www.checkbiotech.org ; www.raupp.info ; www.czu.cz

Insect resistance (IR) transgenes offer the advantage to agricultural plants
of protection from herbivory. There is concern that should IR transgenes
escape from the agricultural setting through pollen or seed flow, the
advantage conferred by the transgene will not only allow them to persist,
but to 'take over' natural populations, January 2006 by Colleen K. Kelly.

Transgene take-over is seen as a problem in that a transformed plant may
be unavailable to the herbivores natural to the system, making them more
vulnerable to extinction through lowered population size, and so on up the
food chain.

To address the concern that resistance transgenes might persist in the
natural system, Kelly et al. have produced an analytical model targeting the
ecological interaction between IR transformed and untransformed plants in
the natural community. Successful establishment of a novel allele in a
population is a combination of not just the allele's ability to disperse
through pollen and propagule, but also the novel allele's compatibility with
the genome of the natural population and the ecological dynamic between
plants with and without the new allele, i.e., effective gene flow. Kelly et
al.'s analytical model specifies the overall character of interactions
between factors, allowing predictions outside the range of tested
conditions. By so doing, the model not only assesses the risk of any
particular transgene, it also identifies points in the dynamic that are
sensitive to or may best reward manipulation for control of transgene
impact.

Kelly et al. approached the problem of insect resistance transgenes in
natural populations by recognizing that temporal fluctuations are the
central character of the ecological dynamic: year to year variability in
herbivory is the rule in both natural and agricultural systems. The
appropriate class of models is therefore a storage dynamic, called so
because the long-term persistence of a population through periods of low
reproduction is 'stored' in either long-term reproductive capacity or
dormant propagules. Storage models focus on the probability of recruitment
into the reproductive class. The action of the selective factor is thus most
important at immature stages of the plant, a schedule also consistent with
herbivory, where the same amount of herbivore damage can kill young or small
plants but has little effect on larger, mature plants.

For a competitive interaction between plants with and without an IR allele,
the dynamic is a two-member lottery model comprising one plant type that is
more sensitive to the selective factor than the other?the untransformed and
transformed lineages, respectively. Differential sensitivity dictates that
when the selective factor is present (here, herbivory), the resistant type
has the advantage. However, when the selective factor is absent, the
resistant type has no advantage, and if there is any net cost associated
with resistance, that cost will set the resistant type at a competitive
disadvantage for the period the selective factor is not acting. Whether
transformed and untransformed plants may stably coexist and in what relative
abundances or whether the IR transgene will take over the population depends
on 1) the relative frequency of good and bad conditions (high and low
herbivory), 2) the relative advantage the IR transgene gives a transformed
plant, and 3) the relative disadvantage, if any, the IR transgene carries
with it. The differential sensitivity (DS) model was applied to oilseed rape
(OSR), where it was found that under levels of herbivore variability
established in the field, it takes relatively little disadvantage of
carrying the transgene to limit domination of the natural population by the
IR allele.

This may be treated as a general conclusion. However, the larger point is
not that IR transgenes may be relatively easily contained. Rather, the
ecological model provides a tool with which to determine how best to do
this, as well as to assess how well it has been done. In the model, all
terms are ratios of the character in question in the transformed versus
untransformed plants. The risk of a transgene can thus be assessed under
protected conditions and calibrated by the response of the untransformed
plant under more natural conditions, as at least a first pass evaluation.

It may be possible to manipulate either costs or benefits in order to
contain the transgene. Benefit, which is quantified in the model as growth
in the absence of competition, by definition is maximized for commercial
return on the crop, and so may not be available for manipulation. Costs may
therefore be the more likely target for manipulation: if you are going to
have a magic helmet then you must have an Achilles heel. Some costs are a
function of resistance itself, e.g., additional protein construction. It is
not possible to have the transgene without these costs and the trade-off
between costs and benefits in this case would be in choosing the transgene.
As with any 'cost', its usefulness as a control will come in two parts: the
extent to which it does not cut into commercial returns on the transgene;
and the reliability of its genetic linkage to the transgene over time.

The model delineates control possibilities in addition to costs inherent to
the transgene. Costs most amenable to manipulation are included in two
composite variables: seedling competitive ability (â) and seeds viable in
the first season after seed set (?). â includes factors such as overtopping,
and this is where construction costs would be taken into account. ? is not
simply seed set; ? determines not just seedlings in year t + 1, but the
character of the seed bank. ? interacts with the behavior of seeds in the
seed bank (germination fraction, persistence from season to season) to
produce seedlings in future seasons. It is an essential part of the
population persistence of a species that has a chance of producing few or no
successful offspring in any one year. ?, the number of seeds that make it
through the first winter viable, is the first level of control for any novel
allele. If ? is low, then there are few viable seeds to remain in the seed
bank and the capacity to get through bad years is severely limited. If ? is
high, then control shifts to the germination fraction ?. If ? is high, then,
again, there are few seeds in the seed bank to get through bad years. If ?
is low, control shifts to S, the fraction of seeds that survive from one
year to the next. Persistence over hard times is then limited by a low S.
Pollen viability, ç, where male sterility manipulation may be applied, plays
a similar role to Y.

The equations of the model may be iterated numerically but Kelly et al. also
provide a useful calculation for doubling time to assess the rate of spread
of the transgene at early stages (when hemizygotes, individuals with only
one copy of the transgene, comprise approximately less than 20% of the
population). Although it requires the same information as the more detailed
calculations that gave rise to the above conclusions, the doubling time
equation is easier to calculate and provides a reasonable estimate of
hemizygote spread.

The focus on the natural population may seem to imply that the ecological
interaction will be of importance only once the allele arrives there. In
fact, it is likely that the ecological dynamic will have an effect at every
step of the journey of the allele from crop to natural community. As
introgression of the allele into the natural genome proceeds, the increment
of protection that the allele offers will decrease in the context of the
already well-protected wild genome; any cost it incurs is likely to have
greater impact in a natural situation in which nutrient supplements become
less and less available with increasing distance from the 'home'
agricultural field. The model can be applied to determine this, by
specifying the values of the factors that go in the applicable ratios.

The goal of the model is to clarify the components and importance of fitness
in the interaction between individuals with and without IR alleles in
nature. The model may be usefully modified to include pathogens and seed
predators that work either on the seed while it is still retained on the
parent plant or in the seed bank. However, the model is also of significance
to the basic ecology of sexually compatible invasive-native pairs where the
active difference is in vulnerability to local herbivores, pathogens, or
seed predators, whether the invasive individual is a crop, unwanted alien,
or new mutation.

References

GM Science Review Panel. (2003) GM science review (first report): an open
review of the science relevant to GM crops and food based on interests and
concerns of the public. Department of Trade and Industry, London, pp.
109-194

Information Systems for Biotechnology (2004) ISB News Report, January 2004,
available online: [www.isb.vt.edu]

Kelly CK, Bowler MG, Breden FM, Fenner M, Poppy GM. (2005) An analytical
model assessing the potential threat to natural habitats from insect
resistance transgenes. Proceedings of the Royal Society of London B 272,
1759-1767

Hendry AP, Taylor EB, McPhail JD (2002) Adaptive divergence and the balance
between selection and gene flow: Lake and stream stickleback in the misty
system. Evolution 56, 1199-1216

NERC Centre for Population Biology, Imperial College (1999) The global
population dynamics database. Available online:
http:www.sw.ic.ac.uk/cpb/cpb/gpdd.html

Kelly CK, Hanley ME (2005) Juvenile growth and palatability in congeneric
British herbs. American Journal of Botany 92, 1586-1589

Kelly CK, Bowler MG (2005) A new application of storage dynamics:
differential sensitivity, diffuse competition and temporal niches. Ecology
86, 1012-1022

Belsky AJ, Carson WP, Jensen CL, Fox GA (1993) Overcompensation by plants ?
herbivore optimization or red herring? Evolutionary Ecology 7, 109-121

Colleen K. Kelly
Senior Research Associate, Department of Zoology
University of Oxford, South Parks Road, Oxford OX1 3PS UK
colleen.kelly@zoo.ox.ac.uk

[www.isb.vt.edu]

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