Conservation Genetics
The basis for an evolutionary
conservation
2
• Genetic consequences of small population
size and extinction.
• Defining conservation and management
units based on population genetics.
Conserving Gene Diversity in
Declining Populations
• Loss of genetic diversity primary issue in assessing
genetic extinction risks
• Decreases ability of populations to respond
adaptively to future environmental change
• Declining populations face two threats related to loss
of genetic variation:
– Long-term: loss of heterozygosity
– Short-term: Inbreeding depression (ID).
ID is reduced fitness in a given population as a result of
breeding of related individuals. Inbreeding, results in more
recessive deleterious traits manifesting themselves.
Hardy-Weinberg Equilibrium
The gene pool of a non-evolving population remains constant
over multiple generations; i.e., the allele frequency does not
change over generations of time.
The Hardy-Weinberg Equation:
1.0 = p2 + 2pq + q2
where p2 = frequency of AA genotype; 2pq = frequency of Aa
plus aA genotype; q2 = frequency of aa genotype
A population not in Hardy-Weinberg equilibrium
indicates that one or more of the five evolutionary
agents are operating in a population
Five agents of evolutionary change
Genetic Drift and Effective Population Size
1. Genetic drift is the reason why we worry about African cheetahs
and other species that exist in small populations.
1. Drift is more pronounced in smaller populations.
1. Lower genetic diversity therefore lower ability to adapt to changing
conditions.
EFECTIVE POPULATION SIZE (Ne)
The average number of individuals in a population that
actually contribute genes to succeeding generations by
breeding. Ne << N
Ne can be reduced by the following factors:
a. a higher proportion of one sex may mate;
b. some individuals will pass on more genes by having more
offspring in a lifetime than others
c. any severe past reduction in population size may result in
the random loss of particular genotypes.
The relationship between Ne and a fixation index. Small populations
become inbred more rapidly than large populations, often leading to
inbreeding depression.
Genetic Drift
• Genetic drift: Random fluctuation in allele frequencies
over time by chance
• important in small populations
– founder effect - few individuals found new
population (small allelic pool)
– bottleneck effect - drastic reduction in
population, and gene pool size
9
Long-term Threat: Loss of Heterozygosity
Amos & Balmford. 2001. Heredity 87:257-265.
• Loss of variability (He) is related to:
– Lowest Ne reached by declining population
– Time (generations) population remains at lowest Ne
• Loss of He: Ht = Ho (1-[1/2Ne])t, where Ho is initial
heterozygosity, Ht is heterozygosity after t
generations after a decline to size Ne
• e.g. After 5 generations, large population reduced to
Ne of 20 will retain 88% of heterozygosity at neutral
loci
Relationship between allelic diversity remaining after a single-generation
bottleneck and the original number of alleles for different population sizes.
A Genetic Bottleneck is a Form of Genetic Drift
In a genetic bottleneck, allele frequency is altered due to a
population crash.
Once again, small bottlenecked populations = big effect.
Genetic Bottleneck
A genetic bottleneck creates random genetic changes without regard to
adaptation.
A severe genetic bottleneck occurred in northern elephant seals.
Other animals known to be affected by genetic bottlenecks include the
cheetah and both ancient and modern human populations.
Endangered Species Are in the Narrow Portion of a Genetic
Bottleneck and Have Reduced Genetic Variation
Example of Genetic Effects of An
Extreme Bottleneck: Mauritius Kestrel
Groombridge et al. 2000. Nature 403:616.
• Severe population decline due to
habitat destruction and effects of
DDT on hatching success of eggs
• 1974: population = 4 birds; single
pair source of all birds in
subsequent population
• Under intensive management
population increased to 400-500
birds by 1997 but experienced six
generations at < 50 birds
Mauritius Kestrel Exhibits Genetic
Scars of Near Extinction
• Mauritius kestrel has
72% lower allelic
diversity (A) and
85% lower
heterozygosity (He)
than mean of nonendangered Kestrels
• Analysis of museum
skins indicates much
higher levels of
variation before
decline
Causes of Low Variation in Small
Populations
• Low variation is likely a consequence of
being small rather than a cause.
• Lack of variation is due to the ecological
process that made a population small rather
than the reason it is small.
• Greater importance of ecology vs genetics in
short-term conservation decisions (Lande
1988. Science 241:1455-1460)
Inbreeding Depression in
Declining Populations
• Loss of fitness due to increased production of
homozygous offspring due to matings
between relatives in bottlenecked
populations.
• Mechanism: increased exposure of
deleterious recessives in homozygote which
were previously masked in heterozygous
individuals
Issues Related to Inbreeding
Depression
• Effects of inbreeding maybe
transitory
• After being exposed to selection
in homozygous individual
deleterious mutations are
purged from population gene
pool
• Example: increase in hatching
success in butterfly populations
founded form single pairs over
time
• Effect of purging not universal may only affect some traits in
some populations
Recovering From Inbreeding
Depression
• Solution: outcross inbred population to another
outbred population by introducing individuals from
outbred population.
• When no outbred population exists some fitness
recovery still possible when individuals from other
inbred populations used because each small
population will be fixed (by chance) for different
alleles.
• Examples: Swedish adders (Madsen et al. 1999.
Nature 402:34-35) and Illinois Prairie Chickens
(Westemeier et al. 1998. Science 282:1695-98).
Recovery of Fitness by Introduction of
Immigrants Into Inbred Populations of
Adders and Prairie Chickens
Estimating Levels of Adaptive
Variation Using Neutral Markers
• Neutral markers (e.g. microsatellites)
frequently used to measure levels of variation
in small populations endangered species
• Assumption: level of variation in neutral
markers is correlated with adaptive variation
Correlation Between Molecular and
Quantitative Measures of Genetic
Variation
(Reed & Frankham 2001. Evolution 55:1095-1103)
• Meta-analysis of studies which measured molecular
variation and quantitative variation in same
organisms.
• Quantitative variation: life history traits, morphology,
direct measures of heritable variation in above traits.
• Assumption: quantitative variation more closely
related to fitness-related variation in organisms
Correlation between molecular and
quantitative variation varies widely among
studies
Magnitude of correlation is low
Conclusions
(Reed and Frankham 2001)
• Molecular measures of genetic
variation have only a very limited
ability to predict quantitative
genetic variability
• When information on a populations
short-term evolutionary potential is
required quantitative variation
should be measured directly
Comparison of Estimates of Qst
and Fst
• Increase in studies examining relationship
between differentiation in neutral molecular
(Fst) and quantitative (Qst) variation
• Reviews:
– Merila &Crnokrak. 2001. J. Evol. Biol. 14:892-903.
– McKay & Latta. 2002. TREE 17:285-291.
• Lack of correlation often found but exceptions
occur
• Reason: Fst reflects history and Qst reflects
selection
Koskinen et al. 2002. Contemporary
fisherian life history evolution in small
salmonid populations. Nature 419:826-830.
• Grayling (Thymallus
thymallus) populations
founded in small Norwegian
lakes with different thermal
regimes ~ 100 ybp
• Contrasted differentiation in 17
microsatellites (Fst) with
differentiation in life history
characteristics (e.g. growth
rate) (Qst)
Qst values > Fst
values in all
populations
Fst reflects history
of
small populations
created from
colonization events
Qst reflects adaptive
response by fish to
different thermal
environments
Concordance: Gene tree = species tree
Speciation
Two species of tree frogs
morphologically and
reproductively isolated
Gene trees are contained in
species trees
Use of Genetic
Markers to Identify
“Units of
Conservation” in
Natural Populations
• e.g. Daugherty et al.1990. Neglected taxonomy and
continuing extinctions of tuatara (Sphenodon). Nature
347:177-179.
• Ancient reptilian lineage - restricted to 12 island groups
off of New Zealand
• For conservation purposes all populations classified as
belonging to one species (S. punctatus) despite earlier
work suggesting multiple species
• Analysis of phylogenetic relationships among
individuals using allozyme loci
3 phylogenetically
distinct lineages
identified
1 previously
unrecognized
species restricted
to single island no special status
“Bad Taxonomy
Can Kill”
Distribution maps of Galápagos tortoises throughout the
archipelago and on Santa Cruz
Russello M A et al. Biol. Lett. 2005;1:287-290
Bayesian phylogenetic tree of extant and extinct Galápagos tortoise taxa
Russello M A et al. Biol. Lett. 2005;1:287-290
Identifying Conservation Management
Units: ESUs and MUs
• Evolutionary Significant Units (ESUs):
Population(s) within a species with high
conservation value because they contain a
significant portion of evolutionary history
and/or potential
• Management Units (MUs) (Moritz 1994):
Genetic distinct hence demographically
distinct populations that should be managed
as separate “stocks”
Management Units
• MUs (Moritz 1994): Populations that show
significant differences in allele frequencies
regardless of phylogenetic relationships of
alleles
• Populations exchange so few migrants so as
to be demographically distinct = separate
stocks
• Contrast with ESUs which are operationally
defined as being reciprocally monophyletic for
mtDNA alleles (Moritz 1994)
MUs are nested within ESUs
Criticism of Moritz’s (1994) Definition of
ESUs - Crandall et al. (2000)
• Adaptive variation is what we seek to conserve
• Phylogenetically-defined ESUs focus solely on
historical relationships and ignore adaptive
differences between populations
• Problem scenarios:
– Populations with adaptive differences maintained by
selection but with high gene flow not identified as ESU
– Populations with low gene flow but no adaptive differences
will be inappropriately designated as ESUs
Defining ESUs on the Basis of
Ecological and Genetic
Exchangeability (Crandall et al. 2000)
• Populations classified on the basis of whether they
show recent or historical ecological or genetic
exchangeability
• Genetic exchangeability:
– Rejected (+) when gene flow is low or accepted (-) when
gene flow is high or populations are genetically similar
• Ecological exchangeability:
– Rejected (+) when evidence for population differentiation in
traits that reflect adaptive divergence (e.g. life history traits,
morphology)
– Accepted (-) when no divergence in putative adaptive
variation
Black Rhinos in S.
Africa
-high gene flow
-similar habitat use
-no separate ESUs
Puritain Tiger Beetles in
Connecticut and
Chesapeake Bay
-low gene flow/fixed mtDNA
variants between pops
-use different habitats
-separate ESUs
-
-
+
+
+
-
Value of Exchangeability
Criteria
• Logical scheme for identifying ESUs
that excludes populations that show no
evidence for adaptive differentiation
• What constitutes evidence for adaptive
differentiation?
• Focus of future debate within
conservation biology/genetics
Wildlife Forensics
A wildlife CSI?
Wildlife Forensics
• Molecular genetic techniques can identify products of
illegal harvest of protected species
• Examples:
Detection of Illegal hunting and sale of meat from protected whales
by Japan and Norway (Baker and Palumbi 1996)
IWC instituted a global moratorium on commercial whaling in 1985.
Japan and Norway continued to hunt few species (minke) for
“scientific purposes” - meat sold commercially.
• Issue: Were protected species also being illegally harvested and
meat sold as from species that could be hunted?
Genetic Analysis of Whale Meat
• “Undercover” purchase of supposedly-legally
hunted fresh whale meat (i.e. minke) in
Japanese markets
• Illegal to transport tissues from protected
species
• PCR-amplification of whale mtDNA control
region sequence in hotel room in Tokyo
• Sequenced in US labs
Analysis of 16 Whale Meat Samples
Samples 19b, 41, 3
11, WS4 from
Protected species
19b - Humpback
41, 3, 11, WS4 Fin whales
16, 13, 28 Porpoise and dolphin
Conclusions
• Results of analysis: stricter controls over sale
of “scientifically harvested” whale meat
• Meat harvested prior to harvest bans
genotyped to monitor distribution
• Other applications: species identity of caviar
and seal penises, population origin of
poached chimps
FIN