ZOO 526

Zoo Biology 16:377389 (1997)

RESEARCH ARTICLES

Minimizing Kinship in Captive Breeding

Programs
Margaret E. Montgomery,1* Jonathan D. Ballou,2 Roderick K. Nurthen,1
Phillip R. England,1 David A. Briscoe,1 and Richard Frankham1
1

Key Centre for Biodiversity and Bioresources, School of Biological Sciences, Macquarie
University, Sydney, Australia
2
Department of Zoological Research, National Zoological Park, Smithsonian Institution,
Washington, DC

Captive populations of endangered species are managed to preserve genetic diversity and retain reproductive fitness. Minimizing kinship (MK) has been predicted to maximize the retention of gene diversity in pedigreed populations with
unequal founder representation. MK was compared with maximum avoidance of
inbreeding (MAI) and random choice of parents (RAND) using Drosophila melanogaster. Forty replicate populations of each treatment were initiated with unequal founder representation and managed for four generations. MK retained
significantly more gene diversity and allelic diversity based on six microsatellite loci and seven allozyme loci than MAI or RAND. Reproductive fitness
under both benign and competitive conditions did not differ significantly
among treatments. Of the methods considered, MK is currently the best available for the genetic management of captive populations. Zoo Biol 16:377389,
1997. 1997 Wiley-Liss, Inc.
Key words: inbreeding; genetic diversity; heterozygosity; reproductive fitness; mean
kinship

INTRODUCTION

Many threatened and endangered species have become so reduced in population size that they require captive breeding to ensure long-term survival. It has been
estimated that approximately 2,000 vertebrate species may have to be captive bred to

Received for publication 12 September 1996; revision accepted 2 June 1997.

*Correspondence to Richard Frankham, Key Centre for Biodiversity and Bioresources, School of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia.
Email: rfrankha@rna.bio.mq.edu.au

1997 Wiley-Liss, Inc.

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avoid extinction [Soul et al., 1986; Tudge, 1995]. Captive populations are often
characterized by few founders and relatively small population sizes [Hedrick, 1992]
and suffer both inbreeding depression and a loss of genetic variation [see Soul and
Wilcox, 1980; Frankel and Soul, 1981; Soul, 1986, 1987; Wilson and Peters, 1988;
Ballou et al., 1995].
For a captive population to survive it must (a) remain large enough or be managed in such a way that erosion of genetic variability by random genetic drift is
minimized and (b) avoid inbreeding depression. Inbreeding and loss of genetic variability increase the risk of extinction [Frankham, 1995a,b].
The importance of genetic considerations in captive breeding management is well
recognized [Ellis and Seal, 1995; Mallinson, 1995] although, previously, many captive
populations were allowed to reproduce unmanaged. As a consequence, the founder representation within the population may be skewed by large contributions from only a few
founders, resulting in a loss of alleles due to drift, an increase in the inbreeding level and
strong selection for the captive environment [Ralls and Ballou, 1986a,b].
Several alternative genetic management strategies have been proposed. The minimizing kinship (MK) procedure acts to maximize the retention of gene diversity by
minimizing the overall level of relationship in the population [Falconer and Mackay,
1996]. MK was consistently the best strategy for maintaining gene diversity when
compared with alternatives using computer simulations [Ballou and Lacy, 1995]. The
maximum avoidance of inbreeding (MAI) procedure [Kimura and Crow, 1963] does
not take founder representation into account but acts to minimize any further inbreeding. MAI is the simplest procedure, and knowledge of pedigrees prior to management is not necessary for its application. The advantage of MK over MAI is only
expected to occur when the starting population has unequal founder contributions.
MK is currently recommended and widely used in the genetic management of captive populations worldwide [Ballou and Lacy, 1995].
The Ballou-Lacy conclusions were based on a single locus, neutral model that
ignored linkage, recombination, and mutation. These conclusions have not been validated in living organisms. Endangered species themselves are unsuitable for such
validation as they are typically slow breeders, expensive to maintain, and exist in
low numbers. Indeed, their very status as endangered precludes their use in experimental evaluation of alternative management strategies.
Drosophila melanogaster is a widely used and convenient model for evaluating theory in population and quantitative genetics and animal breeding [Frankham,
1982]. It has also proved to be a useful model for evaluating conservation genetics
theory [Ralls and Meadows, 1993; Frankham, 1995a; Frankham, 1997].
The objective of this study was to compared MK, MAI, and random choice of
parents (RAND) for their ability to maintain genetic variation and reproductive fitness in model experiments using Drosophila.
METHODS

The outbred base population (T94) was established from 79 wild-inseminated Drosophila melanogaster females captured at Tyrrells Winery, Polkobin
in eastern New South Wales, Australia, in February 1994. The T94 population
was maintained for one generation in captivity prior to founding the lines for the
MK, MAI and RAND populations and subsequently as a randomly mating population of size 1,000.

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379

TREATMENTS
Foundation of Lines

Forty lines were each initiated with 10 T94 founders and maintained for
three generations using pedigrees that maximized the distortion of founder representation (Fig. 1a). At generation three (the split point), seven inbred individuals were derived from only two founders, whereas the other eight founders
were represented by only a single outbred male (Fig. 1a). The seven inbred individuals were the result of two generations of fill-sib mating and had inbreeding
coefficients of 0.375. At the split point, each line was separated into MK and
MAI/RAND (management detailed below). MAI and RAND did not separate until generation four, as all eight available individuals were mated at random at the
split point for both these treatments.
For all three treatments, there were a further four generations of management
after the split point, each with four females and four males. If a line contained a
mating that failed to produce offspring prior to the split point, it was removed from
the experiment. Lines that had failed matings following the split point continued
with replacement flies taken from the productive vials in such a way as to minimize
any further inbreeding. Thirty-one replicates of each treatment type (MK, MAI, and
RAND) proceeded into the final generations of management. There were 26 complete sets of MK, MAI, and RAND, 10 incomplete sets and 4 lines that failed in all
treatment types. All lines were maintained as pedigreed single pair matings on PS
medium [Frankham et al., 1988] in vials at 25C.
Minimizing Kinship

All four inbred females were mated with the outbred male at the split point
(Fig. 1b). This equalized the founder representation in the population to the extent possible. In following generations (G4 - G7) family sizes were equalized
and any further inbreeding minimized using the method described by Kimura
and Crow [1963]. The difference between MK and MAI occurred at the splitpoint generation. Following this, they were maintained in the same way. Although
there was only one generation of different management between MK and MAI,
this represented full implementation of the MK regime under discrete generation
conditions.
Maximum Avoidance of Inbreeding

All eight individuals were randomly mated at the split point (Fig. 1c), resulting
in a single outbred mating and three full-sib matings. In following generations (G4G7), family sizes were equalized and any further inbreeding minimized [Kimura and
Crow, 1963].
Random Mating

This represented a non-management control regime. At the split point, all

eight individuals were randomly mated as for MAI (Fig. 1d). In following generations (G4-G7), four females and four males were taken at random from all the
available progeny. Relative family sizes were estimated from pupal numbers and
random numbers used to choose parents from the four families [Woodworth et
al., 1994]. Parents were mated at random, with no restriction on sib-mating.

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Fig. 1. a: Pedigree used to generate unequal founder representation at the split point. The outbred
male is represented by a filled-in symbol. b: Management scheme used for the MK treatment subsequent to the split point. c: Management scheme used for the MAI treatment subsequent to the split
point. d: An example of the RAND treatment subsequent to the split point.

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381

REPRODUCTIVE FITNESS
Captive Fitness

The productivity of single-pair matings of the MK, MAI, RAND, and base
population flies was measured at the conclusion of the experiment (generation seven).
A single pair of virgin flies was placed in a vial, allowed to mate and oviposit for 3
days, and then removed. The number of emergent offspring from each vial were
counted from day 9 to day 16 (essentially all emergences). Ten replicate vials were
set up for each population of each treatment. The parents were raised in a single-pair
vials to avoid maternal environmental effects. The proportions of matings that failed
to produce offspring were also recorded.
Competitive Fitness

The reproductive fitness of the three treatments and base population was
determined at the conclusion of the experiment, using the competitive index [Jungen and Hartl, 1979]. This involved testing each line for overall fitness in competition with the same marked compound autosome strain (C(2L) b; C (2R) cn
bw) as detailed by Frankham et al. [1988]. Ten pairs of virgin line flies and 30
pairs of virgin compound flies were placed in a bottle and allowed to compete
during mating, egg laying, and egg-adult development. Although compound and
test flies can mate, no offspring result as all progeny are aneuploid. One bottle
was set up for each line of each treatment, plus 12 bottles of the T94 base population. Parent flies were allowed to mate and oviposit for 3 days and then removed. All parents were raised in single-pair vials to avoid maternal environmental
effects. As a ratio of one line fly to three compound parent flies was used, the
competitive index for each treatment is nine times the ratio of wild type to compound flies [Jungen and Hartl, 1979]. As ratios are not normally distributed, statistical analyses of competitive fitness were done on the proportion of line flies
to total number of emergences (arcsine square-root transformed), as recommended
by Jungen and Hartl [1979].
GENETIC VARIATION
Protein Electrophoresis

Changes in genetic variation were monitored in the base population (sample

size = 130 individuals), and in the treatment lines at the split point (all available
parents) and after the final generation of management (all available parents). Seven
polymorphic gene-enzyme systems were assayed: acid phosphatase, -glycerophosphate
dehydrogenase, alcohol dehydrogenase, malate dehydrogenase, 6-phosphogluconate dehydrogenase, and phosphoglucomutase, as described by Borlase et al. [1992], plus
esterase, as described by Richardson et al. [1986].
Microsatellite Variation

The base population (sample size = 72 individuals) and the treatment populations after six generations of management (all available parents) were assayed for
microsatellite variability using the methods of England et al. [1996]. Six polymorphic loci were used: DmAC1 and DmAC9 both located on chromosome 2, DmAC2
and DmAC4 located on the X chromosome, DmAC3 located on chromosome 3, and

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Montgomery et al.

DmAC7 whose location is autosomal but unknown. DNA was extracted from each fly
and two multiplexed polymerase chain reactions (PCR) containing 1 Ci[32P]dATP
performed. The PCR products were then electrophoresed on a 6% denaturing polyacrylamide gel and visualized by autoradiography.
EXPECTED INBREEDING COEFFICIENTS

Expected inbreeding coefficients for the MK and MAI treatments were calculated using the coancestry matrix method of Cruden [1949]. The pedigrees were
entered into the CRUDEN computer program [Yoo, 1990], assuming that there
were no failed matings before or after the split point. The expected inbreeding
coefficient for the RAND treatment was generated using PEDGEN [Ballou, 1995]
based on the average of 10,000 simulations. Expected and actual inbreeding values will diverge when matings fail.
DATA ANALYSES

The inbreeding coefficients were computed from the pedigrees using the
coancestry matrix method of Cruden [1949]. The inbreeding coefficients, competitive fitness, captive fitness, allozyme, and microsatellite results were compared using general linear model (GLM) analyses of variance with treatments (MK vs. MAI
vs. RAND) and founder groups as the two factors. GLM analyses were also performed on MK vs. MAI and RAND (MAI/RAND) as MAI and RAND were very
similar in all characteristics. One-tailed tests of MK vs. MAI/RAND were used, as
the prediction is directional. It should be noted that tests of significance were not
based on the standard error given in Table 1, but were based on GLM analysis of
variance where founder group effects had been removed.
Microsatellite and allozyme data were pooled and averaged for each line, for
each measure of genetic variation (gene diversity, proportion of loci polymorphic,
and allelic diversity). These data were then analyzed in a similar manner to that used
for the unpooled microsatellite data.
Statistical tests on proportions (all data except captive fitness, allozyme,
and microsatellite allelic diversity) were performed on arcsine square-root transformed data to normalize values. Two outliers from the MAI treatment were removed from the competitive index data. The exclusion or inclusion of these values
did not affect the conclusions from the experiment. All statistical tests were computed using the MINITAB statistical package version 8 [Ryan et al., 1994] with
a significant level of 0.05.
TABLE 1. GLM analysis of variance of inbreeding coefficient (F) in the MK, MAI, and RAND
managment treatments
Source

df

adj MS

MK vs. MAI vs. RAND

Founder groups
Error

2
35
55

0.3972**
0.0066**
0.0033

**P < 0.01

df, degrees of freedom; adj ms, adjusted mean square.

Minimizing Kinship in Captive Breeding

383

RESULTS

The MK management method reduced the inbreeding coefficient (F) to zero at

generation four (Fig. 2). The average F for both the MAI and RAND treatments
continued to rise. At the conclusion of the experiment, the inbreeding coefficient
derived from the pedigrees was significantly lower in MK than in MAI or RAND
(0.280 0.007, 0.441 0.012, and 0.498 0.015, respectively) (Table 1).
Allozyme gene diversities were not significantly different among the three treatments (Tables 2 and 3) (F2,54 = 0.39, P = 0.68), although MK was the highest. When
MK was tested against MAI/RAND, the P-value was still non-significant (F1,55 =
0.78, P = 0.19). There was no significant difference among treatments (MK vs. MAI
vs. RAND) or between MK and MAI/RAND for percentage of loci polymorphic or
allelic diversity. The allozyme data at the split point confirmed that the experiment
was progressing as designed because the outbred male flies (average heterozygosity
= 0.287) were different from the inbred female flies (average heterozygosity = 0.130)
prior to management.
Microsatellite gene diversities were significantly different among MK, MAI,
and RAND following management (Tables 2 and 3) (F2,55 = 4.99, P = 0.010). MK
was significantly higher than MAI/RAND (F1,56 = 9.29, P = 0.002). Allelic diversity
for microsatellites was significantly different among MK, MAI, and RAND (F2,54 =
4.82, P = 0.012) and between MK and MAI/RAND (F1,55 = 8.96, P = 0.002). There
was no significant difference among treatments or between MK and MAI/RAND for
percentage of loci polymorphic (F2,55 = 1.64, P = 0.20 and F1,56 = 2.30, P = 0.07,
respectively). There was no significant difference between MAI and RAND for any
measure of genetic variation when measured with either microsatellites or allozymes.

Fig. 2. The expected inbreeding coefficient (F) based on simulation (Pred) compared with the observed F (Obs) based on pedigrees in the MK, MAI, and RAND management treatments.

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Montgomery et al.

TABLE 2. Mean heterozygosity (H), percentage of loci polymorphic (P), and allelic diversity (A)
in the outbred base population (T94), and the levels remaining in the MK, MAI, and RAND
management treatments measured using allozymes, microsatellites, and combined allozyme and
microsatellite data
T94
Allozymes

Microsatellites

Allozyme/microsatellites

H
P
A
H
P
A
H
P
A

0.28
100
2.71
0.51
100
4.50
0.38
100
3.54

MK
0.19
44.7
1.48
0.30
67.2
1.95
0.24
55.1
1.70

0.01
3.1
0.03
0.02
3.5
0.07
0.01
2.3
0.04

MAI
0.17
42.9
1.47
0.25
60.8
1.77
0.21
51.8
1.62

RAND

0.01
2.7
0.03
0.02
3.8
0.05
0.01
2.4
0.03

0.17
41.5
1.44
0.27
63.9
1.82
0.21
51.8
1.61

0.01
2.5
0.03
0.02
3.9
0.06
0.01
2.5
0.03

Gene diversities for the combined allozyme and microsatellite data were significantly different among MK, MAI, and RAND following management (F2,54 =
3.92, P = 0.03; Table 2) and MK was significantly higher than MAI/RAND (F1,55 =
7.60, P = 0.004). Percentage of loci polymorphic did not show a significant difference among the three treatments (F2,54 = 1.44, P = 0.25) or between MK and MAI/
RAND (F1,55 = 2.78, P = 0.051). Allelic diversity for the combined allozyme and
microsatellite data was significantly higher in MK than in MAI or RAND (F2,54 =
4.53, P = 0.015) and there was a highly significant difference between MK and MAI/
RAND (F1,55 = 9.20, P = 0.002).
There was no significant difference in reproductive fitnesses (F2,51 = 0.04, P =
0.96; Table 3) among the three treatments when measured under captive conditions,
though MK was the highest (Fig. 3a). When compared with MAI/RAND, MK was
not significantly better (F1,52 = 0.08, P= 0.39). The number of failed matings per line
showed a non-significant difference among treatments and between MK and MAI/
RAND (F2,51 = 0.24, P = 0.79 and F1,52 = 0.35, P = 0.28) (Fig. 3b).
Under crowded, competitive conditions there was also no significant difference in reproductive fitness among the three treatments (F2,50 = 0.16, P = 0.86; Table
3) or between MK and MAI/RAND (F1,51 = 0.07, P= 0.40). All three treatments were
significantly reduced when compared to the base population (Fig. 3c).
There was a highly significant founder group effect on pedigree inbreeding
coefficient (Table 1), all measures of allozyme genetic variation (Table 3), all measures of microsatellite variation (Table 3) and both benign and competitive reproducTABLE 3. GLM analyses of variance of the allozyme, microsatellite, and combined allozyme/
microsatellite heterozygosities in the MK, MAI, and RAND management treatments
Allozymes

Allozyme/
microsatellite

Microsatellites

Source

df

adj MS

df

adj MS

df

adj MS

MK vs. MAI vs. RAND

Founder groups
Error

2
35
54

0.001
0.017**
0.003

2
35
55

0.022*
0.027**
0.004

2
35
54

0.008*
0.011**
0.002

*P < 0.05.
**P < 0.01.

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385

Fig. 3. Reproductive fitness in the MK, MAI, and RAND management treatments for captive fitness
(a); percentage of failed mating in the productivity (b); competitive fitness (c). The error bars are
twice the standard error of the mean.

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Montgomery et al.

TABLE 4. GLM analyses of variance of the benign and competitive fitnesses in the MK, MAI,
and RAND management treatments
Benign fitness

Competitive fitness

Source

df

adj MS

df

adj MS

MK vs. MAI vs. RAND

Founder groups
Error

2
34
51

26.2
1,708.9**
621.1

2
34
51

0.0040
0.0615**
0.0256

**P < 0.01.

tive fitness measures (Table 4). The difference among founder groups in pedigree
inbreeding coefficient means that founder groups differed in the number of matings
that failed to produce offspring.
DISCUSSION

There are two important findings from this study. First, MK retained more genetic variation than either MAI or RAND. This validates the prediction of Ballou
and Lacy [1995]. The difference between the significance of allozyme results and
microsatellite data can be attributed to statistical power. Microsatellite analysis surveyed a total of 31 alleles, but allozymes only 20 alleles. The pooled allozyme and
microsatellite data showed significantly higher gene diversity and allelic diversity in
MK and there was a non-significant trend for percentage of loci polymorphic.
Second, there were no significant differences among the three treatments in
reproductive fitness, although MK was the best or equal best in all cases. The lack of
difference among treatments in reproductive fitness is surprising, given that there
was a substantial difference in inbreeding coefficients between MK, MAI and RAND
(0.28 vs. 0.44 vs. 0.50, respectively). We have previously detected fitness differences associated with smaller differences in inbreeding and fewer replicates [Borlase
et al., 1993; Woodworth et al., 1994]. However, in a related experiment on equalization of founder representation, we also found no difference in fitness [Loebel et al.,
1992]. All three treatments showed evidence of inbreeding depression in that all had
lower fitnesses than the base population for all measures of fitness.
The lack of difference between MAI and RAND in genetic variation and reproductive fitness was not surprising, as they were separated for only three generations
and differed only slightly in their level of inbreeding. The difference between MAI
and RAND is generated by the variance in family size of the RAND treatments and
is expected to accumulate over time. Borlase et al. [1993] found that populations
maintained with equal family sizes had significantly greater genetic variability and
reproductive fitness after 10 generations than those maintained with variable family
sizes in populations of the same census size.
This study examined only one pedigree chosen to give maximum distortion in
founder representation and so provided the maximum expected difference between
MK and MAI. However, there is no reason to believe that MK would not be the best
strategy for retaining gene diversity in populations with different pedigrees. The advantage of MK over MAI is expected to be related primarily to distortion in founder
representation.
There are no reasons to believe that our results with Drosophila will not apply

Minimizing Kinship in Captive Breeding

387

to wildlife populations generally. We are aware of no case where results with Drosophila have yielded conclusions at variance with those from similar work in other
polymorphic outbreeding species [Frankham, 1982, 1995a, 1997]. In captive populations of many endangered species, the benefits of MK may be greater than that exhibited in this experiment. The ability to reuse under-represented individuals in
successive generations and breeding seasons allows them to make greater contributions. The practicalities of Drosophila meant that females were restricted to a single
mating in the current study.
A further important finding of this study was the significant differences among
founder groups in inbreeding depression, indicating that deleterious alleles of large
effect were contributing to inbreeding depression. All lines had the same inbreeding
coefficient at the split point, because lines with failures were removed. In the following generations, individual lines were more likely to have matings fail across all
treatment types descendent from the same founding group. Such founder effects in
inbreeding depression have been described previously in Tribolium castaneum, dairy
cattle, and Peromyscus polionotus [Pray and Goodnight, 1995; Miglior, 1994; Lacy
et al., 1996, respectively]. The founder effect in reproductive fitness indicates that
founder groups differed in content of deleterious genes. Such differences indicate
that at least part of inbreeding depression is due to relatively few genes of large
effect. Lethal alleles have been found in the Tyrells population that we used [Woodworth, 1996]. Inbreeding depression in Drosophila melanogaster is reputed to be
half due to lethals and half due to deleterious genes of small effect [Simmons and
Crow, 1977].
These results verify the predicted advantage of MK over alternative procedures
in maintaining genetic variation. There was no significant difference in reproductive
fitness, but MK was best or equal best in all tests. MK is currently the best method
for the genetic management of endangered species. Breeders of endangered species
in captivity can use MK with confidence that it is the best known management method
for retaining genetic variation.
CONCLUSIONS

1. MK retained more genetic variation than both the maximum avoidance of

inbreeding and RAND.
2. There was no significant difference between the three treatments in reproductive fitness.
3. These results verify the predicted advantages of MK over alternative genetic
management procedures for retaining genetic diversity.
4. Founder groups differed in their contents of deleterious genes, indicating
that deleterious alleles of large effect were contributing to inbreeding depression.
ACKNOWLEDGMENTS

We thank Dean Gilligan for comments on a draft manuscript and Craig Angus,
Edwin Lowe, Heidi Manning, Matt Traini, and Alexandra Wilson for technical assistance. This work was supported by Australian Research Council and Macquarie University Research Grants. This is publication No. 217 of the Key Centre for Biodiversity
and Bioresources, Macquarie University.

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