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Section 11 Genetics Management of Captive Populations. Traditionally, the objective of captive breeding programs was simply preservation of species and increase of numbers. Now, managers of zoos, botanic gardens, and wildlife parks almost universally accept the necessity to retain

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Section 11

Genetics Management of Captive Populations

Traditionally, the objective of captive breeding programs

was simply preservation of species and increase of


Now, managers of zoos, botanic gardens, and wildlife

parks almost universally accept the necessity to retain

species as dynamic evolutionary entities and to maintain

genetic health both for long-term viability and hopefully

for subsequent release to natural habitats.

  • Captive breeding programs can assist conservation efforts

  • by:

  • establishing populations in secure ex-situ locations

  • educating and engaging the public on conservation issues

  • providing a focus for fund-raising efforts for


  • providing individuals for research on the basic biology of

    the species, knowledge can then be applied to

    conservation of the species in the wild

  • providing individuals for reintroduction programs

Extent of Captive Breeding and Propagation Activity

Approximately 1,150 zoos and aquaria worldwide currently

house about 1,232,000 individual animals, including

584,000 individual fish, 202,000 mammals, 351,000 birds,

74,000 reptiles, and 21,000 amphibians.

About 5 -- 10% of the available space in zoos are used for

endangered species.

With the changes in priority, there could be breeding

space for about 800 endangered species in zoos and

wildlife parks.

In contrast, an estimated 2,000 -- 3,000 species ofterrestrial vertebrates alone will require captive

breeding within the forseeable future.

Unfortunately, zoos can only maintain a certain number

of individuals and these small, breeding groups can

rapidly become inbred and potentially non-viable.

By the early 1980s, zoo managers recognized that their

contribution to conservation could best be made through

regional and international cooperative breeding programs

and through collaborations with in-situ conservation


In North America, Species Survival Plans (SSP),

coordinated by the American Zoo and Aquarium Association,

were first developed in 1981.

SSPs involve the coordinated management of all captive

individuals held by cooperating institutions, and are now

in place for many endangered species.

Regional and international studbooks are used to make

recommendations on which animals should be bred, with

whom, how often, and where.

Individual institutions permit their animals to be managed

under one genetic and demographic objective, determined

by the coordinator, and animals are frequently moved

among participating institutions for breeding to optimize

genetic management.

Similar programs have been developed in Australia,

Europe, Japan, New Zealand, South Africa, and Central


Information on pedigrees, individual histories, breeding

experiences, and health records are collected at each

zoo and maintained by the International Species

Information System (ISIS) in Minnesota.

  • Zoos also contribute to both ex-situ and in-situ

  • conservation through involvement with the Conservation

  • Breeding Specialist Group (CBSG) of the Species

  • Survival Commission of the IUCN.

  • Their programs include:

  • Conservation Assessment and Management Plans (CAMPs)

  • that provide initial assessments of the global status

  • and initial research and management

  • recommendations.

  • Population and habitat viability assessments that provide

  • detailed quantitative assessment, evaluation of

  • management options, and recommendations for

  • conservation action.

  • Zoo conservation planning.

  • Providing expertise relating to captive breeding.

  • Coordinating meetings and workshops on topics required

  • to advance conservation.

  • Stages in Captive Breeding and Reintroduction

  • Captive breeding and reintroduction may be viewed as a

  • process involving the following six stages:

  • Decline of wild populations and its genetic consequences

  • Founding a captive population

  • Growing the captive population to a secure size

  • Managing the captive population over generations

  • Selecting individuals for reintroduction

  • Managing the reintroduced population (probably

  • fragmented) in the wild.

Genetic issues important in the first stage are the rate

of decline of the wild population, the size to which it

declines, and the resulting loss of genetic diversity and

inbreeding it has suffered prior to captive breeding.

Captive populations must be managed through 3 phases,

foundation, growth, and maintenance.

Management during each of these phases focuses on

different priorities.

During foundation, population size is usually small, and

knowledge of the husbandry of the species lacking.

During this phase, management focuses on basic research

to develop husbandry techniques and efforts to ensure

reproduction of founders.

During the growth phase, the focus is on rapid reproduction

and expansion of the population to multiple facilities.

During the maintenance phase, the population is managed

at zero population growth, at a size determined by the

genetic goals of the program. Typically, individuals are not

removed from the captive population (e.g. for reintroduction)

until the population size approaches this target size.

Founding Captive Populations

Potential founders may come from different sources or

be of unknown origin.

It is therefore essential to resolve any taxonomic

uncertainties, or the need for separate management

units prior to foundation.

This avoids outbreeding depression or a population of

undesirable hybrids.

It was not until late in the program that it was discovered

that several of the founders of the Asiatic lion captive

breeding program were identified as actually African

lions, resulting in termination of the program, but only

after substantial resources had been expended in its

development and support.

The founding process sets the genetic characteristics for,

and ultimately affects the conservation value of, the

captive breeding program.

If the population is to encompass the genetic diversity

in the wild and minimize subsequent inbreeding, then a

fully representative sample of founders is required.

Some selection is however inevitable during the foundation

as typically only a moderate proportion of wild-caught

individuals successfully breed in captivity.

For example, of the 242 wild-caught golden lion tamarins

in the captive breeding program, only 48 individuals

contributed to the current gene pool with 2/3 of the

gene pool prior to management being derived from just

one prolific male.

The need to acquire a solid genetic base, the effects of

selection in reducing the number of contributing founders,

and economics all argue for establishing populations with

large numbers of founders.

Unfortunately, most captive breeding populations have

become established using an inadequate number of


Some captive populations were only founded when the

endangered species was at a “last gasp”, when few

founders were available.

Founders for most other captive breeding programs were

the few animals (or ancestors of animals) that were

already in captivity at the time the program was


Genetic Consequence of Small Founder Numbers

Population bottlenecks at foundation lead to loss of genetic

diversity, resulting in inbreeding, and reduced fitness.

To avoid bottlenecks, it is recommended that a minimum of

20 -- 30 genetically effective founders by used.

As discussed earlier, the relationship between number

of founders and the proportion of heterozygosity that

they capture is given by:

H = [1 - (1/2Ne)]

Thus, even 10 contributing founders capture 98% of

the heterozygosity in an outbreeding species while

30 founders captures over 98% of the heterozygosity.

The number of founders required to capture allelic

diversity depends more on the number and frequency

of alleles, but typically requires more individuals than

needed to capture heterozygosity, with more founders

needed if rare alleles are present.

For a locus with two alleles, the probability that a

random sample of n founders contains at least one

copy of each allele P(A1, A2) is given by:

P(A1, A2) = 1 - (1 - p)2n - (1 - q)2n

Where p is the frequency of A1 and q is freq. of A2.

At least 30 founders are need to meet the recommendation

of 95% certainty of capture of allele with frequency of


For the rarer allele, at a frequency of 1%, even 50

founders only have about a 60% chance of capturing the


Rare alleles are unlikely to be sampled unless founder

numbers are very high.

Growth of Captive Populations

The second phase of captive breeding programs is to

multiply the population size as rapidly as possible up to

the desired size set by the genetic and demographic

objectives of the program.

Genetic management is de-emphasized during this phase

as it may conflict with the goal of rapid population


Offspring must be produced from all adults, not just the

genetically most valuable.

Some animals display strong mating preferences and may

refuse to mate in genetically ideal crosses.

If a genetically undesirable pairing is broken up in a

monogamous species, new pairings may not mate for

several years, slowing population growth.

Genetic management during this phase is usually limited

to avoiding pairings between close relativesl.

How is Target Population Size Set?

The current goal of most captive breeding programs for

endangered species is to retain 90% of the genetic

diversity for 100 years.

For a population with a stable size, the effective

populations size required to meet this goal is inversely

proportional to the generation length as:

Ne = 475/L,

where L is the generation length in years.

The founding phase has a significant impact on the

required Ne, and it is likely to be greater than the

value predicted.

The required number of individuals depends critically on

the founder effects, Ne/N ratio, generation length, and

on how quickly the population increases after the


The Ne/N ratio depends on variance in family size, sex-

ratio, mating system, and fluctuations in N.

Genetic Management of Captive Populations

Genetic Deterioration in Captivity -- As the population

approaches its target size, the focus increasingly shifts

to more intense genetic management.

The objective becomes maintaining demographic stability

and counteracting deleterious genetic changes including:

inbreeding depression, loss of genetic variation,

accumulation of new deleterious mutations, genetic

adaptations to captivity that are deleterious in the wild,

outbreeding depression.

Inbreeding depression, loss of genetic diversity and

genetic adaptation to captivity are expected in all closed

captive populations.

The accumulation of new deleterious mutations is only a

long-term concern and is of unknown importance.

The most immediate threat during foundation is

inbreeding depression.

The effects of inbreeding depression, loss of genetic

diversity, and mutational accumulations are all more

severe in smaller than larger populations.

Conversely, genetic adaptation to captivity is more

extensive in larger than smaller populations.

While this is beneficial in captivity, its deleterious

effects are only felt when the population is returned to

the wild.

All deleterious changes in captivity are likely to be more

deleterious when populations are reintroduced into harsher

wild environmental conditions.

Loss of Genetic Diversity -- Captive populations of

threatened species lose genetic diversity at foundation,

and because of small subsequent population size.

We can recast an earlier equation to illustrate both the

effect of Ne/N and the effect of founder, versus

subsequent population numbers, as follows:

Ht/HO = [1 - (1/2Nfo)]{1 - 1/[2N(Ne/N)]}t - 1

Where, Nfo = number of effective founders.

Ht/HO = [1 - (1/2Nfo)]{1 - 1/[2N(Ne/N)]}t - 1

Reflects the effect

of subsequent pop.


Reflects the

Founder Effect

From this equation, genetic variation in captive breeding

programs can be retained by:

Maximizing the initial genetic variation by using

adequate numbers of founders.

Minimizing the number of generations by breeding from

older individuals, or using cryoprservation

Maximizing population size

Maximizing Ne/N

Current Genetic Management of Captive Populations --

The current target of genetic management is a loss of

genetic diversity, and a concomitant increase in inbreeding

coefficient, no more than 10% over 100 years.

Unfortunately, due to small founder numbers and/or

limitations in space, such goals are unattainable in many

populations, and the genetic objective is often relaxed.

Targets may be lowered to 80% for 100 years, or

90% for 50 years.

Maximizing Ne/N

As captive breeding resources are

clearly limited, and the number of species requiring

captive breeding to save them from extinction is

increasing, it is important to maximize Ne for each

species using the minimum number of individuals.

The following procedures can be used to maximize Ne/N

Equalizing family size so that Ne approximates 2N -- this

recommendation can double the effective captive

breeding resource and it is being applied in practice.

Equalizing the sex-ratio of breeders -- i.e. avoiding harems

if possible. This is difficult to achieve in mammals as

most are polygamous and many breed best with harem


Many mammals are maintained in harems to avoid injury or

death from male-male aggression, and this is sometimes

practiced for species that do not naturally have harems.

Equalizing population sizes across generations -- Following

the foundation and growth phases, captive populations

are typically maintained at relatively stable sizes.

Maximizing generation length -- The may be done by

(a) allowing parents to reproduce from sexual maturity,

with successively euthanasia of offspring as new siblings

are produced (not ethically acceptable to many),

(b) retaining all offspring, but only using later-born

siblings to be parents of subsequent generations

(wasteful in terms of resources), (c) delaying reproduction

until they are older; this risks death, or sterility before


(d) breeding parents when young, and then avoiding

reproduction (often with contraceptives) until older, and

breeding them again, or (e) cryopreservation of embryos,

or gametes; often the technology to do this is not

available for the species.

The procedures, while theoretically sound, are not

widely practiced, although there is some use of (d).

Minimizing Kinship

The individuals used to found captive populations typically

make very unequal contributions to subsequent generations.

A range of procedures including

Maximum avoidance of inbreeding

Genome Uniqueness

Founder Importance

Minimizing kinship

But what is the optimum way to manage pedigreed captive

populations of threatened species?

Ballou and Lacy (1995) compared the above four

procedures using both theoretical predictions and

computer simulations and found that minimizing kinship

was best for retaining genetic variation.

In brief, minimizing kinship involves choosing individuals

with the lowest relationship in the population as parents

of subsequent generations.

This reduces inequalities of founder contributions.

The kinship (or coancestry) of two individuals is directly

related to inbreeding, and, in fact, is the inbreeding

coefficient of their offspring (if they had them).

The mean kinship is:


mki = kij/N


Where kij is kinship between i and j, and N is the

number of individuals in the population.

The rationale behind the use of mean kinship in genetic

management is illuminated by noting the relationship of

average mean kinship to genetic diversity (Ht/Ho):

1 - mk = Ht/Ho

where mk is the average mean kinship in the population.

Consequently, if kinship is minimized, heterozygosity

is maximized.

Individuals with low mean kinships have fewer relatives

in the population of individuals with high mean kinship and

therefore, carry fewer common alleles and thus are the

most valuable individuals.

Under a mean kinship breeding program, individuals with

lower mean kinship are given breeding priority.






The kinship of Robert to

the other named individuals

is zero.

Kinship of Louise and Rita

is most easily obtained by

computing the inbreeding coefficient of hypothetical

offspring X from a mating between them using the

pedigree method.
























Paths n FA Contribution to FX

LFAHR 5 0 (1/2)5

LGAHR 5 0 (1/2)5

LFBHR 5 0 (1/2)5

LGBHR 5 0 (1/2)5

FX = 4/32 = 1/8

Thus, KL-Ri = KRi-L = FX = 1/8

The kinship of Rita with herself is the probability that 2

random gametes from her contain alleles that are

identical by descent.

As Rita is NOT inbred, she does not herself contain alleles that are identical by descent.

If she is labeled with a genotype of A5A6, then Rita’s

kinship with herself is:

kRi-Ri = P[both A5] + P[both A6] = 1/4 + 1/4 = 1/2

This is the same value as the F for the progeny of selfing.

Robert is inbred, so his kinship with himself is increased,

as follows:

kRo-Ro =1/2(1+FRo)

and since Robert results from a full-sib mating, his

inbreeding coefficient FRo = 1/4, and

kRo-Ro =1/2[1+1/4] = 5/8

Kinship and mean kinship for the named individuals in the


Thelma Louise Rita Robert Mean k

Thelma 5/8 9/32 1/8 0 0.258

Louise 9/32 5/8 1/8 0 0.258

Rita 1/8 1/8 1/2 0 0.187

Robert 0 0 0 5/8 0.156

Rationale behind use of mean kinship in genetic

management is due to: 1 - mean k = Ht/HO.

Thus, if kinship is minimized, heterozygosity is maximized.

Individuals with low mean k are most valuable. They have

fewer relatives in the population than individuals with

higher mean k and therefore carry fewer common alleles.

Under a mean kinship breeding program, individuals with

lower mean k are given breeding priority.

Managing by mean k would then increase the contribution

of genes from Robert and decrease those of Thelma and


When applying minimizing kinship to threatened

populations, the mean k for each individual is calculated

from pedigrees.

Parents to be used for breeding are chosen as those with

the lowest mean k.

Two additional considerations are required to determine

specific matings:

Mates are chosen such that matings between individuals

with quite different mean kinships are avoided as they

limit management options in the future.

For example, if a valuable individual is mated to one of

low value, increasing the contribution of the under-

represented individual also increases the contribution

of its over represented matel.

Matings of close relatives is avoided to minimize


Limitations of Management by Minimizing Kinship:

Does not directly address the probable changes in

reproductive fitness.

Does not necessarily minimize inbreeding, but it is very

close to minimization of inbreeding strategy.

Equalization of family sizes minimizes genetic adaptations

to captivity for a given sized population however,

maximization of Ne is a single, large population promotes

genetic adaptation to captivity.

Reproductive Technology & Genome Resource Banks

Reproductive technologies, developed for use in domestic

animals, promise to have significant input to conservation

of threatened species.

Artificial Insemination (AI) -- AI with frozen semen can

be used in transportation of genetic material, rather

than animals, with great reductions in cost.

AI can also be used to equalize sex-ratios of breeders by

inseminating females with semen from males other than

local dominant, or sole, male.

Based on available data, AI is only being used routinely in

the management of the black-footed ferret, cheetah,

giant panda, and whooping crane and its use is just

beginning in elephants.

Cryopreservation -- Cryopreservation of gametes,

embryos, seeds, or tissues has many potential benefits for

conservation, as it literally deep-freezes tissues, and the

genes they contain, away from the deleterious

environmental and genetic influences.

In threatened species, cryopreservation of sperm or

embryos in genome resource banks provides a valuable

means for extending the generation interval, and slowing

inbreeding and loss of genetic diversity.

In animals, live animal populations must still be maintained,

so that females are available to be inseminated, or to

raise embryos.

In a few cases, related domestic species can act as

surrogate mothers.

This has been carried out with African wildcat and

Indian desert cat (into domestic cats), gaur (into

cattle), and mouflon sheep (into domestic sheep).

However, most species are unlikely to be able to be

raised in abundant domestic surrogates.

Cryopreservation of germ cells and embryos is currently

only applicable to a small proportion of animals, as the

technology needs to be customized for each species, and

is available mainly for domestic mammals and their close


Cloning -- Cloning has the potential to aid in conservation

of threatened species.

This is easily achieved via cuttings or tissue culture in

plants, where many copies of each individual can be made.

In animals, nuclear transplanting has been used to clone

a variety of domestic animals, and the endangered gaur.

Cloning may contribute to the conservation of endangered

animals in the future.

For example, biopsies can be collected from endangered

animals and used to expand numbers rapidly in captivity

while retaining the wild population.

The founders could be used to generate the target

population size with essentially no loss of genetic diversity.

However, at this stage, cloning of animals is not possible

for any but a few species closely related to domestic

species and it is very expensive.

Furthermore, the technology requires surrogate mothers

and an ample supply of these is unlikely to be available

for threatened species.