Gene Flow by Pollen: Implications for Plant Conservation Genetics
Norman C. Ellstrand
Oikos, Vol. 63, No. 1. (Feb., 1992), pp. 77-86.
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OIKOS 63: 77-86. Copenhagen 1992
Gene flow by pollen: implications for plant conservation genetics
Norman C. Ellstrand
Elistrand, N. C. 1992. Gene flow by pollen: implications for plant conservation
genetics. - Oikos 63: 77-86.
The absence of gene flow, genetic isolation, is frequently emphasized in conservation
genetics. However, the presence of gene flow can play an equally important role in
determining the genetic fate of populations. Here, I first review what is known of
patterns of gene flow by pollen. Gene flow by pollen is often substantial among plant
populations. I next review the expectations for gene flow patterns in the small
populations typical of endangered species. Then, I consider what role gene flow can
play in plant conservation genetics. Depending on the specific situation, such gene
flow could be either beneficial or detrimental. Geographically disjunct populations
might not always be as reproductively isolated as previously thought, and thereby less
vulnerable to detrimental drift-based processes. On the other hand, conspecific or
heterospecific hybridization may lead to extinction by outbreeding depression or
genetic assimilation. Also, the field release of transgenic plants may lead to the
escape of engineered genes by crop-wild plant hybridization. Such "genetic pollution" could have profound effects on the fitness of wild species with the potential for
disrupting natural communities. Gene flow can be an important force in plant
conservation genetics, and its potential role should be considered in any plant
conservation management program.
C. Ellstrand, Depr of Bocany & Plant Sciences and Program in Genetics. Univ. of
California, Riverside, CA 925214124, USA.
1%'.
Natural populations of rare, endangered, and threatened species are typically small and geographically isolated. Small populations (with "population" defined as
a spatially discrete group of conspecific individuals) are
especially vulnerable to evolutionary hazards that may
hasten their extinction. If small populations are genetically isolated from conspecifics, their effective population size may be so small that the resulting inbreeding
depression may cause a considerable drop in reproductive performance, especially in outcrossing species
(Frankel and Soul6 1981, Franklin 1980, Beardmore
1983, Simberloff 1988). Furthermore, drift itself may
cause the fixation of deleterious alleles (Franklin 1980).
Genetic isolation of small populations might also lead to
depletion of their genetic variation by drift (Wright
1931, Karron 1987). Such genetically depauperate
populations are less likely to respond to the selective
pressure of a changing environment and may be more
likely to suffer extinction (Franklin 1980, Beardmore
1983, Lande and Barrowclough 1987, Simberloff 1988).
Accepted 28 January 1991
0
OIKOS
OIKOS 63:I (1992)
In such cases, it is the absence of gene flow that is a
problem for the populations involved.
On the other hand, the presence of gene flow may not
always be a blessing. Small populations that are not
genetically isolated may be vulnerable to other hazards.
If a small population in one environment receives immigrant genes from a population adapted to another
environment, such gene flow may prevent or disrupt
local adaptive differentiation (Antonovics 1976,
Simberloff 1988). These maladapted populations suffering "outbreeding depression" (sensu Templeton
1986) are more apt to go extinct. Also, if a common,
sexually compatible species is sympatric with the
smaller populations of a rare species, then the rare
species is vulnerable to extinction via hybridization (genetic assimilation). While the near extinction of the red
wolf by hybridization with the coyote (Mech 1970) is
perhaps the best known example of the danger of genetic assimilation, the threat of extinction via hybridization has been recognized for many taxa of plants and
animals (e.g., Cade 1983, Small 1984, Echelle and Connor 1989, Rieseberg et al. 1989).
The likelihood of any of these foregoing threats depends on the amount of gene flow - the movement of
genes from one population to another (Slatkin 1985a) that a population receives. Inbreeding depression and
depletion of genetic variation are most likely when gene
flow is extremely low, and outbreeding depression and
extinction via hybridization are most likely when gene
flow is relatively high. Furthermore, population genetics theory predicts that the importance of gene flow
should increase as population size decreases (e.g.,
Wright 1969, Antonovics 1976). But for any population,
a little bit of gene flow goes a long way. Gene flow of
one individual per generation is sufficient to eliminate
the effects of genetic drift (Wright 1931). And. a gene
flow rate of rn per generation is much more than sufficient to counterbalance a selective differential, s, of the
same magnitude (Haldane 1930). Thus, gene flow can
play a crucial role in the genetic fate of small populations.
For certain species, such as animals restricted to caves
(Caccone and Sbordoni 1987), strong ecological isolation may ensure genetic isolation. However, in plants,
gene flow can occur by propagules capable of traversing
ecological barriers. For example, pollen and spores may
be able to travel across regions inhospitable to adult
plants. In such cases, knowledge of gene flow patterns
and the ecological factors that influence those patterns
can help conservation biologists predict the genetic fate
of small populations and plan management programs
accordingly.
Here, 1 will briefly review what is known of patterns
of gene flow by pollen. I restrict my review to pollenbased gene flow because: 1) it is generally thought to be
more important than gene flow by seed in maintaining
the genetic integrity of populations (Levin and Kerster
1974. Levin 1981), and 2) hybridization is the source of
the previously mentioned gene flow-based hazards in
plant conservation genetics such as genetic assimilation
and outbreeding depression. The data reveal gene flow
by pollen to be an often substantial, but highly variable,
parameter. I revicw the expectations for gene flow patterns in small populations typical of endangered species.
I conclude with several implications for plant conservation genetics
Gene flow by pollen
Contemporary plant population geneticists vary in their
assessments of the importace of gene flow. For plant
evolutionists, the common view is that gene flow is
highly restricted (Levin 1981). At the other extreme,
forest geneticists frequently consider gene flow to be
extensive (Muona 1990). A third relatively new view is
that gene flow in plants is idiosyncratic, ranging from
very low to very high, and varying among species, populations, individual plants and even over a season
(Grant 1985, Hamrick 1987, Slatkin 1987, Ellstrand
1991). The existing estimates of gene flow by pollen
lend support for the third view.
Four general approaches are used to estimate gene
flow by pollen: 1) measuring pollen dispersal from point
sources. 2) measuring gene dispersal from point and
block sources, 3) inferring gene flow from natural population genetic structure, and 4) "paternity" analysis of
progeny in sink populations.
Most frequently, gene flow has been estimated by the
first two methods. The first approach involves measuring pollen movement either indirectly from pollinator foraging distances (e.g., Schmitt 1980) and the dispersal of pollen analogues (e.g., Campbell and Waser
1989) or directly with marked o r naturally polymorphic
pollen (e.g., Handel 1976, Thomson and Thomson
1989). The second approach involves creating experimental populations using source plants bearing a genetic marker surrounded by plants fixed for alternate
alleles. Progeny testing of seed harvested at varying
distances from the source identifies successful fertilization and fruit set (e.g., Handel 1983, Smyth and
Hamrick 1987). When data from either method are
summarized into a single curve, a common pattern
emerges. Pollen tends to be dispersed very close to the
source. with the frequency of pollinations declining rapidly with distance. The skewed, leptokurtic dispersal
curves derived from studies measuring dispersal from a
source have become almost axiomatic (Willson 1983,
Levin and Kerster 1974, Richards 1986). Extrapolation
from these data have served as the basis of the conclusion by plant evolutionary biologists that gene flow
among populations should be very restricted, "that the
immigration rate is likely to be much less than 1%"
(Levin 1984).
But data from the other approaches of measuring
gene flow suggest that gene flow in plants commonly
exceeds 1 %. One of these approaches infers gene flow
from existing population structure. A number of statistical methods have been developed to use allele frequency distributions to indirectly estimate the gene flow
parameter. him, the average number of immigrants per
generation. One common method estimates Nrn using
the frequencies of "private" alleles, those observed in a
single population (Slatkin 1985b, Barton and Slatkin
1986; see Ellstrand 1991 for a critique of the method);
the other estimates Nnz from overall allelic differentiation among populations as measured by Wright's (1951)
FsT or Nei's (1973) GsT statistics (Crow 1986). Govindaraju and Hamrick have mined the many allozvme datasets to calculate hTrnfor dozens of plant spedies. They
found that gene flow estimates vary considerably among
species from very low (Nrn < < 0.1) to very high (Nnz >
> 10.0) (Hamrick 1987, Govindaraju 1988a, 1989), but
in most cases, gene flow is high enough to be evolutionarily significant (i.e., high enough to counteract drift;
N m > 1.0). These estimates vary closely with the pollination biology of the species involved (Hamrick 1987,
Govindaraju 1988a, 1988b, Hamrick et al. 1991) such
that species with characteristically high selfing rates
have very low gene flow estimates. This trend suggests
that gene flow by pollen may account for much of the
total gene flow occurring in these populations.
The final method measures gene flow immigration
directly by paternity exclusion. First, multilocus genotypes of all reproductive individuals in the population
are determined. A comparison of the multilocus genotype of the maternal plant (or, in the case of gymnosperms, the megagametophyte) with that of its progeny allows for reconstruction of the paternal gametic
contribution. This simple paternity exclusion gives the
gene flow rate as the fraction of seeds unambiguously
sired by parents outside of the local population (Ellstrand and Marshall 1985, Hamrick and Schnabel1985).
Refined statistical methods have been developed to correct the estimates for undetected alien gametes whose
genotypes mimic local ones (Adams and Birkes 1990,
Devlin and Ellstrand 1990). These studies almost always
show that plant populations spatially isolated by hundreds to thousands of meters are not genetically isolated. In many cases, the rate of gene flow over these
large distances is moderate to high (reviewed by Ellstrand and Hoffman 1990, Ellstrand 1991).
The apparent conflict between the data from the first
two approaches with those from the second two occurs
because the data on dispersal from a source have been
misinterpreted. Measuring dispersal around a source
almost always truncates the actual dispersal curve, excluding long distance dispersal events and giving an
illusion that dispersal stops at the edge of the study site
(Grant 1985, Ellstrand 1991). Because leptokurtic
curves are characterized by tails that contain more long
distance dispersal events than an equivalent normal distribution, extrapolation to long distances is dangerous
indeed (Hamrick 1987). When the dispersal distribution
tails of many individual plants are summed, substantial
interpopulation gene flow is not so surprising, especially
because evolutionarily important gene flow is equivalent to one immigrant per generation in the case of
drift or a few percent per generation in the case of
moderate selection (Slatkin 1985a, Hamrick 1987, Ellstrand et al. 1989, Ellstrand 1991). Therefore, all of the
data suggest that gene flow by pollen can be evolutionarily significant in plants. The only species likely to have
consistently highly restricted gene flow by pollen are
those with very high selfing rates (e.g., Golenberg
1987).
All four types of studies suggest that gene flow may
vary considerably within species. Pollen dispersal studies have shown that, within a species, dispersal curves
may vary considerably with the genotype of a plant
(Tonsor 1985), with vector (Schmitt 1980, Peakall
1989). with plant density (Levin and Kerster 1969),
among seasons (Campbell and Waser 1989), and over a
OIKOS 63 1 (1992)
season (Palmer et al. 1988). Paternity studies have demonstrated that gene flow rates may vary by more than an
order of magnitude among the populations of a single
species. For example, paternity studies in populations of
the tree Pseudotsuga menziesii have measured interpopulation mating rates from 0.2% to 52% (Neale 1983,
El-Kassaby and Ritland 1986, Adams and Birkes 1990).
And natural populations of wild radish isolated by 100
to 1000 m were found to have interpopulation mating
rates varying from 3% to 18% (Ellstrand et al. 1989).
Also, when Govindaraju (1989) used population structure data to calculate N m for subsets of populations of
Pinus rigida and Eucalyptus caesia, he found the exclusion or inclusion of certain populations had a strong
effect on the gene flow rate calculated, suggesting
strong interpopulation variation in average gene flow in
these species. In addition, immigration rates may vary
strongly among individuals within a population. Gene
dispersal studies often show
andlor directionality in the spatial distribution of progeny heterozygous
for marker alleles (Handel 1982, Smyth and Hamrick
1987. A paternity study in a wild radish population
(Devlin and Ellstrand 1990) demonstrated that certain
individuals set only seeds sired by local fathers, while
others had as many as 20% of their seeds fertilized by
fathers occurring at least 150 m beyond the edges of the
population. Clearly, the evidence supports the conclusion that gene flow is often both substantial and highly
variable.
Gene flow by pollen in small populations
One factor often cited as a source of gene flow variation
is population size. Generally, the rate of gene flow by
pollen is expected to increase as population size decreases. Two reasons are offered for this expectation: 1)
As population size increases, the number of targets for a
fixed amount of "pollen rain" increases and, conscquently, the average rate of fertilization by that pollen
should decrease (Handel 1983). 2) For zoophilous spccies, optimally foraging pollinators will spend more time
within large populations than small populations, affecting proportionately more intrapopulation matings (Levin 1981). The mathematical model of Pedersen et al.
(1969) showed that gene flow rates decreased with increasing size of the recipient population; the relationship was especially strong at short isolation distances.
Experiments involving crop species using one large
source population and smaller sink populations fixed for
alternate marker alleles have also shown the same relationship between population size and gene flow rate
(Crane and Mather 1943, Bateman 1947, Bond and
Pope 1974). Experiments of this type, to my knowledge,
have yet to be conducted on natural species. On the
other hand, paternity studies that measure gene flow by
pollen are typically conducted in small natural pop-
ulations, often numbering fewer than one hundred individuals. T h e interpopulation mating rates measured by
these studies are typically quite high (Ellstrand 1988,
1991).
The size of the source population relative to the sink
may be an equally important determinant of interpopulation mating. For example, discussions of the genetic
relationship of small marginal populations and large
central populations often assume that gene flow from
the larger populations will be so large as to prevent local
differentiation in the small ones (Antonovics 1976). It is
reasonable to assume that larger populations will be
broadcasting much more pollen than small ones. Data
from a few studies support this assumption. Grant and
Antonovics (1978) estimated approximately 35% gene
flow by pollen into small proximal populations of the
grass Anthoxanthum odoratum from a large central population. In an experimental study, Ellstrand et al.
(1989) found essentially no mating among three small
populations of wild radish a few hundred meters apart,
but substantial gene flow into them from very large
populations almost a thousand meters away. In summary, smaller populations are expected to mate with
other populations than large populations, and they are
more likely to mate with large populations than other
small ones.
Implications for plant conservation
genetics
Gene flow by pollen cannot b e ignored as a potential
factor in plant conservation genetics. The available data
demonstrate that, at least for outcrossing species, interpopulation mating commonly occurs at rates that are
evolutionarily important. While rarity of a species is not
closely correlated with its breeding system, obligate outcrossing is known to be the breeding system of a substantial number of rare species and the characteristic
breeding system of tropical, island. and climax communities where plant species are becoming increasingly
vulnerable (Carlquist 1974, Levin 1975, Karron 1987).
Also. the data show that gene flow may vary substantially over time and space. In particular, population size
plays a role in determining some of that variation. Both
theory and data suggest that the small populations typical of rare plant species should receive gene flow by
pollen (if available) at higher rates than relatively large
populations. Furthermore, if small populations are
within mating distance of both relatively large and relatively small populations, the large populations are much
more likely to be a gene flow source. These trends have
several implications for plant conservation genetics.
Because gene flow rates vary with ecological circumstances, and because gene flow may play either a constructive or destructive role in conservation genetics,
the specific consequences of gene flow will vary from
80
case to case. In some cases, gene flow will not be importat in plant conservation genetics simply because it will
be impossible. If a species is reduced to a single population isolated from compatible congeners, then all
matings will occur only within that population. But
cases of plant species with no opportunity for gene flow
are apt to b e the exception rather than the rule.
Many endangered plant species occur in more than
one population, and these are often within 10 km of
each other. For most outcrossing species, at least some
of the populations will be genetically united by gene
flow. For outcrossers with strong-flying migratory pollinators, gene flow by pollen may occur at even greater
distances, (on the order of 20 km or more [depamphilis
and Wyatt 19891). Furthermore, many endangered
plant species are syrnpatric or parapatric with natural
populations of more common native o r introduced congeners, permitting opportunities for gene flow by interspecific hybridization. For example, the great majority of California's 187 plant taxa listed as endangered or
threatened occur in multiple populations and have
nearby congeners as potential mates (Anonymous
1989).
The most obvious consequence of gene flow by pollen
to plant conservation genetics is that interpopulation
gene exchange should increase the effective size of the
populations and reduce the threat of genetic drift-based
hazards such as the depletion of genetic variation and
inbreeding depression. Although rare plant species are
typically genetically impoverished compared to widespread congeners, gene flow may account for the fact
that many rare plant species are nearly as polymorphic
as their widespread congeners (Karron 1987). Likewise,
gene flow may explain why evidence of inbreeding depression has been so rarely observed in the well-studied
small populations of rare and endemic outcrossing species (e.g., Emerson 1939, Karron 1989, Meagher et al.
1978, McClenaghan and Beauchamp 1986, Prentice
1988, but contrast the developmental abnormalities observed by Prentice 1984, Ledig 1986).
However, gene flow is more likely to be a bane than a
boon for rare plants. Intraspecific gene flow can create
the hazard of outbreeding depression, "a fitness reduction following hybridization" within a species (Templeton 1986). The proposed mechanism for this fitness
reduction is the breakdown of co-adaptation to local
conditions in the hybrids or segregants (Templeton
1986, Waser and Price 1989). Outbreeding depression
for interplant matings at a spatial scale as short as 100 m
has been well documented for Ipomopsis aggregata and
Delphinium nelsoni (Price and Waser 1979, Waser and
Price 1983, 1989, 1991) and occurs in many other species (reviewed by Sobrevila 1988, Waser 1991). The
fitness decline can be substantial. In Ipomopsis aggregata, offspring from 100 m matings were 32% less fit
than progeny from 10 m matings (Waser and Price
1989). Furthermore, Svensson (1988, 1990) showed that
progeny from 75 to 100 m matings of Scleranthus annuus
OIKOS 63:l (1992)
suffered a 19% to 36% decrease in male fertility relative
to those from 6 m matings.
The hazard of outbreeding depression will be especially severe for those plant populations experiencing a
dramatic increase in gene flow. Increased gene flow
could arise under a variety of conditions: (1) if disturbance reduces the size of a population so that the fraction
of seeds sired by immigrant pollen increases, (2) if disturbance fragments a previously continuous stand of
plants so that the fraction of immigrant pollen increases,
or immigrant pollen arrives from a more distant source,
or (3) if a common subspecies expands its range and
becomes parapatric o r sympatric with an endemic or
rare subspecies. Because outbreeding depression is
manifest as reductions in seed set (despite sufficient
pollination) and progeny fitness, it will be difficult to
distinguish from inbreeding depression without knowledge of gene flow patterns. However, identification of
the cause of the fitness decline is critical because the
management "cure" for one problem will rapidly exacerbate the other!
Interspecific gene flow is perhaps the greatest gene
flow hazard in plant conservation genetics. Despite occasional isolating mechanisms, many plant species, especially perennials, are often capable of congeneric hybridization, and occasionally even intergeneric hybridization (Grant 1981). Rare and endangered taxa are
frequently sympatric or parapatric with more common
congeners. While the congeners could be other native
species, they could also be introduced weeds, crops, or
other domesticated plants. The opportunities for interspecific hybridization will be greatest for those pairs
of species with maximum sexual compatibility (including ecological factors such as shared phenology and
pollinators) and will be even more likely when the populations of the common species are substantially larger
than those of the rare species. Under such conditions a
substantial fraction of the zygotes in the rare species
may be sired by the common species.
Depending on the species involved, interspecific hybridization can drastically reduce the fitness of the hybridizing individuals. The decreased fitness can be
manifest as early as reduced seed set or as late as the
production of hybrid progeny that are sterile or have
reduced vigor (Levin 1978, Grant 1981). The magnitude
of the drop in fitness can be substantial. For example,
hybridization of species of Gilia in the section Arachnion typically results in high levels of fruit set, but more
than half of the seeds produced are aborted; in contrast,
crosses within species result in very few or no aborted
seeds (Grant and Grant 1960. Grant 1964). Also, naturally occurring hybrids of Carduus nutans and C. acanthoides are almost completely sterile (Warwick et al.
1989). And even if hybrid progeny are not sterile, if the
parent species are well-differentiated ecologically, their
offspring may only be able to grow and reproduce in
rare, intermediate microsites (Anderson 1948). In fact,
the fitness costs associated with hybridization are often
6 OIKOS 63:l (1992)
so strong that secondary isolating mechanisms may
evolve in one of two sympatric congeners to reduce or
to prevent pollination and fertilization altogether (the
"Wallace Effect" [Grant 1981; Wallace 18891). Clearly,
hybridization between a rare species and a common
sympatric congener may impose a substantial fitness
cost, but the rare species will often lack the genetic
variation to evolve new isolating mechanisms. Furthermore, the evolutionary response may impose its own
cost. As an illustration, white flower morphs are in high
frequency in the normally pink Phlox pilosa when that
species is in sympatry with P. glaberrima; white-flowered individuals enjoy much lower rates of interspecific hybridization then pink-flowered plants, but suffer a
15% drop in seed set, possibly because they are less
attractive to pollinators (Levin and Kerster 1967, 1970,
Levin 1978).
Interspecific hybridization poses a conservation problem even without direct fitness costs to the parents of
hybrid progeny. Substantial heterospecific mating may
be sufficient to cause extinction via genetic assimilation.
The problem has been well recognized in bird conservation genetics (Cade 1983). Closely related plant species
that are geographically well isolated may be fully interfertile and
viable progeny (Grant 1981).
Natural or human-mediated range extensions may bring
these species in sympatry. If a rare or endangered population comes in close enough contact with a numerically larger or reproductively more vigorous heterospecific population for gene flow to occur, then a considerable fraction of the progeny will be interspecific
hybrids. In the absence of selection against hybrids,
continued hybridization and introgression may eventually lead to genes from the common species "swamping
out" those of the rare species. In a few cases,
assimilation has been recognized as a threat to certain
plant species. For example, the island endemic, Cercocarpus traskiae, exists as a population of only seven
adult plants on Santa Catalina Island and is sympatric
with the more abundant C. betuloides; allozyme analysis
identified at least two of the seven adults to be interspecific hybrids (Rieseberg et al. 1989). The threat of
genetic assimilation may come from introduced weeds
or domesticated plants as well. A major threat to many
endangered sunflower (Helianthus) species is hybridization with the weedy annual sunflower, H. annuus
which has dramatically expanded its range with human
disturbance (Rogers et al. 1982). Hybridization with a
domesticated species has been implicated in the extinction of at least five plant species (Small 1984), and the
threat continues. For example, the rare Juglans hindsii
freely hybridizes with the Eommon ornamental walnut
J. regia (Munz 1959). The genetic problems created by
interspecific hybridization may be much more common
for plants than suspected. More than 90% of California's listed threatened and endangered plants occur
sympatrically or parapatrically with at least one congener (Anonymous 1989).
81
Table 1. Traits of rare species at risk for gene flow-mediated hazards.
Breeding system
Obligate outcrossing (Dioecy, self-incompatibility,etc.)
OR
If self-fertile, high outcrossing rate
For outbreeding depression:
Population structure
Differentiation
Multiple populations with at least two within mating distance (generally < 10 km)
Strong between populations
For problems of interspecific hybridization:
Proximity of congener
Compatibility of congener
Magnitude of gene flow source
Sympatric or parapatric (generally < 10 km)
Compatible enough to redily affect fertilization (seed set is not required; see text)
Congener population numerically greater than vulnerable population (generally at
least twice as many individuals)
OR
Congener population reproductively more vigorous than vulnerable population (in
terms of pollen production or pollen export)
In summary, the role of gene flow in plant conservation genetics will be idiosyncratic with the species and
populations involved. Gene flow is expected to play
some role in the genetic fate of rare outcrossing species
that have multiple populations within 10 km of each
other and those that are within mating distance of a
more numerous sexually compatible congener. For
those rare species with no local differentiation, gene
ilow should play a beneficial role, ameliorating the genetic hazards associated with small population size.
More frequently, gene flow will be detrimental. Outbreeding depression among conspecific populations, reduced seed set or progeny vigor after interspecific hybridization, and genetic assimilation are all possible genetic threats to rare species. Table 1 summarizes traits
of rare species that make them high risks for gene
flow-mediated hazards.
The escape of engineered genes
Gene flow by pollen may soon have another important
impact on plant conservation biology because hybridization between crous and their wild relatives can act as
an avenue for the transfer of engineered genes into
natural populations (Colwell et al. 1985, Ellstrand 1988,
National Research Council 1989, Young 1989, Ellstrand
and Hoffman 1990). The risk, in part, depends on the
nature of the gene transferred (Tiedje et al. 1989, Ellstrand and Hoffman 1990). In the past, the sorts of traits
incorporated during domestication and crop improvement, such as dwarfing. were often traits that would be
detrimental in the wild. Nonetheless. crop-weed hybridization has been thought to play a major role in the
evolution of certain weeds (e.g., Panetsos and Baker
1967, Harlan 1983, Small 1984).
In contrast, most traits targeted for gene transfer by
crop biotechnologists - salinity tolerance, insect resistance, disease resistance, etc. (Gasser and Fraley 1989) 82
would confer a fitness advantage to wild species. The
incorporation of such genes into natural populations
would represent a sort of "genetic pollution" that could
radically alter niche relationships in natural ecosystems
(Hoffman 1990).
For example, the gene for a protein toxic to many
insect species (especially Lepidoptera) in the bacterium
Bacillus thuringiensis has now been transferred to several crop plants (Gasser and Fraley 1989). Such broad
resistance could represent a substantial fitness boost to
a wild species because the ranges and population sizes
of many natural species are constrained by herbivores.
The most often cited examples involve the explosive
population growth of introduced weeds released from
their natural herbivores and their subsequent population regulation when those animals are introduced for
biocontrol: e.g., prickly pear in Australia (Dodd 1959)
and Klamath weed in the American Pacific Northwest
(Huffaker and Kennett 1959). And growing evidence
suggests that many native species have realized niches
that are regulated by their herbivores (e.g., Parker and
Root 1981, Louda 1982, Cantor and Whitham 1989).
The introduction of a novel insecticidal toxin in a natural plant population has the potential for radically
changing the role of that species in its community.
A t worst, the dramatic increase of a plant species
previously regulated by one or several insects could
make it competitively superior to other members of its
community, leading to a number of local extinctions and
a decline in local biodiversity. Experimental removal of
a "keystone" predator often leads to radical changes in
community structure (examples in Krebs 1985). In any
case, a problem that distinguishes genetic pollution
from other types of pollution is that once the pollutant
has escaped, it has the potential to multiply itself,
thereby frustrating attempts to contain it.
Opportunities for the dispersal of engineered crop
genes into natural populations will depend on gene flow
by pollen. For gene flow to occur, the transgenic crop
OIKOS 63.1 (1992)
Table 2. California's ten most important vegtable crops and
their relatives in California (from Munz 1959).
Crop
Asparagus
Broccoli
Carrot
Cauliflower
Celery
Corn, sweet
Lettuce
Onion
Potato
Tomato
Does the same
How many other
species occur in the congeners occur in
California flora
the California flora
Yes
Yes*
Yes
Yes*
Yes
No
No
No
No
Yes*
*Only as a short-term non-persistent escape from cultivation
must occur within mating distance of a sexually compatible species, either native or introduced (Ellstrand 1988,
Ellstrand and Hoffman 1990). Almost every crop is
capable of hybridizing with a wild species: however,
wild compatible relatives may o r may not co-occur with
the crop (National Research Council 1989). The 10
most important vegetable crops of California (Table 2)
illustrate the range of potential opportunities for hybridization. At one extreme, sweet corn (Zea mays) has
no congeners present in the California flora; gene flow
will not be possible in this region. A t the other extreme,
carrot (Daucus carota) is fully interfertile with the common weed. Queen Anne's Lace, which is the same
species (Munz 1959, Small 1984). Intermediate cases
include crops congeneric with wild species of uncertain
or reduced interfertility (e.g., onion). Interestingly, only one crop on the list is highly selfing lettuce) and eight
are either obligately outcrossing or predominantly outcrossing (Frankel and Galun 1977), suggesting that most
of these vegetable crops are capable of substantial gene
export to natural populations.
While hybridization among crops and wild species is
thought to play a major role in the evolution of both
(e.g.. Harlan 1983, Small 1984, Doebley 1990, Wilson
1990). quantitative details of the rates and patterns of
such hybridization have been rarely sought. Kirkpatrick
and Wilson (1988) used allozymes to describe interspecific mating patterns among cultivars of Cucurbita pepo
(squashes and gourds) and the wild gourd C. texana.
They found alleles specific to the crop in 5% of the
progeny of the nativE species at distances of 1300 rn.
Langevin et al. (1990) measured gene flow by pollen
among cultivated rice and the weed red rice (both
Oryza sativa) growing sympatrically in Louisiana. The
fraction of hybrid seed set by the weed varied with the
sympatric cultivar, ranging from 1 to 52%. They measured progeny vigor and noted that crop-weed "hybrids
were vegetatively robust plants, demonstrating heterosis". Clearly, for this species, genes from the crop d o
not prevent increased vigor in the crop-weed hybrid.
<
h* OIKOS 63 1 (1992)
,
A n experiment by Klinger-et al. (1991) was designed
specifically to address the potential for transfer of engineered genes from crops to weeds using a cultivar of
radish and wild radish (both Raphanus sativus) as a
model system. The cultivar was grown to simulate a
seed multiplication block; the wild radish was grown in
small groups to simulate natural stands of the weed. The
experiment was conducted simultaneously at coastal
and inland locations in California. The crop and the
weed were fixed for alternate alleles. The crop marker
was absent in surrounding natural stands. Progeny testing revealed that crop-weed gene flow was extensive for
weed plots planted at the edge of the crop; in some
cases, all of the seeds sampled on a plant had been sired
by crop plants. Crop-weed gene flow rates dropped off
considerably at more distant stations 200 to 1000 m from
the crop. However, some gene flow was detected in the
progeny of the most distant plants (1000 m) at both
experimental locations, and the incidence of gene flow
did not drop off monotonically with distance, suggesting
that gene flow from the crop could occur at distances
much greater than 1000 m.
The data from the three studies detailed above demonstrate that crop-weed gene flow can occur readily
under agricultural conditions, that the gene flow can be
of great magnitude, and that detectable gene flow can
occur over hundreds of meters. Therefore, any plan to
field test a transgenic crop must consider whether the
gene will be expected to have an adverse effect if it
should escape into a natural ecosystem and whether the
crop is even weakly cross-compatible with any members
of the local flora. either native or introduced.
Recommendations for future research
Clearly, gene flow must be considered in any endangered plant species' conservation management program, especially if the species is at "high risk" for gene
flow (see Table 1). First, the presence or absence of
gene flow must be determined. "Paternity" analyses,
using biochemical genetic markers, such as isozymes
and RFLPs, make the identification of immigrant gametes straightforward (Ellstrand and Marshall 1985).
Refined statistical techniques have been developed to
obtain accurate estimates of gene flow rates (Adams
and Birkes 1990, Devlin and Ellstrand 1990).
If no gene flow is detected in the small populations of
an endangered species, then drift-based hazards must
be assessed. Depletion of genetic variation can be evaluated by contrasting genetically-based molecular (Karron 1987) o r quantitative (Primack 1980) characters of
the vulnerable populations or species with control populations or species. Inbreeding depression can be evaluated by measuring fitness in situ or ideally, under
common garden conditions in comparison with individuals from related, larger populations (cf. Holtsford and
83
Ellstrand 1990, Karron 1989). A t best, those studies will
include estimates of male fitness, female fitness, and
survivorship. If substantial inbreeding depression is detected, then common garden experiments
the fitness of i n t e r ~ o ~ u l a t i ohybrids
n
and segregants
may determine whether man-mediated gene flow will
ameliorate inbreeding depression or exacerbate the
situation with outhreeding
Waser and Price 1989).
If -gene flow is detected, then it must be identified as
to whether its source is conspecific or heterospecific. If
conspecific gene flow is occurring, then the possibility of
outbreeding depression should be addressed by cornmon garden ex~eriments.If outbreeding- de~ression
is
.
occurring, then' populations should be managed to reduce gene flow. However, the factors that could be
rates - int e r ~ o ~ u l a t i odistance.
n
n
, ,~ o,~ u l a t i odensitv.
, , ,ovulation
shape, pollen vector, etc. - a r e poorly understood; most
data on the topic come from a few experiments involving contiguous crop populations (Handel 1983).
Many more experiments with discontinuous populations
under natural or semi-natural conditions (e.g., Ell19867
~~f~~~~~~~
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Importance of Belowground Herbivory: Pocket Gophers May Limit Aspen to Rock Outcrop
Refugia
Lisa F. Cantor; Thomas G. Whitham
Ecology, Vol. 70, No. 4. (Aug., 1989), pp. 962-970.
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Genetic Engineering in Agriculture
Robert K. Colwell; Elliott A. Norse; David Pimentel; Frances E. Sharples; Daniel Simberloff;
Waclaw Szybalski; Winston J. Brill
Science, New Series, Vol. 229, No. 4709. (Jul. 12, 1985), pp. 111-112+115-116+118.
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The Development and Application of a Refined Method for Estimating Gene Flow From
Angiosperm Paternity Analysis
B. Devlin; N. C. Ellstrand
Evolution, Vol. 44, No. 2. (Mar., 1990), pp. 248-259.
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Molecular Evidence for Gene Flow among Zea Species
John Doebley
BioScience, Vol. 40, No. 6, Gene Transfer between Crops and Weeds. (Jun., 1990), pp. 443-448.
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Rapid, Geographically Extensive Genetic Introgression After Secondary Contact Between
Two Pupfish Species (Cyprinodon, cyprinodontidae)
Anthony A. Echelle; Patrick J. Connor
Evolution, Vol. 43, No. 4. (Jul., 1989), pp. 717-727.
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Hybridization as an Avenue of Escape for Engineered Genes
Norman C. Ellstrand; Carol A. Hoffman
BioScience, Vol. 40, No. 6, Gene Transfer between Crops and Weeds. (Jun., 1990), pp. 438-442.
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Interpopulation Gene Flow by Pollen in Wild Radish, Raphanus sativus
Norman C. Ellstrand; Diane L. Marshall
The American Naturalist, Vol. 126, No. 5. (Nov., 1985), pp. 606-616.
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Genetically Engineering Plants for Crop Improvement
Charles S. Gasser; Robert T. Fraley
Science, New Series, Vol. 244, No. 4910. (Jun. 16, 1989), pp. 1293-1299.
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Estimation of Gene Flow and Genetic Neighborhood Size by Indirect Methods in a Selfing
Annual, Triticum dicoccoides
Edward M. Golenberg
Evolution, Vol. 41, No. 6. (Nov., 1987), pp. 1326-1334.
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Biology of Ecologically Marginal Populations of Anthoxanthum odoratum. I. Phenetics and
Dynamics
Michael C. Grant; Janis Antonovics
Evolution, Vol. 32, No. 4. (Dec., 1978), pp. 822-838.
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Ecological Risks of Genetic Engineering of Crop Plants
Carol A. Hoffman
BioScience, Vol. 40, No. 6, Gene Transfer between Crops and Weeds. (Jun., 1990), pp. 434-437.
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Inbreeding Effects in Clarkia tembloriensis (Onagraceae) Populations with Different Natural
Outcrossing Rates
Timothy P. Holtsford; Norman C. Ellstrand
Evolution, Vol. 44, No. 8. (Dec., 1990), pp. 2031-2046.
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The Incidence and Effects of Hybridization between Cultivated Rice and its Related Weed Red
Rice (Oryza sativa L.)
Susan A. Langevin; Keith Clay; James B. Grace
Evolution, Vol. 44, No. 4. (Jul., 1990), pp. 1000-1008.
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Pest Pressure and Recombination Systems in Plants
Donald A. Levin
The American Naturalist, Vol. 109, No. 968. (Jul. - Aug., 1975), pp. 437-451.
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Natural Selection for Reproductive Isolation in Phlox
Donald A. Levin; Harold W. Kerster
Evolution, Vol. 21, No. 4. (Dec., 1967), pp. 679-687.
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Density-Dependent Gene Dispersal in Liatris
Donald A. Levin; Harold Kerster
The American Naturalist, Vol. 103, No. 929. (Jan. - Feb., 1969), pp. 61-74.
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Phenotypic Dimorphism and Populational Fitness in Phlox
Donald A. Levin; Harold W. Kerster
Evolution, Vol. 24, No. 1. (Mar., 1970), pp. 128-134.
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Low Genic Differentiation Among Isolated Populations of the California Fan Palm
(Washingtonia filifera)
Leroy R. McClenaghan, Jr.; Arthur C. Beauchamp
Evolution, Vol. 40, No. 2. (Mar., 1986), pp. 315-322.
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Analysis of Gene Diversity in Subdivided Populations
Masatoshi Nei
Proceedings of the National Academy of Sciences of the United States of America, Vol. 70, No. 12,
Part I. (Dec., 1973), pp. 3321-3323.
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Insect Herbivores Limit Habitat Distribution of a Native Composite, Machaeranthera
Canescens
Matthew A. Parker; Richard B. Root
Ecology, Vol. 62, No. 5. (Oct., 1981), pp. 1390-1392.
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Pollinator Foraging Behavior and Gene Dispersal in Senecio (Compositae)
Johanna Schmitt
Evolution, Vol. 34, No. 5. (Sep., 1980), pp. 934-943.
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The Contribution of Population and Community Biology to Conservation Science
Daniel Simberloff
Annual Review of Ecology and Systematics, Vol. 19. (1988), pp. 473-511.
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Gene Flow in Natural Populations
Montgomery Slatkin
Annual Review of Ecology and Systematics, Vol. 16. (1985), pp. 393-430.
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Rare Alleles as Indicators of Gene Flow
Montgomery Slatkin
Evolution, Vol. 39, No. 1. (Jan., 1985), pp. 53-65.
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Gene Flow and the Geographic Structure of Natural Populations
Montgomery Slatkin
Science, New Series, Vol. 236, No. 4803. (May 15, 1987), pp. 787-792.
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Realized Gene Flow Via Pollen in Artificial Populations of Musk Thistle, Carduus nutans L.
C. A. Smyth; J. L. Hamrick
Evolution, Vol. 41, No. 3. (May, 1987), pp. 613-619.
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Dispersal of Erythronium grandiflorum Pollen by Bumblebees: Implications for Gene Flow
and Reproductive Success
James D. Thomson; Barbara A. Thomson
Evolution, Vol. 43, No. 3. (May, 1989), pp. 657-661.
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The Planned Introduction of Genetically Engineered Organisms: Ecological Considerations
and Recommendations
James M. Tiedje; Robert K. Colwell; Yaffa L. Grossman; Robert E. Hodson; Richard E. Lenski;
Richard N. Mack; Philip J. Regal
Ecology, Vol. 70, No. 2. (Apr., 1989), pp. 298-315.
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Intrapopulational Variation in Pollen-Mediated Gene Flow in Plantago lanceolata L.
Stephen J. Tonsor
Evolution, Vol. 39, No. 4. (Jul., 1985), pp. 775-782.
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Optimal Outcrossing in Ipomopsis aggregata: Seed Set and Offspring Fitness
Nickolas M. Waser; Mary V. Price
Evolution, Vol. 43, No. 5. (Aug., 1989), pp. 1097-1109.
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Outcrossing Distance Effects in Delphinium Nelsonii: Pollen Loads, Pollen Tubes, and Seed
Set
Nickolas M. Waser; Mary V. Price
Ecology, Vol. 72, No. 1. (Feb., 1991), pp. 171-179.
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