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(American Journal of Botany. 1999;86:1114-1120.)
© 1999 Botanical Society of America, Inc.

Population differences in self-fertility in the "self-incompatible" milkweed Asclepias exaltata (Asclepiadaceae)1

Sara R Lipow 2, 5, Steven B Broyles 3 and Robert Wyatt 4, 6

2Department of Botany, University of Georgia, Athens, Georgia 30602; 3Department of Biological Sciences, State University of New York College at Cortland, New York 13045; and 4Institute of Ecology, University of Georgia, Athens, Georgia 30602

Received for publication June 4, 1998. Accepted for publication March 5, 1999.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Individual plants of Asclepias exaltata (Asclepiadaceae) typically express an unusual self-incompatibility system under single-gene control. Hand-pollinations performed in six natural populations detected occasional self-fertile plants. The frequency of self-fertile individuals ranged from 0 to 34.0% and differed significantly among populations. Self-fertility appears to be under genetic control, as the ability of most plants (80.0 %) to set fruit following self-pollinations was identical under natural and greenhouse conditions. Seed- and fruit-set, however, were significantly lower from self- vs. cross-pollinations. Allozyme analysis of the population with the highest frequency of self-fertility revealed that adult plants were not significantly inbred. Finally, fruit-set following within-population cross-pollinations did not differ from that following wide, between-population cross-pollinations.

Key Words: Asclepiadaceae • genetic diversity • mating systems • milkweed • pollinations • pseudo-self-fertility • self-incompatibility


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The study of self-incompatibility systems that enable certain plants to reject self-pollen and thus avoid self-fertilization has been a central topic in plant reproductive biology at least since the time of Darwin (1868) . Self-incompatibility is believed to occur in an estimated 40–100 angiosperm families (de Nettancourt, 1977 ; Charlesworth, 1985 ). In many of these families, however, self-incompatibility has been secondarily lost in some species, so that many self-incompatible species have self-compatible, and predominantly self-fertilizing, relatives. The shift from obligate outcrossing based on self-incompatibility to predominant self-fertilization is associated with numerous well-documented changes in floral structure and function (Stebbins, 1957 ; Wyatt, 1988 ). It is believed to be one of the most common evolutionary pathways in hermaphroditic plants (Stebbins, 1974 ).

The transition from self-incompatibility to self-compatibility obviously requires variation in the breeding systems of individuals and populations. Several studies have demonstrated variation with respect to outcrossing rate by analyzing progeny arrays using allozyme markers (reviewed by Barrett and Eckert, 1990 ). Outcrossing rates are determined, however, not only by plant-to-plant differences in breeding systems, but also by other genetic factors such as inbreeding depression, as well as by local ecological conditions (e.g., distance between neighbors and pollinator abundance). Interactions between these genetic and ecological factors can be complex and, unfortunately, allozyme studies cannot be used to differentiate variation caused by genetic differences from that caused by ecological factors (Barrett and Eckert, 1990 ). Moreover, an understanding of the evolution of self-compatibility from self-incompatibility requires knowledge of individual- and population-level variation with respect to self-incompatibility per se, not simply with respect to outcrossing rate.

A great deal of indirect evidence suggests that variation in incompatibility is common in natural populations. Partially self-fertile plants have been observed in many species that are normally self-sterile (reviewed by Lloyd and Schoen, 1992 ; Levin, 1996 ). Additionally, in several crop species, selective breeding of partially self-fertile individuals from otherwise self-incompatible cultivars has resulted in the formation of self-fertile lines (Robacker and Ascher, 1978 ; Dana and Ascher, 1985 ; Rick, 1988 ). This shows that selection for self-fertility has the potential to lead to rapid evolutionary change.

Despite these indications of variation in self-incompatibility and its obvious evolutionary importance, few studies have attempted to document the extent of this variation in natural populations. A notable exception is the pioneering study of Leavenworthia by Rollins (1963) and Lloyd (1965) . They showed that some populations have functional sporophytic self-incompatibility systems (Lloyd, 1967 ), whereas incompatibility has broken down in other populations, resulting in plants that are self-fertile to varying degrees. The self-fertile races occupy drier habitats and, consequently, must flower earlier in order to complete their life-cycle during the shortened growing season. Solbrig and Rollins (1977) proposed that the earlier flowering phenology led to pollinator limitation, which provided the selective force driving the evolution of self-fertility in Leavenworthia. Additionally, in the rare Aster furcatus, differences between individuals and populations with respect to sporophytic self-incompatibility have been reported to be associated with bottleneck-induced depletion of allelic diversity at the self-incompatibility locus (Reinartz and Les, 1994 ). Finally, Levin (1975 , 1989 ) has reported variation in autogamous seed-set in Phlox drummondii, a species with gametophytic self-incompatibility. This variation is heritable and probably caused by modifier alleles at genes other than the self-incompatibility locus (Bixby and Levin, 1996 ). Such alleles are said to confer "pseudo-self-fertility" (Levin, 1996 ).

The main objective of this study was to examine variation in self-incompatibility within and among populations of Asclepias exaltata. This species possesses a late-acting self-incompatibility system controlled by a single gene, and crosses between plants sharing one or more alleles at this locus are incompatible (Lipow, 1998 ). The incompatibility reaction occurs extremely late, after the formation of a zygote (Sparrow and Pearson, 1948 ; Sage and Williams, 1991 ). In an earlier study of eight plants of A. exaltata from Georgia, we identified one entirely self-fertile individual, and analysis of crossing relationships among its progeny revealed that the observed self-fertility was caused by pseudo-self-fertility (Lipow, 1998 ). Queller (1985) also detected a single self-fertile plant of A. exaltata from Michigan, and several other workers have reported finding occasional self-fertile plants in primarily self-incompatible species of Asclepias (Wyatt, 1976 ; Kephart, 1981 ; Wyatt, Ivey, and Lipow, 1996 ).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Species description
Asclepias exaltata L. is a perennial herb that occurs in forest clearings and along roadsides sheltered by forests. It is native from northern Georgia to Maine and westward to Minnesota and Iowa (Woodson, 1954 ). Like all species of Asclepias, A. exaltata is diploid, with n = 11 (Woodson, 1954 ). Mature plants typically produce one to three stems, each of which typically bears one to six umbels of 10 to 25 flowers (Shannon and Wyatt, 1986 ). Pollen in milkweeds is produced in discrete sacs termed "pollinia." Pollinia of A. exaltata contain ~180 pollen grains, which is more than the number necessary to fertilize all of the 60–80 ovules in a single ovary (S. Broyles, R. Wyatt, and S. Lipow, unpublished data). Thus, pollination with a single pollinium can result in the production of many comose seeds. Pollinia are transported between plants by strong-flying insects, such as bees and butterflies (Broyles and Wyatt, 1990 ). The gynoecium consists of two separate ovaries, of which usually only one matures into a follicle. In A. exaltata, as in most milkweeds, fruit-set is low, typically <5% in natural populations (Wilbur, 1976 ).

Field study
To test whether differences exist between populations of A. exaltata in the fraction of self-sterile individuals and in fruit-set following cross-pollination, plants in six natural populations were hand-pollinated (Table 1). Sample sizes are indicated in Table 2. During the hand-pollinations, a pair of anther wings of a recipient flower was splayed open with the aid of a large-diameter sewing needle. A single pollinium from a flower of a pollen donor was then inserted into the exposed stigmatic chamber, convex margin first, and the anther wings were gently pressed back together (cf. Wyatt, 1976 ).


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  		Table 1. Codes and localities for seven populations of Asclepias exaltata and a list of the studies in which they were included

 

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  		Table 2. Fruit-set from hand-pollinations of plants of Asclepias exaltata growing in six natural populations. Within all populations, there were highly significant differences (P < 0.0001 by two-sample Z tests) between self- and cross-pollinations for the proportion of plants and umbels maturing at least one fruit and for per-flower fruit-set. Comparisons were also made between populations; within a column, proportions sharing the same lowercase letter were not significantly different at the alpha = 0.05 level

 
In each population, plants in bud or in the early stage of flowering were identified and randomly assigned to either a self- or cross-pollination treatment. Any umbel containing opened flowers was clipped off, and, to prevent insect pollination, nylon mesh bags were placed over the remaining umbels. One to two days after opening, five flowers were pollinated on each umbel. One to three umbels were pollinated per flowering stem on up to three flowering stems. Self-pollinations were done using pollinia taken from the same flowers, and cross-pollinations of separate individuals were done using pollinia taken from plants in the self-pollination treatment. One pollen donor was used to pollinate five flowers on each umbel, but pollen from different donors was used for different umbels. All umbels not hand-pollinated were clipped off. Since the self-pollination treatment was applied to the whole plant, there was no possibility that fruit-set from self-pollinations was suppressed by the simultaneous development of competitively superior fruits from cross-pollinations. Approximately 10 wk after pollination, fruit-set was scored.

Plants in the CS and BP populations produced significant numbers of fruits from self-pollinations (see Results). The numbers of filled and unfilled seeds were counted for these fruits, as well as for cross-pollinated fruits from BP. No outcross hand-pollinations were performed for the CS population, so seeds from open-pollinated fruits were counted instead. Unfilled seeds were easily distinguished from filled seeds, as they were shrunken and contained small, apparently inviable embryos.

Greenhouse study
Hand-pollinations were done in the greenhouse, and the resulting fruit-set was compared to that observed in the field. These pollinations also allowed comparison of fruit-set following selfing vs. outcrossing of the same individuals and permitted interpopulation crosses. The 30 plants used were several self-fertile and self-sterile individuals included in the field study of the BP, CS, and SL populations. They were haphazardly chosen, and rootstocks from them were dug up in October 1996 and brought to the greenhouse. Also included were eight plants collected from the BB population in August 1994. All plants were grown in 25-cm pots filled with a custom medium containing pine-bark, vermiculite, perlite, lime, and micronutrients. They were fertilized twice per week, once with Peters 20:10:20 and once with Peters 10:30:20 plus added iron. Supplemental lighting was used to maintain a 14-h photoperiod. The resulting plants were large and vigorous, and they were probably much less limited by light, minerals, and water under greenhouse conditions than under field conditions.

In order to separate plants into self-fertile and self-sterile classes, we performed a minimum of 15 self- and 15 cross-pollinations on each plant; typically, many more were actually performed (mean = 34.8). Any plant that produced at least one fruit that contained filled seeds following self-pollination was considered self-fertile. All hand-pollinations involved five pollinations per umbel, each with pollen from the same paternal plant. Resource competition between developing fruits was unlikely because, at most, two umbels were pollinated per flowering stem with pollen from the same donor. Moreover, in Asclepias, competition among ovaries within umbels is much more intense than competition among ovaries on different umbels (Wyatt, 1980 ).

Allozyme diversity
Allozyme electrophoresis was conducted with tissue from 38 individuals from the CS population. We have reported previously (Broyles and Wyatt, 1993 ) results from an allozyme study of 17 other populations in the Southern Appalachians, including BB and SL, but chose to examine CS as well, because it contains an unusually high frequency of self-fertile individuals (see Results). Leaves were sampled from flowering individuals and stored in plastic bags on ice until enzymes could be extracted in 0.2 mol/L Tris-HCL (pH 7.5) extraction buffer (Broyles and Wyatt, 1990 ). All electrophoretic buffers and stain recipes were identical to those described by Broyles and Wyatt (1990 , 1993 ). The enzymes stained and loci scored included alanine transferase (Alt-1, Alt-2), glutamate dehydrogenase (Gdh-1), glutamate oxaloacetate transaminase (Got-1, Got-2), isocitrate dehydrogenase (Idh-1), malate dehydrogenase (Mdh-1, Mdh-2), menadione reductase (Mnr-1, Mnr-2), 6-phosphogluconate dehydrogenase (Pgd-1, Pgd-2), phosphoglucose isomerase (Pgi-1, Pgi-2), phosphoglucomutase (Pgm-1), and triosephosphate isomerase (Tpi-1, Tpi-2). Statistics of allozyme diversity were calculated using LYNSPROG, a computer program developed by Drs. M. D. Loveless and A. F. Schnabel.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
Field study
Fruit-set was significantly lower from self-pollinations than from cross-pollinations in all populations for which both were determined (Table 2). Overall, self-pollinations yielded fruit from only 15.1% of plants and 1.4% of flowers, whereas cross-pollinations yielded fruit from 53.1% of plants and 7.7% of flowers. Significant variation existed in the frequency of self-sterile individuals among the six populations of A. exaltata that we surveyed. At one extreme, no fruits resulted from selfed plants in the MC population, but 34.0% of selfed plants in the CS population produced fruits. Populations also differed in the frequency of plants producing fruits from cross-pollinations, and the rank order of populations with respect to success rate was the same from self- and cross-pollinations. The SL population had the lowest overall fruit-set; it appeared to suffer more from deer predation and physical damage from high winds (sustained at > 70 km/h) and extreme rainfall (>30 cm) associated with Tropical Storm Fran (6 September 1996) than any other population, including the UH population, located only 10.0 km away.

The number of filled seeds and the proportion of filled seeds were lower from self-pollinations than from cross- (BP population) or open-pollinations (CS population). These differences were significant for the CS population and approached significance for the BP population (Table 3). In all cases, standard deviations were large, reflecting substantial differences among fruits in seed-set.


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  		Table 3. Numbers of filled seeds and proportions of filled seeds from fruits of Asclepias exaltata. Hand-pollinations involving both self- and cross-pollen were done in the BP population. In CS, however, only self-pollinations were performed, but fruits from open- (and presumably outcross-) pollinations were also scored. Means (SD) and the results of Student's t tests are shown. For statistical analysis, an angular transformation was applied to the proportion of filled seeds (Sokal and Rohlf, 1981)

 
Greenhouse study
The results of the greenhouse pollinations reinforce and augment those done in the natural populations. Of 30 plants, 24 behaved similarly in the field and greenhouse with respect to their ability to set fruit following self-pollinations (Table 4). A few plants (four of 30), however, selfed in the greenhouse but not in the field. This is not unexpected as overall fruit-set from self-pollinations (15.7%) was greater in the greenhouse than in the field (1.4%), probably because of the greater resource availability in the greenhouse. Only two plants (6.7%) produced fruit from self-pollinations in the field but not in the greenhouse. Fruit-set following cross-pollinations within-populations was similar to that between populations (Table 5) and overall was 4.2 times greater than from pollinations done in the field. No apparent relationship existed between the distance between populations and fruit-set (Table 5).


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  		Table 4. The number of plants of Asclepias exaltata setting fruit after hand-pollinations with self-pollen. Individual plants from three populations were tested under both field and greenhouse conditions. The symbols "+" and "-" indicate the presence and absence of fruit-set, respectively

 

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  		Table 5. Fruit-set following within-population and between-population cross-pollinations of plants of Asclepias exaltata in the greenhouse

 
Of the 38 greenhouse-grown plants, 15 produced some selfed fruits following self-pollinations. Nevertheless, mean outcross fruit-set (41.3%) exceeded self fruit-set (20.9%) for these plants, and this difference was highly significant [G test with Williams's correction; Gadj = 73.9; P < 0.0001 (Sokal and Rohlf, 1981 )]. Importantly, these self-fertile plants varied greatly in the relative success of self- vs. cross-pollen (Fig. 1). Cross-pollination resulted in significantly higher fruit-set for five of the 12 self-fertile plants tested (individual G tests with alpha = 0.05), but in the remaining seven plants, there were no statistically significant differences between fruit-set from self- versus cross-pollinations. Finally, total per-flower fruit-set from cross-pollinations was greater in self-fertile plants (46.7%) than in self-sterile plants (31.1%), and this difference was highly significant (two-sample Z test: Z = 3.28, P = 0.005, N = 1435).



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  		Fig. 1. Fruit-set for individual plants of Asclepias exaltata following self- (solid bars) and cross-pollinations (unshaded bars) in the greenhouse; asterisks indicate significant differences between self- and cross-pollination. NA: data from cross-pollination not available

 
Allozyme diversity
We found that the highly self-fertile CS population maintained levels of genetic diversity typical of other Southern Appalachian populations of A. exaltata, including highly self-sterile ones such as SL (Table 6). The CS population was polymorphic at 60.0% of the loci surveyed, compared to the mean (± SD) of 64.5 ± 7.8% reported for 18 other populations. Its number of alleles per polymorphic locus (2.56) was also close to the mean of 2.36 ± 0.32. Additionally, the mean observed heterozygosity (H0 = 0.167) of the population was not statistically different from the expected heterozygosity (He = 0.174). Finally, there was neither a significant deficiency nor excess of heterozygotes at any polymorphic locus as determined by calculating Wright's Fixation Index for each locus. These data reveal that most mature individuals in the CS population were not produced by inbred matings.


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  		Table 6. Sample size, percentage of polymorphic loci (P), number of alleles per polymorphic locus (Ap), observed heterozygosity (Ho), and expected heterozygosity (He)

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The main conclusion from this study is that, although most individuals of Asclepias exaltata express a functional genetic self-incompatibility system, remarkably high variation in self-fertility exists within and among populations. The self-fertility probably has a predominantly genetic, rather than environmental, basis as most individuals classified as self-fertile in the field remained so after regeneration from rootstocks in the greenhouse. Moreover, 16 progeny from the cross of a self-fertile and a self-incompatible plant from the BB population were examined previously (Lipow, 1998 ), and five proved to be self-fertile. The pattern of cross-compatibility among these progeny was consistent with the hypothesis that the self-fertility was due to the influence of a modifier allele at a gene other than the self-incompatibility locus. Such modifiers are said to confer pseudo-self-fertility and are the most common cause of self-fertility in otherwise self-incompatible species (Levin, 1996 ).

Although populations of A. exaltata contain individuals with the capacity to self, the allozyme analysis failed to uncover any evidence of past inbreeding. This was even true for the CS population, which contains many self-fertile individuals. This lack of inbreeding is somewhat surprising, since geitonogamous pollinations are common in milkweeds (Pleasants, 1991 ; Shore, 1993 ). Few selfed progeny may be produced in the natural populations because of the lower fruit-set, seed number, and proportion of filled seeds following self- vs. cross-pollinations. Additionally, since the populations are highly outcrossed, selfed progeny that are produced are likely to suffer from inbreeding depression and, consequently, may rarely reach maturity (Husband and Schemske, 1996 ). Fruit production from self-pollinations could also be less common under natural conditions than from hand-pollinations, if competition between developing fruits occurs on self-fertile plants such that fruits from cross-pollinations are preferentially matured (cf. Becerra and Lloyd, 1992 ). Indeed, production of fruit from self-pollinations must be extremely uncommon in Virginia; we have never identified a single self-fertilized fruit during our paternity analyses of over 300 singly sired fruits from seven populations (Broyles and Wyatt, 1991 ; Broyles, Schnabel, and Wyatt, 1994 ), or from 284 fruits from a common garden at the University of Georgia, composed of plants started from seeds collected in Virginia (Broyles and Wyatt, 1995 ).

The frequency of self-fertile individuals varies between populations of A. exaltata and is probably determined by several evolutionary processes. Self-fertility alleles may spread in populations, because, all else being equal, selfing results in the transmission of twice as many genes to the next generation as does outcrossing (Fisher, 1941 ). Selection for self-fertility alleles may also occur in plants whose reproductive output is limited by access to cross-pollen. Such pollen limitation is thought to exist in populations of A. exaltata at least occasionally (reviewed by Broyles and Wyatt, 1997 ). Moreover, results from a diallel cross of eight plants collected from the BB population (Lipow, 1998 ) identified two reciprocal crosses that failed to set fruit, presumably because of shared incompatibility alleles. If allelic diversity is low enough that cross-pollinations regularly fail because of shared self-incompatibility alleles, then this would provide another selective force driving the evolution of pseudo-self-fertility. Finally, self-fertility may result not only in greater success of self-pollinations, but also in higher fecundity from cross-pollinations. Evidence for this comes from the apparent positive association between outcross fruit-set and the frequency of self-fertile individuals observed in the natural populations. This association cannot be explained easily by differences in resource availability between the populations, because outcross fruit-set in the greenhouse was also greater in self-fertile plants than in self-sterile plants.

The forces of inbreeding depression and pollen discounting (reviewed by Barrett and Harder, 1996 ), however, may counter the spread of self-fertility alleles. Pollen discounting occurs when pollen involved in selfing diminishes the pollen pool available for outcrossing. It is probably not important in A. exaltata, because levels of self-fertility probably do not affect the high rates of geitonogamy common in milkweeds (Pleasants, 1991 ; Shore, 1993 ). On the other hand, the effects of inbreeding depression were evident in the significantly lower seed-set from self- vs. cross-pollinations in the BP and CS populations. Theory predicts that self progeny must survive and reproduce at most half as well as outcross progeny in order for inbreeding depression to halt the spread of self-fertility alleles (Lloyd, 1979 ). It would be interesting to quantify inbreeding depression more closely in populations of A. exaltata to determine whether this is the case.

It is difficult to deduce the precise historical causes of the observed variation between populations in the frequency of self-fertile individuals. The frequency of self-fertile individuals was greater for populations in Georgia and North Carolina than for populations in Virginia. The Georgia and North Carolina populations are located at the edge of the range of A. exaltata (Woodson, 1954 ), and they appear to be more isolated and to have smaller population sizes than the populations in Virginia. Thus, we speculate that selection for self-fertility brought on by limitation of compatible pollen and/or genetic drift could have contributed to the greater frequency of self-fertility in Georgia and North Carolina than in Virginia.

In addition to variation in self-fertility, we also observed substantial variation among plants in cross-fertility. In A. syriaca (Morse and Schmitt, 1991 ) and A. incarnata (Lipow, 1998 ), similar between-plant variation in cross-fertility has been observed and shown, through quantitative genetic analyses, to result largely from an interaction between the maternal and paternal parents and from a maternal effect. The interaction resulted in differences in fruit-set between specific combinations of plants, regardless of which plant served as pollen donor or as pollen recipient. It could have been caused by differences in relatedness among parental pairs that resulted in differences in inbreeding depression or by the sharing of self-incompatibility alleles among some parental plants. The maternal effect reflects differences among maternal plants that have a genetic and/or environmental basis (Morse and Schmitt, 1991 ; Lipow, 1998 ). If self-fertility is associated with increased outcross fruit-set, then this could contribute to the maternal effect. Regardless of the precise mechanisms, we suspect that similar interaction and maternal effects account for much of the variation in cross-fertility that we observed in this study.

We found that fruit-set from cross-pollinations within populations was similar to that from cross-pollinations between populations, and no clear effect of distance between populations on fruit-set was apparent. These results differ from those obtained in studies of other milkweeds. For example, cross-pollinations within populations were nearly twice as successful in A. tuberosa (Wyatt, 1976 ) and 1.4 times more successful in A. incarnata ssp. incarnata (Ivey, Lipow, and Wyatt, 1999 ) than were cross-pollinations between populations. It is likely that populations of A. exaltata are less strongly differentiated genetically than populations of A. tubersosa and A. incarnata ssp. incarnata. The geographical range of A. exaltata is consistent with the view that the populations spread from a southeastern refugium in the past 15 000 yr (Broyles, 1998 ). Given the high frequency of long-distance gene flow in populations of A. exaltata (Broyles and Wyatt, 1991, 1994 ) and low genetic differentiation between populations (Broyles, 1998 ), we are not surprised by the high success rate of interpopulation crosses. In contrast, populations of A. tuberosa are morphologically and physiologically differentiated across the species' range and may have diverged much less recently (Woodson, 1947 , 1962 ; Wyatt and Antonovics, 1981 ).

Based on the available data, it is impossible to predict whether pseudo-self-fertility will increase in populations of A. exaltata and, ultimately, result in the evolution of self-compatibility. Many populations of A. exaltata, however, do harbor the variation necessary for this transition. Thus, should conditions favoring selfing arise, populations could follow the evolutionary pathway from self-incompatibility to self-compatibility previously taken by so many species (Stebbins, 1974 ).


   FOOTNOTES
 
1 The authors thank P. Ascher, M. Bulger, J. Hamrick, R. Price, and D. J. Schoen for comments on an earlier version of this manuscript; M. Bulger for help with plant collections; and A. Tull, M. Zimmerman, and M. Smith for excellent greenhouse care. Funding was provided by the W. C. Coker Fellowship and a grant-in-aid from Highlands Biological Station, a grant-in-aid from the University of Virginia's Blandy Experimental Farm, and the National Science Foundation (DEB-9623925). This paper represents a portion of a Ph.D. Dissertation submitted to the Department of Botany at the University of Georgia. Back

5 Author for correspondence, current address: Corvallis Forestry Sciences Laboratory, 3200 SW Jefferson Way, Corvallis, Oregon 97331. Back

6 Address as of 1 July 1999: Highlands Biological Station, P.O. Box 580, Highlands, North Carolina 28741. Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Barrett, S. C. H., and C. G. Eckert. 1990 Variation and evolution of mating systems in seed plants. In S. Kawano [ed.], Biological approaches and evolutionary trends in plants, 229–254. Academic Press, London.

———, and L. D. Harder. 1996 Ecology and evolution of plant mating. Trends in Ecology and Evolution 11: 73–79.

Becerra, J. X., and D. G. Lloyd. 1992 Competition dependent abscission of self-pollinated flowers of Phormium tenax (Agavaceae)—a 2nd action of self-incompatibility at the whole flower level. Evolution 48: 458–469.

Bixby, P. J., and D. A. Levin. 1996 Response to selection on autogamy in Phlox. Evolution 50: 892–899.[CrossRef][ISI]

Broyles, S. B. 1998 Postglacial migration and the loss of allozyme variation in northern populations of Asclepias exaltata (Asclepiadaceae). American Journal of Botany 85: 1091–1097.[Abstract]

———, and R. Wyatt. 1990 Paternity analysis in a natural population of Asclepias exaltata: multiple paternity, functional gender, and the "pollen-donation hypothesis." Evolution 44: 1454–1468.[CrossRef][ISI]

———, and ———. 1991 Effective pollen dispersal in a natural population of Asclepias exaltata: the influence of pollinator behavior, genetic similarity, and mating success. American Naturalist 138: 1239–1249.[CrossRef][ISI]

———, and ———. 1993 Allozyme diversity and genetic structure in southern Appalachian populations of Asclepias exaltata. Systematic Botany 18: 18–30.

———, and ———. 1995 A reexamination of the pollen-donation hypothesis in an experimental population of Asclepias exaltata. Evolution 49: 89–99.[CrossRef][ISI]

———, and ———. 1997 The pollen donation hypothesis revisited: a response to Queller. American Naturalist 149: 595–599.[CrossRef][ISI]

———, A. Schnabel, and R. Wyatt. 1994 Evidence for long-distance pollen dispersal in milkweeds (Asclepias exaltata). Evolution 47: 1032–1040.[ISI]

Charlesworth, D. 1985 Distribution of dioecy and self-incompatibility in angiosperms. In P. J. Greenwood and M. Slatkin [ed.], Evolution-Essays in Honour of John Maynard Smith, 237–268. Cambridge University Press, Cambridge.

Dana, M. N., and P. D. Ascher. 1985 Pseudo-self-compatibility (PSC) in Petunia integrifolia. Journal of Heredity 76: 468–470.[Abstract/Free Full Text]

Darwin, C. 1868 Variation in animals and plants under domestication. Orange, Judd&Company, New York, NY.

De Nettancourt, D. 1977 Incompatibility in angiosperms. Springer-Verlag, New York, NY.

Fisher, R. A. 1941 Average excess and average effect of a gene substitution. Annals of Eugenics 11: 53–63.[ISI]

Husband, B. C., and D. W. Schemske. 1996 Evolution of the magnitude and timing of inbreeding depression in plants. Evolution: 54–70.

Ivey, C. T., S. R. Lipow, and R. Wyatt. 1999 Mating systems and interfertility of swamp milkweed (Asclepias incarnata ssp. incarnata and ssp. pulchra). Heredity 82: 25–35.[CrossRef][ISI]

Kephart, S. R. 1981 Breeding systems in Asclepias incarnata L., A. syriaca L., and A. verticillata L. American Journal of Botany 68: 226–232.[CrossRef][ISI]

Levin, D. A. 1975 Gametophytic selection in Phlox. In D. L. Mulcahy [ed.]. Gamete competition in plants and animals, 207–217. North-Holland, Amsterdam.

———. 1989 Inbreeding depression in partially self-fertilizing Phlox. Evolution 43: 1417–1423.[CrossRef][ISI]

———. 1996 The evolutionary significance of pseudo-self-fertility. American Naturalist 148: 321–332.[CrossRef][ISI]

Lipow, S. R. 1998 Post-zygotic self-incompatibility and self-fertility in the Asclepiadaceae and Apocynaceae. Ph.D. thesis, University of Georgia. Athens, GA.

Lloyd, D. G. 1965 Evolution of self-compatibility and racial differentiation in Leavenworthia (Cruciferae). Contributions Gray Herbarium (Harvard University) 195: 3–195.

———. 1967 The genetics of self-incompatibility in Leavenworthia crassa Rollins (Cruciferae). Genetica 38: 227–242.[CrossRef][ISI]

———. 1979 Some reproductive factors affecting the selection of self-fertilization in plants. American Naturalist 113: 67–79.[CrossRef][ISI]

———, and D. J. Schoen. 1992 Self- and cross-fertilization in plants. I. Functional dimensions. International Journal of Plant Science 153: 358–369.[CrossRef]

Morse, D. H., and J. Schmitt. 1991 Maternal and paternal effects on follicle production in the milkweed Asclepias syriaca (Asclepiadaceae). American Journal of Botany 78: 1304–1309.[CrossRef][ISI]

Pleasants, J. M. 1991 Evidence for short-distance dispersal of pollinia in Asclepias syriaca L. Functional Ecology 5: 75–82.

Queller, D. C. 1985 Proximate and ultimate causes of low fruit production in Asclepias exaltata. Oikos 44: 373–381.[CrossRef][ISI]

Reinartz, J. A., and D. H. Les. 1994 Bottleneck-induced dissolution of self-incompatibilty and breeding system consequences in Aster furcatus (Asteraceae). American Journal of Botany 81: 446–455.[CrossRef][ISI]

Rick, C. M. 1988 Evolution of mating systems in cultivated plants. In L. D. Gottlieb and S. K. Jain [eds.], Plant evolutionary biology, 133–147. Chapman and Hall, New York, NY.

Robacker, C. D., and P. D. Ascher. 1978 Restoration of pseudo-self-compatibilty (PSC) in derivatives of a high-PSC cross in Nemesia strumosa Benth. Theoretical and Applied Genetics 53: 135–141.[CrossRef][ISI]

Rollins, R. C. 1963 The evolution and systematics of Leavenworthia (Cruciferae). Contributions Gray Herbarium (Harvard University) 192: 3–198.

Sage, T. L., and E. G. Williams. 1991 Self-incompatibility in Asclepias. Plant Cell Incompatibility Newsletter 23: 55–57.

Shannon, T. R., and R. Wyatt. 1986 Reproductive biology of Asclepias exaltata. American Journal of Botany 73: 11–20.[CrossRef][ISI]

Shore, J. S. 1993 Pollination genetics of the common milkweed, Asclepias syriaca L. Heredity 70: 101–108.[ISI]

Sokal, R. R., and F. J. Rohlf. 1981 Biometry, 2d ed. W. H. Freeman, San Francisco, CA.

Solbrig, O. T., and R. C. Rollins. 1977 The evolution of autogamy in species of the mustard genus Leavenworthia. Evolution 31: 265–281.[CrossRef][ISI]

Sparrow, F. K., and N. L. Pearson. 1948 Pollen compatibility in Asclepias syriaca. Journal of Agricultural Research 77: 187–199.

Stebbins, G. L. 1957 Self-fertilization and population variability in the higher plants. American Naturalist 91: 337–354.[CrossRef][ISI]

———. 1974 Flowering plants: evolution above the species level. Belknap, Cambridge, MA.

Wilbur, H. M. 1976 Life history evolution in seven milkweeds of the genus Asclepias. Journal of Ecology 64: 223–240.[CrossRef]

Woodson, R. E. 1947 Some dynamics of leaf variation in Asclepias tuberosa. Annals of the Missouri Botanical Garden 34: 353–432.[CrossRef]

———. 1954 The North American species of Asclepias L. Annals of the Missouri Botanical Garden 41: 1–211.[CrossRef]

———. 1962 Butterflyweed revisited. Evolution 16: 168–185.[CrossRef][ISI]

Wyatt, R. 1976 Pollination and fruit-set in Asclepias: a reappraisal. American Journal of Botany 63: 845–851.[CrossRef][ISI]

———. 1980 The reproductive biology of Asclepias tuberosa: I. Flower number, arrangement, and fruit-set. New Phytologist 85: 119–131.[CrossRef][ISI]

———. 1988 Phylogenetic aspects of the evolution of self-pollination. In L. D. Gottlieb and S. K. Jain [eds.], Plant evolutionary biology, 109–131. Chapman&Hall, London.

———, and J. Antonovics. 1981 Butterflyweed re-revisited: spatial and temporal patterns of leaf shape variation in Asclepias tuberosa. Evolution 35: 539–542.

———, and S. B. Broyles. 1997 The weedy tropical milkweeds Asclepias curassavica and A. fruticosa are self-compatible. Biotropica 29: 232–234.[CrossRef][ISI]

———, C. T. Ivey, and S. R. Lipow. 1996 The breeding system of desert milkweed, Asclepias subulata. Bulletin of the Torrey Botanical Club 123: 180–183.[CrossRef][ISI]




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