Transcript What maintains genetic variation? - Carol Lee Lab

Genetic Threats /
Conservation Genetics
Big cats, hungry dogs, and little mice
Florida pocket mouse
Don Waller
Botany - UW
Cheetah
Ivorybilled Woodpecker
•
•
•
The magnificent Ivory-billed
Woodpecker has become a
symbol of the bottomland forest
wilderness that once extended
across the southern United
States. The largest woodpecker
north of Mexico and the third
largest in the world, the Ivorybilled Woodpecker inhabits
mature swampy forests, roaming
large areas in search of dead and
dying trees infested with beetle
larvae, its primary food. Ivorybilled Woodpeckers were
probably never common, but by
the 1930s, their habitat had been
destroyed.
Thought to be extinct for >30
years – rediscovered (?) 2005
NOT SEEN SINCE . . .
Aka the
“Lord God”
bird
Why did it
disappear?
Ivory-billed Woodpecker
“Almost no forests today can
maintain an Ivory-billed
Woodpecker population”
All species exist as populations
What are we doing?
• Why is this the 6th
extinction?
• Why is it “unnatural”?
• What are the causes?
• Why don’t we have an
‘IPCC’ to deal with this
issue?
Why these patterns?
Why these patterns?
Why are most
threatened species
tropical?
Why is human
population growth
rate correlated with
numbers of
threatened species?
Species face many threats
Deforestation
Burning
Erosion
So does genetics matter?
If habitat destruction, over-exploitation, pollution,
and introduced species are driving most species
extinct, should we be concerned about genetics?
Why books & journals about Conservation
Genetics?
.
What uses does it have?
Conservation genetics is a growing field
• Rapid increase in interest and
publications
• Uses multiple approaches . .
– Theory, experiments, & case studies
• New journal:
• Benefiting from population
genetics theory, and perhaps
contributing to it
Outline
• Why is diversity threatened?
– Which species are going extinct?
• Conservation genetics case studies
–
–
–
–
–
Florida Panther, African lions, & cheetahs
Florida pocket mouse & Isle Royle Wolves
Illinois Prairie Chickens – genetic rescue?
Indiana Royal Catchfly & other plants
Did we purge the genetic load in Speke’s gazelle?
• Lessons regarding genetic hazards?
– Short term: Inbreeding
– Long Term Threats:
• Drift and the fixation of mutations
• The loss of quantitative genetic variation
Outline
• Other uses of Conservation Genetics?
– Evolutionarily unique species – ‘living fossils’
• Do bigger branches deserve more protection?
– Forensics, etc.
• Rules for captive breeding & reintroductions
Florida Panther
• Puma concolor coryi
– Sub-species of cougar
– Restricted in its range
– Carnivore: small pop size
• Symptoms:
– Cryptochordism
– Kinked tail & cowlick
– Worst semen quality of any felid (cat)
• What would you do?
Florida Panther
• Built highway underpasses
• Brought in some comely female Texas cougars
– Why from Texas? Why females?
• Effects:
– 8 females introduced, 5 had kittens
– Appears to be working - no kinked tails, 1 cowlick
• Prescription: 20%, then 2.5% / gen. to reduce deleterious
alleles
Lions in Ngorongoro Crater
(Packer et al. 1991)
• 1962 epizootic:
– Down to 9 Females, 1 Male
– 7 more males in 1964-65
– But only 15 founders
• 1975 on: N ~ 75-125
• Symptoms:
– Low genetic diversity
– Sperm abnormalities
– Low reproduction
• In need of genetic rescue?
Cheetahs
• Fastest land mammal
• One of the most
threatened – why?
• Subject to many of the
same genetic problems as
the Florida panther:
– Mis-shapen sperm
– Undescended testicles
– Low infant survival
Cheetahs
• Fastest land mammal
• One of the most
threatened – why?
Missing
variation
Going to the dogs . . Wolves
• Once argued that wolves are adapted to close
inbreeding by virtue of their pack structure
• Tested in captive wolves in Scandanavia
• Inbreeding produced declines in:
–
–
–
–
–
Juvenile weight
Reproductive success
Longevity
Sight - congenital blindness emerged
Laikre & Ryman (Cons Biol 1991)
Gray wolves on Isle Royale
Wayne et al. 1991
• Migrated to island in 1949
– Only 1 mtDNA haplotype => 1 pair?
– Feed on moose mostly
• Population increased to 50 (1980)
• Declined to 14 by 1990
– Susceptible to canine parvovirus
• Genetics
– 50% loss in Het (vs. 40-65% loss predicted from Ne est)
– Restriction fragment results:
Island
Mainland
Average % difference
% Fixed
28%
42%
68%
15%
Royal catchfly – Silene regia
• Large populations produce
abundant viable seeds
• Small populations (<50-100)
produce seeds but these are
inviable
• Why?
Fitness declines in small populations
• Fewer seeds and sharp pop. declines in small pops
of Gentiana germanica (Fischer & Matthies 1998)
• Seed & seedling size and survival decline in smaller
pop’s of Gentiana pneumonanthe
(Oostermeijer et al.1994)
• Seed viability declines in smaller populations in
Silene regia (Menges 1991)
Extinction and Ne in Clarkia pulchella
Newman & Pilson 1997 founded
experimental populations of this
annual plant with the same N, but
different Ne's (due to relatedness
of founders)
after 3 gen's, the low Ne pop. had
lower germination and survival
only ~ 21% of large Ne pop’s
At end, only 31% of low Ne pop's
remained vs. 75% of large Ne pop's
Conclusion:
Ne matters to persistence
Genetic rescue in Scarlet Gilia
• Heschel and Paige (1995) found
that adding pollen from a distant
population to two small
populations significantly increased
their seed size and germination
percentage, whereas transferring
pollen to a large population had no
effect.
– Cons. Biol. 9: 126-133.
• Termed ‘genetic rescue’
The Beach Mouse
• Peromyscus polionotus
• Florida island beach mouse
• Lacy et al. (1996; 1998) investigated 3
subspecies
• Inbreeding affected many traits:
Litter F:
Mom's F:
P.p. s
many char's
P(litter) & litter size
P.p. r
litter size
litter size
"Effects of selection on inbreeding depression varied
substantially among populations, perhaps due to different
histories of inbreeding and selection"
P.p.l.
**
NS
The Beach Mouse
The genetic load was unequally partitioned among founder pairs
– different founders contributed to different parts of the load
(affecting different fitness components)
Thus, inbreeding depression for individual fitness components
reflects a few highly deleterious alleles.
Such genetic loads tend to diverge among natural populations
due to both drift and selection (purging).
Inbreeding depression is universal
different alleles contribute to inbreeding depression of
different fitness components in different environments.
Speke’s Gazelle
• Smallest gazelle, a
migratory ungulate, native
to Somalia and Ethiopia
• Threatened by the loss of
grazing land to livestock +
hunting + drought + habitat
fragmentation + . . .
Height: at shoulder 1.6-2 ft.
Length: 3.1-3.5 ft.
Weight: 33-55 lbs.
The Speke’s Gazelle story
• In the late 1960s, the St. Louis Zoological Park
became concerned about the fate of Speke's
gazelle (Gazella spekei). Because of warfare in
Somalia, they decided to start a captive-breeding
program using all the animals in captivity he
could locate: 1 male and 3 females.
• The descendents of this bottlenecked population
appeared to show less inbreeding depression.
• Were deleterious recessive mutations purged by
selection from this population?
Templeton, A. R., and B. Read. 1983. The
elimination of inbreeding depression in a captive
herd of Speke's gazelle. pp 241–261 in C. M.
Schonewald-Cox et al., Ed. Genetics and
conservation: a reference for managing wild
animal and plant populations. Addison–Wesley,
Reading, Massachusetts.
The Speke’s Gazelle story
• Templeton & Read claimed that this inbreeding
purged much of the genetic load, but . . .
• Willis & Wiese ‘97 and Kalinowski et al. 2000
questioned this result and their analysis of the data..
– impact of inbreeding was mostly in the 1st generation, but
selection could not have acted so quickly
– "Evidence for genetic improvement of the SG herd is too weak
for this breeding program to be used as a paradigm for the
breeding of other endangered species"
Sumatran Rhino
Most unique of 5 rhino species but RARE
smallest; also known as Hairy Rhino
~400 on Malay peninsula, Borneo, & Sumatra
Remnant Borneo population of ~70
DNA evidence - unique;
Isolated for 1000's of yrs
Will not breed in captivity (21/39 died)
To inter-breed or not?
What to do?
• Dilemma: genetic rescue or genetic swamping?
– Given an isolated population potentially suffering from
inbreeding, should germplasm from other populations
be introduced?
– Case: Sumatran Rhino
– Case: Florida Panther
• Females from Texas introduced  genetic rescue
– Case: Prairie chickens in Illinois – also rescued
• Danger?
– Locally adapted genotypes can cause “outbreeding
depression”
So what traits do “extinction-prone”
species share?
• Rare!
• Large
Like top carnivores
Why?
– Most large mammals are threatened – and may have
stopped evolving
• Specialized
– Adapted to particular resources
– Or a particular place = Endemic, e.g. to islands
– The Tropics have by far the most diversity, but most of
these species are rare
• Social & / or Migratory
– Passenger Pigeon, bison, Great Auk, etc.
Small Ne
Anything that reduces Ne increases
genetic threats
• Ne = (4Nm x Nf)/ (Nm + Nf)
• As sex ratio skews, Ne 
• In sharp-tailed grouse, the
operational sex ratio is 1:10
• So when N=280, Ne = just 50
– This implies a 1% reduction in
Heterozygosity per generation
• Management goal: reduce skewing
of sex ratios in small populations
Genetic process in large vs. small
populations
Large, outcrossing
Small inbred
Favorable
Mutations
 Time
Occasional sweeps
regular simultaneous sweeps
Neutral
Mutations
Drift to fixation low variation
Drift sustains variation
Deleterious
mutations
Deterministic selection
low load - short-lived
Drift allows mut’s of moderate
effect to fix => drift load
What happens under inbreeding?
• Homozygosity & gene identity (idd) INCREASE
Note: There is no change in allele frequency
This causes deleterious recessive mutations to co-occur
causing . .
• Inbreeding Depression
= decline in fitness upon inbreeding
Reflects deleterious recessive alleles
• Variance among families & lines INCREASES
but DECREASES within lines
• Possible loss of lines & families
(this can decrease overall genetic diversity)
Inbreeding affects the
Frequencies of genotypes
Increased homozygosity
Within population (consanguineous) inbreeding changes the frequency of
genotypes (but not alleles) by increasing the frequency of
homozygotes while decreasing heterozygotes:
Genotype:
AA
H-W equilibrium
p2
Inbred population p2 + F pq
Aa
aa
2pq
q2
2pq (1-F) q2 + F pq
Deficiency of heterozygotes
Note: symmetric increase in homozygotes
deficiency of heterozygotes => gives formula to est F
What causes inbreeding depression?
• The accumulation of deleterious mutations with
(at least partial) directional dominance:
Genotype
Fitness
Frequency in:
Random mating
population
AA
1
p2
p2 + F pq
Aa
1–hs
2 pq (1 – F)
aa
1–s
2pq
(most selection)
q2
1.0
Fitness
AA
Aa
aa
Inbred population
q2 + F pq
(most selection)
 homozygosity
Inbreeding decline in Drosophila
Data from Ehiobu, Goddard, & Taylor, 1989, TAG 77: 123.
Fitness = viability x fecundity
N=20 for 8 gen’s
N=4 for 3 gen’s
1 gen. full-sib mating
 = .66
Inbreeding depression
e(-A)
Inbreeding depression
Wf = W0 - F pq s (1-2h)
Thus, inbreeding depression will be most
pronounced when:
–
–
–
–
–
There is a lot of inbreeding (F high)
Mutations are highly deleterious (s>0)
(or many)
Mutations are recessive (h~0)
mutations are moderately frequent in the population
(q appreciable, so pq is high)
The load of deleterious recessive
mutations can accumulate
Inbreeding
Small Ne
declines in
performance
Drift & Fixation
Inbreeding
depression
Inability to mate
Loss of S alleles
These are selfincompatibility
genes in plants
What kinds of inbreeding exist?
• Within individual
– Fi = P(2 alleles at a locus are idd)
• Between individuals
– Fj,k = P(allele at a locus in j is idd to allele there in k)
• Within populations
– FIS = deficiency of heterozygotes relative to random mating
• Among populations – due to subdivision
– FST = deficiency of het’s in a subdivided population relative
to the whole population
Types of Genetic Hazard
1.
2.
3.
4.
Inbreeding depression (consanguinity)
Fixation via drift (drift load)
Mutational meltdown
Declines in quantitative genetic variation
ALL genetic hazards can be overcome by
crossing among populations
(although outbreeding depression may be a problem)
 Genetics & ecology interact
Faster
Slower
How do deleterious alleles accumulate?
•
•
•
•
•
Added by mutation; purged by selection
Can become fixed in small populations
Theoretically a function of Ne
How great a threat is it?
How effective is purging by inbreeding or founder
effects in small populations?
– alleles with s < 1 / 2 Ne are invisible to selection
– Thus mildly deleterious mutations will continue to fix
even if strongly deleterious ones are purged
What influences genetic variation?
Mutation
Drift
+
+
Gene flow
Population size
& structure
GENETIC
VARIATION
+/-
Selection
Environment
What kind of variation
do we need to sustain?
• Quantitative genetics: Partitioning phenotypic
variation into genetic and environmental
components: VT = VA + VD + VI + VE
– localizing genes - QTL analysis
– determining the effects of different alleles
– determining the heritability (h2) of traits
(& thus response to selection)
h2 = VA / VT
• Yet we usually use genetic markers to
measure and monitor genetic diversity (easier)
Review: Measures of genetic variation
• Within a population
–
–
–
–
–
–
–
Number of alleles at a locus - n
Proportion polymorphic loci - P
Allele frequency - p
Heterozygosity - He & Ho
Gene Diversity - D
Linkage Disequilibrium - 
Inbreeding - F
• Among populations
– Subdivision: F-st (or G-st)
– Nei’s Genetic distance
Useful tools
• Molecular genetics: Provide techniques to
measure genetic variation and understand
the underlying basis for it. Can also use to
identify “genetic units” in nature like:
– Species
– Evolutionary Significant Units
– Ecotypes
• Ne = the size of an “ideal population” with the
same rate of loss of genetic variation by drift
as the population being described (N)
HOW LARGE?
• Obviously the greater Ne the
lower the rate of loss of
genetic variation
• For long-term maintenance of
H, Ne  1000s seems prudent
• Even in the short-term, Ne 
500 is much better than 50
(as in 50-500 rule)
‘Mutational meltdown' dynamics
SLOW (~100 gen’s)
Mutation - quantitative genetic equilibrium
(Lande 1995)
• Drift - mutation equilibrium approach:
Expected rate of loss of Vg and Het due to drift = 1 / 2 Ne per gen
dVg / dt = Vm - Vg / 2Ne
So, at equilibrium, Vg = 2 Ne Vm
If h2 ~ 0.5, Vg ~ Ve
• How fast is genetic variation produced via mutation?
– Rate of phenotypic divergence via drift among inbred lines
– Rate of response to selection in inbred lines
– Vm ~ 0.001 x Ve
(Lande 1975; Lynch 1988)
• So Ne ~ 500 should allow variation to be maintained
– But only ~10% of Vm is quasi-neutral (potentially adaptive)
– So Vm ~ 0.0001 x Ve => Ne of 5000 needed to maintain variation
Topics in Conservation Genetics
• Evolutionary uniqueness – “living fossils”
– Why conserve the Tuatara?
• How best to breed in captivity?
– Are there rules?
• Where to locate reserves?
– Centers of endemism & biodiversity hotspots
• Forensics
– Where did that whale meat come from?
• Grizzly Bear – demographic monitoring
• Cheetahs
– Why undescended testicles & deformed sperm?
Genetic concerns under captivity?
• Issue: Do small captive populations lose genetic
variation over time? How much?
• Happens because of  inbreeding, small Ne, and
artificial selection
• Geneticists can provide guidelines - take
advantage of genetic planning
Rules for Captive Breeding
1. Minimize the loss of genetic variation
2. Maximize demographic viability
3. Minimize (artificial) selection
Should we intentially inbreed to purge inbreeding
depression?
RESULTS
Forensics??
Minke
(Antarctica)
Minke
(Australia)
Unknown #1a,
2, 3, 4, 5, 6, 7, 8
Minke
(North Atlantic)
Unknown #9
Humpback
(North Atlantic)
Humpback
(North Pacific)
Unknown #1b
Gray
Blue
(North Atlantic)
Blue
(North Pacific)
Steve Palumbi
Unknown #10,
11, 12
Unknown #13
Fin
(Mediterranean)
Fin (Iceland)
Genetic
Forensics
Where did
your sushi
/whale meat
come from?
Trimming Twigs on the Tree of Life
Don Waller
University of Wisconsin
Madison, Wisconsin USA
http://www.tolweb.org/tree/
Which twigs are being pruned?
In broad terms, we are losing just what one would
expect:
– Big, wide-ranging Things – the Big Things that run
the world
– Habitat specialists
– Rare species
– Local endemics
– K-selected species
Are we reducing
the Tree of Life
to bansai form?
Trading Twigs
Are some twigs more important than others?
Which evolutionary contexts are being lost or altered?
Do bigger /basal branches deserve
more protection?
(Recent work suggests that Tuatara have actually
changed significantly in form since the Mesozoic)
Tuatara
Why conserve the
Tuatara?
Sphenodon – endemic to
New Zealand
All by itself
F. Allendorf
‘Living Fossil’
 Only species in this Genus, Family, and Order (!)
The extinction “vortex”
•
•
•
•
•
Loss of habitat and fragmentation leads to
Declines in population size and isolation
leads to inbreeding and smaller colony size
leads to reductions in reproductive success
leads to
'vicious cycle' = positive feedback
Threats multiply and interact
Summary
1. Humans are now causing the 6th greatest wave
of extinction of all time.
2. Agriculture, development, and resource use are
massively reducing and fragmenting habitats.
3. Rare, local (endemic), specialized, and big
species are more prone to extinction.
These commonly occur in the tropics.
4. Habitat loss & fragmentation reduce population
size and increase genetic isolation
5. Small isolated populations lose molecular and
quantitative genetic variation and drift more.
Summary
6. Reduced genetic variation and increased drift
limit the ability of small and isolated populations
to adapt to changing environments.
7. Drift and inbreeding increase the expression of
recessive deleterious mutations, causing
inbreeding depression.
8. Inbreeding effects accumulate over generations.
9. Population-level fixation and inbreeding can
depress fitness even when crosses within inbred
populations reveal no inbreeding effects.
We can expose such effects by crossing a small
population with a big one – allowing “genetic rescue”
Summary
10.Small asexual and inbred populations are also
subject to mutational meltdown – a long-term
threat.
11.Ecological and genetic forces are rarely
independent and can interact to create an
“extinction vortex.”
12.We also use genetic techniques to monitor
exploited populations and species (forensics).
13.We are learning more about genetic threats and
how to use genetic markers to diagnose and
monitor these threats
But this has not yet become routine . .
10 Key genetic issues
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
Effective population size - Ne
Inbreeding (F) and inbreeding depression ()
Out-breeding depression
Accumulation of deleterious mutations (U)
What maintains genetic variation?
Genetic deterioration in captivity
Genetic diversity and extinction
Minimum viable population size
Measuring differences among populations
Relative importance of these genetic issues