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(American Journal of Botany. 1999;86:140-144.)
© 1999 Botanical Society of America, Inc.

Seed provisioning in gynodioeciousSilene acaulis (Caryophyllaceae)1

Lynda F. Delph2,a, Maia F. Baileya and Deborah L. Marr3,a

a Department of Biology, Indiana University, Bloomington, Indiana 47405


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In gynodioecious species, which contain females and hermaphrodites, the outcrossed seeds of females have been found to outperform the outcrossed seeds of hermaphrodites, in spite of the fact that their seeds are not larger in mass. Females do not make pollen. Hence the nutrients that hermaphrodites allocate to pollen, such as nitrogen, might be allocated to seeds by the females, such that individual seeds from females are better provisioned than those from hermaphrodites. Alternatively, females might make more seeds, rather than better provisioned seeds. We tested the hypothesis that seeds from females would be better provisioned for the gynodioecious species Silene acaulis, by comparing seed mass, embryo/endosperm mass, nitrogen and phosphorus content, and energy content for outcrossed seeds from females and hermaphrodites produced in a natural population. We also measured the proportion of flowers that set fruit in both morphs. Seeds from the two sexual morphs were not found to differ significantly for any of the measures of seed provisioning, with seeds from females containing either nonsignificantly less or equivalent amounts of each of the measures as compared to hermaphrodites. However, females set a significantly higher proportion of their flowers to fruit, as compared to hermaphrodites. These results indicate that females do not provision individual seeds more than hermaphrodites in S. acaulis, and alternative hypotheses will need to be examined to explain the difference in the performance of the seeds from the two sexual morphs.

Key Words: Caryophyllaceae • embryo mass • fruit set • gynodioecy • nutrient content • seed mass • Silene acaulis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Many researchers have investigated the effect of offspring size on fitness. Almost without exception, larger offspring outperform smaller offspring in both plants and animals (see reviews in McGinley, Temme, and Geber, 1987, and Azevedo, French, and Partridge, 1997). In plants, for example, seed size has been found to be positively correlated with fitness in over 60 separate studies (Black, 1957; Tossell, 1960; Lawrence, 1963; Cook, 1980; Gross and Soulé, 1981; Wulff, 1986a, b; McGinley, Temme, and Geber, 1987 and references therein; Stamp, 1990; Galen and Stanton, 1991; Jackson, Dewald, and Bohlen, 1992). In particular, large seeds have been found to produce seedlings that have higher rates of survival than seedlings from small seeds in at least nine species (Oexemann, 1942; Spurr, 1944; Black, 1957; Cook, 1980; Schaal, 1980; Morse and Schmitt, 1985; Galen and Stanton, 1991; Jackson, Dewald, and Bohlen, 1992), which may reflect more endosperm in large vs. small seeds (Harper, 1977).

Given these results concerning seed size and progeny performance, the results of some studies comparing the offspring performance of the morphs of gynodioecious species (which contain both female and hermaphroditic individuals) are unexpected. These studies compared seeds produced from controlled cross-pollinations, such that differences in offspring fitness caused by differences in the extent of selfing were eliminated. Outcrossed seeds from females outperformed outcrossed seeds from hermaphrodites, even though the seeds from females were either smaller or equal in mass to those from hermaphrodites, in three of the seven gynodioecious species listed in Table 1: Minuartia obtusiloba (Schrader, 1986), Sidalcea oregana (Ashman, 1992), and Silene acaulis (Shykoff, 1988). In M. obtusiloba, a greater percentage of outcrossed seeds from females germinated than outcrossed seeds from hermaphrodites (Schrader, 1986). Similarly, in S. oregana, seedling growth rates were significantly greater in outcrossed progeny from females than in outcrossed progeny from hermaphrodites (Ashman, 1992). Lastly, outcrossed seeds from S. acaulis females survived the seedling establishment phase over nine times more often than outcrossed seeds from hermaphrodites (Shykoff, 1988).


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  		Table 1. Summary of the characteristics of seven gynodioecious species in which the performance of outcrossed progeny from females (F) and hermaphrodites (H) were compared. Boldface letters indicate that the difference is significant.

 
Shykoff (1988) suggested that although outcrossed seeds from females of S. acaulis are not larger in mass than those from hermaphrodites, they might contain more nutrients such as nitrogen, as a consequence of the females not producing pollen (see also Ashman, 1992, and Poot, 1997). Darwin (1877) also considered the savings that females obtain from not making pollen as a possible explanation for why females of some gynodioecious species make larger seeds or more seeds per fruit than hermaphrodites, and he termed this "compensation." Seeds having higher concentrations of nitrogen have been shown to outperform those with lower concentrations in some plant species (Parrish and Bazzaz, 1985). In addition, Silene pollen contains a relatively high concentration of nitrogen as compared to other floral structures (Carroll and Delph, 1996). Hence, seeds from S. acaulis females may have had higher survival than seeds from hermaphrodites, because they were better provisioned (Shykoff, 1988). In this paper we test whether outcrossed seeds produced by females are better provisioned than those produced by hermaphrodites in S. acaulis. We compared seed mass, embryo/endosperm mass, nitrogen and phosphorus content, and energy content for outcrossed seeds from the two sexual morphs produced in a natural population with the prediction that seeds from females would be better provisioned. In addition, we compared the proportion of flowers that set fruit for the two morphs, as females could put the resources saved by not making pollen into producing more fruit.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Study system
Silene acaulis (Caryophyllaceae) is a long-lived, circumpolar, evergreen cushion plant, occurring in arctic and alpine tundra. We obtained seeds for comparison from a population of S. acaulis var. subacaulescens on Pennsylvania Mountain (Park County, Colorado, 39°15''N, 106°15''W) in central Colorado. S. acaulis occurs in the tundra on Pennsylvania Mountain, above ~3750 m, and the flowers are primarily pollinated by the bumble bee Bombus sylvicola. Our study population is best described as being gynodioecious. Based on primary sex characters, it contains female (or male-sterile) individuals that produce only pistillate flowers (containing a functional gynoecium but no pollen) and hermaphrodites, most of which produce only perfect flowers (containing a functional gynoecium and androecium), but a few that produce a low percentage of pistillate flowers in addition to perfect flowers. The frequency of females in this population is 25% (Shykoff, 1988; Marr, 1997).

Pollinations
To obtain outcrossed seeds from both morphs for comparison, hand pollinations were performed on plants growing in an area of ~40 by 30 m (containing hundreds of individuals) in the natural population on Pennsylvannia Mountain in the summers of 1994 and 1996, at the same site used by Shykoff (1988). Flowers were encapsulated while still in bud with an inverted 1.5-mL microcentrifuge tube, which was held in place by pushing a straight pin through the cap and into the cushion plant. This prevented visitation to the flowers by all potential pollinators (including ants and beetles, as well as all flying insects). Once the flowers opened they were treated as follows: pistillate flowers on female plants were pollinated on the day after opening, whereas perfect flowers on hermaphrodite plants were emasculated in the morning of the day of opening (prior to anther dehiscence) and then subsequently pollinated. Pollinations of these perfect flowers took place, on average, 4 d later, after the styles had grown out past the opening of the corolla. This delay was necessary because the perfect flowers are highly protandrous, with the two anther whorls dehiscing in sequence, prior to elongation and receptivity of the styles (Shykoff, 1992). Pollination was performed by brushing freshly dehisced anthers across the ends of the styles. In order to reduce the chance of biparental inbreeding, all pollen donors were chosen such that they were >20 m from the plant being pollinated. Following pollination, the caps were replaced and then subsequently removed after the styles had shrivelled. Three to six flowers per plant were pollinated. Seeds were collected only after the ripe fruit had split open to disperse the seeds, thereby ensuring that the seeds were fully mature when collected.

Seed mass and embryo/endosperm mass
Outcrossed seeds from hand pollinations were collected from the study site from 23 female and 24 hermaphrodite plants. A mean ± 1 SE of 24 ± 1.5 seeds per plant were weighed to the nearest 1 µg, for a total of 1139 seeds. The data on seed mass were analyzed by first calculating the means for each of the 47 plants and using these values as independent points for the statistical analyses. Means were compared between the sexual morphs with a t test.

Seeds are composed of an outer seed coat, embryo, and endosperm tissue, so the mass of the embryo/endosperm can be determined by subtracting the mass of the seed coat from the total seed mass. Outcrossed seeds from the two sexual morphs were weighed to the nearest 1 µg and then planted in the greenhouse by placing the seeds on top of a soil mix in 196-celled trays. Water was added from below to allow germination and the coat of each seed was retrieved following germination. A total of 434 seeds germinated (232 seeds from 21 hermaphrodites and 202 from 20 females) from which the seed coat could be easily retrieved intact on the day of germination. Data were obtained from an average of 11.1 and 10.1 seeds per hermaphrodite and female plant, respectively. Forceps were used to remove the seed coat from the end of one of the cotyledons, where it typically ends up after the seedling germinates. The seed coat was air-dried for 1 d and then weighed to the nearest 1 µg. The data on embryo/endosperm mass were analyzed by first calculating the means for each of the 41 plants, and these values were used as independent points for the statistical analyses. In addition, the proportion of each seed that comprised the embryo/endosperm was calculated by dividing the embryo/endosperm mass by the seed mass and the mean was determined for each plant. The mean masses of the embryo/endosperm and proportion of the seed comprising embryo/endosperm were compared for the two sexual morphs with t tests.

Nitrogen and phosphorus analysis
Nitrogen and phosphorus contents were measured using the protocol outlined in Ashman and Baker (1992). Outcrossed seeds were collected from 30 female and 24 hermaphrodite plants from the study site. One seed from each parent was weighed to the nearest 1 µg and then digested. Digestions were performed using 50 µL H2SO4 and 100 µL H2O2.

Three to six microlitres of each digest sample were used for both the nitrogen and phosphorus assays. For each trial and in both assays, a standard curve was generated by running samples of known nitrogen or phosphorus content at the beginning and end of each trial. Each measurement was replicated and the two absorbance readings were averaged. By using the regression line of the standard curve, the equivalent amount of standard solution could be calculated for each sample. The concentration of nitrogen or phosphorus per microlitre was calculated by multiplying the sample's equivalent standard solution volume by the standard solution's concentration and dividing by the amount of digested liquid used. The amount of nitrogen or phosphorus per mass of seed was calculated as the product of the digestion concentration and the total digested volume, and the amount of each nutrient per mass of seed was calculated by dividing the per seed value by the seed mass. Comparisons were made between the sexual morphs for the amount of the two nutrients contained per seed and per mass of seed with t tests.

Calorimetry
The energy content of seeds was determined by bomb calorimetry using a Parr 1108 oxygen bomb, calorimeter, and 1710 controller. Ten groups of 50 outcrossed seeds (five groups per sexual morph) were weighed to the nearest 1 µg and then pelleted with 50–60 mg of benzoic acid and burned according to the manufacturer's instructions. Total energy released was calculated from the calorimeter's heat capacity and the increase in temperature. Seed energy content was then found by subtracting the energy added by the benzoic acid and fuse from the total energy released. The mean amount of energy (in kilojoules) contained per seed from each of the ten groups was calculated, and the means for the two sexual morphs were compared with a t test.

Proportion of flowers setting fruit
In order to compare the proportion of flowers setting fruit (fruit set) on females and hermaphrodites, the total number of flowers and fruit produced by 56 female and 63 hermaphrodites were counted in 1994, the same year that seed mass was measured. Plants were chosen to include a range of sizes within each sex, from relatively small to relatively large. Plant area was determined by measuring the maximum width and length of each plant (i.e., cushion) and multiplying these two numbers. This approximates cushion size as a rectangle. Plant area (in square centimetres) did not differ significantly between the sexes for the plants used to determine fruit set (161.4 ± 21.54 vs. 174.1 ± 18.02 for females and hermaphrodites, respectively; t = 0.45, df = 93, P = 0.65). Fruit set was compared between the sexes by a t test with separate variances. The data were arcsine (square-root) transformed prior to analysis, and mean fruit set values are therefore presented as backtransformed values.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Outcrossed seeds from the two sexual morphs did not differ significantly for any of the traits compared: the values were either equivalent (embryo/endosperm per seed, nitrogen per mass of seed, and energy per seed) or seeds from females had nonsignificantly smaller values (seed mass, proportion of seed comprised as embryo/endosperm, nitrogen per seed, phosphorus per seed, and phosphorus per mass of seed) than those from hermaphrodites (Table 2). These results counter the prediction that seeds from females would be better provisioned than those from hermaphrodites.


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  		Table 2. Seed characters [means (SE)] for outcrossed seeds from the two sexual morphs of Silene acaulis.

 
The two sexual morphs did not differ significantly in the number of flowers produced per plant (103 ± 9.6 vs. 94 ± 7.0 for females and hermaphrodites, respectively; t = 0.82, df = 117, P = 0.42). However, the proportion of flowers that set fruit differed significantly between the sexual morphs (t = 3.95, df = 116.8, P < 0.001). Females set significantly more of their flowers to fruit (back-transformed mean = 78%, SE's = + 2.3, - 2.5) than did hermaphrodites (back-transformed mean = 62%, SE's = ± 3.1).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our results do not support the hypothesis that outcrossed seeds from females S. acaulis are in any way better provisioned than those from hermaphrodites. All of our measures of seed provisioning revealed that seeds from females are either nonsignificantly less or equally well provisioned as those from hermaphrodites. Thus it is not the case that slightly greater provisioning of seeds from females for several measures could add up to make an overall difference that could account for the higher survivorship of seeds from females, even though no single measure might show a significant difference.

It appears that S. acaulis females do not use the resources saved by not making pollen for enhancing the provisioning of individual seeds. Instead, we showed that the females set fruit from a higher proportion of their flowers than do hermaphrodites. Similar results for S. acaulis were obtained by Shykoff (1988) from the same site. In addition, data on fruit set from the same subspecies of S. acaulis on a different mountain in Colorado (L. Delph and S. Carroll, unpublished data) and from the other North American subspecies, exscapa, in Canada (Hermanutz and Innes, 1994) also showed significantly higher fruit set by females as compared to hermaphrodites. Moreover, comparable results have been found for Sidalcea oregana, in which Ashman (1994) found nonsignificant differences between females and hermaphrodites for allocation to biomass, phosphorus, and nitrogen per naturally pollinated seed, but on the basis of whole-plant allocation to seeds, females allocated significantly more of the first two currencies.

In contrast, studies on other gynodioecious species growing in their natural populations have shown that females have both higher fruit set and produce seeds (from natural pollination) of greater seed mass than hermaphrodites [Echium vulgare (Klinkhamer, de Jong and Nell, 1994), Ochradenus baccatus (Wolfe and Shmida, 1997), and Schiedea adamantis (Sakai et al., 1997)]. As hermaphrodites in these species are capable of self-fertilization, it is possible that, in addition to compensation effects, the difference in seed mass for these naturally pollinated seeds could be related to whether the seeds on hermaphrodites were selfed or outcrossed. Note that in S. adamantis, selfed seeds from hermaphrodites are significantly smaller in mass than outcrossed seeds from hermaphrodites or females, and outcrossed seeds from the two morphs do not differ significantly in seed mass (Sakai et al., 1997).

Given that our results show that provisioning cannot be the explanation for the greater survivorship of outcrossed seeds from females, we are left to consider other explanations for this phenomenon. One mechanism that has been suggested to explain this difference is that S. acaulis females may produce more fit offspring than hermaphrodites as a result of increased gametophytic selection in their flowers (Shykoff, 1992). Shykoff found that while both flower morphs receive many times more pollen grains than there are ovules, pollen germinates more rapidly on the stigmas of pistillate flowers, resulting in greater numbers of pollen tubes growing down the styles of pistillate as compared to perfect flowers. As suggested by Shykoff (1992), the longer styles of the pistillate flowers, in combination with the greater number of pollen tubes that are growing down their styles, should result in the ovules of pistillate flowers being pollinated by superior pollen donors as compared to ovules from perfect flowers, and this superiority should be reflected in the fitness of the resulting seeds. To test this hypothesis, the effect of pollen tube competition on progeny fitness would need to be examined.

An alternative, but not mutually exclusive, hypothesis for the lower survivorship of outcrossed seeds from hermaphrodites concerns possible pleiotropic effects of the genes that determine sex in this gynodioecious species. In most gynodioecious species, sex is inherited by a nuclear-cytoplasmic interaction (Ganders, 1978; Kheyr-Pour, 1980; Van Damme, 1983, 1991; Gouyon and Couvet, 1987; Sun, 1987; Conner and Charlesworth, 1989; Frank, 1989; Belhassen et al., 1991; Ashman, 1992; Koelewijn and Van Damme, 1995). This includes another species of Silene, S. vulgaris (Charlesworth and Laporte, in press), and data from crosses strongly suggest that this type of sex determination is present in S. acaulis (L. Delph, unpublished data). With nuclear-cytoplasmic inheritance, females are produced when there is a male-sterility gene in the cytoplasm (mitochondrial genome). Hermaphrodites are produced when a nuclear-restorer allele is present that matches the male-sterility gene, or when the cytoplasm is male-fertile. If the restorer alleles were to have negative pleiotropic effects, then this might account for the lower survivorship of seeds from hermaphrodites, as their progeny are likely to contain more restorers. All theoretical models show that stability of nuclear-cytoplasmic gynodioecy requires negative pleiotropic effects of either the restorer alleles or of the male-sterile cytotype (Charlesworth, 1981; Delannay, Gouyon, and Valdeyron, 1981; Gouyon and Couvet, 1985; Frank, 1989). Hence, on theoretical grounds, it is plausible that nuclear-restorer alleles have negative pleiotropic effects in S. acaulis. Furthermore, evidence for negative pleiotropic effects of restorers was shown empirically in a study of Plantago lanceolata, by comparing hermaphrodites with different numbers of restorers (de Haan, Hundscheid, and van Hinsberg, 1997).

In summary, our results refute the hypothesis that females of S. acaulis provision their seeds better than do hermaphrodites. Nevertheless, studies on this and other gynodioecious species reveal that outcrossed seeds from females outperform outcrossed seeds from hermaphrodites. Hence, future studies investigating alternative hypotheses to explain this phenomenon are required before the cause of this morph-differential offspring performance can be understood.


   FOOTNOTES
 
1 The authors thank C. Fenster, C. Lively, and J. Shykoff for comments on a previous draft of this paper, J. C. Randolph for help with the micro-bomb calorimetry, and E. Lacey for discussing her embryo-mass work. This work was funded by National Science Foundation grants to LD (DEB-9319002) and DM (DEB-9411951). Back

2 Author for correspondence (e-mail: ldelph{at}bio.indiana.edu ). Back

3 Current address: Department of Biology, Box 1812, Station B, Vanderbilt University, Nashville, Tennessee 37235. Back


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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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