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The effect of timing of pollination on the mating system and fitness ofKalmia latifolia (Ericaceae)¹

^a Department of Biology, Indiana University, Bloomington, Indiana 47401

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Plant mating systems are known to vary within species and some immediate ecological factors have been found to be associated with the geographic distribution of selfing. The environmental condition of the maternal plant may influence the production of selfed seed relative to outcrossed seed. This study investigated the effect of late pollination on the mating system of Kalmia latifolia, a long-lived perennial shrub. A 2 x 2 experimental design was used to determine whether reproductive success declines over the course of the flowering season and whether there was an interaction between pollination time (early vs. late in the season) and pollen type (self-fertilized vs. outcrossed). An interaction of this sort would indicate context-dependent fitness of selfed seeds compared to outcrossed seeds and, thus, show an ecological influence over a plant's mating system. Relative fitness was assessed in terms of female reproductive success. Timing of pollination did not affect abortion of outcrossed seeds; however, delay in pollination increased abortion of selfed seeds by 34.7%. Thus, it appears that plants selectively aborted selfed seeds rather than outcrossed seeds and this selection was more intense at the end of the season. An ecological factor such as time of pollination may affect the mating system of K. latifolia.

Key Words: Ericaceae • facultative response • fruit set • Kalmia latifolia • plant mating systems • pollination • reproductive assurance • resource provisioning • seed set • selfing rate

	INTRODUCTION

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Many ecological factors have been found to affect the fitness consequences of outcrossing and self-fertilization as reproductive strategies in plants (reviewed in Uyenoyama, Holsinger, and Waller, 1993; Barrett and Harder, 1996; and Holsinger, 1996). Pollen limitation (Zimmerman, 1980; Campbell and Motten, 1985; Rathcke, 1988), mode of self-pollination (Lloyd, 1979), adjustment of resource allocation (Schoen and Lloyd, 1984), number of possible outcrossing mates (Holsinger, Feldman, and Christiansen, 1984; Kohn and Barrett, 1994), and density of outcross pollen (Barrett and Husband, 1990; Holsinger, 1990) are known to affect the evolution of selfing. Fewer studies have examined the impact of the environmental condition of the maternal plant (i.e., resources available for seed provisioning) on the subsequent production of selfed seed relative to outcrossed seed. Immediate ecological factors such as xerism of the environment (Marshall and Allard, 1970; Hamrick and Allard, 1972; Brown, Marshall, and Albrecht, 1974; Brown, Zohary, and Nevo, 1978; Clegg, 1980), marginality and exposure of habitat (Wyatt, 1986), and elevation (Phillips and Brown, 1977) have been found to be associated with selfing.

Many researchers have also examined the potential for resource limitation to intensify fruit and seed competition (Janzen, 1977; Charnov, 1979; Stephenson, 1981; Lee and Bazzaz, 1982; Stephenson and Bertin, 1983; Bawa and Webb, 1984; Lee, 1984; Marshall, 1988; Marshall and Ellstrand, 1988; Marshall and Folsum, 1991) and the potential for maternal plants to improve fitness by fruit and seed abortion (Willson and Burley, 1983; Stephenson and Bertin, 1983; Stephenson and Winsor, 1986; Gorchov and Estabrook, 1987; Casper, 1988; Lee, 1988; Herrera, 1990). In this study I explore the possibility that differential effects of timing of pollination on outcrossed vs. selfed seed production may underlie associations between environmental conditions and patterns of plant mating systems.

In a mixed mating system (where some seeds are produced from self-fertilization and others from outcrossed fertilization), any force that influences the degree of selectivity of fruit or seed abortion can modify the mating system of the plant. For example, if selfed seeds are more likely to be aborted than outcrossed seeds when resources are limited within a plant, then resource limitation can increase a plant's outcrossing rate (since rate is defined as the proportion of seeds that result from outcrossing). Therefore, interactions between resource levels and the type of pollen a plant receives (e.g., selfed vs. outcrossed) are possible, and significant interactions may indicate a context-dependent modification of a plant's mating system.

As the flowering season progresses, resources available for provisioning fruits and seeds often decline (Delph, 1986; Sage and Webster, 1987; Karoly, 1992; Casper and Niesenbaum, 1993). The potential of certain ecological conditions, such as resource richness early in the season and resource poverty late in the season, to affect a plant's mating system has received little attention. Any environmental pressure that differentially affects the number of selfed vs. outcrossed seeds produced necessarily affects a plant's mating system.

In this study, I examined the effect that receiving pollen late in the flowering season has on the mating system of Kalmia latifolia, a long-lived perennial shrub. Electrophoretic analysis of proteins from naturally pollinated seeds shows that, although some individuals can outcross as few as 30% of their seeds, outcrossing rates average over 90% (Levri, unpublished data). A 2 x 2 experimental design was used to determine whether reproductive success declines over the course of the flowering season and whether there was an interaction between pollination time (early vs. late in the season) and pollen type (self-fertilized vs. outcrossed). I tested the interaction between time of pollination and type of pollen because this interaction would indicate context-dependent fitness of selfed seeds compared to outcrossed seeds. Relative fitness was assessed in terms of percentage inflorescence maturation, percentage fruit maturation (from flower to fruit), total number of seeds initiated per fruit, percentage seed abortion, and percentage germination of seeds.

	MATERIALS AND METHODS

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Pollinations
In the summer of 1996, 25 plants on a rocky outcrop (Bald Knob) near Mt. Lake Biological Station (in Pembroke, Virginia) were chosen and assigned to controlled pollinations. Natural pollinators were excluded from all treated inflorescences throughout the season with bridal veiling over each inflorescence. Bridal veiling fails to exclude all insect visitors, but insects small enough to penetrate veiling are considered incapable of moving pollen between flowers (Jaynes, 1988; Rathcke and Real, 1993). In order to determine the effect of timing of pollination ("early" or "late" in the flowering season) and type of pollen (selfed or outcrossed) on female reproductive success, I deposited selfed pollen on all open flowers in three inflorescences early in the season (22 June–24 June) and on another set of three inflorescences at the end of the flowering season (2 July–3 July). (Plants at this site flowered for the entire month of June in 1994 and 1995, but in 1996 they started flowering 2 wk late and still finished in the first week of July.) At the same intervals, I pollinated three other inflorescences on the same plants with outcrossed pollen (mixed from at least five plants located at least 5 m away from the plant being pollinated). Flowers in the late treatment were the same floral age as flowers in the early pollination treatment. On each plant, one inflorescence of each of the four treatments was grouped on a branch so that flowers receiving different treatments were physiologically linked. All pollinations saturated the stigma with fresh pollen from new flowers and all plants received all four treatments (early selfed, early outcrossed, late selfed, and late outcrossed) with each treatment represented by three inflorescences per plant (25 plants x 4 treatments x 3 replicates = 300 inflorescences total).

Measures of fitness
Relative fitness was assessed in terms of percentage inflorescence maturation (matured infructescences/total inflorescences treated), percentage fruit maturation (fruits matured/number of flowers), total number of seeds initiated per fruit, percentage seed abortion (aborted seeds/total initiated seeds), and percentage germination of matured seeds (germinated/sown). Early infructescence and fruit initiation were not noted, so rates of infructescence and fruit abortion are unknown. In October, I collected and counted all fruits. One fruit from each replicate of each treatment on each plant was randomly chosen and dissected to measure seed set.

Seeds were submerged in water to ascertain viability. In this system, dramatic size differences distinguish unfertilized, aborted ovules (~0.3 mm) from fertilized seeds (~0.9 mm; Jaynes, 1988). Unfertilized, aborted ovules were not counted in this study. In addition, differences in mass distinguish fertilized, aborted seeds from fertilized, matured seeds in this system. Viable K. latifolia seeds sink and aborted seeds float (Jaynes, 1988), and the numbers of sinking and floating seeds were counted. Tetrazolium dye was used to verify the accuracy of floating as an indicator of viability. Seeds were cracked open and allowed to sit in a 0.5% tetrazolium solution at 37°C for 18 h. Out of 20 floating seeds, two picked up some stain, indicating viability. Out of 20 seeds that sunk, all 20 indicated viability with tetrazolium. The floating technique was found to be a useful indicator of seed viability ( = 0.01, P < 0.93, R = 0.76, N = 40). Therefore, percentage seed abortion was calculated as the proportion of floating seeds/total seeds.

The procedure for germination followed the protocol of Jaynes (1988). Ten presumably viable (i.e., sinking) seeds from one fruit per treatment per plant were sown into a 2.5 x 2.5 cm cell containing a mix of perlite, Canadian peat, and sphagnum peat (1:2:1) and placed under intermittent mist spray in an Indiana University greenhouse in late November of 1996. Germination was monitored and recorded at 5 wk postsowing as 70% of seeds germinate under optimal conditions by that time (Jaynes, 1988). In this study, seeds were not allowed a dormant, cold period and seed germination was much lower than under optimal conditions.

Data analysis
For each measured response, I averaged replicates within a treatment on a plant to avoid pseudoreplication. All proportions (percentage inflorescence maturation, percentage fruit maturation, percentage seed abortion, and percentage germination of seeds) were arcsine square-root transformed to meet the assumption of equal variance for analyses. A mixed-model ANOVA was performed using maternal plant as a random effect and type of pollen, time of pollination, and a type-by-time interaction as fixed effects for each measured response (infructescence maturation, fruit maturation, number of seeds initiated, seed abortion, and seed germination). All analyses were performed using the JMP statistical program (SAS, 1989).

	RESULTS

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Infructescence maturation
Late-pollinated inflorescences failed to mature 16.0% more often than early-pollinated inflorescences when selfed and outcrossed treatments are combined (Fig. 1a). There was a significant effect of the identity of the maternal plant on infructescence maturation. Self-pollinated inflorescences seemed to be less likely to develop than outcrossed inflorescences, but this trend was not significant (Table 1). Also, a significant interaction between timing of pollination and type of pollen was not detected in the pattern of infructescence maturation.

View larger version (20K): [in this window] [in a new window]    Fig. 1. Effects of time of pollination and pollen type on components of plant fitness. For all graphs, x's denote outcrossed pollen, diamonds denote selfed pollen, and error bars indicate 1 SE of the mean. (a). Infructescence maturation (R = 0.46). (b). Fruit maturation (R = 0.52). (c). Seeds initiated per fruit (R = 0.41). (d). Seed abortion (R = 0.67). (e). Seed germination at 5 wk (R = 0.68).

Initiated seeds
Outcrossed flowers initiated 2.9 times more seeds per fruit than selfed flowers ( = 138.22 ± 4.29 seeds initiated/outcrossed fruit, = 52.18 ± 3.44 seeds initiated/selfed fruits). Delay in pollination significantly reduced the total number of seeds initiated by 51.7% (Fig. 1c). Although delay in pollination reduced the total number of seeds initiated in self-pollinated flowers by 71.5% and in outcrossed flowers by 40.7%, an interaction between type of pollen and time of pollination was not detected (Table 1). No effect of plant on seed initiation was detected.

Seed abortion
Seed abortion in selfed flowers was 25.2% higher than in outcrossed flowers. Late pollination did not affect seed abortion in outcrossed flowers; however, delay in pollination significantly increased seed abortion in selfed flowers by 34.7% (Fig. 1d). There was a significant interaction between type of pollen and time of pollination, and a significant effect of plant on seed abortion rates (Table 1). Outcrossed flowers matured nearly three times more seeds per fruit ( =126.2 ± 12.8) than selfed flowers ( = 44.7 ± 13.0).

Seed germination
At 5 wk postsowing, there was a significant effect of time of pollination, type of pollen, and maternal plant on germination rates (Table 1). Pollinating late in the flowering season reduced the germination of outcrossed seeds by 41.2% and selfed seeds by 54.5% (Fig. 1e); however, no interaction was detected.

	DISCUSSION

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An interaction between type of pollen and time of pollination had a significant effect on seed abortion rates. Timing of pollination did not affect abortion of outcrossed seeds; however, delay in pollination increased abortion of selfed seeds by 34.7%. The flowering season was particularly short in 1996, but even when the difference in timing in the early and late pollination treatments was only 8–10 d, a significant interaction between time of pollination and source of pollen was found. It is likely that more significant effects would be evident in years when plants flower for longer periods of time. A flower receiving a mixed pollen load early in the season may be likely to have a higher selfing rate, compared to another flower of the same age 8–11 d later in the season. Thus, time of pollination may influence a plant's mating system.

Self- vs. outcross-pollination
Researchers often find differences in seed set between controlled self- and cross-pollinations. Two main factors cause such differences: partial and/or late-acting self-incompatibility (SI) (Seavey and Bawa, 1986; Barrett, 1988; Becerra and Lloyd, 1992; Manicacci and Barrett, 1996) and early-acting inbreeding depression (Seavey and Bawa, 1986; Johnston, 1992; Husband and Schemske, 1996). The mechanism of SI in K. latifolia is almost entirely unknown. Jaynes (1968) found no evidence for S-alleles expressed in pollen tube growth in pure loads of selfed vs. outcrossed pollen. The reduction of selfed seed initiation in later flowers in this study would suggest a context-dependent expression of partial SI, except that outcrossed seed initiation also suffered (suggesting a reduction in pollen performance, see below).

The observed disproportionate increase in selfed seed abortion in late flowers suggests that either late-acting SI or early-acting inbreeding depression may be context dependent. Perhaps plants selectively abort selfed seeds rather than outcrossed seeds and this selection was more intense at the end of the season. Alternatively, early-acting inbreeding depression may be as susceptible to environmental factors, such as resource limitation late in the season, as late-acting inbreeding depression is (Dudash, 1990). Late-acting SI mediated by pollen and resource availability and/or early-acting inbreeding depression enhanced by stress may underlie patterns of seed set in K. latifolia.

Early vs. late pollinations
A number of nonexclusive mechanisms may account for the reduction in the success of late flowers compared to early flowers, including (1) limitation of resources available for seed provisioning, (2) pollen quality, (3) pistil receptivity, and (4) dichogamy (the temporal separation of male and female function).

1) As the flowering season progresses, resources available for provisioning fruit and seeds may decline in K. latifolia as they decline in other systems (Delph, 1986; Sage and Webster, 1987; Karoly, 1992). This decline in resources may drive the differences between early and late pollinations. In addition, perhaps because resources become more constrained late in the season, plants are more likely to abort selfed seeds.

Resources have also been proposed as a mechanism affecting patterns of selfed and outcrossed seed production in K. latifolia in response to another ecological factor, the fungal leaf-spot, Cercospora kalmiae. Infection damages leaf tissue and may reduce the amount of resources available for the plant to provision developing fruits (Levri and Real, 1998). Artificially damaged branches, with lowered resources, produced proportionally more outcrossed seeds, suggesting that there were insufficient resources remaining to provision selfed seeds. Healthy branches, on the other hand, could provision not only a higher number of total seeds, but also proportionally more selfed seeds. Thus, K. latifolia may provision outcrossed seeds preferentially and provision selfed seeds only if resource levels are sufficient. These resource levels may decline due to artificial removal of leaf area, natural destruction of leaf area facilitated by a fungal pathogen (Levri and Real, 1998), or the natural progress of flowering season. The results of the current study taken together with the results of the artificial manipulation of leaf area and the natural association between high disease damage and low selfing rates (Levri and Real, 1998) are consistent with the hypothesis that resource limitation can constrain a plant's mating system by limiting the production of selfed seeds more than outcrossed seeds.

2) In naturally pollinated flowers, fruits from later flowers may be more likely to fail than fruits from earlier flowers because pollen may be more limiting later in the season. Pollen quantity does not explain the pattern observed in this study as all flowers were pollinated by hand with a maximal pollen load. However, pollen quality may be implicated if later flowers were pollinated with a lower quality of pollen. Pollen performance may be influenced by maternal and paternal condition (Young and Stanton, 1990; Mutikainen and Delph, 1996), which may be influenced by time.

Even though pollen was collected from flowers of the same floral age at each interval, reduced viability of pollen later in the season may have affected the initiation of outcrossed and selfed seeds. If the number of seeds initiated influences the sink strength of an infructescence, fruit, or seed, reduced seed initiation could account for reduced inflorescence maturation, fruit maturation, seed maturation, and seed germination later in the season. However, since no interaction between time of pollination and pollen type was detected in the number of seeds initiated, I suspect that reduced pollen potency late in the season may be insufficient to explain the significant effect of an interaction between time of pollination and pollen type on seed abortion. That is, some postzygotic mechanism (such as inbreeding depression or selective abortion) may intervene so that the interaction between time of pollination and type of pollen has a significant effect on seed abortion but not seed initiation. For example, plants may be more selective and abort more seeds as resources are depleted at the end of the season.

3) Pistil receptivity, governed by resource limitation, physiological constraint, or some other factor, may be lower in later flowers than in earlier flowers. (4) In addition, the temporal division of male and female function (as in Aquilegia caerulea; Brunet, 1996) may account for the observed differences between early and late flowers. Increased pollen viability early in the season would be consistent with the observed pattern of seed initiation. In this population, K. latifolia is not completely dichogamous as flowers are capable of autogamy; however, they may be partially dichogamous and such a mechanism may help to explain the observed variation in autogamy (Rathcke and Real, 1993; Levri, unpublished data).

Conclusion
Late pollination reduced inflorescence maturation, fruit maturation, seed initiation, seed abortion, and seed germination. However, late pollination did produce some viable seeds and, most importantly, most of them were outcrossed. An apparent shift in outcrossing rate may be associated with a disproportionately high abortion rate of selfed seeds. Such selective abortion rates of flowers pollinated later in the season may contribute to a plant's overall selfing rate, but the relative importance of time of pollination compared to the influence of other factors, such as pollen limitation (Rathcke and Real, 1993; Levri, unpublished data), may be small. An examination of resource availability relative to pollen availability promises a better test of whether selective abortion based on self vs. outcrossed pollen drives the mating system in this system.

Plants that selectively abort seeds may have a higher fitness than those that randomly abort (Stephenson and Winsor, 1986; Casper, 1988). In addition, plants that can change the proportion of seeds aborted (i.e., facultative response) may have a higher fitness than plants that are constrained in the proportion of seeds they can abort (i.e., fixed response), especially for long-lived perennials.

	FOOTNOTES

 
¹ The author thanks Ed Levri and Stasia Skillman for assistance in the field and Keith Clay, Sandy Davis, Lynda Delph, Dana Dudle, Ed Levri, Paul McElhany, Helen Young, and an anonymous reviewer for critical comments on the manuscript. This work was partially funded by grants from the University of Virginia's Mt. Lake Biological Station, the Biology Department at Indiana University, and the Indiana Academy of Sciences.

Current address: Department of Biology, Seton Hill College, Greensburg, Pennsylvania 15601.

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