 7

Artificial Selection

Artificial selection is one of the best-understood aspects of the domestication


process (Price and King, 1968) and is the only genetically based mechanism that is
unique to domestication. Artificial selection may be applied either inadvertently
(unconsciously) or intentionally (consciously). This chapter provides examples of
inadvertent and conscious artificial selection and discusses the differences between
artificial and natural selection. It ends by describing how artificial selection
experiments can provide insights regarding mechanisms of gene expression and
the evolution of quantitative traits.

Inadvertent Artificial Selection


Personal biases and preferences often influence the selection of breeding
stock (Muntzing, 1959) and such biases may be very subtle. Inadvertent artificial
selection by animal caretakers is commonplace. Frankham et al. (1986) proposed
that unconscious selection for tameness is inevitable in captive populations of
animals. Marliave et al. (1993) reported that ten generations of laboratory rearing
of the coonstripe shrimp (Pandalus danae) resulted in inadvertent selection for
reduced intensity of escape responses. Regular handling of the shrimp in a
study of protandric hermaphroditism would often injure individuals with
intense tail-flip escape responses. By the tenth generation, the intensity of escape
responses had become greatly reduced and dopamine levels (frequently associated
with emotional reactivity) were reduced to only 5.5% of the level in wild
stock. Hybrids between wild and ‘domestic’ shrimp were intermediate for both
variables.
Waples (1991) claimed that some salmon hatcheries in the Pacific Northwest
(USA) have inadvertently selected for early-season spawning by collecting
eggs only from early-spawning wild fish. (The number of eggs taken per year is
frequently on a quota basis.) In addition, conscious selection for early spawning

©CAB International 2002. Animal Domestication and Behavior


(E.O. Price) 43

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44 Chapter 7

is often applied to hatchery-raised broodstock, since they produce young that are
larger at traditional release times or can be released earlier in the spring.
These early-released fish may have higher survival rates providing unpredictable
(undesirable) springtime water conditions do not occur.
Inadvertent artificial selection may also account for an acceleration in sexual
development and improved sexual vigor in a long-standing laboratory population
of oriental fruit flies (Dacus dorsalis). In a comparison of a domestic stock of
D. dorsalis maintained in the laboratory for about 330 generations with wild
D. dorsalis collected from three islands in Hawaii, Wong et al. (1982) found that
100% of the domestic females had mated by day 12 after eclosion whereas 90% of
the wild females were not mated until day 25. In addition, the mating speed
(proportion of flies mating per hour) of male domestic flies was about four times
that of the wild males and the domestic females mated about twice as fast as the
wild females. The authors concluded that the laboratory rearing system employed
over the 28 years of propagating the laboratory population had selected for early
sexual development and rapid mating behavior (i.e. sexual vigor). It should be
noted that the wild flies used in this study were older than the laboratory flies
(28–30 days vs. 9–10 days), since it took them longer to reach sexual maturity.
Could mating speed have been influenced by the different ages of the two stocks at
testing? To what extent are mating speed and early sexual maturation related in
this species? It is also possible that light intensity could have confounded the
results of the mating speed experiment. Copulations were monitored for 4 h
starting at 10.00 and 11.00. Wild fruit flies mate more frequently under low
light conditions, which may correspond with the cooler and more humid times
of the day. Selection for sensitivity to light intensity may have been relaxed
in long-standing laboratory populations of fruit flies because of the constant
temperature and humidity of the laboratory environment. Hence, domestic stocks
may be more active in the middle of the day. Koyama et al. (1986) reported that
sexual activity in a laboratory strain of melon flies (Dacus cucurbitae) was initiated
earlier in the afternoon (i.e. at higher light intensity) than in a comparable wild
population.

Conscious Artificial Selection


Artificial selection has been demonstrated for a plethora of phenotypic traits. The
average rate of phenotypic change in response to (conscious) artificial selection
stands in sharp contrast to the relatively slow rate of evolutionary change in
free-living populations of wild animals (Lush, 1945; Haldane, 1949). In but a few
generations of intense artificial selection, populations of animals have been altered
with respect to a wide variety of traits (Siegel, 1975; Plomin et al., 1980; Grandin,
1998; Rauw et al., 1998).

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Artificial Selection 45

Artificial selection of dog breeds

The variety of physical and behavioral traits seen in the many breeds of domestic
dogs (C. familiaris; Scott and Fuller, 1965) reflect the genetic changes that can be
realized in a species through conscious artificial selection and hybridization. Dog
breeds are more diverse in shape and conformation than any other domestic
animal species.
It is estimated that selective breeding of dogs for specific functions and
appearance began about 5000 years ago (Case, 1999). Dogs resembling today’s
greyhounds represent one of the oldest breeds and were often shown on paintings
and pottery in Egypt and western Asia as early as 2900 BC. The ancient Romans
were also heavily involved in the systematic breeding of dogs. Written records
from the fifth century BC describe dogs used for herding, sport, war, arena
fighting, scent hunting and sight hunting. The aristocracy also kept smaller ‘house’
dogs. Mastiff breeds were developed primarily in the area of Tibet and were later
used in war by the Babylonians, Assyrians, Persians and Greeks. Wolf-like breeds
similar to today’s spitz were developed early and are the likely ancestors of
modern-day huskies, Keeshond and other arctic breeds. Pointers were developed
early on to hunt small game and most of the sheepdog breeds probably originated
in Europe and were selected to herd livestock.
The majority of exisiting purebred dog breeds have their origins in some type
of working animal (Case, 1999). The greatest era for the proliferation of dog
breeds was in the Middle Ages in western Europe, spanning the 13th to 15th
centuries AD. Notable during this period were the many breeds (e.g. deerhounds,
wolfhounds, otterhounds, bloodhounds, etc.) established to hunt different species
of game (Menache, 1997).

Artificial selection in other species

Artificial selection has not only been used to establish various breeds within
domestic animal species but it has been used to establish populations differing in
very specific characteristics. For example, Bernon and Siegel (1983) demonstrated
the extent to which sexual performance in male chickens (G. domesticus) can be
artificially selected in 20 generations (Table 7.1). Koteja et al. (1999) selected
laboratory mice (M. domesticus) for activity wheel use and, after 13 generations,
reported a 2.2-fold increase in number of revolutions per day. Interestingly, the
increase was in running speed not time spent in the wheels and the selection-line
mice ‘traversed’ 12.1 km per day. Especially noteworthy is the work on selecting
silver foxes (V. vulpes) for nonaggressive behavior towards man (i.e. tameness)
which began in 1959 at the Institute of Cytology and Genetics in Novosibirsk,

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46 Chapter 7

Siberia (Belyaev, 1979). This selection has resulted in a line of foxes that show little
fear of people and resemble domestic dogs in their behavior (Trut, 1999; Fig. 7.1).
The unselected control population still exhibits wild-type behavior, including
strong defensive responses toward humans.
Domestic farm animals artificially selected for production traits have shown
remarkable gains in recent decades (see review by Rauw et al., 1998). Growth
rate of broiler chickens (G. domesticus) has increased from 10 g day−1 in 1960 to
45 g day−1 in 1996. Growth in Norwegian meat-type pigs (S. scrofa) has increased
from 629 g day−1 in 1960 to 962 g day−1 in 1996 due to selection. Milk yield of
dairy cows (Bos taurus) has typically doubled since the early 1950s.

Table 7.1. Mean (± SE) total number of mounts and completed matings
exhibited by male chickens after 20 generations of artificial selection for high
and low levels of sexual performance.a (From Bernon and Siegel, 1983.)

Selection Number of Number of Number of


line subjects mounts completed matings

High 44 31.2 ± 1.9 24.4 ± 1.4


Control 63 7.2 ± 0.8 5.2 ± 0.6
Low 77 0.5 ± 0.1 0.3 ± 0.1
aDuring eight 10-min tests with females.

Fig. 7.1. Silver foxes


selected for nonaggressive
behavior toward humans
show little fear of people and
resemble domestic dogs in
their behavior. (Photo courtesy
of Institute of Cytology and
Genetics, Novosibirsk,
Siberia.)

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Artificial Selection 47

How Artificial and Natural Selection Differ


Certain theoretical differences exist between artificial and natural selection.
Artificial selection is goal-oriented from the standpoint that man selects those
individuals for breeding whom he believes will produce (transmit) a desired
phenotype. Thus, all artificial selection occurs prior to reproduction. In natural
selection, some selection occurs prior to reproduction because some individuals do
not live long enough to breed. Differential reproduction is the essence of the
natural selection process. In the latter, selective advantage can only be measured
‘ex post facto’, after an animal’s contribution to future generations is determined.
Natural selection is goal-oriented only from the standpoint that it is directed
towards maximizing individual fitness (i.e. the number of reproducing offspring
left for future generations). Artificial selection may reduce fitness by providing a
selective advantage for nonadaptive traits. In artificial selection, the breeder not
only decides which animals will serve as breeding stock but also the number of
breeding opportunities for each individual. In both artificial and natural selection,
an animal producing only a few offspring may contribute as many or more repro-
ducing offspring for the next generation than one that produced many young.
However, this is more likely under artificial selection because it is typically a more
intense selection process.
Darwin, in an 1859 letter to Lyell (cited in Richards, 1998), contrasts artificial
and natural selection. First, Darwin noted that artificial selection brings about
changes more rapidly than natural selection. Animal scientists agree that the
intensity of artificial selection is usually much greater than the intensity of
selection occurring in nature (Lush, 1945). Secondly, Darwin maintained that
man can only select for the external and visible phenotypic characteristics of the
organism. While this was true when Darwin was alive, successful selection has
now been demonstrated for a host of physiological traits (e.g. nerve conduction
velocity, Hegmann, 1975; adrenocortical response, Jones et al., 1994) thanks
to modern-day technological advances. Thirdly, Darwin believed that artificial
selection is pursued to meet man’s desires and whims rather than necessarily for
the good of the individuals comprising the population. It is difficult to argue this
point when so much of artificial selection is directed at very specific phenotypic
traits with little impact on general fitness. Coppinger and Coppinger (2001) have
noted that in domestic dogs, hair color strongly influences who gets mated
to whom. Current interest in longevity and lifetime reproductive success in
economically important species (i.e. animals reared for food and fiber) constitutes
a rare exception to Darwin’s observation. Reed and Bryant (2000) and others
have demonstrated that experimental populations of insects maintained in
the laboratory under a shortened generation-interval breeding program exhibit
reduced longevity, presumably because of the random accumulation of deleteri-
ous alleles negatively affecting this trait. There is an apparent trade-off between
longevity and early progeny production. This result is interesting, considering
that shortened generation intervals are recommended to attain the most rapid
response to artificial selection. Youngson and Verspoor (1998) cite several reports

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48 Chapter 7

supporting the hypothesis that the lifetime reproductive success of hatchery-


reared Atlantic salmon (S. salar) is reduced relative to their wild counterparts
because of selection for production traits and the effects of domestication.

Lessons Learned from Studying Artificial Selection


Darwin proposed that the breeding of domestic animals constituted a ‘grand
experiment’ from which the laws of organic nature and the existence of natural
selection could be established (Richards, 1998) and one could gain a better
understanding of individual inheritance (Bartley, 1992). He argued that since
artificial selection could produce relatively large changes in organisms, natural
selection could also. Darwin believed that artificial selection could be used to
test the importance of specific characters on survival and reproduction (i.e.
how natural selection works). This hypothesis has been supported in several ways.
Artificial selection should proceed more rapidly in the direction of more favorable
genetically homeostatic conditions (Lerner, 1954). Hetzer and Miller (1972) artifi-
cially selected for backfat thickness in Duroc pigs over 16 generations. Selection in
both directions was successful but the rate of genetic change was 1.8 times greater
for the high backfat line (Fig. 7.2). Increased fat deposition is considered beneficial
for many traits associated with fitness. Ricker and Hirsch (1985) provided
evidence for the existence of favorable, co-adapted gene complexes (genes that
work together well) in their study selecting for geotaxis (gravity-oriented behavior)
in D. melanogaster. Their work represents one of the longest selection experiments
ever conducted, with more than 600 generations of intermittent artificial selection
recorded over a 26-year period. A case was made for the possible loss of previously
established co-adapted gene complexes and the establishment of new co-adapted
gene complexes (utilizing genes associated with extreme geotaxis expression) in
the later generations of the geotaxis lines, particularly the low (negative response)
line. In the earlier generations of selection (up to generation 450), the geotaxis
scores of the flies in each line would regress (reverse) if selection was relaxed, as if
some previously optimal genetic state was being sought. Relaxed selection in the
later generations did not have this effect, even though genetic variability still
existed at the loci affecting geotaxis as shown by both lines responding to reverse
selection. Belyaev (1979) strongly believed that during domestication, previously
existing co-adapted gene complexes are lost and new co-adapted gene complexes
become established after many generations of artificial selection for specific traits.
Differences in response to relaxed and reversed selection in artificially selected
lines can prove useful in identifying the existence of such favorable combinations
of heterozygous gene complexes at loci affecting the selected traits.
Daniels and Bekoff (1990) have proposed that unconscious passive artificial
selection is occurring on a grand scale in nature as people alter the environment
through such practices as pesticide use, construction of dams on waterways
and industrial emissions. While such environmental perturbations are, in fact,
unnatural (i.e. artificial), the mechanism of action is still natural selection. Humans

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Artificial Selection 49

Fig. 7.2. Selection for high and low levels of backfat thickness in Duroc pigs
over 16 generations (Hetzer and Miller, 1972).

are not selecting breeding stock prior to reproduction. Similarly, the environment
of animals is also artificially altered when translocating them from nature to
captivity. Except when man chooses potential breeding partners, differential
reproduction in captivity is the hallmark of a natural selection process.

Conclusions
Artificial selection is the only genetic mechanism unique to the domestication
process. It is almost always effective in producing phenotypic change when
consciously applied. In some respects, artificial selection serves as a showcase for
how natural selection works. It has provided insights on how evolution proceeds
and how genes are expressed. Phenotypic changes can be rapid when artificial
selection is intensely applied. Artificial selection differs from natural selection
by the fact that it is applied prior to reproduction whereas natural selection
is measured after reproduction, by an individual’s contributions to the next
generation. Artificial selection can be a double-edged sword, since it is typically

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50 Chapter 7

applied to one or a few specific traits rather than the entire phenotype. Selection
for specific traits may result in unexpected effects on correlated characters, some
of which may counter breeding objectives or jeopardize animal welfare. It has also
been hypothesized that artificial selection for specific characters may sometimes
break up co-adapted gene complexes (i.e. groups of genes that work well together).
No matter what the outcome, artificial selection studies on captive wild and
domestic animals have proved to be the ‘grand experiment’ that has greatly
enhanced our understanding of individual inheritance.

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