How environmental factors affect pollen performance: ecological and evolutionary perspectives
Lynda F. Delph
Environmental conditions, such as soil fertility and herbivory, are known to affect the ability of a plant to provision its offspring and thereby affect both the number and the size of the seeds produced by that plant (see Roach and Wulff 1987, Hendrix 1988, Marquis 1992, Stephenson 1992). Seed size, in turn, has been shown to influence speed of germination, seedling survivorship, vegetative growth rate, and reproductive output, especially under competitive conditions (e.g., Schaal 1980, Roach and Wulff 1987). In short, the growing conditions of the parent plant influence both the number and quality of its offspring and hence the fitness of the plant. As with seeds, pollen depends completely upon the sporophyte for providing the resources necessary for development. As with seeds, mature pollen grains are packed (primed) with enzymes and mRNA’s (see Stephenson et al. 1992) and they also contain energy (e.g., starches and lipids) and nutrient (e.g. phytate) storage products (see Stanley and Linskens 1974, Baker and Baker 1979, Jackson et al. 1982, Wetzel and Jensen 1992). These storage products or their precursors are secreted by the tapetal “nurse” cells of the anther during pollen development (Wang et al. 1992a, b, McCormick 1993) and, as with seeds, these products are known to be metabolized upon germination and pollen tube growth. For example, phytate is metabolized into phosphorus and myoinositol precursors that are used for cell wall and membrane synthesis (Jackson and Linskens 1982, Dickenson and Lin 1986). These storage products are thought to play important roles during the germination and the initial stages of pollen tube growth (see Vasil 1974, Mulcahy and Mulcahy 1982, Wetzel and Jensen 1992). As pollen tubes grow towards the ovules, they become increasingly dependent upon the specialized tissue surrounding the transmitting tract within the style for their sustenance (Dickinson et al. 1982, Mulcahy and Mulcahy 1982, Taylor et al. 1994, Cheung et al. 1995, Wu et al. 1995). In short, pollen, like seeds, requires resources from the parent plant to mature, germinate, and initiate growth.
Not surprisingly, a number of recent studies; have shown that environmental conditions, such as herbivory, soil fertility, and mycorrhizal infection, can affect pollen production on plants by altering flower number and/or pollen production per flower (e.g., Stephenson 1984, Stanton et al. 1987, Sacchi et al. 1988, Allison 1990, Young and Stanton 1990a, Lau and Stephenson 1993, 1994, Stephenson et al. 1994, Havens et al. 1995, Lau et al. 1995, Quesada et al. 1995). A few studies have demonstrated that environmental conditions during anther development can also affect the chemical composition of pollen (Stanley and Linskens 1974, Herpen and Linskens 1981, Herpen 1986, Lau and Stephenson 1994). For example, Cucurbita pepo pollen from plants grown in high phosphorus soils contain a greater concentration of phosphorus than pollen from C. pepo plants grown in low phosphorus soils (Lau and Stephenson 1994). Other studies have shown that pollen grain size, like seed size, may also vary with growing conditions (see Stephenson et al. 1994). Obviously, environmental conditions that reduce pollen production have the potential to negatively affect fitness through male function by decreasing the amount of pollen that is available for a plant to donate to conspecifics (e.g., Devlin et al. 1992). Moreover, it is reasonable to speculate that adverse growing conditions can also depress fitness through male function by reducing the quality (i.e. the performance) of the pollen that a plant produces, especially under conditions of pollen competition (Schlichting 1986).
Pollen performance can be measured as the growth rate of pollen tubes and the ability of pollen tubes to achieve fertilization in competition with pollen from other plants. In this regard, it is important to note that the number of pollen grains deposited onto stigmas exceeds (on at least some flowers on most plants) the number required to fertilize all of the ovules (see Stephenson et al. 1995) and that pollen from several donors is often deposited onto the same stigma (e.g., Ellstrand 1984, Meagher 1986). In this paper, we focus on the effects of environmental conditions during pollen development on pollen performance. We conclude by examining the ecological and evolutionary implications of environmental plasticity in pollen performance.
EFFECTS OF HERBIVORY ON POLLEN PERFORMANCE
Although the number of studies examining the effects of herbivory on the male function of plants is small compared to those that examine the female function, herbivory and foliar leaf damage have been shown to decrease flower number (e.g., Hendrix and Trapp 1989, Allison 1990, Mauricio et al. 1993) and to decrease pollen production per flower (Frazee and Marquis 1994, Strauss et al. 1996). However, less is known about the effects of herbivory and foliar damage on pollen performance. Here we review three studies that have investigated how leaf loss affects various aspects of pollen performance.
Cucurbita texana is an annual, monoecious vine that is native to Texas and Mexico. It is thought to be either the wild progenitor of the cultivated squashes, gourds, and pumpkins (C. pepo) or an early escape from cultivation (Decker and Wilson 1987). It is completely cross fertile with C. pepo. After a period of vegetative growth, this wild gourd produces one flower (either staminate or pistillate) in the axil of each leaf. The leaves of C. texana produce bitter compounds called cucurbitacins that deter most herbivores (Metcalf and Rhodes 1990), but cucumber beetles (Acalymma vittata and Diabrotica spp.) are adapted to ingesting cucurbitacins in the leaves of Cucurbita species. These beetles cause a characteristic pattern of holes, typically 1.0-1.5 cm in diameter, in the portion of the leaves serviced by the smallest veins.
Quesada et al. (1995) performed a study designed to simulate the timing, magnitude, and location of herbivory by cucumber beetles. They used a paper punch to remove 10 to 15% of the area of each leaf on one experimental branch of nine plants of C. texana. Another branch on the same plants served as control. They found that the partially defoliated branches produced significantly fewer staminate and pistillate flowers (i.e. more flower buds aborted during development), significantly fewer pollen grains per staminate flower, and marginally smaller pollen grains than undamaged branches on the same plants.
They then performed a similar simulated herbivory study on 20 plants of the wild gourd except this time they examined pollen performance via a pollen mixture experiment. They placed equal amounts of pollen from the partially defoliated branches and from a tester line (inbred line of C. pepo) onto stigmas of C. pepo. They also placed equal amounts of pollen from undamaged branches of C. texana and the tester line onto other stigmas of C. pepo. They found that pollen from the control (undamaged) branches was more likely to sire a seed than pollen from the damaged branches when competing against pollen from the tester line. They concluded that leaf damage not only decreased pollen production but it also adversely affected pollen performance (the ability to achieve fertilization under competitive conditions).
The effect of simulated leaf loss on pollen performance has also been studied with the bee-pollinated perennial Lobelia siphilitica (Mutikainen and Delph 1996). Observations of plants growing in a natural forest population revealed that plants just coming into flower had typically lost 50% of their leaves (L. Delph, unpublished data). This leaf loss was a result of a combination of leaf senescence and herbivory. Mutikainen and Delph (1996) simulated this leaf loss by removing the bottom one-third to one-half of the leaves of plants growing in a greenhouse, after they had bolted but well before any of the flowers were fully developed. Plants were matched by developmental stage, leaf number, and plant height with a set of control plants from the same maternal sibship. Pollen from control and experimental (partially defoliated) donors was applied separately to receptive flowers on plants from a different maternal sibship to determine if in vivo growth rates differed by treatment. Pollen tubes were subsequently stained and counted. They found that pollen tubes from control donors were longer in a significant fraction (80%) of the crosses as compared to tubes from donors whose leaves had been removed. This is the first study, we think, to directly show that leaf loss affects pollen lube growth rates in vivo. Assuming that in vivo differences in pollen tube growth rates lead to differences in fertilization under conditions of pollen competition, then leaf damage can potentially reduce the number of seeds that a plant sires.
In a similar experiment, complete defoliation of Silene vulgaris plants was found to result in a two-fold decrease in pollen tube growth rates in vitro (L. Delph, C. Weinig, and K. Sullivan, unpublished data). In addition, a set of competitive crosses directly demonstrated that pollen tube growth rate affects the ability of a pollen grain to achieve fertilization and that this ability could be affected by leaf loss. Crosses allowing pollen competition between individuals of known genotype at the phosphoglucomutase locus revealed that control fathers sired 15% more seeds than defoliated fathers.
EFFECTS OF OTHER ENVIRONMENTAL CONDITIONS DURING POLLEN DEVELOPMENT ON POLLEN PERFORMANCE
The adverse effects of leaf damage on the male function of plants is due, it appears, to reductions in the resources available for pollen production and to differences in the quantity and/or quality of the storage products within those grains that are produced. In this context, it is not surprising that other environmental stresses that adversely affect resource availability have also been shown to reduce pollen production. These stresses include soil fertility (e.g. Vasek et al. 1987, Young and Stanton 1990b, Lau and Stephenson 1993, 1994, Havens et al. 1995), mycorrhizal infection (Lau et al. 1995), and prior fruit and seed production (e.g. Vasek et al. 1987, Delph 1990, Young and Stanton 1990a, Stephenson et al. 1994, Lau et al. 1995). In addition, pollen grain size is also known to vary with resource availability during pollen development (see Stephenson et al. 1994; Lau et al. 1995). For example, C. pepo plants infected with mycorrhiza produce larger pollen grains than uninfected plants (Lau et al. 1995).
Recently, there have been a few studies that demonstrate that environmental stresses during pollen development can also affect pollen performance. For example, pollen from Raphanus raphanistrum (wild radish) plants grown under low nutrient conditions in a greenhouse sired fewer seeds than pollen from plants grown under better soil nutrient conditions when pollen of the two types of plants was applied together on stigmas (Young and Stanton 1990b). In Cucurbita pepo, pollen from plants grown in high nitrogen soils in the field was 5% larger and sired more seeds than pollen from plants grown in low nitrogen soils when equal amounts of the two types of pollen were applied together on a stigma (Lau and Stephenson 1993). Moreover, this study demonstrated that the difference in the ability to sire seeds was due to differences in pollen performance rather than differences in pollen or zygote viability. A further study using C. pepo revealed that the concentration of soil phosphorus also affected pollen performance and the ability to sire seeds in competition (Lau and Stephenson 1994). Chemical analyses of the pollen in this study also revealed that the pollen from the high P soils contained a greater concentration of phosphorus than pollen from the low P soils, perhaps indicating that soil fertility affects the chemical composition of pollen which, in turn, affects pollen performance and the ability to achieve fertilization.
The temperature during pollen development has also been shown to affect the chemical composition of pollen (see Stanley and Linskens 1974, Herpen 1986) and some aspects of pollen performance (Herpen and Linskens 1981, Kuo et al. 1981, Herpen 1986, Polito and Weinbaum 1992, Jakobsen and Martens 1994, Johannsson et al. 1994). For example, Johannsson et al. (1994) grew C. pepo, C. texana, and their F1 hybrids under cool (20 [degrees] C) and hot (30 [degrees] C) conditions in growth chambers. Pollen collected from the three types of plants growing in the cool and hot chambers was germinated in vitro and pollen tube lengths were measured. Analysis revealed significant effects of plant type and germination temperature on pollen tube growth. Moreover, the pollen tubes from the C. texana plants in the cool chamber grew longer than the pollen tubes from the plants in the hot chamber (Johannsson et al. 1994). Furthermore, results from a crossing experiment showed that plants grown in cool conditions sired more seeds than the ones that developed in hot conditions (M. Johannsson and A. Stephenson, unpublished data). This study indicates that the temperature during pollen development has the potential to influence fitness through male function.
A study that examined more realistic temperature variations (i.e. not constant) under field conditions was performed on Silene acaulis, a long-lived cushion plant that is circumpolar in the northern hemisphere, occurring in arctic and alpine tundra (L. Delph and S. Carroll, unpublished data). Soil temperature during flower development was altered by placing one-meter diameter shields of reflecting material (aluminized mylar) around S. acaulis plants, with a hole cut out for the actual cushion. These shields reflected the sunlight and lowered soil temperature in the root zone by just over 1 [degrees] C. Crosses with pollen from these plants revealed that pollen tubes from cold-stressed donors were significantly shorter than pollen tubes from nearby control donors. These results indicate that relatively cold root temperatures experienced during the time of flower maturation that are nonetheless well within the range of natural temperature variation had an effect on pollen tube growth rates.
The effects of herbivory on pollen performance are consistent with the effects of other pollen-performance studies in showing that differences in the provisioning of pollen grains during their development can affect pollen performance. If plants differ in their degree of resistance to herbivory, then these differences in resistance could also impact plant fitness. Not only would resistant plants benefit from the lack of herbivory for the more traditionally measured aspects of plant fitness (see review by Marquis 1992), our results indicate that resistant plants would also have pollen that performed better in pollen competition than that of nonresistant plants. However, before we can conclude that poor pollen performance caused by herbivory leads to a selective advantage for resistant plants, we need to know the magnitude of pollen performance effects in natural populations. Nevertheless, pollen performance is clearly a highly plastic trait, and is significantly affected by both stress and resource enhancement of the parent plant during pollen development. Moreover, natural levels of variation in the condition of the parent plant are sufficient for the observed alteration of pollen performance.
While this paper focuses only on herbivory and other environmental conditions affecting pollen during its development, pollen performance is also known to be affected by environmental conditions during germination and pollen tube growth in the style (see Mulcahy et al. 1992, Stephenson et al. 1992). For example, temperature during pollination (Elgersma et al. 1989), the location of the pollen on the stigma (Thomson 1989), the density and composition of the pollen load (Stevenson et al. 1992), and the competitive environment within the style (Cruzan 1986, 1990, Niesenbaum and Schueller, in press) have all been shown to affect either the rate of germination and/or pollen tube growth rates.
Some studies have focused on determining whether the observed variation of pollen performance within populations is heritable, in either the narrow or broad sense (Snow and Mazer 1988, Havens 1994, Quesada et al. 1996). This focus is justified given that some additive genetic variation is necessary in order for the variation in pollen performance to have evolutionary significance (Schlichting et al. 1990, Walsh and Charlesworth 1992). The results presented here indicate that much of the variation observed in pollen performance is not genetically based, but this does not rule out the possibility of a heritable component to pollen performance. For example, two studies suggest that heritable variation in pollen tube growth rates does exist. Quesada et al. (1996) selected on increased pollen tube growth rates in Cucurbita hybrids and found that this led to an increase in sporophytic vigor, indicating both an overlap in the genes affecting sporophytic vigor and pollen vigor, and heritable variation in these traits. Working with Hibiscus moscheutos, Snow and Spira (1997) showed that pollen tube growth rates of this plant, which grows in marshes of varying salinity, was not affected by exposure to salinities ranging from 0 to 10 g/kg or by application of fertilizer. These results, in combination with another study showing that there is substantial variation among donors in pollen performance and that donor rank does not vary among different recipients (Snow and Spira 1991), suggest that some of the variation is genetically based.
If pollen performance is related to fitness, then why has selection not eliminated variation in performance? For example, if the difference in siring ability seen in the S. vulgaris defoliation experiment had been a highly heritable one, rather than environmentally induced, the difference in siring would correspond with a selection coefficient of 0.27. We discuss ways in which genetic variation in traits affecting pollen performance can be maintained, and relate this question back to the highly plastic nature of pollen performance.
Interactions at the among-population scale. – If populations that differed in some way also differed in terms of which pollen genotypes achieved the highest fitness, then this could lead to genetically based variation in pollen performance within populations. If gene flow is limited among the populations, and antagonistic pleiotropy did not constrain simultaneous adaptation to the different environments, then different genotypes would be favored by selection in the different populations, leading to population-level differentiation in fitness traits (e.g., Rausher 1984, Shaw 1986). Genetic variation in fitness traits could occasionally occur within populations, depending on the balance of selection against alternate genotypes from other populations and the level of migration between populations. Similarly, high gene flow from a population where pollen petition does not occur (i.e., pollen of relatively low performance has the same access to ovules as pollen of high performance because excess pollen is not normally delivered) to one where it does, would result in a mixture of low and high performance genotypes within a population.
Alternatively, if antagonistic pleiotropy does constrain selection for adaptation in the different environments and gene flow between populations via pollen is high, then genotype-environment interactions might exist, and the ability of selection to discriminate among genotypes would be limited. In other words, genotypes achieving high fitness in one population would achieve relatively low fitness in other populations, and this trade-off would lead to the maintenance of genetic variation within populations. In the past, pollen dispersal was thought to be so highly restricted (e.g., Levin and Kerster 1974, Handel 1983) that little gene flow occurred among populations. However, more recently, gene flow via pollen from outside of populations has been shown to be greater than previously thought, by both paternity-analysis studies (Ellstrand and Marshall 1985, Broyles and Wyatt 1990, Godt and Hamrick 1993) and studies of population genetic structure based on both organelle and nuclear genes (McCauley 1994).
Interactions within populations. – Negative genetic correlations between pollen performance and other stages in the life cycle would also maintain genetic variation (Walsh and Charlesworth 1992). Walsh and Charlesworth (1992) suggest that this would result in a negative correlation between pollen vigor and progeny vigor, but this is not necessarily the case. It is also possible that a trade-off could exist between something other than the growth rate of the progeny. For example, pollen vigor may be affected by the allocation of nutrients to the pollen grains by the maternal plant, as discussed in this paper. According to sex allocation theory, greater allocation to male function might come at a cost to female function (Charnov 1982). If so, and if this allocation had a genetic basis, then a negative genetic correlation might exist between allocation to the androecium and the gynoecium of flowers. Hence, a relatively good pollen donor would be a relatively poor seed parent. Preliminary evidence for such a tradeoff exists for Hibiscus moscheutos: significant negative phenotypic correlations were found at the within-flower level for allocation of both nitrogen and phosphorus to the androecium and gynoecium (Fundyga 1996). If the phenotypic correlations are caused by underlying genetic correlations and there is a relationship between nutrient content and fitness, then genetic variation would be maintained by this allocation trade-off.
Of course, a mutation during meiosis in any of the approximately 23 000 different genes expressed by pollen during meiosis would introduce genetic variation into each generation. Moreover, because plants lack a germ line, a mutation in any somatic cell that eventually leads to a pollen mother cell would be represented in 50% of the pollen grains produced by that cell lineage (see Schlichting et al. 1990). Apparently, mutation alone can account for the maintenance of some variation in pollen tube growth rates in natural populations (Charlesworth and Charlesworth 1992).
The high degree of phenotypic plasticity in pollen performance unveiled by our studies and others, points to a novel mechanism for maintaining genetic variation that does not involve genetic correlations with other fitness traits or for differentiation among populations. Rather, it takes the form of genotype-environment interactions on a fine scale within populations. We have shown that environmental variation in the form of herbivory, soil nutrient level, and soil temperature during pollen development affects pollen performance. Furthermore, the degree of variation in environmental conditions needed to result in substantial variation in pollen performance occurs within populations. For example, a 10% difference in leaf loss to herbivores or a 1 [degree] C soil temperature differential were sufficient for significantly altering pollen performance, and these ranges in leaf loss and temperature are commonly found within populations.
Plasticity in pollen performance, in and of itself, would not be sufficient to prevent the loss of genetic variation, although conceivably it could slow the process. However, if genotypes respond differently to environmental variation in terms of pollen performance (i.e., variation exists among genotypes in the degree of phenotypic plasticity), then this could actually promote the maintenance of genetic variation in pollen performance [ILLUSTRATION FOR FIGURE 1 OMITTED]. Genotype-environment interactions might come about if the pollen performance of some genotypes is more buffered against environmental perturbation, such as herbivory, than others. In other words, while pollen of one donor may exhibit the fastest rate of growth when grown under benign conditions, different genotypes may respond differently to negative conditions, leading to a shift in donor rank. As long as a single genotype is not the most fit in all environments, such genotype-environment interactions will promote the maintenance of genetic variation within populations (Gillespie and Turelli 1989, Rawson and Hilbish 1991).
Our studies point to the potential for an additional mechanism maintaining genetic variation, but we do not know if there are genotype-environment interactions in pollen performance in natural populations. There are, however, several studies using cultivated species that indicate that such interactions may be important (see Stephenson et al. 1992). For example, Zamir et al. (1981) applied equal amounts of pollen from a cool tolerant wild tomato and a warm tolerant cultivar onto the stigmas of the cultivar. When the pollen was deposited under cool conditions, the wild tomato pollen fertilized more of the seeds than when the mixture: was deposited under warm conditions, indicating that genotype-environment interactions can influence pollen performance, at least under artificial circumstances.
In order to determine whether genotype-environment interactions are responsible for maintaining variation in natural populations, experiments need to be performed that incorporate a range of pollen donors and environmental conditions, such that crossing reaction norms can be found if they exist. Moreover, the idea that some genotypes may be more buffered than others raises the additional question of whether the ability to buffer pollen performance against environmental heterogeneity comes with a cost, such as not being the fastest in some environments. Additional work is needed before we can understand the evolutionary significance of variation in pollen performance. However, the high degree of plasticity in pollen performance, in response to factors that affect the ability of the maternal plant to provision pollen, does not detract from the potential for this significance; rather it adds a new dimension to the balance between selection and variation within populations.
This research was supported by NSF grants DEB-9319002 to L. E Delph and BSR-9109270 and DEB-9318224 to A. G. Stephenson, and a Marsden Fund grant (LLO501) to L. Delph. Many thanks to S. Strauss and S. Armbruster for inviting us to be a part of the symposium on herbivory and pollination, and to them and O. Pellmyr for comments on an earlier draft. Thanks also to J. Villinski for sharing an idea.
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