Genetic management of fragmented populations is one of the major, largely

unaddressed issues in biodiversity conservation. Many species across the planet

have fragmented distributions with small isolated populations that are potentially

suffering from inbreeding and loss of genetic diversity (genetic erosion), leading to

elevated extinction risk. Fortunately, genetic deterioration can usually be remedied

by augmenting gene flow (crossing between populations within species), yet this is

rarely done, in part because crossing is sometimes harmful (but it is possible to

predict when this will occur). Benefits and risks of genetic problems are sometimes

altered in species with diverse mating systems and modes of inheritance. Adequate

genetic management depends on appropriate delineation of species. We address

management of gene flow between previously isolated populations and genetic

management under global climate change.

Genetic management of fragmented populations involves the application of evolutionary genetic theory and knowledge to alleviate problems due to inbreeding

and loss of genetic diversity in small population fragments. Populations evolve

through the effects of mutation, selection, chance (genetic drift), and gene flow

(migration). Large outbreeding, sexually reproducing populations typically contain

substantial genetic diversity, while small populations typically contain reduced

levels. Genetic impacts of small population size on inbreeding, loss of genetic

diversity, and population differentiation are determined by the genetically effective

population size, which is usually much smaller than the number of individuals.

Inbreeding reduces survival and reproduction (inbreeding depression), and thereby

increases extinction risk. Impacts are generally greater in naturally outbreeding than

inbreeding species, in stressful than benign environments, for fitness than peripheral traits, and for total fitness compared to its individual components. Inbreeding

depression is due to increased homozygosity for harmful alleles and at loci

exhibiting heterozygote advantage. Inbreeding depression is near universal in

sexually reproducing organisms that are diploid or have higher ploidies.

Species face ubiquitous environmental change and must adapt or they will go

extinct. Genetic diversity is the raw material required for evolutionary adaptation.

However, loss of genetic diversity is unavoidable in small isolated populations,

diminishing their capacity to evolve in response to environmental changes, and

thereby increasing extinction risk.

Most species now have fragmented distributions, often with adverse genetic consequences. The genetic impacts of population fragmentation depend critically

upon gene flow among fragments and their effective sizes. Fragmentation with

cessation of gene flow is highly harmful in the long term, leading to greater

inbreeding, increased loss of genetic diversity, decreased likelihood of evolutionary

adaptation, and elevated extinction risk, when compared to a single population of

the same total size. The consequences of fragmentation with limited gene flow

typically lie between those for a large population with random mating and isolated

population fragments with no gene flow.

Inbreeding is reduced and genetic diversity enhanced when a small isolated inbred

population is crossed to another unrelated population. Crossing can have beneficial or harmful effects on fitness, but beneficial effects predominate, and the risks of

harmful ones (outbreeding depression) can be predicted and avoided. For crosses

with a low risk of outbreeding depression, there are large and consistent benefits on

fitness from gene flow within outbreeding species that persist across generations.

Benefits are greater in species that naturally outbreed than those that inbreed, and

increase with the difference in inbreeding coefficient between crossed and inbred

populations in mothers and zygotes. However, benefits are similar across invertebrates, vertebrates, and plants. There are also important benefits for evolutionary

potential of crossing between populations.

The progeny of crosses between some populations exhibit harmful effects on

fitness (outbreeding depression). These are primarily due to populations being

different taxa, having fixed chromosome differences, being genetically adapted to

different environments, having a long history of isolation, or combinations of these.

Even if outbreeding depression occurs as a result of crossing, it is often only

temporary, as natural selection acts to remove it, especially in large populations.

The risks of inbreeding and outbreeding depression, and the prospects for genetic

rescue are often altered in species with different mating systems or modes of

inheritance (compared to outbreeding diploids), such as self-incompatible, selffertilizing, mixed mating, non-diploids, and asexual.

The first step in conservation management is to delineate groups for separate versus

combined management. However, there are many problems with species delineation, including diverse species definitions, a lack of standardized protocols, and poor

repeatability of delineations. Definitions that are too broad will lead to outbreeding

depression if populations are crossed, while those that split excessively may preclude

genetic rescue of small inbred populations with low genetic diversity. To minimize

these problems, we recommend the use of species concepts based upon reproductive isolation (in the broad sense) and advise against the use of Phylogenetic and

General Lineage Species Concepts. We provide guidelines as to when taxonomy

requires revision and outline protocols for robust species delineations.

The number and geographic location of genetically differentiated populations must be

identified to determine if fragmented populations require genetic management. Clustering of related genotypes to geographic locations (landscape genetic analyses) is used

to determine the number of populations and their boundaries, with the simplest

analyses relying on random mating within, but not across populations. Evidence of

genetic differentiation among populations indicates either that they have drifted apart

(and are likely inbred), or that the populations are adaptively differentiated. The current

response when populations are genetically differentiated is usually to recommend

separate management, but this is often ill-advised. A paradigm shift is needed where

evidence of genetic differentiation among populations is followed by an assessment of

whether populations are suffering genetic erosion, whether there are other populations

to whichthey could be crossed, andwhetherthe crosseswould be beneficial or harmful.

Having identified small geographically and genetically isolated populations, we

need to determine whether they are suffering genetic erosion, and if so, whether

there are any other populations to which they could be crossed. We should next

ask whether crossing is expected to be harmful or beneficial, and if beneficial,

whether the benefits would be large enough to justify a genetic rescue attempt.

Here we address these questions based on the principles established in the

preceding chapters.

When the decision is made to augment gene flow into an isolated population,

managers must decide on how to augment gene flow, when to start, from where to

take the individuals or gametes to be added, how many, which individuals, how

often, when to cease, etc. Even without detailed genetic data, sound management

strategies for augmenting gene flow can be instituted by considering population

genetics theory, and/or computer simulations. When detailed data are lacking,

moving some individuals into isolated inbred population fragments is better than

moving none, as long as the risk of outbreeding depression is low.

With more detailed genetic information, more precise genetic management of

fragmented populations can be achieved, leading to improved retention of genetic

diversity and lower inbreeding. Using mean kinship within and between populations (estimated from modeling, pedigrees, genetic markers, or genomes), and

moving individuals among fragments with the lowest between fragment mean

kinships provides the best means for gene flow management. Populations should

then be monitored to confirm that movement of individuals has resulted in the

desired levels of gene flow, and that genetic diversity has been enhanced

Adverse genetic impacts on fragmented populations are expected to accelerate

under global climate change. Many populations and species may not be able to

adapt in situ, or to move unassisted to suitable habitat. Management may reduce

these threats by augmenting genetic diversity to improve the ability to adapt

evolutionarily, by assisted translocation, or by ameliorating non-genetic threats.

Global climate change amplifies the need for genetic management of fragmented

populations.

Genetic management of fragmented populations is one of the most important

issues in conservation biology, but is very rarely addressed in a satisfactory

fashion.

2. Due to human activities, most species have fragmented distributions, many with

small isolated population fragments that will experience loss of genetic diversity,

become increasingly inbred, be unable to adapt to future environments, and

have elevated extinction risks.

3. If populations of naturally outbreeding species are inbred, they should be

presumed to be experiencing inbreeding depression and managed appropriately

without waiting for specific evidence of inbreeding depression.

4. Inbreeding depression, loss of genetic diversity, and loss of evolutionary

potential can be reversed by augmenting gene flow from a genetically different

population.

5. Crossing between populations is occasionally harmful (outbreeding depression),

but this is largely predictable and a less serious problem than inbreeding

depression.

6. The expression of outbreeding depression is often temporary because natural

selection removed such harmful effects in all investigated cases.

7. Some species definitions are unsuitable for conservation purposes (especially the

Phylogenetic and General Lineage Species Concepts) and many species

delineations lack robust scientific support. For conservation purposes we

recommend that species delineations be based on reproductive isolation in the

broad sense.

8. We strongly urge that standardized species delineation protocols be devised for

conservation purposes, including appropriate species concepts, geographic sampling

regimes, sample sizes, characters, habitat characteristics, and statistical analyses.

9. When population differentiation is detected within a species, it is important to

distinguish whether this is due to drift (where augmentation of gene flow should

be evaluated) or differential adaptation (where separate management is usually

indicated).

10. We recommend augmentation of gene flow for isolated population fragments of

outbreeding species that are suffering inbreeding and low genetic diversity,

provided the proposed population cross has a low risk of outbreeding depression

and the predicted benefits justify the cost.

11. Fitness benefits from crossing for selfing species do not persist over generations

(but evolutionary rescue should), so genetic rescue attempts for them are less

likely to be justified. Fitness benefits from crossing in mixed mating species do

not persist as well as they do in outcrossing species.

12. Choosing among genetic management actions (and inactions) needs to assess

the overall risks and benefits of different scenarios. Doing nothing is a choice

that is often harmful to the persistence of populations and species.

13. We recommend managing gene flow among isolated population fragments by

minimizing mean kinship. If kinship analyses are not feasible, we advocate

management of gene flow to maximize genetic diversity, based on conservation

genetics principles.

14. Species will need to be even more adaptable to cope with projected global

environmental change, increasing the need for genetic management.

15. Threatened species need integrated management across populations,

disciplines (including genetics), institutions, and political boundaries, as

exemplified by the One Plan approach.

Final messages for managers of wild animal

and plant populations

• The persistence of species with fragmented distributions is heavily dependent

upon active genetic management.

• It is indefensible to passively manage small isolated populations to extinction

(without augmenting gene flow) if there are other populations of the same species

adapted to similar environments and without fixed chromosomal differences,

from which gene flow can be augmented.

• Almost any regime of augmented gene flow is likely to be beneficial in such

circumstances, thereby reducing unnecessary population extinctions.

• Augmenting gene flow is likely to be a highly cost-effective management option,

improving prospects for species to persist in the face of other threats.

• Management practices will have to facilitate ongoing adaptation to rapidly

changing environments.

• Should you require assistance to implement genetic management, there are

conservation and evolutionary geneticists who can assist you.