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Genetic
Variation
and
the
Natural
History
of
Quaking
Aspen
The
ways
in
which
aspen
reproduces
underlie its
great geographic
range, high
levels
of
genetic variability,
and
persistence
Jeffry
B. Mitton and Michael C. Grant
In
the
fall,
sightseers
take to the
highways
of North America to
enjoy
the brilliant colors that are
revealed as deciduous trees
recycle
the
dominant
greens
of
chlorophyll.
In
the western
United States and
Canada,
the
most colorful tree
in
the fall is the
quaking
aspen,
Pop-
ulus tremuloides.
Brilliant
yellows,
rich
golds,
and
shimmering
shades
of
red
shine,
contrasting
with the
various
green
shades
of the conifers.
Quaking aspen
earns its
name for
the distinctive
fluttering
of
its
leaves,
even
in
the
most
gentle
breezes.
Early
French-Canadian
trappers
called
the
tree
an
aspen
because
of
its similar-
ity
to
Populus
tremula,
a
closely
related
species
in
Europe
and
Asia.
One
of
the
legends
attached to
the
aspen
reflects
Judeo-Christian
in-
fluences.
The
aspen quake
in
fear
today,
according
to
folklore,
because
Jesus
Christ was crucified
on
a
cross
of
aspen.
In
addition
to the esthetics
of
quaking
leaves
and
brilliant fall
colors,
extraordinary
features
of
the
natural
history
and
genetics
of as-
pen
lend
it
special appeal
for
natu-
ralists and
laboratory
scientists.
Quaking aspen
merits
a
variety
of
superlatives:
It is
North America's
most
widely
distributed
native
tree
species
and the second
most
widely
distributed
in the world
(Barnes
and
Jeffry
B. Mitton and
Michael
C. Grant
are
professors
in the
Department
of
Environmental,
Population,
and
Organ-
ismic
Biology
at the
University
of Colo-
rado,
Boulder,
CO
80309.
?
1996
American Institute
of
Biological
Sci-
ences.
The most
massive
known
organism,
the
6-million-kilogram
quaking
aspen
clone we
call
Pando,
highlights
remarkable
features of
the
species
Han
1993,
Jones
1985).
The world's
most
massive individual
organism
is
a
quaking
aspen
(Grant
et al.
1992).
Individuals
may
reach
ages
in
excess
of
1
million
years
(Barnes
1966,
Grant
1993,
Kemperman
and
Barnes
1976).
And
quaking aspen
may
also
be
the most
genetically
variable
plant
species
studied
to date
(Cheliak
and
Dancik
1982).
Quaking
aspen
is an
intriguingly
multifaceted
species,
varying
from a
twisted
dwarf
bush with
a
height
of
less than
1 m
to
straight
stems reach-
ing
30
m
tall
and 60
cm
in
diameter.
Although
aspen
commonly
exists
as
an
early
successional
species,
sprout-
ing profusely
after a
fire
or an ava-
lanche,
it is
a climax
species
in
some
environments.
Broad
geographic
and
environmental
range
Quaking
aspen
can be
found
from
the
mountains
of
Mexico to
north-
ern
Alaska,
from the
Atlantic to
the
Pacific
(Figure
1),
from sea
level
to
3700
m. It thrives
in a
variety
of
plant
communities,
especially
those
subject
to
major
disturbances,
from
the
spruce-fir
forests
of the
Rocky
Mountains to the deciduous
forests
of New
England.
In
the eastern
and
central
parts
of North
America,
as-
pen
tends to
be distributed
nearly
continuously, occurring
in
many
different
plant
associations
(Graham
1963).
In the much more
arid
West,
aspen
tends to
be restricted
to
high
plateaus
and mountain
sides.
At the
lower
limit of its
elevational
range
(approximately
2200
m in
the
Rocky
Mountains
of
Colorado),
aspen
oc-
casionally
grows
on
north-facing
slopes
with
ponderosa
pine,
Pinus
ponderosa,
and
Douglas-fir,
Pseudo-
tsuga
menziesii.
More
commonly,
aspen
grows
in the
lodgepole
pine,
Pinus
contorta,
elevational
range.
At the
highest
elevations,
aspen
is
observed
in
scattered
stands
within
spruce-fir
forests
of
Engelmann
spruce,
Picea
engelmannii,
and
sub-
alpine
fir,
Abies
lasiocarpa.
In rare
locations
(e.g.,
at the
University
of
Colorado's
Mountain
Research
Sta-
tion
in the Front
Range),
aspen grows
at
tree
line
(elevation
of 3600
m)
in
association
with stunted
Engelmann
spruce,
subalpine
fir,
and
limber
pine,
Pinus
flexilis.
The
aspens
at
this elevation
are
short,
being
twisted
and
pruned
by
winter
winds.
Life
history
The
quaking
aspen
is a
member
of
the willow
family
(Salicaceae)
and
is
closely
related
to
various
poplars
such
as
cottonwoods.
One
other
as-
January
1996
25
QUAKING
ASPEN
e.
Fruiting
branchlet,
x
1/2.
BIGTOOTH
ASPEN
Figure
1.
Morphological
detail and
distributions of
quaking aspen (Populus
tremuloides)
and
biotooth
aspen (Populus
grandidentata).
From Preston 1976.
pen species
is found
in
North
America,
the
bigtooth aspen, Pop-
ulus
grandidentata.
As
the
name
implies,
the leaf
margins
of these
trees show
regular, easily
recogniz-
able serrations
in
contrast to the
finely
dentate,
nearly
smooth leaf
margins
of P.
tremuloides
(Figures
1 and
2).
Aspen
flowers
are
small,
relatively inconspicuous
and
pro-
duced
in
strings
called catkins. The
entire
flowering sequence,
includ-
ing
seed
maturation,
is
completed
in
the
early
spring
before the tree leafs
out.
In
the Front
Range
of Colo-
rado,
we have observed
that most
females
produce
seeds each
year.
Seed
production
appears
to be
positively
correlated with
age
and
size of the
stem. Old
stems
have
been
known to
produce
54 million
seeds
in
a
single
season
(Schopmeyer
1974),
and seed
viability
generally
exceeds
90%
in
Colorado.1 The
mature seeds are
widely
scattered as
self-contained,
windblown
dispersal
units with the
easily
observed
para-
chute-like
structures that
give
the
related cottonwoods their
common
name.
Their
ability
to
reproduce
1MC
Grant,
unpublished
data.
sexually
(via
seeds)
partly
underlies
the
remarkable
levels of
genetic
vari-
ability
in
this
species.
Despite
enormous
crops
of viable
seeds,
successful
seedling
establish-
ment
appears
to be a rare event
in
the semiarid
West
(Kemperman
and
Barnes
1976,
Romme
1982,
Romme
and
Despain
1989),
but the estab-
lishment
of new trees from seeds
appears
to be common
in
the
moist,
humid
forests of New
England.
Al-
though
most of
the seeds shed
by
aspen
are
capable
of
germinating,
several
factors,
singly
and
in
combi-
nation,
dramatically
limit success-
ful
establishment.
In
fact,
many
botanists
argue
that
widespread
quaking
aspen
establishment from
seeds
probably
has not occurred
in
the western
United States
since the
last
glaciation,
some
10,000
years
ago
(Einspahr
and Winton
1976,
McDonough
1985),
although
some
local
patches
have
certainly
arisen
more
recently.
In
these
regions,
the
seedlings usually
wither and die be-
fore their roots
reach
an abundant
and reliable source of
water,
or
they
do not
receive
adequate sunlight.
In
addition,
aspen seedling
establish-
ment
can be
dramatically
reduced
by
ungulate browsing
(Beetle 1974,
Olmstead
1979).
The
availability
of
sites suitable
for new
colonization,
particularly following
fires
(DeByle
and Winokur
1985,
Jelinski
and
Cheliak
1992,
Jones
1974,
Kay
1993),
plays
a
major
role
in
deter-
mining seedling
establishment.
At
present,
we know of no
direct
way
to test the
hypothesis
that the
majority
of the
quaking aspen
indi-
viduals
in
the
Rocky
Mountains were
established several thousand
years
ago,
when those environments were
substantially
wetter than
they
are
today.
However,
we do
now have
clear evidence
of one
major
distur-
bance
in
the
Rocky
Mountains that
has
produced
thousands of
new as-
pen seedlings-the
1988 fire
in
Yel-
lowstone National Park.
Following
the severe fire of 1988
(Kay
1993,
Turner and
Romme
1994),
large
regions
of
Yellowstone
were suc-
cessfully
colonized
by young
seed-
lings
in
regions previously
devoid of
aspen. Apparently,
the last
previous
episode
of this scale
occurred
nearly
300
years ago
(Romme
1982,
Romme and
Despain
1989).
Al-
BioScience
Vol.
46 No.
1
26
ct
et
though
these
episodes
qualify
as rare
on a
human time
scale,
they
are
sufficiently frequent
to influence the
ecological
genetics
of
quaking
as-
pen
(Jelinski
and Cheliak
1992).
If
seedling
success is so
rare,
why
are
aspen
so abundant
and
widespread
in
the
semiarid West?
One
impor-
tant answer
to this
question
lies
in
aspen's
ability
to
reproduce
asexu-
ally.
Asexual
reproduction
Unusual,
but not
unique among
for-
est tree
species, quaking
aspen
regu-
larly reproduces
via a
process
called
suckering.
An
individual
stem can
send
out lateral
roots
that,
under
the
right
conditions,
send
up
other
erect
stems;
from all
aboveground
appearances
the new stems look
just
like individual trees.
The
process
is
repeated
until
a whole
stand,
of what
appear
to be individual
trees,
forms.
This collection
of
multiple
stems,
called
ramets,
all form
one
single,
genetic
individual,
usually
termed
a
clone. Observers
usually
fail to
ap-
preciate
the critical
underground
portion
of the
aspen
clone
respon-
sible for asexual
reproduction-the
root
system.
A
search
through
a
lodgepole pine
or
spruce-fir
forest
may
detect
just
a
few,
widely spaced, suppressed
stems
of
aspen
beneath a dense
canopy
of
conifers.
But when a fire
or
an ava-
lanche clears
out the
standing crop
of
conifers,
the
true
expanse
of the
aspen
root
system
may
be revealed
by
a
vigorous production
of abun-
dant
new ramets
throughout
the dis-
turbed
area,
testimony
that the root
system
cannot
be assessed
by simply
counting aboveground
stems.
Persistent root
systems
allow as-
pen
to
colonize,
occupy,
and even
prefer
disturbed
sites,
justifying
their
general
characterization as an
early
successional
species.
After a fire
has
removed the
conifers,
the ramets
that
sprout
from a
healthy,
mature
root
system may grow vertically
as
much as a meter
in
a
single
summer
season
(Bailey
et al.
1990,
Crouch
1981),
while the
density
of new
shoots
may
exceed
400,000
per
acre
(Schier
et al.
1985).
The root
system
of
aspen grows aggressively;
adja-
cent stems can be
spaced
more than
30
m
apart
(DeByle
and Winokur
Figure
2. A
close-up
of
quaking
aspen
leaves.
1985).
During spring
growth
and
when stems have
been
damaged (e.g.,
by
fire),
the
hormonal
suppression
of root
suckering
diminishes,
and
many
new stems
may
be
produced
from the
relatively
undamaged
roots.
At the
same
time,
aspen
clones tend
to be intolerant
of shade
(Jones
and
DeByle
1985)
and
typically
succumb
to succession
by
conifer
species
in
a
few hundred
years
if
left undisturbed
(e.g.,
by
fire,
avalanche,
mud
slide,
or
logging).
Quaking
aspen
clone and stand
size influence
the
biology
of several
associated
species.
For
example,
the
species
diversity
of insectivorous
birds increases
with the size of
as-
pen
stands
(Johns
1993).
Immense and ancient
The
quaking
aspen
has demonstrated
a remarkable
ability
to
spread
and
persist
in
a
given
location
via the
process
of root
suckering.
In
the
most
spectacular
example
for
which
detailed
information
is available
(Barnes
1966,
Kemperman
and
Barnes
1976),
the
clonal
growth
of a
single quaking aspen
clone covers
43 hectares and contains
more than
47,000
individual
stems-a sizable
forest
in
and
of itself.
Largely
in
response
to the attention
given
to a
giant fungus,
Armillaria
bulbosa,
in
a
Michigan
forest
(Gould
1992,
Smith et al.
1992),
we resurrected
the data
on this enormous
aspen
clone
showing
it to
be,
by
far,
the
most massive
living
organism
known,
weighing
more than
6
mil-
lion
kg
(Grant
et
al.
1992).
This
mass
(estimated
for both
above- and
belowground parts)
more
than
triples
that of its
nearest
rival,
the
giant
sequoia
(Sequoiadendron
giganteum)
named General Sherman.
We have nicknamed the
giant
as-
pen
clone Pando
(Grant
1993),
a
Latin
word
meaning
I
spread.
Pando,
an
exceptionally
beautiful
male
clone,
is located
in
the
Wasatch
Mountains
of south-central
Utah,
straddling
the
highway
to Fish
Lake
(Figure
4).
The
spectacular
size of
this clone
appears
to
reflect a rare
balance of
the
frequency
and
inten-
sity
of environmental
disturbances,
particularly
fire,
that
encourages
the
persistence
of
quaking aspen.
The
fire
frequency
has been sufficient
to
prevent
conifer
succession,
yet
the
local environment
has
been stable
enough
to allow
healthy,
vigorous
growth
and asexual
reproduction
for
perhaps
1
million
years.
Over the last several
decades,
space
for
a US Forest Service
camp-
ground
and
several
privately
owned
cabins has been
cut
out
of this
natu-
ral
wonder. We are concerned
that
this
colonization of
Pando
by
hu-
mans
dramatically
reduces the
like-
lihood of
periodic cleansing
by
natu-
ral fires. These
changes
may
mark
the
beginning
of
the end for Pando.
The true
age
of
aspen
clones
at
present
can
only
be inferred
from
indirect means
and,
therefore,
re-
mains
something
of a
mystery.
While
the
age
of
most
temperate
forest
trees can
be estimated
by
counting
the
annual
rings
in
a
core extracted
from the
trunk,
cores
extracted from
an
aspen
stem mark the
age
of that
ramet,
not the
age
of the clone.
In
a
study
of
aspen
in
the Front
Range,
we selected
and cored
five
of the
largest
ramets from
each of 104
clones. The
average age
was 65
years;
the
oldest ramets
were
approxi-
mately
120
years
old.
But
biologists
most familiar
with
natural
aspen
dynamics propose
that
these
western
clones are
ancient,
perhaps
on the order
of
10,000
years
(Kemperman
and
Barnes
1976),
and
conceivably
as much
as
1 million
January
1996
27
Figure
3.
A clone of
aspens
in
winter.
years
(Barnes
1966, 1975),
and
po-
tentially
immortal.
Part of the ratio-
nale behind current
age
estimates
for
aspen
clones is that sexual re-
production
is
effectively
frustrated
by
the
rarity
of a favorable
suite of
conditions
in
semiarid environ-
ments. Clonal
age,
in
the strictest
sense,
truly applies only
to the
indi-
vidual
genome,
which is the
single
element of
clone
identity
that
would
be continuous
across such time
spans.
No
physical
tissue such
as
root
or stem or leaf
presently
in
existence would have been
in
exist-
ence
from
the
original seedling.
Per-
haps
DNA
sequence
data
from
vari-
ous
parts
of a clone could be used
to
estimate
age
from the accumulation
of mutations.
Surely
somatic muta-
tion
(Keim
et al.
1989)
would have
occurred
frequently enough
that dif-
ferent areas
of the clone would re-
tain different mutations.
Extreme
longevity
is not limited
to
aspen,
but it
appears
to be a
common
attribute of clonal
species.
In a
survey
of clonal
plants,
Cook
(1983)
listed bracken fern
(Pterid-
ium
aquilinum),
red fescue
(Festuca
rubra),
sheep
fescue
(Festuca
ovina),
and velvet
grass
(Holcus
mollis)
all
as
having
clones older than 1000
years.
Aspen
is listed as
having
clones
in
excess of
10,000
years
of
age,
while
creosote bush
(Larrea
trid-
entata)
and
huckleberry
(Gay-
lussacia
brachycerium)
are credited
with
ages
in
excess of
11,000
years
and
13,000
years, respectively.
Patterns of sex ratio
Individual
clones of
quaking
aspen
are either male or female
(i.e.,
dioe-
cious),
in
contrast
to the much more
common situation
in
which
indi-
vidual
forest
trees
produce
both
ovules and
pollen.
This
separation
of sexes
among
different
individu-
als,
the
standard
in
vertebrates,
leads
to some
interesting patterns
in
plants.
For
example,
sex
ratio varies
with environmental conditions
in
several dioecious
species;
male indi-
viduals
generally predominate
in
environments
imposing
moisture
stress while females tend
to
pre-
dominate
in
moist areas
(Freeman
et
al.
1976).
The sex ratio of
aspen
may vary
among
environments.
In
particular,
males and females show
dramati-
cally
different
distributions
along
elevational
gradients
in
the
Rocky
Mountains.
At low elevations
in
the
Front
Range,
females are
more com-
mon
than males. However,
the
pro-
portion
of females
declines with el-
evation,
and above 3200
m,
more
than 90% are male
(Grant
and
Mitton
1979).
The mode
of sex-
determination
remains
a
mystery,
but it
seems
that the
primary
ratio is
1:1
(Grant
and Mitton
1979). If,
as
our observations
indicate,
sex
is
determined
strictly by
a
genetic
mechanism,
then these observed
gra-
dients
in sex ratio
necessarily
derive
from differential
establishment and
survival. Differential
establishment,
survival,
and
growth
can be best
demonstrated
by
studies of
genetic
variation.
Genetic variation
Genetic
variation
in
and
among
populations
has been measured
most
commonly
with
electrophoretic
sur-
veys
of
protein
variation.
Proteins
from leaves or buds are
separated
by
size and
charge
in
a starch
gel
sub-
jected
to an electric
current.
Genetic
variation is revealed
as different rates
of
migration
of
proteins
through
the
gel,
and the
pattern
of the
proteins
on
the
gel
reveals the
genotypes.
Quaking aspen
is a
diploid spe-
cies
and, therefore,
has
two
genes,
or
alleles,
coding
for each
protein;
heterozygotes
have two
different
alleles,
and
homozygotes
have
two
identical
alleles. The level of
genetic
variation
in
a
population
is
usually
presented
as
the
average heterozy-
gosity,
H,
for the
proteins
in
the
survey.
The distribution
of the
geno-
types
in a
population
is
compared
with the distribution
expected
in
a
large,
randomly mating population,
at
equilibrium,
undisturbed
by
natu-
ral selection. The
deviation of a
ge-
notypic
distribution
from
the ex-
pected
distribution is
measured with
the
inbreeding
coefficient, F,
which
varies
from -1.0 to 1.0.
A
perfect
fit
to the
expected
distribution of
geno-
types produces
a value
F
of
0.0,
while values
of
-1.0
and 1.0
indicate
extreme
excesses and deficiencies
of
heterozygotes, respectively.
Population genetics
theory
pre-
dicts
that
genetic
variation
main-
tained
by
a
species
will increase
with
the environmental
variation
experi-
enced
by
a
species,
with
its
popula-
tion
size,
and
with the size of
the
geographic
range.
All
of
these vari-
ables
predict
high
genetic
variation
for
quaking
aspen,
and
the
predic-
tion is accurate.
Quaking aspen
ap-
pears
to be the most
genetically
vari-
able
species
of
plant
investigated
to
date.
An
electrophoretic
survey
of
pro-
tein
variation
revealed that
more
than 90%
of the
enzymes
analyzed
were
genetically
variable
(Cheliak
and Dancik
1982),
in
comparison
with the
average
of
50%
for
all
plant
species
that have been
ana-
lyzed
(Hamrick
and
Godt
1989).
Surveys
of
DNA
markers
are consis-
tent with the
survey
of
proteins,
indicating high
levels of
genetic
variation
(Chong
et al.
1994,
in
press,
Liu and
Furnier
1993a,
b,
Rogstad
et al.
1991).
Of
the
aspen
measured,
those
in
Alberta,
Canada,
have
the
highest
levels of
genetic
variation
and
large
BioScience Vol. 46
No.
1
28
.3
*-i
excesses of
heterozygotes
(Cheliak
and Dancik
1982).
Genetic varia-
tion at
26
polymorphic enzyme
loci
was studied
in 222
clones
sampled
from seven localities
in
Alberta. The
observed
proportion
of
heterozy-
gotes
exceeded
the
expected pro-
portions
in
every
one of the
sample
localities. The
average heterozygos-
ity
of
clones
was
expected
to be
42%,
but the observed
heterozygos-
ity
was 52%.
The
inbreeding
coeffi-
cient from this
survey
was
F
=
-0.24,
indicating
a
substantial excess
of
heterozygotes. Similarly,
excesses of
heterozygotes
were observed
in
a
survey
of six
prairie
and
montane
populations
in
Waterton Lakes Na-
tional
Park,
Alberta
(F
=
-0.10;
Jelinski
and Cheliak
1992).
In
contrast to the studies in
Alberta,
substantially
lower levels
of
genetic
variation were
reported
in
electrophoretic surveys
of
aspen
in
Minnesota
(H
=
22%;
Lund et al.
1992)
and
Ontario
(H
=
25%;
Hyun
et al.
1987).
Observed
genotypic
proportions
fit
expected
levels
in
Minnesota
(Lund
et al.
1992)
and
Colorado
(Mitton
and Grant
1980),
but a
strong
deficiency
of
heterozy-
gotes
was
reported
for the
popula-
tions
in
Ontario
(F
=
0.46;
Hyun
etv
al.
1987).
The level of
genetic
variation in
populations
of
aspen
varies with the
environmental
conditions.
High
lev-
els of
genetic
variation and
excesses
of
heterozygotes
are
found
in
semi-
arid
environments,
while much less
genetic
variation and
deficiencies of
heterozygotes
are found
in
the rela-
tively
moist eastern forests.
We
hypothesize
that these
re-
gional
differences
in
genetic
varia-
tion
reflect
the
aridity
of
the cli-
mate,
the
propensity
for clonal
reproduction,
the
longevity
of
the
clones,
and the
predominant
modes
of
natural selection. Clonal
repro-
duction is
more common
in
arid
environments,
and clones
may
be-
come
larger
and older
in
more arid
climates
(Barnes
1966,
Kemperman
and Barnes
1976).
Heterozygotes
often exhibit
superior longevity
in
forest
trees
(Mitton
and
Jeffers
1989),
and the extreme
ages
of
clones
may amplify
the
advantages
of het-
erozygotes.
Natural selection favor-
ing
heterozygous genotypes
main-
tains
high
levels of
genetic
variation.
Figure
4. Some of the
beautiful
silvery-white
trunks of
Pando,
the
giant aspen
clone.
Given that
high
levels of
genetic
variation and excesses of
heterozy-
gosity
in
aspen
are
associated with
environmental
variation,
we would
expect
the
frequencies
of alleles also
to
vary
among
environments. Gen-
eral
support
for this
hypothesis
is
found
in
the
study
of
genetic
varia-
tion
in
156 clones
in
six
natural
populations
in
ecologically
diverse
habitats
in
Waterton Lakes National
Park
(Jelinski
and
Cheliak
1992).
These
populations
were
chosen for
their
environmental
range-some
are situated on the
prairie,
others
are montane.
Although
the
popula-
tions
were,
on
average, only
6.7
km
distant from one
another,
substan-
tial
genetic
differentiation
in
allelic
frequencies
was observed
among
populations.
If
the differentiation
among populations
is
produced
by
natural
selection,
we should be able
to measure
differences
among geno-
types
in
some trait or set
of
traits,
such as survival or
growth
rate,
that
directly
influences clonal fitness.
Growth rate
The
growth
rate of
aspen
is inti-
mately
tied to
its environment
(Grant
and Mitton
1979,
Jelinski
1993).
Ideally,
one would measure
growth
of entire clones
by measuring
their
biomass
including
the extensive root
systems,
but this
approach
is
not
feasible.
Pragmatically,
one measure
of
growth
rate
of
aspen
can be taken
from the annual increment
in
the
radius of a stem.
Traditionally,
for-
esters
removed
a
core
from a tree
and counted the
rings
to estimate
age
and to measure the
widths
of
annual
rings
to estimate
growth
rate
and
the
variability
of
growth
rate.
One
study
in
Waterton Lakes Na-
tional Park
used
multiple
regression
to
predict
growth
rates of
aspen
as a
function of
elevation,
slope
posi-
tion,
age,
and
exposure
to the wind
(Jelinski
and
Cheliak
1992).
This
study
revealed that
growth
rate
of
aspen
declines with
elevation,
steep-
ness
of the
slope, age
of the
ramet,
and
exposure
to
wind. These
vari-
ables
explained
56%
of the varia-
tion
among
individuals
(Jelinski
1993).
Similarly,
a
study
of
104
clones in the
Front
Range
revealed
that
growth
rate decreased dramati-
cally
with elevation
(Grant
and
Mitton
1979).
The
growth
rate of
aspen
also
differs
between the sexes.
In
an
elevational transect that
ranged
from
below 1900
m
to above 3000
m in
the Front
Range,
the
growth
rates of
both males and females declined with
elevation
(Grant
and Mitton
1979).
At all
elevations,
the
growth
rate
of
females
surpassed
that of males
by
approximately
12%. Sakai and
Burris
(1985)
compared
measure-
January
1996
29
ments taken
in
1956 and 1981
to
study
the
growth
of 23 clones of
quaking aspen growing
in
field
tri-
als
in
lower
Michigan.
This com-
parison
did not reveal
any
differ-
ence between the sexes of
the
average
annual
ring
width,
but the
growth
of the clones differed. Over the
25
years
of this
study,
the area
occu-
pied
by
female clones increased
by
292%,
while
the area
of male
clones
increased
by only
219%. The basal
area of females
(area
covered
by
the
ramets at
ground
level)
and the
num-
ber of ramets
(205
for
females,
129
for
males)
also exceeded those
in
males.
A
study
of
growth
in male
and
female
clones of
bigtooth aspen
re-
vealed trends consistent
with
the
differences found
in
quaking
aspen
(Sakai
and Sharik
1988).
Seven male
and seven female clones were
mea-
sured
for
size,
number
of
ramets,
and basal
area at the
University
of
Michigan Biological
Station near
Hickory
Corners. The researchers
reported
that the area
of female
clones was 41%
greater
than
males,
the number of
female ramets 52%
greater,
and the basal area
of fe-
males 56%
greater.
Furthermore,
over a
29-year period
between
mea-
surements,
the increase
in
female
clonal area
was 23%
greater
than
in
males,
and the increase
in
female
basal
area
was
32%
greater
than
in
males
(Sakai
and Sharik
1988).
These studies
of
sex-dependent
growth
rates
revealed
consistent
growth
advantages
of females
over
males,
data
apparently
inconsistent
with the
widely
held
notion that
higher
energetic
investment
by
fe-
males
in
sexual
reproduction
reduces
their
growth
rates.
Furthermore,
the
superior
growth
rate
of females
at
all
elevations
appears
to be incon-
sistent
with the
strong predominance
of
males seen
at
higher
elevations.
However,
the actual
energy
expen-
ditures
of
female clones
versus
male
clones
have
yet
to be measured.
At least
some of
the
variation
in
growth
rates
among
clones
is influ-
enced
by
genetic
variation,
because
two studies
of
growth
rate
have re-
ported
the
radial
growth
of ramets
to increase
with
enzyme
heterozy-
gosity.
The first
of these studies
ex-
amined
104
clones
in
the
Front
Range
(Mitton
and Grant
1980).
Cores were taken from five of
the
largest
ramets
in
each
clone,
and the
genotype
of each clone was identi-
fied at three
genes coding
for en-
zymes.
Growth rate decreased
with
elevation and with the
age
of
the
ramet,
but it increased
with het-
erozygosity.
Similar results were
obtained
in
a
study
of
growth
rates
of
aspen
in
Waterton Lakes
Na-
tional Park
(Jelinski
1993).
From
each of 156
clones,
cores
were ex-
tracted
from five
of the
largest
ramets,
and
genotypes
were identi-
fied at
14
polymorphic
enzyme
loci.
The
growth
rates
of the most het-
erozygous
clones
were
approxi-
mately
35%
higher
than those of the
most
homozygous
clones.
Although
population
geneticists
have
usually presumed
genes coding
for
enzymes
to be a random
sample
of the
genome,
this
assumption
may
not be correct
for all
genes,
in
all
species,
under all
environmental
conditions.
Enzymes catalyze
meta-
bolic
reactions,
and
genetic
varia-
tion of
a
few
enzymes
has been
dem-
onstrated
to influence
flux
through
known metabolic
pathways
(Koehn
et al.
1983,
Powers et al.
1993).
Consequently,
this
genetic
variation
might
be related to
differences
in
physiology,
growth,
and survival
among
genotypes.
Currently, geneticists
debate
whether
protein
polymorphisms
contribute
directly
to
differences
in
physiology
and
life
history
or
whether
they
are
neutral
genetic
markers that
detect differences
in
performance
attributable
to
other
loci
(Mitton
and Grant
1984).
If
enzyme
polymorphisms
are
simply
convenient,
neutral
markers,
then
any genetic
marker
should
reveal
the associations
with fitness
that
have been
reported
for
protein
poly-
morphisms.
But
if
the
associations
are attributable
to biochemical
dif-
ferences
among protein
genotypes,
then
heterozygosity
at a different
set of
genetic
markers,
such
as
DNA
markers
in the form of
restriction
fragment
length polymorphisms
(RFLP)
or variable
numbers
of tan-
dem
repeats
(VNTR),
should
not be
correlated
with
components
of
fit-
ness.
Even
looking
beyond
the
quaking
aspen,
we
know of
only
one
study
that used
both
protein
genetic
varia-
tion
and
DNA
markers to determine
whether correlations
with
fitness are
found
with
both sets of markers.
Pogson
and Zouros
(1994)
employed
this rationale
in
a
study
of the
scal-
lop,
Placopecten
magellanicus.
Shell
height
was used to estimate
growth
rate,
and
heterozygosity
was esti-
mated with
genes coding
for seven
enzymes
and
eight
DNA markers.
The
correlation
between
heterozy-
gosity
at the
enzymes
and shell
height
was
positive
and
significant,
while
the correlation
between
the
DNA
markers and
shell
height
was
not
significantly
different
from
zero. At
the
least,
we
can conclude
that
genes
coding
for
enzymes
and
DNA
mark-
ers
provided
different
insights
into
fitness
differentials
in
this
popula-
tion.
More
strongly,
we
conjecture
that
enzymes
themselves
periodically
fall under
the direct
influence
of
natural selection.
Conclusions
The extreme
size
and,
perhaps,
age
of the
clone we called
Pando
serves
to
highlight
some of the
remarkable
features
of the beautiful
forest tree
species,
quaking
aspen.
Many years
of
ecological genetic
studies
of as-
pen
biology
have
revealed several
general
patterns.
The
ability
for as-
pen
to
reproduce
and
disperse
via
seeds,
even
if
such
reproduction
and
dispersal
only
occurs
on
a wide-
spread
basis on
intervals
of
several
hundred
or several thousand
years,
clearly
underlies
its
great geographic
range
and
its
remarkably high
levels
of interclonal
genetic
variability.
Further,
aspen's
ability
to
repro-
duce
and
regenerate
asexually
fol-
lowing major
disturbances
contrib-
utes
to
its
ability
to
persist
in a
given
region
for
long periods
of
time.
This
same
vegetative
capability
also
con-
tributes
to its
ability
to
persist
across
long spans
of
time when
circum-
stances
are not
favorable
for seed-
ling
establishment.
The
ability
to
span
both
spatial
and
temporal
en-
vironmental
heterogeneity
is a
criti-
cal
characteristic
of
this extraordi-
nary species.
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