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Chapter 8
In the absence of artificial selection, natural selection provides the basic selective
mechanism for genetic change in captive populations. When artificial selection is
administered, man does not necessarily select those individuals with the greatest
fitness (for captivity) as breeding stock for his selection programs. That is the
role of natural selection. Differential mortality and reproduction, including repro-
ductive failure, among artificially selected populations is one way that natural
selection in captivity is manifested. This chapter focuses on the various ways that
natural selection in captivity is expressed, namely mortality and reproductive
failure, and changes in these parameters over generations in captivity. The
underlying objective is to demonstrate that natural selection does not cease once
a population of animals is brought into captivity, but rather continues to operate
regardless of whether or not artificial selection is applied.
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52 Chapter 8
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reproductive failure are listed in Fig. 8.1. Improper breeding posture was the
major cause of reproductive failure. Some male ferrets were unable to successfully
restrain the female in a correct breeding position to allow copulation (Williams
et al., 1991). Semen characteristics were similar in the successful and unsuccessful
ferrets. Sharpe et al. (1998), working with ruffed grouse (Bonasa umbellus), found that
of 63 eggs collected from wild nests, 59 (94%) were fertile compared to only 29
of 157 eggs (18%) collected from 11 captive-reared birds. Only three of the 11
captive-reared birds produced fertile eggs. In addition, of the 59 fertile eggs
collected in the field, 36 (61%) hatched whereas only 11 of the 29 (38%) fertile
eggs from captive birds hatched.
Clark and Price (1981) found that of 21 first-generation captive-reared female
wild Norway rats (R. norvegicus) that gave birth for the first time, only nine (43%)
reared at least some of their offspring to weaning age. One litter was cannibalized
at birth and 11 litters were abandoned at various stages before weaning. In con-
trast, 100% of 49 domestic first-time mothers (Long–Evans and Sprague–Dawley
strains) reared all or part of their litters to weaning age under the same laboratory
conditions. Litter sizes at parturition for these captive-reared wild females
averaged about two-thirds the number of pups as for the domestic females
(6.4 ± 1.0, 9.7 ± 1.8 and 10.4 ± 2.8 for the wild, Long–Evans and Sprague–
Dawley domestic females, respectively). Interestingly, litter sizes of wild-caught
female Norway rats are comparable to those of domestic females whether they are
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54 Chapter 8
living in nature or housed in the laboratory (Miller, 1911; Davis, 1951; Boice,
1972). This observation suggests that captive rearing reduces the litter sizes of wild
female rats and that the constraints on litter size gradually disappear through
the process of domestication (i.e. natural selection in the laboratory). Wyban
and Sweeney (1991) reported that seven of 74 (9.5%) captive female shrimp
broodstock (Penaeus vannamei) were responsible for more than 50% of the total
nauplii production in a lifetime reproduction trial. Nineteen females (26%) pro-
duced approximately 75% of the nauplii. The offspring of the highest-producing
female were reared to adult size and the reproductive success of 18 of her
daughters was compared to the reproductive success of 18 female control shrimp.
After 85 days, the high-producing female’s daughters had produced 4.5 million
nauplii from 81 spawns, with an average hatch rate of 47% while the control
females produced only 1.2 million nauplii from 46 mates with an average hatch
rate of 30%. Similarly, Bray et al. (1990) demonstrated that less than 25% of
first-generation captive-reared female Penaeus stylirostris shrimp produced nearly
70% of the larvae.
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mothers and in family groups without siblings. Abuse rates were higher with
experienced mothers and when mothers were sick.
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56 Chapter 8
In general, natural selection in captivity is most intense during the first few
generations following the transition from field to captive environments. Evolution
and adaptation to the captive environment occur rapidly during this time because
of the change in direction and intensity of natural selection on so many different
traits and the relatively large number of correlated characteristics affected
(Price et al., 1993). The degree of adaptation to the captive environment will
increase as the frequencies of ‘favorable’ genes increase in response to selective
pressure.
An improvement in reproduction (i.e. fitness) over the initial generations in
captivity can reflect the climb to a new adaptive peak as individuals become
increasing well-adapted to the captive environment over successive generations
(Fig. 8.2). King and Donaldson (1929) reported a marked increase in the
reproductive success of wild genotype female Norway rats (R. norvegicus) during
the first nine generations in captivity (Table 8.1). During this period the animals
were maintained under the same conditions and were fed the same diet. Breeding
stock for each generation was selected only from litters in which all animals
survived to 60 days of age. Unfortunately, the investigators failed to maintain
an unselected control population. Consequently, it was not possible to determine
the effect of this selection on the traits observed. Although conscious (and,
perhaps, unconscious) selection for ‘vigor’ was practiced, it seems plausible
that much of the marked improvement in reproductive success seen during
the first few generations of breeding in captivity was due to natural rather than
Fig. 8.2. Relative adaptation (i.e. fitness) is reversed for wild and domestic
stocks in natural and captive environments represented by separate adaptive
peaks. Adaptation is typically intermediate for wild × domestic hybrids in both
environments.
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artificial selection. Litter sizes of the captive wild rats reached levels comparable to
domestic and free-living wild rats after about 20 generations of breeding in captiv-
ity and the length of the reproductive period (between first and last litters) eventu-
ally doubled from 204 to 440 days (King, 1929, 1939). Wallace (1981) reported an
increase in the percentage of female wild house mice (M. musculus) that successfully
bred in her laboratory between the wild-caught and first-generation labora-
tory-reared generations (88.2% of 120 females and 97% of 98 females, respec-
tively). Fertility in subsequent generations was confounded by inbreeding.
Blottner et al. (2000), in a study measuring changes in testicular activity of gerbils
(M. unguiculatus) over generations of laboratory rearing, reported that the F2
generation of gerbils exhibited significantly greater testis weights, testis/body
weight ratios and testicular testosterone concentrations than the F1 generation
offspring of gerbils trapped in their native Mongolia. They postulated that the
intensified spermatogenesis and hormone production seen in the F2 generation
reflects the relatively rapid changes in reproductive parameters that frequently
occur under relatively constant laboratory conditions. Kawahara (1972) reported
on the breeding success of an unselected population of Japanese quail (Coturnix
japonica) following the transition from nature to captivity (cages). Starting with 268
wild-caught individuals, the percentage of birds that had layed eggs by 20 weeks
of age was 50, 61 and 67% in the first three generations, respectively. In a
domestic control strain, all females were in lay by 20 weeks of age. Searle (1984)
noted that wild-caught common shrews (Sorex araneus) successfully weaned only
eight of 15 litters (53%) conceived in nature but born in the laboratory. In con-
trast, 12 of 14 litters (86%) conceived and born in captivity to wild-caught females
were successfully reared to weaning age. Females pregnant at the time of capture
not only did not have as long to adapt to their new environment prior to giving
birth but some of them might not have been otherwise predisposed to reproduce
in captivity.
Table 8.1. Percentage of female wild-genotype Norway rats that gave birth to
offspring during the first nine generations in captivity. (From King and Donaldson,
1929.)
Wild-caught 20 30
2 59 63
3 60 70
4 54 81
5 56 89
6 52 88
7 54 89
8 53 91
9 51 94
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58 Chapter 8
Fig. 8.3. Linear regression of pupal yields (viable pupae per live female) for
colonies of Mediterranean fruit flies reared in the laboratory for 12 generations
using three different husbandry techniques. The C flies were given fruitless
guava branches and papaya fruit (for oviposition and larval development), the E
strain was reared on papaya fruit but without guava branches for five generations
and then switched to an artificial diet and oviposition substrate. The F flies were
reared on the artificial diet and oviposition substrate starting with generation 1
(Leppla et al., 1983).
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the domestic stock in the fifth generation (138 vs. 320 eggs per mated female,
respectively). In addition, the wild stock required 42–45 days to complete each
generation while the domestic stock cycled every 35–38 days. Egg development
in the two stocks did not differ but larval development was about 2 days longer
and the pre-oviposition period was about 4–5 days longer in the wild flies. Leppla
et al. (1980) compared the development, survival and reproduction of wild and
laboratory strains of the cabbage looper (Trichoplusia ni) when exposed to a new
rearing regimen. The wild stock was derived from field-trapped animals and the
laboratory stock had been maintained in captivity for about 75 generations
(6 years). The two stocks had similar development and survival rates during
the first ten generations but differed in reproduction. A higher proportion of
laboratory females mated, mated more frequently and produced a greater average
number of viable eggs. Successive generations of both strains showed an initial
decline in fecundity, with population recovery by the fifth generation for the
laboratory stock and the eighth generation for the wild strain. Proshold and
Bartell (1972) reported that it took nearly nine generations of laboratory rearing
for a wild-type population of tobacco budworms (Heliothis virescens) to mate as
frequently as a comparative laboratory population.
Frankham and Loebel (1992) compared the reproductive fitness of a wild-
caught population of D. melanogaster with a population obtained from the same site
in nature and bred in captivity for eight generations. Both populations were tested
at the same time under the same conditions. The reproductive fitness index of the
captive population was twice that of the wild population (60.0 vs. 30.7, respec-
tively). Increased insect density and a dietary change were cited as the two most
important factors responsible for the changes in fitness observed. Sgrò and Par-
tridge (2000) investigated changes in life-history traits of D. melanogaster associated
with using two relatively common laboratory rearing techniques. Populations of
fruit flies were maintained in the laboratory for 2 years either in bottles, where
adults could produce offspring only until day 14 (discrete, short generations), or in
population cages, where there was no restriction on offspring production (over-
lapping, unconstrained generations). After 2 years, bottle-reared flies showed a
marked increase in early adult fecundity (eggs laid) and remating, and a decrease
in late adult fecundity compared to cage populations and wild flies freshly caught
in the field from the origin site of the laboratory populations. This result was not
unexpected considering the intensity of natural selection for reproduction in the
early-adult stage of the bottle-reared flies. Observations such as these highlight
the need to account for the genetic adaptation of wild populations to captivity
(i.e. natural selection in captivity) when studying evolutionary theory with captive
animals and in programs dealing with conservation and biological control.
Economopoulos and Loukas (1986) demonstrated a link between the food avail-
able to captive olive fruit flies (Dacus oleae) and genetic changes over generations in
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60 Chapter 8
the laboratory. The study focused on changes in allele frequencies at the alcohol
dehydrogenase (ADH) locus when field-collected olive fruit flies were brought
into the laboratory and fed an artificial larval medium. After four generations in
captivity, the experimental populations showed a marked increase in the I allele
and a decrease in the frequency of allele S. Control flies kept on olives in captivity
showed no allele frequency changes at the ADH locus, suggesting that the larval
medium may have been directly linked to the genetic changes observed. This was
confirmed by providing olives rather than the artificial medium to the experimen-
tal population after 24 generations of captive breeding. In only one generation,
the I allele decreased from 28.3% to 8.1% and the S allele increased from 21.7%
to 48.2%. Alcohol dehydrogenase is involved in the metabolism of a variety of
alcohols and serves as a detoxifying agent. Thus, it is important during larval
growth and development in different types of fruits. It was apparent that the I and
S alleles have somewhat different functions in the metabolism of alcohols found in
ripe olives and that the frequencies of I and S alleles in the population reflect the
nature of alcohols found in the larval medium.
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Conclusions
Natural selection in captivity is ultimately manifested in differential mortality and
reproductive success. Those animals that come into captivity with the fewest
pre-adaptations for their new environment should theoretically experience the
most intense natural selection. A number of studies were cited in this chapter
that showed enhanced reproductive success of long-standing captive populations
of animals relative to stocks of wild counterparts recently introduced into
captivity. These comparative studies supported the concept of natural selection in
captivity presented here but did not account for possible sampling error (see
Chapter 3) and the potential confounding influence of other genetic mechanisms
such as artificial selection, inbreeding and genetic drift. An ideal experiment to
demonstrate natural selection in captivity is to show an improvement in reproduc-
tive success over the first few generations in captivity in the absence of artificial
selection and any changes in housing and management systems. Although there is
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62 Chapter 8
some evidence in the literature that appears to meet these criteria, several care-
fully controlled studies with different taxa are needed to positively confirm the
merit of this hypothesis.
The nature, timing and intensity of natural selection in captivity may be
dependent on housing and management conditions employed and the trait in
question. For example, the study by Economopoulos and Loukas (1986) demon-
strated how a change in diet can have a relatively rapid effect on gene frequencies
in captive olive fruit flies (D. oleae). Other traits (e.g. maternal and predatory
behaviors, etc.) may be more conservative and resistant to the effects of natural
selection in the captive state.
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