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A Framework for Assessing the

Risk of Transgenic Crops
JAMES F. HANCOCK

The environmental risks of many transgenic crops can be evaluated without additional experimentation by using already available information
on the biology of the crop, the presence of compatible relatives, and the transgene phenotype. The level of crop invasiveness and the location of
compatible relatives can be determined by consulting local floras and the crop literature. Decisions about invasiveness can be bolstered by determining the number of weediness traits carried by the crop and its congeners. The potential impact of transgenes can be ranked by their likely effect
on reproductive success, ranging from neutral to advantageous to detrimental. This scheme can identify not only the low-risk transgenecrop combinations that are safe to deploy but also those that either are too dangerous to release or require additional experimentation.
Keywords: genetically modified crops (GMOs), genetic engineering, invasiveness, gene flow, introgression

here is considerable international concern about the

release of transgenic crops. These concerns have stalled
research, particularly in Europe, where the further development of genetically modified crops has been essentially
stopped. At the forefront have been fears about the risk of
transgene escape into natural populations and an alteration
of the natural balance (Colwell et al. 1985, Ellstrand 1988,
Rissler and Mellon 1996, Marvier 2001). These risks are very
real, and in many instances knowledge is insufficient to allow
deployment of transgenic crops; however, there are cases
where environmental risk can be assigned on the basis of
existing knowledge about the biology of the crop, the proximity of wild relatives, and the phenotypic effects of the
transgene.
Further delays of many biotechnological advances might
be minimized if there were a consistent protocol that could
be used to rank transgenic crops according to their environmental risk. Lengthy delays in release could be avoided by deciding at the onset of research and development what types
of environmental research are needed for future deployment.
In some cases, previous knowledge can be used to decide
that a transgenic crop is of very low risk, and development and
subsequent deployment can proceed rapidly with little additional environmental research. In other cases, transgenic
crops might be deemed of such high risk that their development is foolhardy and should not progress at all. In many other
cases, the transgenic crop might be considered intermediate
in risk and would require varying levels of environmental research before release. Such early analyses could save consid512 BioScience May 2003 / Vol. 53 No. 5

erable time at the point of release by identifying what environmental research should be done during the developmental stage. In this way, when the transgenic crop is ready for
commercialization, it can indeed be released.
This article presents a decisionmaking framework based on
answers to three questions about risk factors: (1) Is a compatible relative present in the areas of deployment? (2) Is the
native relative or crop highly invasive? (3) Will the engineered trait significantly affect the invasiveness of the crop or
native relative? There are other risks involved with the release
of transgenic crops, such as nontarget effects of novel toxins
or development of resistance in native populations, but the
emphasis here will be placed on fitness effects and the potential
to increase invasiveness.
The outlined framework is based on the assumption that
the potential invasiveness of a plant species can be predicted
if we have knowledge about its biology, its distribution, and
the likely fitness impact of a transgene. The factors limiting
gene flow between compatible relatives can be largely ignored, as transgenes will eventually escape into the natural environment if there is a compatible relative near the transgenic

James F. Hancock (e-mail: hancock@msu.edu) is a professor in the Department

of Horticulture, Michigan State University, East Lansing, MI 48824. He is an
evolutionary botanist who also breeds blueberries and strawberries, using
both conventional and biotechnological approaches. He is the author of a
forthcoming book, Plant Evolution and the Origin of Crop Species, which
will be published by CAB International. 2003 American Institute of Biological
Sciences.

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crop (Hancock et al. 1996, Ellstrand 2001), unless the transgenic crop produces no viable gametes or has a system incorporated that prevents embryo viability. With acceptance
of this reality, decisions on risk can focus on evaluating the
invasive characteristics of potential recipient species and
determining whether the transgene itself will have a significant impact on the fitness of those species. North American
crops will be used as examples, but the protocol may work in
any part of the world, depending on the array of crops and
the native progenitors present.

Previous research on risk of gene

escape and crop invasiveness
Numerous authors have pointed out that transgene flow
from engineered crops to their wild relatives could result in
the evolution of increased invasiveness in wild relatives and
in the evolution of pests that are resistant to newly developed
control strategies (Dale 1992, Rissler and Mellon 1996, Snow
and Palma 1997, Hails 2000). Invasive species are defined
here as those that readily increase in numbers and aggressively
spread, outcompeting other species for resources. This applies
in both agronomic and native environments. A species is
considered to have increased invasiveness if its abundance
noticeably increases and it outcompetes a species that it
theretofore could not.
The likelihood of hybridization between crops and their
wild relatives has been measured in numerous studies (Ellstrand 2001). Although the early consensus was that such hybridizations occurred infrequently, research in the last decade
has shown that they are relatively common (Ellstrand et al.
1999, Desplanque et al. 2002) and that crop alleles can persist for long periods in natural populations (Klinger and Ellstrand 1994, Arriola and Ellstrand 1996, Linder et al. 1998).
Factors such as breeding system, flowering time, hybrid viability, and isolation distance can alter the rate of gene escape
(Hokanson et al. 1997, Hancock et al. 1996), but if compatible relatives are within the cloud of crop pollen, genes will
escape.
The first determination that should be made concerning
the risk of transgene escape is whether compatible relatives
exist in the area of deployment. The literature on breeding contains much information on what wild species are compatible
with cropsbreeders frequently want to find potential gene
sources outside the immediate crop speciesand considerable work has been done on elucidating the wild progenitors
of crops. Several large compilations of crop histories provide
portals to the literature (see Sauer [1993], Zohary and Hopf
[1993], Smartt and Simmonds [1995], Hancock [2003]).
Local floras can be used to provide information about the
geographical ranges of species and their invasiveness. Most
floras describe the location and relative abundance of native
species and whether crops persist in the wild. When local
floras representing California (Munz and Keck 1973) and
the southern United States (Radford et al. 1968) and eastern
parts of the United States (Gleason and Cronquist 1963)
were examined, Hancock and colleagues (1996) found that

about 62 percent of the crops that had come under APHIS

(Animal and Plant Health Inspection Service, US Department
of Agriculture) oversight were not persistent in native environments and thus could be considered noninvasive. Another 21 percent persist for a few generations in native environments but eventually disappear. These have slightly higher
native fitness than the nonpersistent crops, but they can still
be considered noninvasive, because they do not spread outside the agroecosystem. About 17 percent fall into the persistent
category; these can be ranked as invasive, because they readily reproduce outside the agroecosystem and spread. The
nonpersistent species are probably of minimal risk in genetic engineering, unless the transgene incorporated has dramatic fitness effects; those in the persistent, invasive class fall
into the high-risk category, both as pollen donors and as
weeds. Those in the persistent but noninvasive category
would be intermediate in risk, depending on the nature of the
transgene and the presence or absence of compatible relatives.
A set of traits associated with plants ability to readily invade disturbed habitats can be used to provide supplementary information on the potential invasiveness of a crop and
its wild progenitors. In a widely cited pair of papers, Baker
(1965, 1974) listed traits associated with the most successful
weeds: broad germination requirements, seed dispersal over
short and long distances, discontinuous germination, vigorous vegetative reproduction, rapid growth to flowering,
brittle propagules, continuous seed production, vigorous
competitors, self-pollination, polyploidy, unspecialized pollinators, long-lived seeds, very high seed output, and plastic
seed production (see box 1). Although Baker was most concerned with identifying those traits associated with success in
disturbed habitats, the same traits can contribute to invasiveness in natural environments.
Keeler (1989) found that what are considered to be the
worlds 17 worst weeds possessed on average 85.6 percent (0.12
Box 1. Traits associated with the most successful
weeds (Baker 1965, 1974)
Broad germination requirements
Discontinuous germination
Long-lived seeds
Rapid growth to flowering
Continuous seed production
Self-pollination
Unspecialized pollinators
High seed output
Seeds produced in many habitats
Seed dispersal over short and long distances
Vigorous vegetative reproduction
Brittle propagules
Vigorous competitors
Polyploidy

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standard error, or SE) of Bakers weediness traits, whereas a
group of 20 randomly selected species had 59 percent (0.20
SE) and crop plants had 42 percent (0.14 SE). This suggests
that the invasive potential of a species can often be characterized by evaluating the number of weediness traits it contains. This classification system is not foolproofKeeler observed considerable variability in each of the categoriesbut
all of the serious weeds had more than 65 percent of the
weediness traits. If this ranking scheme is combined with
information on crop persistence in the wild, it can aid in the
identification of high- and low-risk species. For example, it
is unlikely that the addition of a transgene to a crop that
does not persist in nature and has few weediness characteristics (i.e., less than 40 percent) will make it highly invasive,
unless the transgene has very powerful effects on the phenotype; however, even a subtle change in the phenotype of an
already invasive species with numerous weedy traits (more
than 80 percent) could make it much more problematic. For
those species that persist in native environments and carry
intermediate numbers of weediness traits, risk would be difficult to predict; additional experimentation would be
necessary.

The environm ental impact of transgenes

The potential impact of individual transgenes can be determined by evaluating their phenotypic effect. Although current information may be insufficient to rank the relative risk
of many transgenes, transgenes can be grouped by the type
of impact they have on reproductive fitness: The impact can
be neutral; detrimental; variable, depending on the weediness
of the recipient species; variable, depending on the degree of
natural biological control; or advantageous.
Transgenes that have a neutral effect on fitness might
spread in natural populations through genetic drift, but they
would have no subsequent impact on fitness. Few transgenes
can now be clearly classified in this category, except for the reporter genes used to recognize transformants such as nptII and
B-glucuronidase. These genes have been inserted into a wide
array of genomes without any noticeable effects on phenotype, as long as their placement does not disrupt gene function or regulation. Some of the genes intended to remove toxic
substances through phytoremediation, such as pentaerythritol
tetranitrate reductase (French et al. 1999), can be considered neutral if they have no phenotypic effect on noncontaminated soils and no negative pleiotropic effects.
Other genes, however, such as mercuric ion reductase
(Rugh et al. 1996) and organomercurial lyase (Bizily et al.
2000), should be considered detrimental because they reduce plant fitness in the absence of heavy metal contamination. Genes with detrimental effects will be selected against
in the natural environment and will not spread. Many of the
traits associated with crop domestication fall into this category. The weediness of wild species has been increased in agronomic fields through crop hybridization (Ellstrand and Hoffman 1990), but there is little evidence of the reverse, where
crop genes have affected the fitness of a wild species in its
514 BioScience May 2003 / Vol. 53 No. 5

native environment. In spite of many substantial advances in

breeding for resistance to pests, drought, cold, and salinity,
studies have not yet shown that the native fitness of the wild
species was noticeably changed through hybridization with
the crop progenitor. However, genes with detrimental effects
could become important if population sizes of the compatible relatives of the genetically modified crop are very small
and endangered. In this case, the bombardment of the native
populations by a deleterious gene could result in their extinction through swamping, whereby the fitness of the natural population would be reduced to the point that it could
no longer persist (Rissler and Mellon 1996). I am not aware
of any North American crop relatives that fall into this category, but the possibility exists in other parts of the world.
Examples of transgenes that fit into the detrimental category are male sterility, altered fiber quality, changes in lignin
biosynthesis, and altered fruit ripening and storage characteristics. Transgenes incorporated for biological production
of proteins, such as serum albumin, could also fall into the
detrimental category even though they do not have a direct
negative effect, because such genes could have negative
pleiotropic effects on overall plant vigor. Many of the transgenes used to alter the amino acid composition of proteins
for improved nutrition must also be placed in the detrimental category, at least initially, until it can be proved that they
do not have negative pleiotropic effects on growth and
development.
The transgenes that produce herbicide and pest resistance
will vary in their fitness potential, depending on the invasiveness of the recipient species and the level of natural control. Genes for viral, fungal, and pest resistance fall into a group
whose incorporation into natural populations could increase
fitness, if the pest is currently controlling natural populations.
The role of disease in controlling natural populations is just
beginning to become clear, but there are at least a few examples where the removal of insect pests has been shown to have
significant impacts on the reproductive success of native
species (Marvier and Kareiva 2000). Some of the transgenes
already deployed that fall into this category are Bt genes for
insect resistance in a number of crops; phytophothora, PLRV,
and PYV resistance in potato; PRSV resistance in papaya; and
CMV, WMV2, and ZYMV in squash. Herbicide resistance
genes fall into a separate category, because they are selectively neutral in the natural environment, though if they
were incorporated into already weedy species, they could
abolish a valuable method of control. Examples of these
transgenes are those providing resistance to phosphinothricin,
glyphosate, and sulfonylurea in a wide array of crops.
Transgenes that change the environmental tolerance of a
species or alter its patterns of growth and development could
result in dramatic adaptive shifts and have a major impact on
fitness. For example, juvenility in trees might be reduced by
overexpression of a regulatory gene such as LEAFY (Pea et
al. 2001), allowing for earlier reproduction and possibly
greater overall reproductive success because of more frequent flowering. The cold tolerance of species might be altered

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by the overexpression of the transcription factor CBF1
(Jaglo-Ottosen et al. 1998, Jaglo et al. 2001), in which case the
adaptive range of the species would shift to more northern
climates. If they escaped, transgenes such as metallothioneins
(Cai et al. 1995), which are used in phytoremediation to remove heavy metals, could also allow a native species to invade
new, heavy-metal-laden habitats.
It should be noted, however, that many of the transgenes
that dramatically alter the physiological tolerances of crop
species can also have negative fitness effects that would make
them deleterious in the native environment. Stabilizing selection has operated in natural populations to optimize physiological function, and the kinds of genes sought by farmers
will often be radically different from those that promote
overall fitness in wild plants under intense competition. For
example, overexpression of CBF1 might increase cold tolerance, but it dramatically alters the development of Arabadopsis thaliana and Brassica oleraceae, resulting in reduced vigor
(Jaglo-Ottosen et al. 1998, Jaglo et al. 2001). Earlier reproduction in a woody species could result in reduced fitness, because the plant might be weakened by early reproduction or
might ultimately produce far fewer seeds. The plants engineered for phytoremediation may not grow as rapidly as
their antecedents and may be outcompeted in natural environments. If super-genes do emerge that are dramatically
more powerful than conventionally derived ones, they may
often have complex effects with negative impacts on overall
fitness in nature. In such cases, the transgenes can be deemed
safe for development.
One fear that has been expressed is that transgenes will have
unexpected epistatic or pleiotropic effects in natural populations. While this possibility cannot be completely excluded,
it is highly unlikely; the constructs that have been selected for
deployment in crops have already faced numerous phenotypic
screens, from the initial transformations to the final field
screens before release. If there is doubt about their overall effects in the crop, further research is indeed warranted before
deployment, but it is improbable that the transgenes will act

differently in the crops than in their progenitor genome or that

they will have more extensive epistatic or pleiotropic effects
than native genes. Genes have been moved from native species
to crop species by breeders without any unexpected ramifications, and as discussed earlier, substantial gene flow has occurred between conventionally bred crops and wild species
without any apparent dramatic, unexpected alterations in
phenotype.

A fram ework for estim ating the environmental

risk of trangenic crops
The considerations outlined above suggest that there are two
major factors that influence the environmental risk of transgenic genotypesthe potential invasiveness of the species and
the relative impact of the transgene on fitness. Of course,
species have differing geographical ranges, and estimates of
invasiveness may vary from country to country. In addition,
a transgene deemed safe in one area may be risky in another.
The relative risk of a transgenic crop needs to be determined
for all geographic regions in which it will be deployed. The
availability of compatible relatives and the biology of the
crop itself determine the degree of invasive potential the
crop possesses. Various crops are grouped in table 1 into
what will be referred to here as species categories, in accordance
with their invasive potential. In addition, several degrees of
risk are associated with particular transgenes, depending on
whether the fitness impact of the genes is neutral or selectively
advantageous. These are outlined in table 2 and will be referred
to as transgene categories. The overall environmental risk of
the transgenic crop can be determined by combining these two
categories.
The six species categories shown in table 1 are
S-1: Crops that have no compatible relatives, carry few
weediness traits (less than 40 percent), and do not persist in natural environments
S-2: Crops that have no compatible relatives, carry intermediate numbers of weediness traits, rarely escape, and
do not persist in natural environments

Table 1. Invasive biology of crop species and their compatible relatives in North America.
Category

Biology

Examples of crops in North America

S-1

No compatible relatives. Crop carries only a few

weediness traits and does not escape or persist.

Broccoli, cabbage, cauliflower, citrus, cucumber, cotton, eggplant,

pea, potato, soybean, sugarcane, tomato, and watermelon

S-2

No compatible relatives. Crop carries an intermediate

number of weedy traits but rarely escapes and does
not persist.

Peanut and beans

S-3

No compatible wild relatives. Crop carries many weediness

traits and can escape and persist.

Barley and wheat

S-4

Has compatible relative. Crop or relative carries

only a few weediness traits. Crop can escape but does
not persist. Native relative does not aggressively spread.

Celery, lettuce, maize, melon, pepper, squash, and tobacco

S-5

Has compatible relative. Crop or relative carries

intermediate numbers of weedy traits. Crop can escape
and persist. Native relative does not aggressively spread.

Apple, asparagus, beet, blueberry, carrot, cranberry, onion, pear,

poplar, plum, radish, spruce, and strawberry

S-6

Has compatible wild relative. Crop or relative carries

many weediness traits. Crop can escape and persist.
Native relative spreads aggressively.

Oats, rapeseed, rice, sorghum, and sunflower

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S-3: Crops that have no compatible wild relatives, carry
many weediness traits, and can escape and persist in
natural environments
S-4: Crops that have compatible relatives, carry few
weediness traits, and can escape but do not persist in
natural environments; their compatible relatives also
carry few weediness traits and do not aggressively spread
S-5: Crops that have compatible relatives, carry intermediate numbers of weediness traits, and can escape
and persist in natural environments; their compatible
relatives also carry intermediate numbers of weediness
traits but do not aggressively spread
S-6: Crops that have compatible wild relatives, carry
many weediness traits, and can escape and persist in
natural environments; their compatible relatives also
carry many weediness traits and aggressively spread

The five transgene categories presented in table 2 are

T-A: Transgenes that are selectively neutral in the natural environment
T-B: Transgenes that have negative impacts on fitness
T-C: Transgenes for herbicide resistance
T-D: Transgenes for pest resistance
T-E: Transgenes that alter environmental tolerance or
development
The relative risk of deployment of transgenic crops is
shown in table 3. According to this scheme, any transgenes that
do not have nontarget influences are safe for deployment in
S-1 crops without further experimentation. Crops such as
potato and soybean have no compatible relatives in the United
States. Thus, transgenes cannot escape into native relatives,
do not persist in native environments, and have so few weediness traits that even dramatic changes in their adaptations
(T-E) are highly unlikely to make them invasive. In addition,
it is relatively easy to control them without herbicides, so the
incorporation of T-C transgenes is unlikely to cause major pest
problems.
All transgenes except those with major impacts on adaptation are probably safe to deploy in S-2 crops without further experimentation. These species would have no compatible relatives, so transgenes could not escape, but the crop could
escape and would have enough weediness traits that a dramatic
change in its adaptations (T-E) could make it invasive. T-C
genes would be of low risk, because it is relatively easy to

control an S-2 crop without herbicides, and because to date

these species have not evolved resistance to the available
herbicides. Most pest resistance transgenes (T-D) would also
be of low risk, as there are no reported incidences, to my
knowledge, where a single pest has been shown to play a
major role in preventing a crop from becoming a weed. More
scrutiny would have to be placed on genes that confer broad
rather than narrow resistance, because their spectrum of
target organisms would be larger.
Only T-A and T-B genes are safe to deploy in both S-3 and
S-6 species. S-6 crops such as sorghum and rice already spread
aggressively in native environments, so any change in their fitness might make them a greater pest, and beneficial transgenes
associated with environmental tolerances (T-E) and pest resistance (T-D) could escape through pollen flow and further
increase the invasiveness of the native species. S-3 species
such as barley and wheat have no compatible relatives, so there
is no risk of transgene escape. The crop itself, however, is persistent in native environments, so any increase in its fitness
through increased adaptation (T-E) or pest resistance (T-D)
might make it more invasive. Herbicides are used to control
the S-3 and S-6 species as weeds, so the deployment of genotypes with T-C must be carefully evaluated. S-6 species are
strong competitors and have large population sizes, so the
escape of deleterious alleles is unlikely to have a negative impact on the species.
Only T-A and T-C genes are safe to deploy in S-4 species.
Crops such as maize, melon, and squash carry few weediness
traits and do not persist in native environments. Even dramatic
changes in these crops adaptations are unlikely to produce a
greater agronomic pest; however, beneficial transgenes associated with environmental tolerance (T-E) and pest resistance (T-D) could escape into natural populations and alter
their fitness characteristics. These would require a case-by-case
evaluation of the role of these factors in limiting their range.
S-4 species are at best only modest competitors, so the escape
of deleterious alleles could have a negative impact on their natural populations. T-C genes are relatively safe for deployment in S-4 crops, because the crops and their relatives are easy
to control without herbicides and to date they have not
evolved resistance to the available herbicides.
The T-A, T-B, and T-C genes are safe to deploy in S-5
crops such as apple or strawberry. Because these crops have
intermediate numbers of weediness traits and do escape, a

Table 2. Relative fitness impact of transgenes.

Category

Fitness impact

Examples of transgene use

T-A

Neutral in the native environment

Marker genes

T-B

Detrimental in the native environment

Male sterility, altered fiber quality, altered fruit ripening, and storage

T-C

Variable, depending on invasiveness of crop or native

relative

Herbicide resistance

T-D

Variable, depending on level of biological control

Viral, fungal, and pest resistance

T-E

Potentially advantageous in the native environment

Cold, drought, and metal tolerance; improved nutrient uptake;

altered development

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Table 3. Transgenic crops safe to release without further experimentation.
Crop category

Transgene category

Transgene characteristics

S-1

T-A, T-B, T-C, T-D, T-E

There are no compatible relatives, and the crop has so few weediness traits that even the most
dramatic changes in phenotype are highly unlikely to make it invasive. The crop is easy to control
without herbicides.

S-2

T-A, T-B, T-C, T-D

There are no compatible relatives, but the crop has enough weediness traits that a dramatic
change in its adaptations could make it invasive. A lack of pest resistance is unlikely to be the
primary factor preventing invsasiveness. The crop is relatively easy to control without herbicides.

S-3

T-A, T-B

There are no compatible relatives, but the crop itself is weedy, so any change in its fitness might
make it more invasive. Herbicides are also needed for the crops control.

S-4

T-A, T-C

The crop or native relative has so few weediness traits that even the most dramatic
changes in phenotype are highly unlikely to make it invasive in agronomic systems; however,
advantageous and detrimental transgenes could escape into natural populations and significantly
alter their fitness. It is relatively easy to control the crop and its relatives without herbicides.

S-5

T-A, T-B, T-C

The crop or native relative has enough weediness traits that a dramatic change in their
adaptations could make it invasive; however, advantageous transgenes could escape into natural
populations and positively alter their fitness. The escape of detrimental traits is unlikely to have
long-term influences on native populations, because population sizes are large. It is relatively
easy to control the crop and its relatives without herbicides.

S-6

T-A, T-B

The crop is already invasive, so any positive change in its fitness might make it a greater pest.
Beneficial transgenes associated with environmental tolerances and pest resistance could
escape into natural populations and alter their fitness. The escape of detrimental traits is
unlikely to have long-term influences on native populations, because population sizes are large.
In addition, herbicides are needed for the control of the crop and its relatives.

dramatic change in their adaptations could allow them to be

more invasive. Beneficial transgenes associated with environmental tolerance (T-E) and pest resistance (T-D) are also
risky, since they could escape into natural populations and alter species fitness. Detrimental traits (T-B) could also persist in native populations and diminish their fitness if native
population sizes are low, but this is much less likely in S-5 than
in S-4 species, which are stronger competitors. It is relatively
easy to control the crop and its relatives without herbicides,
so the deployment of T-C should not dramatically affect
control.

Cases where additional experim ents are needed

The types of further experimentation that are needed will depend on the type of croptransgene combination (table 4).
The risk involved in the deployment of any transgene can be
deemed low and needing no further experimentation if the
phenotypic effects of the transgenes closely mimic conventionally deployed or native genes (Hokanson et al. 2000).
This would fit a number of genes for pest resistance (T-D),
many of which affect aspects of plant development such as
flowering time, and alterations in environmental tolerance (TE). If similar genes are already in natural populations, the genes
have already faced the sieve of natural evolution and are

unlikely to have a major impact. Examples of similar phenotypes include the pest resistance previously mentioned, developmental processes such as early flowering or photoperiod insensitivity, and physiological tolerances to cold or salt.
If the native species already carries a phenotype that is being
engineered into the crop, it is unlikely to have a significant impact on fitness.
This approach, in which transgene phenotypes are used to
assign risk, was recommended by the first group of scientists
who evaluated the environmental risks of transgenic crops
(Tiedge et al. 1989) and in the National Research Council report (CLS 1989) Field Testing Genetically Modified Organisms:
Framework for Decisions. Unfortunately, although many of the
transgenes that have an impact on resistance are similar to conventionally deployed resistance genes (Hokanson et al. 2000),
many are not. Also, many of the other types of transgenes influencing physiological traits will produce phenotypes that are
unique to the species or have broader effects than the native
genes. These situations will require further experimentation,
depending on the invasive characteristics of the transgenic crop
species.
Among those crops that are not invasive themselves and that
do not have compatible relatives but do have intermediate
numbers of weediness traits (S-2), it will be necessary to

Table 4. Various croptransgene combinations that require further experimentation.

Transgene category

Crop type

Further research needed

T-A

None

T-B

S-4, S-5, S-6

None.

T-C

S-3, S-6

Document that any wild recipient species can still be controlled as agronomic weed.

T-D

S-1, S-2

Show that a similar phenotype exists in wild populations. If not, measure levels of native
biological control. If levels are significant, test fitness of transgenic crop and hybrids in
representative native environments.

T-E

S-1

Document that wild recipient species is not endangered.

Show that a similar phenotype exists in wild populations. If not, test fitness of transgenic crop
and hybrids in representative native environments.

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determine whether the genes causing dramatic change in
the crops adaptations or development (T-E) could make
them more invasive. If clearly deleterious pleiotropic effects
are observed in the initial field and greenhouse trials of the
transgenic crop, the transgene can be downgraded to T-B and
further experimentation will not be necessary. However, if no
clear negative interactions were observed, the fitness of the
transgenic crop will need to be tested at multiple sites in a
range of the natural environments found adjacent to crop
fields. Crowley and colleagues (2001) have provided a model
of how this can be done.
In the other crops that are not invasive themselves but
have proximal native relatives (S-4 and S-5), further research
will be warranted for the genes associated with detrimental
traits (T-B), pest resistance (T-D), and dramatic alterations
in physiology and development (T-E). The fitness impact of
T-E transgenes will have to be determined on the crop, as well
as on F1 hybrids and backcrosses with native plants (Rissler
and Mellon 1996). Likewise, beneficial genes associated with
pest resistance might also escape from these transgenic crops
into the native populations, so their fitness impact must also
be examined (Bartsch et al. 1996, 2001). As previously noted,
a similar phenotype might have been reported from native
sources, which would eliminate the need for further experimentation, but if this is not the case, the transgenes influence
on fitness would have to be measured on F1 hybrids and
backcrosses with native plants (Rissler and Mellon 1996). In
the case of deleterious genes (T-B), before the transgenic
crop can be released, it will be necessary to document that the
population sizes of wild compatible relatives are large. If the
population sizes of native relatives are very small and can be
classified as endangered, the transgenic crop should not be released.
Among the crops that can persist in nature with or without native relatives (S-3 and S-6), further research will need
to be conducted on the impact of transgenes associated with
pathogen or insect resistance and physiological or developmental shifts. In the case of S-3 crops without native relatives,
the effect of the transgene on fitness will only have to be
measured on crop genotypes across a wide array of natural
environments (Crowley et al. 2001); however, with S-6 crops
that have compatible relatives, the fitness of F1 and backcross
individuals will have to be tested also in the native environment. Transgenes associated with herbicide resistance should
not be incorporated in either S-3 or S-6 crops, because farmers will lose a valuable means of controlling them as agronomic
weeds.

Conclusions
The environmental risk of many transgenic crops can be
evaluated with little further study than that conducted during their development.When the biology of the crop is known
and the nature of the transgene is understood, low- and
high-risk categories can be clearly identified without additional
experiments. In the middle-risk category, further experimentation is necessary only if phenotypes similar to that of
518 BioScience May 2003 / Vol. 53 No. 5

the transgene cannot be identified in native populations.

Careful evaluation of the fitness characteristics of transgenic
genotypes during the developmental stage also can obviate the
need for additional experimentation. If such measures are employed early during research and developmentbefore a
company tries to release a transgenic cropcostly mistakes
may be averted. Evaluation efforts should be aimed at identifying the low-risk transgenic crops for which commercialization can move rapidly; the medium-risk categories of
crops, for which ecological research must be conducted alongside the biotechnology; and the high-risk transgenic crops,
whose further development should be discouraged.

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