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Evidence for long-distance pollen dispersal in milkweeds (Asclepias exaltata).

Ehrlich and Raven (1969) challenged the view that plant species are evolutionary units held together by the cohesive force of gene flow. They cited evidence, primarily from crop species, to argue that pollen movement within and between populations is limited and unlikely to maintain species integrity of spatially separated populations. Empirical studies of natural populations also showed further that pollinators tend to move short distances, that most pollen is transferred over relatively small areas, and that seed dispersal also is limited (Levin and Kerster 1974). Although he noted that gene flow may be greater than previously thought, Levin (1981) still argued that gene dispersal occurs over too small a spatial scale to account for the maintenance of species identity in plants.

Usually, pollen-mediated gene flow has been estimated indirectly from pollinator flight distances (Levin and Kerster 1974), dispersal distances of pollen analogues and dye particles (Murawski and Gilbert 1986; Campbell and Waser 1989), genetic diversity statistics (Hamrick 1987), or effective pollination distances from a few individuals with unique genetic markers (Schaal 1980; Smyth and Hamrick 1987). Although these studies have provided detailed data on potential pollen dispersal within populations, actual genetically effective pollen dispersal distances among natural populations rarely have been measured because identifying paternal parents of seeds directly is difficult. Recently, paternity testing has enabled population biologists to measure effective pollen dispersal distances within populations (Schnabel 1988; Devlin and Ellstrand 1990b; Broyles and Wyatt 1991; Broyles 1992), between populations (Ellstrand and Marshall 1985; Hamrick and Loveless 1989; Godt and Hamrick 1993) and between populations of different species (Kirkpatrick and Wilson 1988; Arnold et al. 1993).

In milkweeds, hundreds of pollen grains are dispersed together in discrete packages termed "pollinia," whose dispersal pattern depends on the pollinating insects. For example, Morse (1982) determined that pollinia of Asclepias syriaca remain on bumblebees for several hours, thus increasing the probability of outcrossing and long-distance dispersal in this clonal species. Pleasants (1991), however, showed that 71% of the pollinia recovered following dispersal by honeybees were inserted into stigmatic chambers on other flowers within 1 m of the radioactively labeled pollen source of A. syriaca. Similarly, Shore (1993) estimated the rate of intraramet self-pollination in natural populations of A. syriaca at 66%. In both natural and experimental populations of A. exaltata, effective pollen dispersal, determined by paternity testing, is extensive: the mean is more than three times greater than that inferred from bumblebee and butterfly flight distances between plants (Broyles and Wyatt 1991).

Because hundreds of pollen grains are dispersed in each milkweed pollinium, we predict that pollen-mediated gene flow should be high between populations, as dispersal of a single pollinium can result in the maturation of a large multiseeded fruit. Moreover, slow turnover rates for pollinia on pollinators can increase the probability that some pollinia will be dispersed long distances. In this study, we used paternity analysis to measure pollen-mediated gene flow among populations of A. exaltata L.

Asclepias exaltata is a perennial herb native to woodland habitats in eastern North America from northern Georgia to Maine and westward to Minnesota and Iowa (Woodson 1954). Asclepias exaltata is entirely self-incompatible and relies on strong-flying insects, such as bees and butterflies, to transport pollinia between plants. Pollinia of A. exaltata contain approximately 180 pollen grains, nearly three times the number necessary to fertilize all of the 60-80 ovules in a single ovary. Thus, pollination with a single pollinium can result in the production of a follicle with many comose, wind-dispersed seeds. Previous studies of this species have documented many aspects of its reproductive biology (Shannon and Wyatt 1986a,b; Wyatt and Shannon 1986; Broyles and Wyatt 1990a,b; Wyatt and Broyles 1990), potential for hybridization (Kephart et al. 1988; Wyatt and Hunt 1991; Wyatt and Broyles 1992; Broyles and Wyatt 1993), and mating patterns within populations (Broyles and Wyatt 1990a,b, 1991, 1994).

MATERIALS AND METHODS

To measure pollen-mediated gene flow between populations of Asclepias exaltata, we performed a paternity analysis on seeds collected from six populations in Shenandoah National Park in northern Virginia. The genetic structure of these populations has been reported in a survey of allozyme variation of southern Appalachian populations by Broyles and Wyatt (1993). These populations are polymorphic at 65% of their loci, maintain 2.32 alleles per polymorphic locus, and have expected heterozygosities of 19%. Both A. exaltata and A. syriaca are locally abundant throughout the Park. Asclepias syriaca grows in fields, meadows, and exposed roadsides, whereas A. exaltata occupies forest clearings and roadsides sheltered by forests. Populations of both species are interspersed and sometimes mixed throughout the northern half of the Park.

In June 1990, leaves were sampled from 48 flowering individuals per population, yielding a total of 288 individuals. Individuals that were not sampled from these populations were pruned to remove all flower buds, thus ensuring that the pool of potential pollen parents included only the 48 local individuals (and plants outside the target population). Initial population sizes before pruning were not recorded, but all populations were small (fewer than 100 flowering individuals). Isolation distances, determined by measuring the minimum distance separating the target population from the nearest conspecific population, ranged from 0.05 km for Mile Post 54 and Lewis Mountain to 1.0 km for Fisher's Gap. We collected all 241 fruits produced in these six populations in September. An accidental mowing of several plants in the Lewis Mountain population reduced the number of fruits collected there to 22. Twelve seeds from each fruit were germinated and prepared for enzyme electrophoresis.

Paternity Analysis. - Two paternity exclusion methods were used. In the "seed-by-seed" method, we employed the exclusion algorithm described by Ellstrand (1984) for the individual seeds of each fruit. This algorithm proceeds by comparing the microgametophytic (paternal) genotype of each seed with those that could be produced by individuals within the population. If no match is found for a given seed, then a gene-flow event is inferred. The observed (apparent) proportion of seeds that have no possible fathers within the target population is a minimum estimate of gene flow (Ellstrand 1984; Hamrick and Schnabel 1985). The power of this analysis depends heavily on (1) the number of distinct genotypes in the target population, which in our study was always less than the number of individuals; and (2) the amount of available genetic variation, which can be summarized by calculating the average exclusion probability across all polymorphic loci (Brown et al. 1989). Exclusion probabilities for the six populations of A. exaltata varied from 0.81 at Lewis Mountain to 0.92 at Fisher's Gap.

[ILLUSTRATION OMITTED]
TABLE 1. Number of distinct genotypes, exclusion probabilities, and
isolation distances for six populations of Asclepias exaltata in
Shenandoah National Park.

                      Distinct    Exclusion    Isolation
                       geno-       proba-      distance
Population             types       bilities      (km)

Fisher's Gap             43        0.917         1.0
South Skyland            33        0.874         0.8
Skyland Lodge            34        0.897         0.2
Mile Post 54              8        0.863         0.05
Old Rag Overlook         40        0.865         0.4
Lewis Mountain           25        0.807         0.05
Mean                     31        0.871         0.5
Standard deviation       13        0.037         0.36


Regardless of the power of the seed-by-seed exclusion method, the result will always be an underestimate of true pollen gene flow, because many of the pollen genotypes produced by plants external to the target population will be identical to those produced within the target population. To estimate the proportion of undetected (cryptic) gene flow, we used Devlin and Ellstrand's (1990a) Monte Carlo procedure, which gives an approximate maximum-likelihood solution for total pollen gene flow (apparent + cryptic). This procedure simulates pollen gene flow by assuming that allele frequencies of successful immigrant pollen represent gametes chosen randomly from the surrounding populations. In this analysis, for each target population, we used allele frequencies of a synthetic population generated by combining the five remaining populations.

As noted by Devlin et al. (1988), additional genetic information concerning paternity is available when matings are correlated (i.e., shared paternity of seeds within fruits). Because milkweed fruits are usually sired by a single pollen donor (Broyles and Wyatt, 1990a, 1994), the entire progeny array of a fruit (or a sufficient subset of the array) can be considered in determination of paternity (Broyles and Wyatt, 1990a,b, 1991). For example, if the maternal genotype at a locus is heterozygous for alleles A and B and the progeny array contains genotypes AA, AB, and BB, then the paternal genotype must have been heterozygous for alleles A and B. Proceeding locus-by-locus, we can determine unambiguously the multilocus, diploid, paternal genotype for each singly sired progeny array. Paternal genotypes not present in the reference population are assumed to represent gene-flow events, and the proportion of fruits sired by single individuals outside the target population is an estimate of pollen gene flow. We could use this "progeny-array" method for 225 of the fruits sampled from the six populations. The remaining 16 fruits were sired by multiple pollen donors (i.e., more than two paternal alleles were observed for at least one locus) and were excluded from both the progeny-array and seed-by-seed analyses.

It is clear that the progeny-array method will be much more powerful than the seed-by-seed exclusion method. We would argue, in fact, that given the few distinct genotypes in each of the six target populations and the many loci used, the progeny-array method should identify all pollen-mediated gene flow events. It is not clear, however, whether the disadvantage of seed-by-seed exclusion can be circumvented through the use of the Monte Carlo procedure. A comparison of the two sets of results can thus provide an empirical test of the effectiveness of the Monte Carlo method in estimating total pollen gene flow when matings are correlated.

Calculation of Indirect Estimates of Gene Flow. - The proportion of genetic variation found among populations ([G.sub.ST]) in Shenandoah National Park was calculated using the equations of Nei (1973, 1977) and averaging [G.sub.ST] across all polymorphic loci. The number of migrants per generation (Nm) was calculated by the following relationship (Wright 1951):

Nm = 1 - [F.sub.ST]/4[F.sub.ST].

In this relationship, Nei's [G.sub.ST] (1977) is equivalent to a multiallelic [F.sub.ST]. The number of migrants per generation was calculated from allele frequencies of the adult plants and of seedling populations. Seedling population sizes equaled the number of fruits sampled multiplied by 12.

Enzyme Electrophoresis. - Leaves sampled from flowering plants in each population were placed in plastic bags and stored on ice until enzymes could be extracted in 0.2 M Tris-HCl (pH 7.5) extraction buffer (Broyles and Wyatt 1990a). Seeds were germinated on moist filter paper in petri dishes. Seedlings were grown under Sylvania Gro-Lux Lights with an 18-h photo-period at a constant temperature of 21 [degrees] C. Tissue from young green cotyledons or true leaves was [TABULAR DATA OMITTED] excised and ground in 0.2 mL of extraction buffer. The enzyme extract was absorbed onto 3 mm x 8 mm wicks cut from Whatmann 3 MM chromatography paper. Sample wicks were stored at -70 [degrees] C until electrophoresis could be performed.

Wicks were loaded into a vertical slot in 10.8% starch gels. Sixteen polymorphic isozymes from 12 enzyme stains were resolved using three electrophoretic buffer systems (Broyles and Wyatt 1993). All electrophoretic buffers and stain recipes were identical to those described by Broyles and Wyatt (1990a, 1993). These enzymes included alanine transferase (Alt-2); fluorescent esterase (Fle-2); glutamate oxaloacetate transaminase (Got-1, Got-2); glutamate dehydrogenase (Gdh-1); isocitrate dehydrogenase (Idh-1); leucine aminopeptidase (Lap-1); malate dehydrogenase (Mdh-1, Mdh-2); menadione reductase (Mnr-1, Mnr-2); phosphoglucomutase (Pgm-1); 6-phosphogluconate dehydrogenase (Pgd-1); phosphoglucose isomerase (Pgi-2); and triosephosphate isomerase (Tpi-1, Tpi-2). A standard wick from a plant heterozygous for Fle-2, Pgm-1, Pgi-2, and Mnr-1 was placed in the center of each gel. Resolution of Alt-2 was variable, and many seedlings that developed slowly failed to express this enzyme.

RESULTS

The percentage of immigrant pollen, as determined from progeny arrays, ranged from a low of 29% in the Fisher's Gap population to 50% in Lewis Mountain. Fisher's Gap was the most highly isolated population, separated from the nearest conspecific population by 1.0 km. However, the Lewis Mountain population was isolated only by 0.05 km, and we therefore expected pollen-mediated gene flow to be high. Averaged over all populations, 39% of the fruits were sired by individuals located outside of each target population. The percentage of immigrant pollen was negatively correlated with isolation distance but not significantly so (Kendall's [Tau] = -0.690, N = 6, P [greater than] 0.1).

[ILLUSTRATION OMITTED]

The seed-by-seed exclusion analysis, incorporating cryptic gene flow, provided lower estimates of percent immigrant pollen, ranging from 14% at South Skyland to 38% at Lewis Mountain. "Total" (apparent + cryptic) pollen gene flow from this analysis accounted for only 65% of that determined by analysis of progeny arrays. Even in the populations with the greatest potential for gene flow detection (such as Mile Post 54, which had only eight distinct genotypes, and Fisher's Gap, which had the highest exclusion probability), the 95% confidence intervals from the Monte Carlo simulations did not include the value estimated from the progeny-array method. The degree to which gene flow was underestimated varied considerably among populations (17%-55%) but was not correlated with either the number of distinct genotypes (r = 0.347, N = 6, P [greater than] 0.45) or the exclusion probability (r = 0.155, N = 6, P [greater than] 0.75) of the target population. In addition, the relative levels of pollen gene flow for the six populations differed slightly from those found using the progeny-array analysis. The correlation between the two sets of estimates was positive (r = 0.734, N = 6, P [less than] 0.10).

Levels of genetic differentiation were low among populations of Asclepias exaltata flowering plants ([G.sub.ST] = 0.099) and seeds ([G.sub.ST] = 0.056) in Shenandoah National Park. Genetic differentiation measured for seeds was 43% lower than that for adult plants in these populations. Nm calculated from [G.sub.ST] was 2.3 and 4.2 for flowering plants and seeds, respectively. We obtained an estimate of Nm from the paternity analysis by multiplying the rate of gene flow by 0.5 (to compensate for the haploid nature of microgametophytes) and the number of individuals per population. Nm calculated from paternity data was 6.1 (seed exclusion method with cryptic gene flow) and 9.4 (progeny array method), three to four times greater than the estimate based on [G.sub.ST] of adult plants.

Two fruits (0.8%), one from Fisher's Gap and one from Lewis Mountain, contained seeds that were almost certainly sired by individuals of A. syriaca. All seeds analyzed from these two fruits were heterozygous for four alleles diagnostic for A. syriaca (Pgm-1f, Fle-2c, Mdh-1a, and Mdh-2a) and for alleles diagnostic for A. exaltata (see Broyles and Wyatt 1993). For example, although Mdh-1a was common ([P.sub.i] [greater than] 0.95) in populations of A. syriaca near Lewis Mountain, its frequency in Shenandoah populations of A. exaltata was 0.008 (Broyles and Wyatt 1993). The other three diagnostic alleles show similar frequency shifts between species, thus the probability of finding a plant of A. exaltata homozygous for all four alleles would be vanishingly small. Several stems of A. syriaca were found within 0.1 km of the A. exaltata population at Fisher's Gap, but Lewis Mountain was isolated by at least 0.5 km from the nearest A. syriaca source.

DISCUSSION

Gene Flow as a Cohesive Force in Asclepias exaltata. - Levels of pollen-mediated gene flow, as estimated from the six populations of Asclepias exaltata in Shenandoah National Park, are among the highest reported for small, natural populations of herbaceous, insect-pollinated species. Our results, in fact, are very similar to levels of immigrant pollen found for both animal- and wind-pollinated forest trees (e.g., Friedman and Adams 1985; Harju and Muona 1989; Hamrick and Murawski 1990; Adams and Birkes 1991). In contrast, for four other herbaceous species, minimum estimates of pollen gene flow over distances comparable to those used in our study have averaged 10% in Raphanus sativus (Ellstrand et al. 1989), 8.5% in Curcurbita foetidissima (Kohn and Casper 1992), 8% in Phlox drummondii (Levin 1983), and 5% between patches of Curcurbita pepo and C. texana (Kirkpatrick and Wilson 1988). When cryptic gene flow was taken into account, average pollen gene flow for C. foetidissima increased only to 10.8% (Kohn and Casper 1992), but Devlin and Ellstrand (1990a) demonstrated that true levels of pollen gene flow in R. sativus may be twice as great as those estimated from simple exclusion. Even if the pollen gene flow estimates reported for other herbaceous species were doubled, however, they would still be considerably less than those observed in A. exaltata.

Although the high levels of pollen gene flow reported here would appear to be sufficient to counterbalance the differentiating forces of local selection and genetic drift (Wright 1951, 1969; Antonovics 1968; Levin 1984; Ellstrand and Marshall 1985), several factors could reduce its effectiveness. First, studies with crop species have found an inverse relationship between percentage of immigrant pollen and population size (reviewed by Handel 1983), thus pollen-mediated gene flow should be somewhat less in larger, unmanipulated populations of A. exaltata. Second, because pollen gene flow in A. exaltata is highly kin structured (i.e., all progeny resulting from any one gene flow event are full sibs), it is less able to counterbalance divergence caused by genetic drift than it would be with a comparable level of gene flow by unrelated individuals (Fix 1978; Rogers 1987; Rogers and Jorde 1987; Levin 1988). Third, gene-frequency divergence among populations could be increased if gene-flow rates vary greatly over time (Nagylaki 1979; Levin 1988; Whitlock 1992). This might be expected if the diversity of pollinators of A. exaltata also shows temporal variation, because turnover rates of pollinia are known to vary among pollinators (Morse 1982; Pleasants 1991; Broyles and Wyatt 1991; Broyles 1992).

Despite these caveats, our results strongly suggest that, at least in the southern Appalachian Mountains (from northern Georgia to northern Virginia), pollen gene flow is acting as a cohesive force that can maintain A. exaltata as an evolutionary unit. Within this region, A. exaltata is common along shaded roadsides and powerline cuts, and distances between populations of 0.05 km-1.0 km are typical. Large, strong-flying insects, such as bumblebees, fritillary butterflies, and migrating monarch butterflies, can potentially visit plants in several populations. In addition, because milkweed seeds have a plumose coma that enables them to be dispersed great distances (Morse and Schmitt 1985; Sacchi 1987), we would expect occasional long-distance seed gene flow to contribute further to lowering genetic differentiation among A. exaltata populations. Consistent with this general argument is the observation that relative levels of genetic differentiation among 18 southern Appalachian populations of A. exaltata ([G.sub.ST] = 0.093) are less than half the average for other outcrossing, animal-pollinated species ([G.sub.ST] = 0.197) (Broyles and Wyatt 1993). Levels of genetic differentiation for A. exaltata in this region are, in fact, more similar to values reported for outcrossing, wind-pollinated species [G.sub.ST] = 0.099; Hamrick and Godt 1989).

In the northern (e.g., Maine) and western (e.g., Iowa and Minnesota) boundaries of the range of A. exaltata, however, populations are more difficult to locate and frequently consist of fewer, more isolated plants than southern Appalachian populations. Because A. exaltata may have difficulty maintaining high pollinator constancy over the longer distances between populations, we predict that pollen-mediated gene flow, as well as overall fruit set, is lower in those sparsely populated regions. As a consequence, we would also expect to find greater genetic diversity among populations than was observed for the central portion of the range (Broyles and Wyatt 1993).

Indirect Versus Direct Estimates of Gene Flow. - Indirect estimates of gene flow obtained from [G.sub.ST] (Nm = 2.3 and 4.2) severely underestimate realized pollen-mediated gene flow (Nm = 6.1 and 9.4) between these Shenandoah populations in 1990. Antagonistic patterns of seed and pollen dispersal may partly explain this disparity. For example, seed dispersal into vacant habitats can increase genetic differentiation (and lower indirect gene flow estimates) if seeds are few and underrepresent genetic variation in the region (Wade and McCauley 1988). Even though seed dispersal could give rise to greater genetic differentiation than pollen dispersal, levels of genetic differentiation among these populations of A. exaltata are still lower than expected.

Temporal variation in pollen gene flow can contribute to the difference in direct and indirect measures of gene flow. We measured pollen gene flow in a single season of a long-lived perennial. The current population genetic structure is the result of microhabitat selection, and seed and pollen dispersal that have occurred throughout many years. Furthermore, pollen-mediated gene flow may be strongly correlated with annual variation in the composition of pollinators, weather conditions, and flower densities. Despite these differences, gene flow as low as one individual per generation is a strong evolutionary force and can counteract genetic drift even in small populations (Wright 1931, 1951). Therefore, even indirect estimates indicate that gene flow will have a significant impact on the population genetic structure of A. exaltata.

Variation in Pollen Gene Flow Rates among Populations. - The percentage of immigrant pollen for the six populations of A. exaltata tended to decrease with increasing isolation distance, but the rank correlation was not statistically significant. If we include an estimate of percent immigrant pollen (11.4%) into a highly isolated ([greater than] 1.0 km) population located near Mountain Lake Biological Station in Giles County, Virginia (Broyles and Wyatt 1991), this relationship is strengthened (Kendall's [Tau] = -0.781; P [less than] 0.05). Levels of pollen gene flow in A. exaltata thus appear not to be as idiosyncratic as was found in previous studies of seven populations of Raphanus sativus (Ellstrand and Marshall 1985; Ellstrand et al. 1989) and 13 patches of Curcurbita foetidissima (Kohn and Casper 1992), both of which found no relationship between isolation distance and percentage of immigrant pollen. Note, however, that gene flow into the Mountain Lake population is only about one-third as great as the lowest level observed in Shenandoah National Park, where the six study populations are all essentially nested within a much larger matrix of populations. This was not true for the Mountain Lake population, in which large phenological differences between the target population and the nearest conspecific populations augmented the spatial isolation. Ellstrand et al. (1989) have suggested that the size of the pollen source populations relative to the reference population may be a more important determinant of the level of immigrant pollen than the physical distance separating donor and recipient populations.

Progeny-Array Analysis Versus Seed-by-Seed Analysis. - The seed-by-seed analysis, incorporating cryptic gene flow, accounted for nearly 35% less gene flow than the progeny-array method. The discrepancy between the methods appears to have two underlying causes. First, unless foreign pollen donors are homozygous for one or more alleles not present in the target population, it is likely that some percentage of the hundreds of pollen genotypes carried in each immigrant pollinium will be cryptic (i.e., identical to some of those produced by plants within the target population). When an immigrant paternal genotype is similar to genotypes found in the target population, perhaps only a few seeds will actually express a pollen genotype novel to the target population. In these cases, the progeny-array method still correctly assigns all the seeds to pollen immigration. In this study, only 57% of the seeds within fruits sired by immigrant pollen had non-cryptic pollen genotypes. Moreover, all seeds had cryptic pollen genotypes in 4 of the 14 fruits sired by immigrant pollen at South Skyland and in 8 of the 25 fruits sired by immigrant pollen at Old Rag Overlook. The progeny-array method will, however, fail to detect gene flow only when immigrant pollen arrives from a plant with the same multilocus genotype as a plant in the target population.

Second, when matings are correlated events and each paternal parent sires many seeds, the Monte Carlo simulations do not compensate for the relatively low power of seed-by-seed exclusion, because the actual mating patterns violate an important assumption of the estimation procedure. Similar to the mixed-mating model for estimation of levels of outcrossing (Clegg 1980; Brown et al. 1989), Devlin and Ellstrand's (1990a) procedure assumes that each pollen genotype is drawn randomly and independently from a uniform population of pollen. Thus, just as Schoen and Clegg (1984) found that the mixed-mating model underestimated outcrossing rates when matings are correlated, so we found that the Monte Carlo method of Devlin and Ellstrand (1990a) inherently underestimates total pollen gene flow. The effect of correlated matings on gene-flow estimation appears to deserve further study, especially because correlated matings have been reported in Ipomoea purpurea (Schoen and Clegg 1986), Mimulus guttatus (Ritland 1989; Dudash and Ritland 1991), and Acacia melanoxylon (Muona et al. 1991), and probably occur in many other angiosperms. Correlated matings will certainly occur in taxa like milkweeds, which have their pollen packaged in multiples, such as Mimosoid legumes and orchids.

Hybridization between A. exaltata and A. syriaca. - The best documented case of hybridization in milkweeds involves A. exaltata and A. syriaca, which hybridize frequently when the two species are sympatric (Kephart et al. 1988; Wyatt and Broyles 1992). In a survey of allozyme variation, Broyles and Wyatt (1993a) observed several low frequency alleles ([P.sub.i] [less than] 0.05) in Shenandoah populations of A. exaltata that were believed to be diagnostic for A. syriaca. Inter-specific hybridization appears to have introduced novel genetic variation into some populations of A. exaltata. Thus, our finding that a low level of hybridization occurs via long-distance pollen movement between A. exaltata and A. syriaca is consistent with previous studies.

The frequency of interspecific pollen movement from A. syriaca is low and similar to the frequency of interspecific matings reported for other insect-pollinated species. For example, frequent movement by solitary bees (Xenoglossa strenua) between Cucurbita pepo and C. texana separated by 1300 m resulted in frequent pollen exchange, yet only 5% of the seeds produced in experimental gardens were interspecific hybrids (Kirkpatrick and Wilson 1988). Even in Louisiana irises, which are viewed as a classic example of hybridization and introgression (Anderson 1949), less than 1% of the seeds produced by Iris hexagona were sired by I. fulva when the two species are grown in parapatric stands (Arnold et al. 1993). Nevertheless, our estimate of hybridization between these two milkweeds may be conservative as most of the A. exaltata plants used in the study flowered before plants of A. syriaca.

In summary, the reliance on large, strong-flying insects with slow turnover rates of pollinia permits A. exaltata to disperse hundreds of pollen grains in durable pollinia over great distances. Extensive pollen-mediated gene flow should increase the proportion of total genetic diversity found within populations of A. exaltata and should be great enough to counterbalance the diversifying effects of genetic drift and natural selection. Finally, high levels of pollen gene flow allow hybridization between A. exaltata and A. syriaca to occur even when the two species are spatially separated and may serve to maintain novel, low-frequency alleles within populations of A. exaltata.

ACKNOWLEDGMENTS

We thank W. W. Anderson, W. E. Friedman, D. E. Giannasi, J. L. Hamrick, J. M. Pleasants, and S. L. Sherman-Broyles for comments on an earlier draft of this manuscript; D. Grise for help with electrophoresis; and the National Park Service for allowing us to study milkweeds in Shenandoah National Park. This research was supported by National Science Foundation Doctoral Dissertation Improvement Grant no. RR90727F and the Department of Botany at the University of Georgia. This paper represents a portion of a doctoral dissertation submitted to the Department of Botany at the University of Georgia.

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Author:Broyles, Steven B.; Schnabel, Andrew; Wyatt, Robert
Publication:Evolution
Date:Aug 1, 1994
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