Genetic Engineering of Trees Enhance Resistance to Insects

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Dec 10, 2012 (4 years and 9 months ago)

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Genetic
Engineering
of
Trees
to
Enhance
Resistance
to
Insects
Evaluating
the
risks
of
biotype
evolution
and
secondary
pest
outbreak
Kenneth
F.
Raffa
ontrol
of
insect
pests
has
of-
ten
been
suggested
as
a
prom-
ising
use
of
the
emerging
gene-insertion
technology.
The
most
commonly
proposed
strategies
would
improve
microbial
pathogens
of
in-
sects,
incorporate
defects
into
pest
populations,
and
transfer
genes
that
encode
for
insect-resistance
proper-
ties
into
plants.
Although
some
ad-
vantages
and
risks
of
these
strategies
have
been
discussed
in
general
terms,
there
is
little
conceptual
framework
for
applying
theoretical
principles
to
specific
policy
decisions
(Simonsen
and
Levin
1988).
In
this
article,
I
develop
an
approach
to
estimating
risk
by
concentrating
on
one
strate-
gy-genetic
transfer
of
resistance
properties
into
otherwise
susceptible
hosts
(Vaeck
et
al.
1987)-in
one
commodity
frequently
cited
as
a
ben-
eficiary
of
biotechnology-wood
products
(Dandekar
et
al.
1987,
Far-
num
et
al.
1983,
Sederoff
and
Ledig
1985).
Such
an
approach
should
im-
prove
our
ability
to
evaluate
and
reduce
the
potential
for
inadvertent
deleterious
alteration
of
forest
ecosys-
tems.
It
may
serve
as
a
model
for
other
transgenic
applications.
I
focus
on
one
potential
danger,
biotype
evolution,
which
is
the
selec-
tion
for
insect
populations
that
can
tolerate
the
new
resistance
property
(Gould
1988).
I
do
not
consider
here
Kenneth
F.
Raffa
is
an
associate
professor
in
the
Entomology
and
Forestry
Depart-
ments
at
the
University
of
Wisconsin,
Madison,
53706.
His
research
focuses
on
tree-insect
interactions.
?
1989
American
Institute
of
Biological
Sciences.
In
general,
the
risks
are
greatest
in
large
forested
expanses
the
impact
of
reduced
insect
popula-
tions
on
wildlife
and
nutrient
cycling,
problematic
escaped
plant
material,
and
the
great
value
of
these
technol-
ogies
as
research
tools.
Rationale
for
genetic
enhancement
of
tree
resistance
Much
of
the
impetus
for
transferring
foreign
genes
into
trees
arises
from
the
unsuitability
of
traditional
pest
control
tactics.
For
example,
use
of
insecticides,
a
staple
of
insect
control
in
many
annual
crops,
is
limited
in
forestry,
where
it
is
often
infeasible,
ineffective,
or
environmentally
unac-
ceptable.
Application
costs
can
be
high
because
forests
occur
in
im-
mense,
often
inaccessible
tracts;
trees
require
a
large
amount
of
vertical
coverage;
and
protection
must
extend
over
many
growing
seasons,
rather
than
just
one.
Moreover,
forests
are
often
intended
for
multiple
uses
such
as
recreation,
watershed
manage-
ment,
and
grazing,
in
addition
to
wood
production.
Most
forest
insect
management
programs
are
based
on
a
combination
of
silvicultural
(stand
density,
rota-
tion
schedule,
species-age
composi-
tion,
and
site
selection)
and
biological
controls.
Although
often
effective,
these
tactics
also
have
limitations.
In
many
cases,
environmentally
sound
and
entomologically
efficacious
rec-
ommendations
cannot
be
adopted
be-
cause
they
are
not
cost
efficient.
Breeding
for
resistance
against
in-
sects
has
not
been
pursued
in
forestry
to
the
same
extent
as
in
agriculture.
Although
heritable
resistance
to
some
pests
has
been
identified,
operational
problems
have
precluded
implemen-
tation.
For
example,
difficulties
asso-
ciated
with
breeding
large
plants,
which
require
long
periods
before
sexual
maturity,
can
be
prohibitive
and
pose
formidable
barriers
to
a
scientist's
career.
Adding
to
this
prob-
lem
is
the
legacy
of
nineteenth-
century
high-grading,
the
cutting
of
only
superior
trees,
which
left
defec-
tive
and
pest-infected
specimens
as
the
genetic
base
of
present
forests
(Barrett
1980).
Genetic
improvement
of
trees,
whether
by
traditional
methods
or
biotechnology,
can
be
highly
compat-
ible
with
silvicultural
and
biological
insect
control
tactics.
The
attractive-
ness
of
using
gene
alteration
to
accel-
erate
tree
improvement
has
also
been
heightened
by
the
conversion
to
more
intensive
tree
management.
When
most
forests
were
relatively
unman-
aged,
insect
feeding
did
not
necessar-
ily
translate
into
commercial
losses
because
companies
simply
purchased
tracts
as
they
matured
rather
than
actively
cultivating
trees.
However,
intensively
managed
plantations,
seed
orchards,
and
energy
farms
comprise
more
sizable
grower
investments.
These
growing
conditions
also
favor
the
survival
and
reproduction
of
some
insects,
just
as
in
agriculture
(Scho-
BioScience
Vol.
39
No.
8
-
524
walter
1985).
The
Technical
Associa-
tion
for
Pulp
and
Paper
Industries
predicted
that
genetically
engineered
pest
resistance
would
provide
the
greatest
improvement
to
be
gained
by
biotechnology
over
current
practices,
with
significant
impact
within
3-5
years
(Stomp
1987).
Genetic
engineering,
however,
could
also
impose
novel
and
unprec-
edented
selective
pressures
on
forest
insect
populations.
The
anticipated
efficiency
and
efficacy,
as
opposed
to
the
practical
limitations
of
insecti-
cides
and
traditional
resistance
breed-
ing,
pose
major
risks
that
have
not
yet
been
addressed
in
forest
ecosystems.
Resistant
insect
biotypes
cause,
at
the
least,
a
loss
of
efficacy
and
product
failure.
However,
some
resistant
bio-
types
could
cause
greater
problems
than
existed
before
the
novel
genes
were
deployed.
Because
trees
serve
as
both
commercial
and
natural
re-
sources,
and
because
naturally
regen-
erating
forests
located
near
planted
stands
comprise
major
terrestrial
eco-
systems,
these
risks
must
be
addressed
before
large-scale
outplantings
can
be
deemed
judicious.
General
principles
of
biotype
evolution
Generally
accepted
principles
have
emerged
from
several
well-established
disciplines,
particularly
the
study
of
pesticide
resistance,
crop
breeding,
and
plant-insect
coevolution,
that
can
be
applied
to
tree
gene
manipulation.
First,
there
is
no
physiological
mode
of
insecticide
action,
if
applied
with
sufficient
intensity,
that
cannot
be
overcome
by
insect
populations.
Syn-
thetic
insecticides
include
a
wide
va-
riety
of
exotic
molecules
that
the
tar-
get
organisms
did
not
previously
encounter
in
their
evolutionary
histo-
ries.
Yet
resistant
races
have
emerged
against
all
of
them,
often
in
manners
that
confer
cross-resistance
to
related,
and
even
unrelated,
chemicals
(Croft
et
al.
1982).
So
one
cannot
argue
that
genetically
engineered
resistance
is
immune
to
counteradapted
biotypes
because
genes
can
be
introduced
from
organisms
unrelated
to
the
host
plant.
The
pattern
and
intensity
of
selec-
tive
pressures,
rather
than
the
actual
mode
of
toxicity,
most
strongly
af-
fects
the
emergence
of
resistant
races
(Brattsten
et
al.
1987,
Tabashnik
and
Red
pine
defoliated
by
Neodiprion
serti-
fer.
Photo
by
David
Hall.
Croft
1982).
Factors
such
as
fre-
quency
of
application,
refugia
among
wild
hosts,
and
persistence
of
addi-
tional
selective
pressures
such
as
nat-
ural
enemies
are
critical.
Coevolu-
tionary
theory
reinforces
this
lesson.
In
natural
ecosystems,
long-lived
trees
maintain
defensive
capacity
against
insects,
despite
the
enormous
differ-
ences
in
their
generation
times,
partly
because
of
the
conflicting
and
varying
selective
pressures
imposed
by
the
ag-
gregate
environment
(Edmunds
and
Alstad
1978,
Fritz
et
al.
1986,
Raffa
and
Berryman
1987,
Whitham
1983).
Second,
there
are
numerous
exam-
ples
in
which
new
or
more
severe
pest
problems
than
occurred
before
treat-
ment
have
arisen
(Forgash
1984).
A
common
sequence
is
reduction
of
the
target
insect's
natural
enemies,
fol-
lowed
by
target
insect
resistance,
fol-
lowed
by
unchecked
damage.
Natural
enemies
usually
evolve
resistance
more
slowly
than
the
target
(Croft
and
Strickler
1983),
and
so
new
pes-
ticides
must
be
employed.
The
result
is
a
classic
pesticide
treadmill.
In-
creased
target-pest
problems
can
also
follow
the
introduction
of
resistant
plant
varieties.
For
example,
adapta-
tions
to
resistant
cultivars
of
a
pre-
ferred
crop
species
can
enhance
a
pest's
ability
to
attack
normally
less-
susceptible
crops
(Gould
1979).
Cross-resistance
can
take
unpredict-
able
forms,
including
immunity
against
currently
effective
methods.
For
example,
Gould
et
al.
(1982)
demonstrated
that
mite
adaptations
to
resistant
plant
cultivars
can
de-
crease
their
susceptibility
to
organo-
phosphates.
Previously
innocuous
nontarget
in-
sects
can
also
be
elevated
to
pest
status
through
natural-enemy
elimi-
nation,
competitive
release,
and
sometimes
direct
physiological
ben-
efit.
Mite
populations
commonly
rise
after
pyrethroid
or
DDT
applications
to
which
the
target
pest
and
mite
natural
enemies,
but
not
the
phytoph-
agous
mites,
are
susceptible.
For
ex-
ample,
the
only
major
outbreak
of
the
spruce
spider
mite,
Oligoncyhus
un-
unguis
Jacobi,
in
natural
forests
fol-
lowed
aerial
DDT
sprays
against
the
western
spruce
budworm,
Choristo-
neura
occidentalis
Freeman
(Furniss
and
Carolin
1977).
Likewise,
new
plant
cultivars
have
inadvertently
cre-
ated
new
pests
by
altering
existing
host-insect
relationships
(Oka
and
Bahagiawati
1984,
Pathak
1975).
In
some
cases,
the
desired
plant
property,
such
as
high
yield
or
resis-
tance
to
another
pest,
bestows
added
benefit
to
another
herbivore
in
the
form
of
direct
nutritive
properties
or
toxicity
to
parasites
(Campbell
and
Duffy
1979).
For
example,
the
green
revolution
introduced
several
high-
yielding
cultivars
that
resulted
in
new
pest
complexes
(Harlan
1980,
Pathak
1975).
Naturally
coevolved
systems
also
provide
numerous
examples
where
host
defensive
chemicals
favor
adapted
herbivores
by
repelling
pred-
ators
(Eisner
et
al.
1974),
inhibiting
gut
pathogens
(Andrews
et
al.
1980),
or
providing
a
food
base
(Bernays
and
Woodhead
1982).
Therefore,
identi-
cal
standards
must
be
applied
to
trees
genetically
engineered
for
properties
other
than
pest
resistance,
as
any
al-
teration
of
the
host
is
likely
to
affect
the
selective
pressures
on
closely
adapted
herbivores.
Third,
biotype
formation
is
not
an
occasional
aberration,
but
rather
an
inevitable
outcome
of
certain
condi-
tions.
More
than
428
arthropod
spe-
cies
developed
insecticide
resistance
by
1980
(Geourghiou
and
Mellon
1983),
and
24
of
the
25
major
agri-
cultural
pests
in
California
comprise
either
secondary
pest
outbreaks
or
September
1989
I
525
Table
1.
Mechanisms
by
which
insect
evolutionary
responses
to
genetically
altered
trees
could
deplete
efficacy,
contribute
to
more
severe
problems
with
target
pests,
and
create
new
pest
problems.
Each
mechanism
has
been
observed
in
response
to
insecticides
and/or
new
plant
cultivars.
+:
Outcome
that
could
result
from
a
particular
mechanism.
See
text
for
explanation
and
examples.
Outcome
Loss
of
Aggravated
target
Nontarget
pest
Mechanism
efficacy
pest
problems
emergence
Physiological
adaptation
No
cross-resistance
with
current
tactics
+
Cross-resistance
with
current
tactics
+
+
+
Cross-resistance
between
introduced
and
existing
defenses
in:
Primary
host
+
+
Secondary
hosts
+
+
+
Natural
enemy
suppression
by
toxin
+
+
+
Altered
host
availability
patterns
after
biotype
evolution:
Primary
pest
threshold
surpassed
+
+
Predisposition
to
secondary
pests
+
-
+
Competitor
elimination
--
+
Selection
for
host-preference
shifts
-+
+
pest
resurgences
facilitated
by
insecti-
cides
(Forgash
1984,
Metcalf
1980).
Immune
biotypes
have
also
emerged
against
such
control
practices
as
Ba-
cillus
thuringiensis
(McGaughey
1985)
application
and
alternate
crop
rotation
(Krysan
et
al.
1986).
The
potential
mechanisms
of
insect
response
to
and
adverse
consequences
of
genetic
engineering
in
trees,
and
the
mechanisms
by
which
each
could
arise,
are
summarized
in
Table
1.
Tree
longevity
intensifies
these
risks,
because
a
single
host
generation
may
span
several
hundred
insect
genera-
tions,
a
full
order
of
magnitude
more
than
is
normally
required
for
insect
biotypes
to
emerge
against
insecti-
cides
(Forgash
1984,
Metcalf
1980)
and
resistant
cultivars
(Sosa
1981).
Given
these
possibilities,
and
the
complexities
of
biological
systems
outside
controlled
laboratory
condi-
tions,
one
alternative
is
to
conclude
that
the
effects
of
tree
gene
manipula-
tions
simply
cannot
be
predicted,
and
therefore
implementation
should
be
avoided.
However,
this
carte
blanche
disapproval
is
itself
fraught
with
risk:
development
and
application
will
continue
with
or
without
the
input
of
ecologists,
and
general
reservations
will
simply
not
carry
much
weight
as
legal
decisions
are
rendered,
financial
markets
are
explored,
and
ordinances
from
international
to
local
levels
are
modified
to
compete
for
sources
of
jobs
and
revenue.
Also,
molecular
bi-
ologists
have
been
subjected
to
such
a
cacophony
of
hypothetical
worst-case
scenarios
that
specific
concerns
must
be
detailed,
lest
real
dangers
be
like-
wise
summarily
dismissed.
By
sug-
gesting
ways
of
using
ecological
fac-
tors
to
lessen
the
risks
of
biotype
evolution,
forest
ecologists
can
pro-
vide
some
direction
to
future
deci-
sions
and
research
needs.
Without
such
input,
single-strategy
approaches
become
more
likely,
and
these
ap-
proaches
are
surely
the
most
detrimen-
tal.
The
approach
suggested
here
con-
sists
of
developing
the
ability
to
char-
acterize
specific
host-pest
targets
ac-
cording
to
general
levels
of
risk,
devising
tactics
for
reducing
the
chances
of
target
and
nontarget
bio-
type
evolution
in
systems
deemed
to
have
an
acceptable
level
of
risk,
and
initiating
long-term
strategies
for
fos-
tering
the
environmentally
safe
use
of
plant
genetic
engineering
in
forestry.
Selection
of
target
systems
Experiences
with
insecticides
and
re-
sistant
cultivars
indicate
that
detailed
knowledge
of
each
target
host/pest
system
is
required
before
judicious
decisions
can
be
made.
However,
the
enormous
diversity
of
insect
biolo-
gies,
host
physiologies,
and
tree-
growing
conditions
makes
a
case-
by-case
appraisal
unwieldly
and
undirected.
Therefore,
a
framework
for
transferring
general
principles
to
specific
evaluations
of
risk
is
pre-
sented.
Four
factors
are
considered:
the
availability
of
local
refugia
for
susceptible
insect
genotypes,
the
ex-
isting
role
of
host
defenses
in
the
pest's
population
dynamics,
the
com-
patibility
of
novel
genetic
defenses
with
alternative
management
prac-
tices,
and
the
ability
of
novel
genes
to
be
transferred
to
plant
progeny.
Refugia
consist
of
untreated
plants,
plant
parts,
or
times
in
which
the
herbivore
can
successfully
feed
and
develop
to
maturity
without
exposure
to
the
novel
trait.
Because
area-wide,
consistent
selection
pressures
acceler-
ate
biotype
formation,
whereas
spa-
tially
disrupted,
intermittent
exposure
favors
preservation
or
restoration
of
previous
gene
frequencies,
an
abun-
dance
of
local
refugia
is
critical.
Ap-
plication
of
this
concept
under
actual
field
conditions
is
complicated,
how-
ever,
because
refugia
for
susceptible
genes
are
determined
by
the
target
insect's
biology,
host
physiology,
plant
community
structure,
applica-
tion
patterns,
and
various
interac-
tions
thereof
(Table
2).
Mere
proximity
between
different
host
types
is
not
sufficient
to
preclude
race
formation
(Bush
1973).
Precau-
tions
must
be
taken
to
avoid
repro-
ductive
isolation,
and
susceptible
genes
can
only
be
preserved
in
sys-
tems
where
there
is
a
high
likelihood
that
some
insects
will
locate
untreated
suitable
hosts
within
their
lifetime
and
interbreed
with
exposed
individ-
uals.
Host
plant
physiology,
distribu-
tion,
and
variability
strongly
affect
the
population
dynamics,
behavior,
and
gene
frequencies
of
herbivorous
insects
(Alstad
and
Edmunds
1983,
Berryman
1976,
Raffa
and
Berryman
1983,
1987).
The
consequences
of
genetic
engineering
on
these
naturally
occurring
constraints
must
be
consid-
ered
with
respect
to
survival
and
re-
productive
rates
by
new
insect
races
or
nontarget
species
released
from
competitors
and
natural
enemies.
For
example,
if
a
counteradaptation
also
conferred
cross-resistance
to
existing
plant
defenses,
the
consequences
would
be
most
severe
in
systems
BioScience
Vol.
39
No.
8
526
where
these
defenses
strongly
regulate
current
insect
population
behavior.
The
specific
effects
and
modalities
of
novel,
relative
to
existing,
host
prop-
erties
and
the
interactions
between
insect
population
and
plant
defense
thresholds
must
also
be
considered.
Compatibility
with
other
pest
man-
agement
practices
is
essential
because
multiple,
conflicting
selective
pres-
sures
imposed
by
the
insect's
overall
environment
reduce
the
chances
of
biotype
evolution.
An
example
of
the
stability
conferred
by
conflicting
se-
lective
processes
in
coevolving
sys-
tems
can
be
seen
in
wild
potatoes
that
emit
aphid
alarm
pheromones
upon
attack
(Gibson
and
Pickett
1983).
Presumably,
tolerance
to
the
plant
defense
would
result
in
decreased
es-
cape
from
predators.
Integrated
pest
management
will
be
hindered
in
sys-
tems
where
the
novel
traits'
mode
of
action
is
similar
to
other
tactics.
For
example,
consider
widespread
out-
planting
of
trees
with
Bt
delta-
endotoxin.
Once
target
pests
became
adapted,
they
could
no
longer
be
con-
trolled
by
judicious
spray
applica-
tions
that
are
currently
employed
only
when
populations
are
high
enough
to
threaten
tree
health.
Altered
gene
expression
must
be
limited
to
planted
individuals
through
sterility
or
other
means.
Without
this
stipulation,
the
level
of
risk
will
be
greatly
raised.
Expressive
progeny
would
disrupt
the
required
pattern
of
refugia.
Also,
the
protection
of
multi-
ple
host
generations
by
an
introduced
gene
could
reduce
the
selective
pres-
sures
on
trees
for
existing
defensive
traits
by
rendering
metabolically
ex-
pensive
(Mooney
et
al.
1983)
alle-
lochemicals
competitively
unfit.
Once
biotypes
evolved
against
the
novel
trait,
forests
could
then
become
ex-
tremely
susceptible
to
attack
and
re-
quire
unprecedented
levels
of
human
protection.
This
process
could
dupli-
cate
the
inadvertent
removal
of
resist-
ant
genes
from
food
crops
during
selection
for
desirable
agronomic
traits
(Harlan
1980),
with
the
result-
ing
heavy
reliance
on
synthetic
insec-
ticides.
The
availability
of
refugia
for
sus-
ceptible
genes,
importance
of
current
plant
defenses
in
insect
population
behavior,
and
compatibility
with
al-
ternative
management
tactics
are
in-
tegrated
into
a
common
model
in
Table
2.
Specific
properties
of
target
insect-tree
systems
that
may
influence
the
likelihood
and
severity
of
heritable
insect
responses
to
genetically
engineered
trees.
For
each
property,
conditions
deemed
more
likely
to
yield
reduced
levels
of
risk
are
proposed.
System
properties
Refugia:
Opportunity
for
nonadapted
insect
survival
Plant
community
structure
Number
of
untreated
trees
Insect
life
history
Mobility
Mating
site
Number
of
trees
oviposited
by
female
Fecundity
Plant
physiology
Distribution
and
expression
of
trait
Insect
life
history
*Plant
community
structure
Available
acceptable
species
Insect
life
history
*Plant
physiology
Number
of
insect
generations/tree
growing
cycle
Insect
population
regulation
Effect
of
existing
host
defenses
on
insect
reproduction
Effect
of
novel
host
plant
defense
on
insect
Action
of
existing
and
novel
defense
mechanisms
Compatibility
of
novel
trait
with
other
pest
management
methods
Biological
control
Host
range
of
major
natural
enemies
Exposure
of
natural
enemies
to
novel
trait
Tolerance
of
natural
enemies
to
novel
trait
Dispersal
capability
of
natural
enemies
Silvicultural
control
Optimal
insect
strategy
for
coping
with
novel
plant
trait
and
patterns
of
suitable
host
availability
Feasibility
of
insect
removal
by
sanitation
Insecticidal
control
(synthetic
and
microbial)
Availability
of
cost-effective
sprays
Mode
of
action
of
directly
applied
and
plant-
incorporated
toxins
*Interaction
between
plant
and
insect
properties.
Figure
1.
By
applying
the
specific
traits
for
each
system
as
outlined
in
Table
1,
potential
targets
can
be
situ-
ated
within
general
zones
of
risk.
Po-
tential
targets
will
be
addressed
in
a
descending
hierarchy,
in
which
the
cropping
system
is
considered
first.
Within
each
cropping
system,
some
major
pests
will
be
evaluated
with
emphasis
on
the
parameters
shown
in
Figure
1.
The
population
behavior
and
management
considerations
per-
taining
to
each
pest
are
discussed
in
turn.
The
objective
is
not
to
address
every
important
pest,
but
rather
to
provide
examples
of
how
specific
cases
can
be
evaluated.
Initially,
biotype
formation
is
con-
sidered
for
the
target
pest
alone.
This
constraint
is
subsequently
relaxed
in
the
discussion
on
nontarget
pest
emergence.
In
practice,
this
distinc-
tion
is
arbitrary,
because
the
tactics
in
Attributes
reducing
risk
High
High
Distant
from
host
Many
Low
Varied
High
Low
Low
Nonlethal?
Dissimilar
Broad
Low
High
High
Conflicting
High
High
Dissimilar
the
latter
discussion
must
also
be
ap-
plied
to
each
target
pest.
Growing
conditions
Commercial
forests.
Large
commer-
cial
forests,
consisting
of
either
natu-
rally
regenerating
stands
or
planta-
tions,
comprise
a
major
portion
of
wood
and
fiber
production.
Planta-
tions
are
usually
even-aged
monocul-
tures
derived
from
seed
orchards,
whereas
the
more
expansive
self-
regenerating
tracts
vary
in
species,
age,
and
genetic
diversity,
depending
on
their
ecological
status
and
logging
practices.
Ownership
is
distributed
among
government
agencies,
large
corporations,
and
regional
timber
companies.
Even
though
the
total
value
of
this
resource
is
enormous,
per-acre
profits
are
low,
and
so
tradi-
tional
methods
of
insect
control
are
September
1989
527
GROWING
CONDITIONS,
INSECT
POPULATION
BEHAVIOR,
AND
POPULATION
MANAGEMENT
FACTORS
AFFECTING
LIKELIHOOD
AND
IMPACT
OF
INSECT
BIOT
EVOLUTION
TO
GENETICALLY
ENGINEERED
TREES
Scarce
.
AVAILABILITY
OF
LOCAL
REFUGIA
?
Abu
\
EDUCED
._
MODERATE
SEVERE
o
intense
weak
Population
Regulation
by
Host
Defenses
V
EDUCED
MODERATE
SEVERE
intense
weak
Population
Regulation
by
Host
Defenses
intense
Population
Reguli
by
Host
Defens
Figure
1.
Conceptual
framework
for
evaluating
the
relative
risks
of
insect
evolution
against
genetically
engineered
trees.
Each
growing
system
is
characte
a
relative
availability
of
local
refugia
in
the
form
of
untreated
plants,
plant
pa
times.
Availability
of
local
refugia
is
determined
by
growing
conditions,
stand
st
and
insect
properties
such
as
vagility,
mating
behavior,
and
host
range.
The
lik
of
biotype
evolution
is
increased
in
systems
where
the
insect
population
is
,
regulated
by
host
tree
properties
and
where
transgenic
resistance
can
dimii
effects
of
other
management
tools
and
selective
pressures.
The
manifold
sel
zones
of
severe,
moderate,
and
reduced
risk
varies
along
the
refuge
ava
continuum.
Note
that
favorable
attributes
of
any
two
parameters
do
not
super
unacceptable
level
of
the
third.
not
cost
effective
in
these
systems.
Likewise,
insecticides
pose
greater
en-
vironmental
hazards
in
large
forests
than
in
other
tree-growing
systems,
because
uses
such
as
watershed
man-
agement
and
recreation
may
exceed
the
importance
of
wood
products.
Although
these
factors
lend
support
to
genetic
engineering
in
large
forests,
widespread,
uninterrupted
deploy-
ment
of
novel
genes
would
post
a
high
likelihood
of
biotype
evolution.
The
availability
of
untreated
refugia
could
be
extremely
small,
because
there
would
be
little
gene
flow
be-
tween
exposed
and
unexposed
in-
sects,
and
harvest
intervals
are
length-
ier
than
for
all
other
conditions
except
landscape
ornament.
There-
fore,
special
precautions
to
preserve
susceptible
insect
genes
must
be
em-
ployed
in
these
high-acreage
commer-
cial
systems.
Short-rotation
intensive
cultivation.
Recent
advances
in
the
development
of
fast-growing
species,
such
as
Pop-
ulus
and
Salix,
may
lead
to
revolu-
tionary
changes
in
the
tree-growing
industries.
In
addition
to
providing
traditional
wood
products,
agrifor-
estry
promises
to
be
a
major
so
energy.
Selected
cultivars
have
tremendous
capacity
for
biom<
duction
(Ek
et
al.
1983),
and
r
cycles
of
only
1-10
years
hav
proposed.
Currently,
these
tr
typically
planted
on
low
acrea
der
intensive
management,
ar
may
yield
high
cash
values.
Short
rotation
times
and
ir
cultivation
methods
are
well
su
the
deployment
of
spatial
and
te
genetic
mosaics.
By
alterating
ant
foreign
genotypes,
mixing
varieties,
and
integrating
plan
tance
with
biological,
cultur
chemical
controls
in
areas
wh
treated
hosts
are
abundant,
the
<
of
biotype
formation
can
be
red
managed
wisely,
genetic
engi
may
even
help
preserve
existin
that
confer
protection
from
insel
current
intense
selection
and
plasm
manipulation
of
fast-g
hardwoods
poses
the
challe
achieving
superior
production
ties
without
sacrificing
pest
re:
(Harrell
et
al.
1981),
as
happl
food
plants.
Gene
transfer
n
may
prove
most
efficient
at
cor
such
multiple
traits.
Seed
orchards
and
high-value
planta-
YPE
tions.
Seed
orchards
are
generally
low-
acreage,
high-value,
intensively
man-
aged
sites.
They
are
often
surrounded
by
indant
large
forests
which
could
provide
a
sub-
stantial
reservoir
of
susceptible,
inter-
mingling
insect
genotypes.
Because
even
low
levels
of
insect
feeding
cause
severe
EDUCED
economic
losses,
biological
controls
are
not
always
satisfactory.
Likewise,
cul-
TE
tural
remedies
may
conflict
with
grow-
ing
practices,
just
as
they
often
do
in
agriculture.
Because
seed
orchards
must
produce
a
consistently
high
yield,
they
weak
provide
a
plentiful,
predictable
resource
a
to
specialized
herbivores
that
have
,es?o
evolved
high
reproductive
capacity
as
an
adaptation
to
a
naturally
scarce,
unpre-
dictable
food
supply.
High-value
planta-
biotype
tion
trees
(e.g.,
Christmas
trees
and
ve-
rized
by
neer)
pose
approximately
the
same
level
lrts,
and
of
risk
as
seed
orchards.
:ructure,
:elihood
Ornamental
trees.
Trees
grown
for
strongly
ornament
and
shade
are
among
the
rush
the
,arating
most
valuable
on
a
per-individual
ba-
ilability
sis,
with
large
lawn
trees
contributing
rcede
an
greatly
to
real
estate
values
(Payne
et
al.
1973).
Extensive
monocultures
are
not
common:
usually
an
age
and
spe-
cies
mosaic
is
strewn
across
the
sub-
urce
of
urban
and
urban
landscape,
through-
shown
out
which
untended
woodlots
are
iss
pro-
scattered
and
around
which
larger
otation
forests
often
occur.
re
been
Several
features
of
this
system
ees
are
could
provide
for
the
critically
needed
ges
un-
susceptible-insect
gene
refugia.
First,
id
they
the
outlying
regions
from
which
ur-
ban
pests
often
arise
could
be
left
itensive
unaltered,
with
alternative
methods
ited
for
being
used
in
the
forests.
Second,
ur-
.mporal
ban
parks
and
woodlots
could
be
left
resist-
untreated
and
municipal
foresters
clonal
could
continue
current
practices.
it
resis-
Third,
not
all
homeowners
would
al,
and
choose
any
one
variety
of
any
one
ere
un-
species.
Introduction
of
foreign
genes
chances
is
already
well
underway
in
this
set-
luced.
If
ting,
as
some
homeowners
plant
Jap-
neering
anese
white
birch
to
avoid
bronze
g
genes
birch
borer
and
Chinese
elm
to
avoid
cts.
The
Dutch
elm
disease.
No
biotype
evolu-
germ-
tion
has
been
reported.
Genetic
engi-
;rowing
neering
in
this
context
would
simply
nge
of
be
a
more
efficient
and
directed
ver-
proper-
sion
of
the
same
process.
sistance
ened
in
Insect
groups
nethods
nbining
Bark
beetles.
Bark
beetles
(Co-
leoptera:
Scolytidae)
are
the
most
BioScience
Vol.
39
No.
8
E
=
.
_
e
c
0i-0
a
,
o_o
o
m
o
0
528
damaging
forest
pests
to
mature
trees
(Coulson
and
Witter
1984).
Silvicul-
tural
tactics
can
reduce
losses,
but
no
method
is
totally
satisfactory.
There-
fore,
these
insects
might
seem
a
logi-
cal
group
to
suppress
by
gene
trans-
ferral.
Bark
beetles,
however,
might
cause
even
greater
problems
after
biotype
evolution
than
they
do
currently,
be-
cause
of
their
particular
relationship
with
host
plants.
Individual
trees
within
a
host
species
vary
greatly
in
their
levels
of
resistance.
All
trees
can
resist
low
numbers
of
beetles
by
se-
creting
repellent
and
toxic
resins,
but
high
attack
densities
mediated
by
ag-
gregation
pheromones
can
exhaust
these
defenses
(Raffa
and
Berryman
1983,
Rudinsky
1962).
Thus
the
in-
teraction
is
quantitative
in
that
the
outcome
is
dictated
by
the
interaction
between
tree
defense
capabilities
and
insect
numbers,
but
it
is
also
discrete
in
that
colonization
attempts
result
in
either
tree
death
or
insect
failure
to
reproduce.
Moreover,
a
tree's
thresh-
old
of
resistance-the
number
of
beetles
required
to
overcome
its
de-
fenses-is
greatly
diminished
by
envi-
ronmental
stresses,
such
as
water
def-
icit,
disease,
lightning,
and
other
insects.
Under
most
conditions,
even
the
most
damaging
bark
beetle
species
usually
attack
stressed
trees
(Rudin-
sky
1962),
because
the
ability
to
de-
tect
weakened
hosts
increases
their
chances
of
reproduction.
If
there
is
a
sudden
increase
in
susceptible
trees
due
to
an
area-wide
stress
such
as
drought,
however,
the
population
can
surpass
a
critical
density
above
which
beetle
behavior
changes
(Berryman
1976,
Raffa
and
Berryman
1987).
Beetle
densities
can
become
high
enough
to
overcome
the
resistance
of
almost
all
trees
in
the
stand,
even
after
the
stress
has
been
removed.
Under
these
conditions,
beetles
func-
tionally
expand
their
own
food
sup-
ply
by
successfully
attacking
healthy
trees,
and
devastating
outbreaks
oc-
cur.
Thus
bark
beetle
population
lev-
els
relate
closely
to
the
vigor
of
their
host
plants
(Berryman
1976).
Natural
enemies
and
temperature
play
impor-
tant
roles,
but
most
forest
managers
associate
beetle
outbreaks
with
old
trees,
dense
stands,
and
physical
stress.
Effective
bark
beetle
management
Neodiprion
lecontei
mating
pair.
Photo:
G.
Lintereur.
maintains
conditions
that
confine
populations
to
a
scavenging
existence
by
promoting
stand
vigor
through
early
rotation,
thinning,
sanitation,
proper
site
selection,
and
age
mosaics.
Because
beetles
compete
with
other
beetles
(not
trees),
we
need
to
provide
conditions
under
which
the
best
bee-
tle
strategy
is
to
orient
away
from
healthy
trees,
and
individuals
that
are
not
repelled
by
healthy
trees
are
at
a
competitive
disadvantage
(Raffa
1988).
This
stability
could
be
reduced
by
deployment
of
a
foreign
gene
confer-
ring
resistance.
If
all
trees,
stressed
and
healthy
alike,
expressed
the
resis-
tance
factor,
the
selective
pressures
on
beetle
populations
would
be
enor-
mous
and
unidirectional.
Behavioral
attributes
that
orient
beetles
to
weak-
ened
trees
would
confer
little
advan-
tage.
The
best
chance
of
beetle
repro-
ductive
success
would
be
offered
by
combined
physiological
immunity
to
both
the
novel
and
current
tree
defen-
sive
traits.
With
the
role
of
host
plant
resistance
removed,
no
effective
control
strategies
would
remain.
Al-
though
dissimilarities
between
natu-
ral
and
exotic
plant
defense
mecha-
nisms
can
reduce
this
possibility,
they
do
not
provide
sufficient
assurance.
Even
if
beetles
only
overcame
the
novel
gene
but
not
natural
resistance
mechanisms,
damaging
conditions
could
still
result.
An
accumulated
pool
of
previously
protected,
stressed
trees
would
become
available,
allow-
ing
populations
to
rise
above
out-
break
thresholds.
A
widespread,
syn-
chronous
appearance
of
suitable
hosts,
as
opposed
to
a
chronic,
scat-
tered
reservoir
of
stricken
trees,
greatly
increases
the
likelihood
of
damaging
bark
beetle
outbreaks
(Raffa
and
Berryman
1987).
The
pat-
tern
would
be
similar
to
what
has
already
proven
to
be
a
failed,
now
abandoned,
fire
control
strategy:
by
suppressing
small
fires,
managers
al-
lowed
tinder
to
accumulate
to
unnat-
ural
volumes,
and
uncontrollable,
devastating
fires
resulted.
Transgenic
trees
might
also
sup-
press
natural
enemy
populations,
be-
cause
most
arthropod
predators
and
parasites
of
scolytids
complete
devel-
opment
within
trees
killed
by
the
bee-
tles.
Once
beetles
evolved
resistance
to
the
novel
property,
not
only
would
there
be
an
enormous
backlog
of
available
hosts,
but
there
could
also
be
a
scarcity
of
natural
enemies.
Al-
though
not
the
principal
factors
reg-
ulating
scolytid
abundance,
these
ar-
thropods
are
important
mortality
agents,
in
whose
absence
tree
losses
would
increase
(Amman
and
Cole
1983).
Moreover,
adverse
effects
would
probably
spread
beyond
treated
stands,
as
emigrants
from
out-
breaks
often
damage
neighboring
for-
ests.
There
are
no
effective
measures
against
such
high
populations
(Berry-
man
1976).
Mosaic
strategies
cannot
provide
sufficient
assurance
that
this
threat
would
be
alleviated.
Leaving
some
trees
untreated
would
mostly
provide
a
reservoir
of
vigorous
plants,
and
so
would
not
maintain
current
selective
advantages
to
beetles
that
orient
to
unhealthy
trees.
Biotype
formation
could
theoretically
be
delayed
by
de-
liberately
stressing
untreated
trees,
but
this
approach
demands
a
level
of
precision
that
far
exceeds
both
cur-
rent
scientific
capabilities
and
antici-
pated
operational
fidelity.
In
an
un-
predictable
environment
of
drought,
lightning,
and
additional
biotic
agents,
the
optimal
proportion
of
un-
treated
stressed
trees
cannot
be
deter-
mined.
Defoliators.
Defoliators
comprise
the
second-most-damaging
insect
group.
The
spruce
budworm,
Choristoneura
fumiferana
Clemens,
is
generally
con-
sidered
the
most
important
forest
de-
foliator
in
North
America
(Coulson
September
1989
529
and
Witter
1984,
Morris
1963).
Bal-
sam
fir,
Abies
balsamea
L.
Mill.,
is
the
most
preferred
and
susceptible
species
(Mattson
et
al.
1983),
although
there
may
be
geographic
variation
in
these
relationships.
Populations
normally
remain
low
for
several
decades,
as
physical
and
biotic
mortality
agents
offset
reproductive
gains.
Outbreaks
occur
when
there
is
an
abundance
of
mature
host
trees
combined
with
sev-
eral
consecutive
years
of
hot,
dry
summers
(Blais
1973,
MacLean
1980).
Once
populations
rise,
out-
breaks
rapidly
expand
to
most
spruce
species.
Intense,
continuous
selection
by
re-
sistant
trees
would
probably
select
for
immune
C.
fumiferana
biotypes,
just
as
widespread
DDT
applications
did
previously
(Randall
1965).
However,
behavioral
and
ecological
attributes
could
possibly
be
used
to
lessen
the
chances
of
biotype
formation
against
this
pest.
If
factors
encoding
for
resis-
tance
were
incorporated
into
Picea
but
not
Abies,
then
a
large
proportion
of
the
population
would
complete
de-
velopment
on
untreated
plants.
Peri-
odic
outbreaks
would
continue
to
oc-
cur
on
the
Abies
refuge,
but
natural
enemies
would
eventually
cause
pop-
ulation
collapse.
Protection
of
the
more
desirable
Picea
at
the
expense
of
the
less
desirable
Abies
would
proba-
bly
be
acceptable
to
forest
managers,
based
on
the
twofold
difference
in
their
pulpwood
values
(Peterson
1988).
Because
young
trees
seem
less
vulnerable
to
attack
(Mattson
1985),
the
possibility
of
limiting
gene
expres-
sion
to
older
trees
should
also
be
considered.
With
such
a
scheme,
genetically
en-
gineered
resistance
could
possibly
be
integrated
into
current
silvicultural
and
biological
controls.
Because
most
natural
enemies
of
budworms
do
not
directly
interact
with
the
plant,
for
example,
there
may
be
less
exposure
to
the
novel
trait
than
with
bark
beetles.
However,
indirect
effects
re-
quire
further
investigation.
If
efficacy
were
lost
due
to
biotype
evolution,
C.
fumiferana
populations
would
not
necessarily
exceed
their
current
virulence.
Host
defensive
mechanisms
mostly
cause
nonlethal
effects,
such
as
smaller
size
and
re-
duced
fecundity,
rather
than
direct
toxicity
(Mattson
et
al.
1983).
This
relationship
could
possibly
reduce
the
selective
pressures
for
cross-resis-
tance,
especially
where
silvicultural
practices
provided
species,
age,
and
variety
mosaics.
One
danger
is
that
resistant
trees,
although
not
directly
affecting
natural
enemies,
would
reduce
their
numbers
by
depleting
the
supply
of
C.
fumifer-
ana,
and
thereby
allow
a
severe
pest
resurgence
once
biotypes
evolved.
Several
factors,
however,
might
re-
duce
this
danger.
First,
most
of
the
major
predators
and
parasites
that
maintain
C.
fumiferana
populations
at
low
levels
between
outbreaks
are
generalists
(Morris
1963)
that
could
subsist
on
alternate
insect
hosts.
Sec-
ond,
the
specialists
that
help
termi-
nate
outbreaks
are
adapted
to
long
periods
of
low
C.
fumiferana
popula-
tion
densities.
Third,
unlike
tradi-
tional
pesticide
treatments
that
con-
tinually
suppress
natural
enemies
while
the
resistant
herbivore
popula-
tion
rises,
a
plant
trait
that
does
not
directly
harm
beneficial
insects
could
allow
their
populations
to
respond
immediately
to
increased
prey
densi-
ties.
Effective
emergency
measures,
including
a
broad
array
of
synthetic
and
microbial
insecticides,
are
avail-
able
to
prevent
major
losses
if
out-
breaks
occurred
despite
the
above
factors
(Schmitt
et
al.
1984).
Although
the
concept
of
conferring
genetic
resistance
against
C.
fumifer-
ana
merits
further
consideration,
a
greater
understanding
of
this
insect's
ecology
and
behavior
is
essential
be-
fore
deployment
can
be
deemed
rela-
tively
safe.
It
is
critical
that
bud-
worms
feeding
on
Abies
and
Picea
do
not
become
reproductively
isolated.
The
high
dispersal
ability
and
multi-
ple-oviposition
behavior
of
the
spruce
budworm
lends
some
confidence
to
this
strategy,
but
additional
research
should
focus
on
gene
flow
and
geo-
graphic
variation
(Hardy
et
al.
1983).
The
specifics
of
the
spruce
bud-
worm-balsam
fir-spruce
system
can-
not
be
generalized
to
all
defoliators.
However,
refugia
may
be
maintained
for
some
other
species
by
restricting
genetic
alterations
to
certain
growing
conditions.
For
example,
the
gypsy
moth,
Lymantria
dispar
L.,
causes
widespread
forest
defoliation,
but
much
of
its
economic
damage
occurs
in
urban
and
suburban
settings.
Therefore,
a
policy
of
deploying
re-
sistant
genes
for
ornamental
or
short-
rotation
production
purposes,
while
practicing
traditional
and
developing
integrated
pest
management
strate-
gies
in
forests,
could
protect
high-
value
trees
yet
exert
only
moderate
selective
pressures
on
the
insect.
Al-
though
large
acreages
would
still
be
periodically
defoliated,
the
actual
economic
and
aesthetic
impact
would
be
greatly
diminished.
Again,
the
spe-
cific
biologies
of
each
insect
must
be
considered,
and
the
inability
of
fe-
male
gypsy
moths
to
fly
dictates
cau-
tion
(Table
2).
A
similar
strategy
with
novel
genes
limited
to
short-rotation
intensive
cultivations
could
be
used
against
in-
sects
such
as
the
cottonwood
leaf
beetle,
Chrysomela
scripta
F.,
and
the
forest
tent
caterpillar,
Malacosoma
disstria
Hubner,
which
can
cause
more
severe
economic
losses
in
inten-
sive
cultivations
than
in
extensive
for-
ests.
Root
insects.
The
impact
of
root-
feeding
insects
has
been
greatly
in-
creased
by
modern
forest
plantation
practices
(Schowalter
1985).
Losses
to
these
species,
primarily
weevils
and
white
grubs,
are
generally
low
in
ma-
ture
stands.
However,
when
new
seedlings
are
established
after
harvest
or
reclamation,
root
injury
due
to
larval
feeding
and/or
adult
stem
gir-
dling
can
devastate
plantings.
Natural
enemies
are
valuable
but
inadequate,
and
applied
biological
controls
have
been
unsuccessful.
Likewise,
there
are
no
totally
acceptable
silvicultural
remedies
against
species
that
feed
on
living
roots.
Detection
is
difficult,
so
soil-permeating,
persistent
insecticides
such
as
lindane
are
sometimes
applied.
These
chemicals
have
been
banned
for
most
other
uses.
Thus,
if
transgenic
resistance
could
be
employed
against
root
insects
without
adverse
effects,
both
tree
production
and
environmen-
tal
safety
would
benefit.
Root-feeding
insects
may
provide
targets
against
which
time-specific
expression
of
resistance
genes
could
reduce
the
chances
of
biotype
evolu-
tion
(Gould
1988,
Raffa
1987).
A
bet-
ter
understanding
of
the
relationship
between
host
age
and
susceptibility
is
necessary,
however,
to
devise
appro-
priate
tactics.
It
is
not
known,
for
example,
whether
losses
are
most
se-
vere
in
young
stands
because
larger
trees
are
more
tolerant
and
can
better
BioScience
Vol.
39
No.
8
530
withstand
feeding,
if
younger
trees
are
more
attractive
or
less
able
to
resist
attack,
or
if
physical
attributes
of
the
soil
created
by
a
closed
canopy
simply
reduce
insect
replacement
rates.
If
large
trees
are
commonly
ex-
ploited
without
suffering
severe
dam-
age,
then
limiting
resistance
expres-
sion
to
young
trees
could
provide
refugia
analogous
to
the
fir
trees
left
untreated
for
spruce
budworms.
If
no
such
reservoir
exists,
biotype
evolu-
tion
would
be
likely.
Moreover,
more
serious
losses
than
currently
occur
could
result.
A
synchronous
large-scale
surge
of
root
insect
populations
rather
than
the
current
steady
mortality
to
young
trees
would
provide
a
vast
sub-
strate
for
species
such
as
the
pales
wee-
vil,
Hylobius
pales
Herbst,
that
breed
in
dead
tissue
and
then
as
adults
girdle
nearby
live
seedlings.
If
a
substantial
reservoir
exists
on
mature
trees
but
temporal
relaxation
of
gene
expression
is
not
provided,
the
consequences
could
likewise
be
devastating.
Increased
root
feeding
on
mature
trees
by
adapted
insects
would
increase
susceptibility
to
bark
beetles
(Raffa
1988),
which
in
turn
could
catapult
scolytid
popula-
tions
across
their
threshold
density
and
result
in
the
massive
outbreaks
de-
scribed
previously.
Seed
and
cone
predators.
These
spe-
cies,
primarily
Lepidoptera,
Co-
leoptera,
and
Hemiptera,
pose
major
limitations
on
seed
orchard
produc-
tivity
because
their
feeding
translates
directly
into
yield
loss.
They
are
only
vulnerable
to
insecticides
for
brief
pe-
riods
of
their
life
cycles,
so
timing
is
critical
for
effective
control.
Because
multiple
pest
complexes
are
the
norm,
seed
orchard
managers
must
sample
with
an
array
of
pheromones,
con-
sider
numerous
action
thresholds,
and
spray
for
each
population
peak.
The
use
of
resistant
trees
to
sup-
press
seed
and
cone
pests
could
prove
more
compatible
with
biological
con-
trol
than
current
methods.
With
fewer
insecticide
applications,
natural
enemy
populations
of
both
target
and
currently
sprayed
nontarget
species
may
rise,
and
multiple
selection
pres-
sures
could
be
enhanced.
Regions
outside
seed
orchards
should
be
left
unmanipulated.
Usually
seed
or-
chards
contain
a
large
array
of
host
lineages,
thus
providing
an
underly-
ing
genetic
diversity
that
would
fur-
ther
reduce
unidirectional
selective
pressures.
The
presence
of
neighboring
un-
treated
refugia
is
not
sufficient
to
pre-
vent
biotype
formation,
however,
as
evidenced
by
numerous
fruit
orchard
pests
with
similar
biologies
that
evolved
insecticide
resistance
(Met-
calf
1980).
Untreated
conebearing
trees
must
be
included
within
each
planting.
The
greatest
risks
would
probably
be
with
species
such
as
Conopthorus
that
enter
cones
as
adults
and
oviposit
in
only
one
or
several
trees,
rather
than
most
Lepi-
doptera,
which
oviposit
externally
on
the
cones
of
many
trees
(Table
2).
If
biotypes
arose
in
a
seed
orchard,
there
is
no
obvious
mechanism
by
which
neighboring
forests
would
be
threatened,
as
food
scarcity
would
probably
remain
a
major
selective
force
in
these
areas.
Wood
borers.
These
Coleoptera
(Bu-
prestidae,
Cerambycidae),
Lepi-
doptera
(Cossidae,
Aegeriidae),
and
Hymenoptera
(Siricidae)
primarily
colonize
weakened
trees.
Forests
can
be
protected
by
early
stand
rotation,
thinning,
judicious
site
selection,
and
sanitation.
In
urban
environments,
however,
numerous
stresses
such
as
root
compaction,
pollution,
and
me-
chanical
damage
render
trees
suscep-
tible
to
wood
borers.
Thus,
insects
such
as
the
bronze
birch
borer,
Agrilus
anxius
Gory,
are
major
pests
of
ornamental
trees.
Forest
manage-
ment
strategies
are
not
applicable
to
homeowners,
and
so
insecticides
are
often
required.
These
applications
are
expensive
and
only
marginally
effec-
tive,
however,
and
insecticide
drift
poses
major
problems
when
large
trees
are
sprayed
in
urban
areas.
Widescale
outplantings
in
commer-
cial
forests
would
pose
some
of
the
same
risks
as
with
bark
beetles
and
are
unnecessary.
As
with
the
gypsy
moth,
however,
wood
borers
may
provide
targets
where
economic
im-
pact
can
be
greatly
reduced,
with
rel-
atively
low
risk
of
biotype
evolution,
by
limiting
gene
alterations
to
high-
value
trees.
Nontarget
pest
emergence
and
biotype-delaying
tactics
In
nature,
all
tissues
of
all
tree
species
are
exploited
by
a
variety
of
insects.
Evaluating
the
influence
of
transgenic
resistance
on
nontarget
insects
is
ex-
tremely
difficult.
Because
of
their
cur-
rent
nonpest
status,
we
know
the
least
about
these
insects.
For
most
com-
mercial
tree
species,
the
complete
guild
of
insect
herbivores
has
not
even
been
cataloged
(Niemela
and
Neu-
vonen
1983).
Although
we
have
insufficient
knowledge
to
predict
nontarget
pest
emergence,
experience
with
pesticides
and
resistant
cultivars
and
observa-
tions
from
natural
coevolved
systems
suggest
some
useful
tactics.
First,
a
mode
of
action
that
is
relatively
spe-
cific
to
the
target
organism
and
as
distinct
as
possible
from
existing
plant
defense
mechanisms
should
be
selected.
Although
unpredictable
forms
of
cross-resistance
can
occur,
this
approach
would
at
least
reduce
the
selection
for
coadaptive
insect
genes
that
provide
immunity
from
both
introduced
and
existing
plant
traits.
Second,
expression
of
novel
prop-
erties
should
be
limited
to
the
tissues
and
times
at
which
the
target
feeds,
and
preferably
expression
should
be
induced
by
the
target
herbivore
(Gould
1988,
Raffa
1987).
Naturally
occurring
tree-insect
systems
provide
examples
of
how
uneven
phytochem-
ical
distribution
can
favor
stability.
Pines
allocate
resin
acids
to
new
but
not
old
foliage,
thereby
protecting
their
photosynthetically
most
produc-
tive
tissues
while
allowing
herbivores
to
graze
the
less-valuable
needles
(Ike-
da
et
al.
1977).
Larvae
that
prefer
the
less-protected
tissue
presumably
out-
compete
those
not
repelled
by
young
needles,
so
physiological
tolerance
to
resin
acids
has
not
evolved
in
most
sawflies.
Likewise,
many
plants
limit
the
expression
of
defensive
traits
to
critical
periods
of
the
growing
season,
certain
age
categories,
or
induction
by
herbivore
activities.
The
potential
adverse
effects
of
ge-
netically
engineered,
whole-plant
expression
can
be
anticipated
by
a
reexamination
of
the
spruce
bud-
worm
example,
depicted
earlier
as
a
possibly
safe
target.
If
the
defensive
property
inadvertently
protected
cor-
tical
tissue
and
thereby
resisted
spruce
bark
beetles,
Dendroctonus
rufipen-
nis
Kirby,
then
the
processes
de-
scribed
earlier
as
favoring
bark
beetle
adaptations
would
operate.
Although
September
1989
531
this
species
is
usually
only
a
moderate
problem,
D.
rufipennis
can
undergo
outbreaks
under
favorable
condi-
tions,
and
it
has
caused
some
of
the
most
severe
losses
ever
recorded
for
any
forest
insect
(Furniss
and
Carolin
1977).
Third,
genotype
mosaics
should
be
employed
within
each
planting,
pro-
viding
mixtures
of
transgenic
traits
superimposed
on
mixtures
of
various
seed
sources.
Untreated
trees
should
be
intermingled
within
each
planting.
This
strategy
could
reduce
the
likeli-
hood
of
oligophagous
and
polypha-
gous
herbivores
emerging
as
new
pests
of
formerly
less-preferred
trees
by
undergoing
genetic
shifts
in
behav-
ior
to
avoid
the
novel
defense
(Gould
1984).
Such
genetic
variation
stabi-
lizes
potential
outbreak
species
like
the
black
pineleaf
scale,
Nuculaspis
californica
Coleman,
in
nature.
Al-
though
this
insect
can
develop
within-
tree
biotypes
that
correspond
to
host
genotypes
(Edmunds
and
Alstad
1978),
diversity
within
the
host
pop-
ulation
provides
a
complex
array
of
selective
pressures
that
renders
the
adaptive
value
of
various
insect
genes,
such
as
those
regulating
movement
and
resource
breadth,
in
opposition
(Alstad
and
Edmunds
1983).
Fourth,
we
should
adopt
a
major
lesson
from
pesticide
usage
and
devise
comprehensive,
preconceived
biotype
management
programs
(Brattsten
et
al.
1987).
Insect
monitoring
is
a
crit-
ical
component
of
this
scheme.
Both
previous
experience
and
theoretical
models
emphasize
that
tactics
for
sup-
pressing
biotype
evolution
are
most
effective
before
the
newly
favored
al-
lele
becomes
common
(Brattsten
et
al.
1987,
Tabashnik
and
Croft
1982).
Both
target
and
nontarget
popula-
tions
should
be
periodically
appraised.
The
population
genetics
of
emerging
biotypes
should
be
thoroughly
stud-
ied,
as
gene
frequencies
and
inheri-
tance
patterns
are
critical
in
determin-
ing
optimal
suppression
methods
(Tabashnik
and
Croft
1982).
Like-
wise,
the
mechanisms
of
biotype
im-
munities
should
be
characterized
to
help
develop
appropriate
countermea-
sures
(Brattsten
et
al.
1987).
Developing
strategies
to
minimize
risks
The
preceding
analysis
suggests
spe-
cific
tactics
for
estimating
and
reduc-
ing
the
risks
of
deleterious
insect
re-
sponses
to
transgenic
trees.
A
scheme
for
integrating
these
actions
in
a
co-
hesive
fashion
is
proposed
in
Table
3.
However,
implementation
of
appro-
priate
tactics
will
require
a
broad,
interdisciplinary
approach
as
an
inte-
gral
component
of
plant
biotechnol-
ogy.
Several
long-term
strategies
must
be
initiated.
First,
specific
guidelines
on
trans-
genic
release
that
consider
the
chances
of
biotype
evolution
and
nontarget
pest
outbreaks
need
to
be
established.
Detailed,
rigorous
regula-
tions
already
apply
to
laboratory
and
field
practices
with
regard
to
human
safety
and/or
accidental
release
(Brill
1985).
Equivalent
standards
should
be
developed
governing
the
impact
of
deliberate
releases
at
the
population
and
ecosystem
levels.
Replacing
ad
hoc
decisions
with
established
guide-
lines
could
also
safeguard
against
the
danger
that
each
deployment
result-
ing
in
no
apparent
and/or
immediate
adverse
effects
will
lead
to
acceptance
of
other
uses
that
are
less
judicious.
Policies
must
be
based
on
research
specifically
directed
at
insect
evolu-
tionary
responses
to
transgenic
plants
Table
3.
Principal
ecological
and
management
strategies
for
reducing
the
risks
and
impact
of
biotype
evolution
associated
with
deployment
of
genetically
engineered
tree
resistance.
Restriction
of
novel
gene
deployment
to
systems
where
multiple,
opposing,
and
ephermeral
selective
pressures
can
be
maintained
Implementation
of
biotype-delaying
tactics
at
planting
Mode
of
action
of
introduced
trait
distinct
from
existing
defense
mechanisms
Temporal
and
spatial
limitations
on
and
herbivore
induction
of
resistance
trait
expression
Host
genotype
mosaics
at
multiple
layers
Intermingling
with
untreated
trees
Biotype
management
Monitoring
of
field
populations
Genetic
characterization:
mode
of
inheritance,
dominance
Physiological
characterization
of
biotypes:
mode
of
detoxification,
development
of
biotype
modality
inhibitors
Integration
with
other
forest
protection
practices
and
multiple
forest
resource
uses
(Gould
1988).
Research
in
this
area
is
critically
lacking.
Laboratory
models
should
be
devised
to
test
specific
hy-
potheses,
such
as
those
emerging
from
Figure
1
and
Table
2.
Comple-
mentary
studies
on
tree-insect
interac-
tions,
insect
population
behavior
and
genetics,
and
community
ecology
should
focus
on
nontarget
pest
emer-
gence.
Development
of
methods
for
restricting
gene
transfer
(Bej
et
al.
1988)
and
limiting
expression
to
spe-
cific
tissues,
times,
and
herbivore
lev-
els
is
a
critical
need
requiring
the
skills
of
molecular
biologists.
Heightened
regulations
always
in-
cur
the
risk
of
being
counterproduc-
tive.
Stipulations
could
become
so
restrictive
as
to
render
genetic
alter-
ations
impractical
and/or
unattrac-
tive,
thereby
reducing
the
benefits
this
tool
can
bring
to
forestry.
However,
some
of
the
systems
where
genetic
engineering
appears
to
have
the
high-
est
margin
of
safety
comprise
large,
well-defined,
and
easily
accessible
markets.
Therefore,
ecological
and
commercial
considerations
are
often,
or
can
be
made,
compatible.
The
recommendation
to
limit
ex-
pressed
resistance
to
planted
stock,
for
example,
is
of
obvious
benefit
to
biotechnology
companies.
Likewise,
species
such
as
Salix
and
Populus,
which
are
most
suitable
for
intensive
short-rotation
systems
and
gene
mo-
saics,
have
also
proven
to
be
particu-
larly
amenable
to
protoplast
manipu-
lation
and
genetic
engineering.
Extension
of
patent
life
should
also
be
considered
as
an
incentive
for
accept-
ing
such
guidelines.
The
attributes
of
some
potential
target
systems
are
likely
to
demand
such
expensive
safeguards
that
de-
ployment
is
not
practical.
This
out-
come
is
not
justification
for
applying
less-restrictive
criteria,
however,
be-
cause
the
potential
consequences
of
an
erroneous
decision
are
too
severe.
This
philosophy
does
not
discrimi-
nate
solely
against
genetic
engineer-
ing,
but
rather
it
is
currently
applied
to
such
traditional
tactics
as
importa-
tion
of
biological
control
agents.
Second,
integrated
risk
manage-
ment
programs
that
involve
all
af-
fected
disciplines
must
be
developed.
Guidelines
regulating
gene
transfers
must
be
compatible
with
overall
for-
est
resource
management.
For
exam-
ple,
wildlife
biologists
may
oppose
a
BioScience
Vol.
39
No.
8
532
particular
approach
because
of
its
ef-
fects
on
insectivorous
birds
or
other
components
of
the
food
web.
Like-
wise,
trees
genetically
engineered
to
resist
foliar
fungal
pathogens
could
possibly
inhibit
endophytes
that
repel
insects
(Carroll
1988),
thereby
caus-
ing
nontarget
insect
outbreaks.
Finally,
ecologists
and
plant
protec-
tion
specialists
should
become
more
involved
in
the
training
of
molecular
biologists.
Although
a
proposed
plant
protection
tactic
may
comprise
a
ma-
jor
scientific
advance
at
the
molecular
level,
its
implementation
could
entail
a
quite
primitive
approach
from
a
population
perspective.
Recent
ad-
vances
from
all
levels
of
biological
organization
must
be
integrated
to
enhance
the
efficacy
and
environmen-
tal
safety
of
pest
management
tools.
More
exposure
to
population
genet-
ics,
population
dynamics,
and
crop
protection
should
be
provided
in
the
core
curriculum
of
students
intending
to
conduct
plant
genetic
engineering.
A
historical
context
of
previous
tech-
nological
capabilities
that
outpaced
ecological
understanding,
such
as
high-grading,
calendar
pesticide
ap-
plication,
and
total
fire
suppression,
would
help
better
prepare
molecular
biology
students
for
the
contributions
they
can
make.
Conclusions
An
approach
has
been
developed
for
using
the
general
principles
of
biotype
evolution
to
generate
specific
esti-
mates
of
risk
with
regard
to
genetic
engineering
in
trees
and
to
devise
pos-
sible
preventive
tactics.
The
major
criteria
include
the
tree-cropping
sys-
tem,
compatibility
with
other
pest
management
techniques,
and
specific
attributes
of
the
target
insect's
biol-
ogy.
This
approach
may
apply
to
other
forms
of
plant
genetic
engineer-
ing,
as
well
as
to
other
biotechnolog-
ical
approaches
to
controlling
insects.
Based
on
these
analyses:
*
In
some
systems,
biotype
evolu-
tion
poses
a
severe
threat.
Possible
adverse
effects
include
both
decreased
efficacy
and
alteration
of
existing
plant-insect
relationships
so
as
to
worsen
current
conditions.
In
other
cases,
genetic
engineering
could
be
more
compatible
with
biological
con-
trol
than
are
current
insecticide
treat-
ments
or
it
could
be
used
to
provide
greater
genetic
diversity
than
tradi-
tional
breeding
methods.
*
In
general,
the
risks
are
greater
in
large
forested
expanses
than
in
seed
orchards,
rapid
rotation
systems,
and
ornamental
plantings.
*
Expression
of
resistance
should
be
nontransferable
to
host
progeny.
*
Genetic
mosaics
involving
spatial,
temporal,
and
herbivore-induced
within-tree
variation,
multiple
sources
of
resistance,
treatment
mixtures,
and
refugia
of
untreated
trees
can
reduce
risk.
Natural
systems
provide
valuable
examples
of
stable
tissue-protection
strategies,
and
these
systems
should
be
emulated
as
models
for
ecologically
sound
transgenic
tactics.
*
Integrated
biotype
management
practices
that
provide
multiple
and
conflicting
selective
pressures,
cou-
pled
with
well-planned
monitoring
of
and
response
to
insect
biotype
emer-
gence,
could
reduce
risk.
Introduced
traits
should
be
based
on
narrow
modes
of
action
that
are
as
distinct
as
possible
from
existing
host
defense
mechanisms.
*
Biotype
evolution
needs
to
be
considered
for
all
gene
transfers,
regardless
of
their
intended
function.
Likewise,
intended
resistance
against
insects
must
accommodate
equivalent
concerns
from
other
ecological
disciplines.
Comprehensive,
multi-
disciplinary
ecological
criteria
gov-
erning
the
release
of
genetically
al-
tered
trees
should
be
researched
and
instituted.
*
Greater
emphasis
should
be
placed
on
the
scope
of
biological
vari-
ation,
the
history
of
pesticide
use,
ecological
feedback,
and
crop-protec-
tion
principles
during
the
training
of
molecular
biology
students
intending
to
develop
transgenic
plants.
Acknowledgments
The
critical
reviews
and
helpful
suggestions
of
L.
Brattsten,
Depart-
ment
of
Entomology,
Rutgers
Univer-
sity;
F.
Gould,
Department
of
Ento-
mology,
North
Carolina
State
University;
W.
J.
Mattson,
USDA
Forest
Service;
R.
T.
Roush,
Depart-
ment
of
Entomology,
Cornell
Univer-
sity;
M.
Wagner,
Department
of
For-
estry,
Northern
Arizona
University;
B.
McCown
and
D.
Ellis,
Department
of
Horticulture,
University
of
Wis-
consin;
R.
L.
Giese,
Department
of
Forestry,
University
of
Wisconsin;
and
S.
Codella,
K.
Klepzig,
and
D.
Robison,
Department
of
Entomology,
University
of
Wisconsin
are
greatly
appreciated.
This
work
was
sup-
ported
in
part
by
the
University
of
Wisconsin-Madison
College
of
Agri-
cultural
and
Life
Sciences.
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