Summary
Introduction
A Perspective on the Origin and Evolution of Crop Plants
The Effects of Evolutionary Forces on The Fate Of Hybrids
The Effects of Structure of the Indigenous Plant Population
Conclusions and Recommendations
References
Summary
While many classes of transgenes are similar to those manipulated by conventional
breeding techniques or evolution, biotechnology offers the potential to introduce genes
into crops which are novel both from the point of view of function and origin. Forces
affecting the rate of spread and increase of hybrids between genetically modified crop
plants and their related species remain qualitatively similar, irrespective of whether
genetic modification was achieved using traditional methods, those of biotechnology or
as a result of the natural evolutionary process. However, the precise effect of the
forces and, consequently, the likely environmental impact of such hybrids, may depend
strongly on the nature of the gene or genes introduced into the native species. The
qualitative similarity between transgenes and the products of conventional or
evolutionary modification suggests that a historical view of the environmental impact of
hybrids between traditionally produced crops or exotic species and their relatives would
be of use in estimating the probable fate of hybrids containing transgenes in the
environment. However, with certain classes of transgenes for which there are no
existing analogues, there will need to be greater care in assessing the possible risks
associated with release into the environment.
This section provides a brief overview of some of the consequences of hybrids
produced naturally and between conventionally bred crop plants and their related
species. Some specific case studies involving the impact of such hybrids on the
agricultural and natural environment will be presented. Finally, a brief review of the
forces responsible for changing the frequency of individuals in populations will be given,
together with examples of important interactions between these forces and other
ecological parameters.
Introduction
The consequences of releasing transgenic crop plants into the environment may have
an impact on the environment in a number of different ways, ranging from the effects of
the transgenic organism itself on indigenous species, to the use of a product derived
from the crop. The purpose of this chapter is to describe the forces that may act on a
hybrid formed between the transgenic crop and its wild relatives. It is highly likely that
such hybrids will be formed when GM plants are released into their centres of origin. It
is extremely important therefore, to discuss the possible impact of such hybrids on that
environment, particularly since centres of origin are usually synonymous with centres of
diversity and may contain very valuable genetic resources.
Since it is a reasonable expectation that transgenes will be transmitted from generation
to generation in a manner which is familiar to geneticists, that is, under the laws of
Mendelian genetics for nuclear genes and under more or less uniparental (often
maternal) inheritance for cytoplasmic genes, examples attesting to the fate of
inter-specific hybrids between non-transgenic species will be considered appropriate
biological models in this context.
A Perspective on the Origin and Evolution of Crop Plants
A study of the evolutionary history of modern crop species shows that a large number
are the products of inter-specific hybridization. Notable examples include wheat, which
has changed from the no longer cultivated, diploid, Einkorn and Emmer, through
several allotetraploid species (including some still in commercial cultivation, e.g.
Triticum durum) to the allohexaploid bread-wheats including T. aestivum. The
bread-wheats contain three different haploid genomes and probably arose as
interspecific hybrids between early crops and indigenous weedy grasses followed by a
doubling in ploidy to recover sexual fertility. The different hybridization events occurred
as the geographic range of cultivation radiated out from the centre of diversity in the
Fertile Crescent, both during and after the Neolithic expansion. While wheat is perhaps
an extreme example with respect to the number of wild species involved in
hybridization, it is by no means an exception (see Simmonds, 1976, for examples).
The above examples are indicative of the extent to which interspecific hybridization
occurred between early crop plants and their weedy relatives. It should be noted that
these hybridization events were of great significance for crop improvement, but they
represent an impact on the crop itself and not on the indigenous species. Regrettably, it
is inevitable that evolutionary studies should have concentrated on the crop plant and
tended to ignore the weed species. In many respects, this is due to a lack of suitable
material from non-domesticated species on which to work. Nevertheless, it leaves the
question unanswered as to the degree of impact of the crop on its indigenous weedy
relatives. However, it is almost inconceivable that such a reciprocal effect did not occur,
altering the indigenous weeds to an extent that unfortunately cannot be estimated.
More recent studies, using modern techniques, have been applied to looking at the
relationship between the three forms of beet, Beta vulgaris (Boudry et al., 1992). The
three forms are inter-fertile and are:
-Beta vulgaris ssp. vulgarissugar-beet, fodder beet & beetroot
-Beta vulgaris ssp. maritimasea beet or wild beet
-Beta vulgaris ssp. unknownweed beet or ruderal beet
Weed beet was first reported as a problem to agriculture in the USA during the 1920's,
with the situation worsening rapidly in California in the 1950's. The problem in northern
Europe became apparent in the 1970's and is a serious problem for some sugar-beet
growers in continental Europe and, to a lesser extent, the UK. The major difference
between weed- and sugar-beet is the requirement for plant vernalization to induce
flowering in the crop. This character is under a simple one-locus, two-allele control with
the allele for bolting dominant to that for non-bolting. The maritime populations of
sea-beet in Europe show great variability for vernalization requirement. However, in the
regions of sugar-beet seed multiplication in France, ruderal beet is homozygous for the
bolting allele. Recurrent hybridization between seed multiplication lines and ruderal beet
has resulted in the transfer of the bolting characteristic to individuals within the
sugar-beet varieties, with the resulting "weed-beet" problems when the crop is grown in
northern Europe. An analysis of cytoplasmic markers in the sugar-beet varieties and
weed-beet suggests that weed beet is the result of a cross between ruderal beet as the
male parent and the crop as the female parent. Studies of ruderal populations around
the peripheries of the main areas of sugar-beet seed production in France show that
both nuclear genes and, less frequently, cytoplasmic genes from the crop have
introgressed into wild or weed populations. The environmental impact of this exchange
of genes is not, however, clear.
The Effects of Evolutionary Forces on the Fate of Hybrids
There is a tendency for workers attempting to quantify the impact of a hybrid between a
genetically modified crop and an indigenous species to concentrate on measuring the
'fitness' of that hybrid. Fitness is only one of a number of evolutionary forces that may
affect the frequency of genes in a population. When a hybrid first appears as the result
of an 'escape' from a transgenic crop, it is likely to be at a relatively low frequency in the
indigenous population and the major determinant of its fate will be random genetic drift.
In addition, the early rounds of sexual reproduction, after such an escape, will be mainly
backcrosses between the hybrid and the native species, making estimation of the
fitness of the hybrid even less relevant in terms of predicting the fate of the crop genes
that it carries. Another force, of particular relevance to these hybrids, is the recurrent
migration of genes from crops into indigenous species. This force will have a magnitude
which will depend on the probability of gene transfer (=hybrid formation) and the scale
on which the crop is grown relative to the size of the indigenous recipient species.
Consider, for example, the case of a transgenic crop which can form hybrids with an
indigenous ruderal or weedy species. As the scale on which the crop is grown
increases, so does the magnitude of gene flow from the crop to the weed. As soon as
the magnitude of this gene flow increases to beyond that of gene exchange of the weed
with other local populations of the same species, the frequency of genes of crop origin
will increase in frequency in the weed population, irrespective of whether the hybrids
show increased relative fitness. Indeed, the magnitude of this directional gene flow
may be sufficient to overcome slight fitness disadvantages of the hybrid. This type of
phenomenon is clearly dependent on the scale on which the crop is grown and, as
such, spread of genes of crop origin may not be detected in the small scale field trials
which would normally precede the full scale commercialization of a transgenic crop
plant.
It is, therefore, perhaps more pertinent when measuring fitness of hybrids between
transgenic crops and their relatives to be reassured about the lack of risk only when the
hybrid can be shown to be markedly less fit than the weedy species or when the
introduction of crop genes into indigenous weeds can be expected to pose no
environmental threat.
The Effects of Structure of the Indigenous Plant Population
In addition to the evolutionary forces acting on the genotypes of hybrids determining
their rate of increase, another factor that needs to be taken into account is the way in
which the recipient population is distributed in space and time. Simplistic estimates can
be made of rates of increase of genotypes, given estimates of the magnitude of the
evolutionary forces acting (e.g. Kareiva et al., 1991). However, these estimates
generally fail to take account of any spatial or temporal heterogeneity of the recipient
populations. This heterogeneity may be due to different magnitudes and/or directions of
evolutionary forces acting in time or space or may simply be due to partial barriers to
gene flow in patchily distributed populations.
Considering a simple neutral gene model, it is easy to show that the probability of a
particular gene reaching fixation in a population depends only on the frequency of that
gene and is independent of the structure of that population (Maruyama, 1970,1971).
However, both the rate of spread of a gene and its rate of increase are strongly
dependent on the structure of that population, being determined by the connectivity of
the patches (number of connections and magnitude of gene flow among them).
In particular, in a highly subdivided population, it is relatively easy for a gene to become
locally abundant (even in the face of a weak selective disadvantage), but it will rarely
spread far. In contrast, the distance spread by a gene in a highly connected population
may be large but it rarely reaches a high frequency in any locality.
Since many agricultural weeds and ruderal species are very patchily distributed, their
spatial structure may well be the major determinant of the rates of increase and spread
of genes introgressed from transgenic crops. Although population genetic theory,
outlined above, allows certain approximate statements to be made concerning the fate
of such genes, there has been insufficient work on more 'ecologically realistic'
population structures to allow reasonable inferences to be made concerning rates of
spread of genes. In particular, if a patchily distributed species suffers repeated local
extinction-recolonization events (a metapopulation, Levins, 1971), while the connectivity
of the patches will be relatively high (and as a consequence the wide spread of genes
outlined above), the prediction of classical theory that a gene will not become locally
abundant no longer necessarily holds. The probability of local abundance will be
determined primarily by the number and origin of founders of a recolonized patch. That
is, the local gene frequencies will be determined principally by founder effects.
Conclusions And Recommendations
1)Given the qualitative similarity of hybrids produced by the natural evolutionary
process and genetic manipulation, i.e. conventional modification and biotechnology,
more emphasis should be placed on the relevance of existing information concerning
the fate of naturally or conventionally produced hybrids in the environment.
2)In the absence of existing information, it may often be preferable to design
appropriate large-scale experiments using conventionally produced 'biological models'
rather than to carry out smaller, more costly, experiments with the products of
biotechnology.
3)The presence of selective advantage in a hybrid is not necessary for its spread in
indigenous species. It is important to recognise the existence of other,
scale-dependent, evolutionary forces such as recurrent migration.
4)The rate of spread and rate of increase of a gene in a population may depend as
much on the spatial and/or temporal structure of the recipient population as on the
biological attributes of the hybrid itself. There is a need for an improved theoretical
basis of description of the fate of genes in more ecologically realistic situations such as
those described by metapopulation models.
References
Abbott, R.J. (1992) Plant Invasions, Interspecific Hybridization and the Evolution of New
Plant Taxa. Trends in Ecology and Evolution, 7, 401-405.
Abbott, R.J., Ashton, P.A. and Forbes, D.G. (1992) Introgressive origin of the radiate
groundsel, Senecio vulgaris L. var. hibernicus Syme: Aat-3 evidence. Heredity, 68,
425-435.
Ashton, P.A. and Abbott, R.J. (1992) Multiple origins and genetic diversity in the newly
arisen allopolyploid species, Senecio cambrensis Rosser (Compositae). Heredity, 68,
25-32.
Boudry, P., Saumitou-Laprade, P., Vernet, Ph. and Van Dijk, H. (1992) Les betteraves
mauvaises herbes: origine et évolution. In: IXème Colloque Internationale sur la
Biologie des Mauvaises Herbes. Editions INRA.
Grant, V. (1981) Plant Speciation (2nd. edn.). Columbia University Press.
Harris, S.A. and Ingram, R. (1992) Molecular systematics of the genus Senecio L. I.
Hybridization in a British polyploid complex. Heredity, 69, 1-10.
Levins, R. (1971) Evolution in Changing Environments (2nd edn) Princeton University
Press.
Kareiva, P., Manasse, R. and Morris, W. (1991) Using models to integrate data from
field trials and estimate risks of gene escape and gene spread. In: MacKenzie and
Henry (eds.), Biological Monitoring of Genetically Engineered Plants and Microbes,
ARS.
Maruyama, T. (1970) On the fixation probability of mutant genes in a subdivided
population. Genetcal Research, 15, 221-226.
Maruyama, T. (1971) An invariant property of a structured population. Genetical
Research, 18, 81-84.
Simmonds, N.W. (1976) Evolution of Crop Plants. Longman, London.
Stace, C.A. (1975) Hybridization and the Flora of the British Isles. Academic Press.
Stebbins, G.L. (1959) The role of hybridization in evolution. Proceedings of the
American Philosophical Society, 103, 231-251.
