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Reproductive Biology |
Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131 USA
Received for publication March 20, 2003. Accepted for publication June 20, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Brassicaceae • maternal stress • nonrandom mating • pollen competition • pollen load size • Raphanus sativus • wild radish
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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, 1996
; Quesada et al., 1996
; Ashman, 2002
; Barrett, 2002
). Although there has been a great deal of study in this field, many issues related to plant mating systems remain unresolved (Charlesworth et al., 1987
; Lyons et al., 1989
; Marshall and Folsom, 1991
; Grant, 1995
). This is in part because of the complexity of plant mating systems. Nonrandom mating can occur between self and nonself pollen, among compatible donors, among too closely or too distantly related conspecifics, and among species (Marshall and Folsom, 1991
; Mitchell and Marshall, 1998
).
Historically, the major foci for study of plant mating have been understanding physiological self-incompatibility (e.g., de Nettancourt, 1997
) and estimating of amounts of inbreeding and its consequences (e.g., Holsinger, 1991
; McCall et al., 1994
; Barrett and Cruzan, 1996
) because these are important events with major implications for plant fitness. More recently, it has been recognized that nonrandom mating among compatible mates might also be of significance (e.g., Marshall and Folsom, 1991
; Marshall, 1998
; Mitchell and Marshall, 1998
). Differential pollen donor success at this level is particularly intriguing because it clearly affects pollen donor fitness and has the potential to result in nonrandom mating through pollen competition or mate choice (Mulcahy, 1974
; Charnov, 1979
; Willson, 1979
, 1982
, 1990
; Queller, 1983
, 1987
; Stephenson and Bertin, 1983
; Willson and Burley, 1983
; Snow, 1990
, 1991
; Andersson, 1994
; Waser et al., 1987
).
For example, previous studies with wild radish have shown that whenever a mixture of pollen from two or more compatible donors is applied to stigmas, mating is nonrandom (Marshall and Ellstrand, 1988
; Marshall, 1991
, 1998
; Marshall and Fuller, 1994
; Marshall et al., 2000
; Marshall and Diggle, 2001
), suggesting that, at least in wild radish, differences in mating success among pollen donors are relatively common. In fact, the differences in pollen donor success are often quite large, with the most successful pollen donor siring more than twice as many seeds as the least successful donor. In addition, some of these studies indicate that the nonrandom mating in wild radish is truly differential mating success of compatible donors and not a subtle effect of the incompatibility system (Marshall, 1998
). However, whether these studies can be generalized to field conditions has been questioned, particularly because, in our initial studies, the sizes of pollen loads applied to stigmas were much larger than those typically found in the field.
Pollen load size is an important consideration because it may affect the opportunity for nonrandom mating (Mitchell, 1997a
, b
; Delph and Havens, 1998
). At very low levels of pollen availability, all pollen donors may have equal success because virtually all pollen grains can fertilize ovules. Once a threshold of pollen grain number is reached, not all pollen grains will fertilize ovules and mating may become nonrandom. Finally, at very high pollen loads, we might see no differences in mating patterns because the stigma is already saturated with pollen. If pollen loads in the field are normally quite low, below a threshold for nonrandom mating, and pollen loads in experiments are always above this threshold, results from greenhouse experiments might not be informative.
Mating patterns in field populations might also be affected by maternal condition. In our previous studies, when the maternal tissue is under stress, pollen donors may sire more equal numbers of seeds (Marshall and Ellstrand, 1988
; Marshall and Fuller, 1994
; Marshall and Diggle, 2001
). Thus, changes in plant condition in the field might obscure results found in the greenhouse.
Alteration of both maternal condition and pollen availability would provide a range of conditions under which nonrandom mating is increasingly less likely. For example, when pollen is not limited and maternal condition is good, there should be substantial opportunity for nonrandom mating (Ter-Avanesian, 1978
; Snow, 1990
, 1991
; Bjorkman et al., 1995
; Niesenbaum, 1999
; Marshall et al., 2000
). Alternatively, when pollen is limited and the maternal condition is poor, the opportunity for nonrandom mating is greatly reduced. However, to our knowledge no studies that vary both pollen availability and maternal condition exist.
Therefore, we chose to examine pollen donor performance under varying pollen availability and maternal conditions in Raphanus sativus. This organism is excellent for this because (1) nonrandom mating is known to occur (Marshall and Ellstrand, 1986
, 1988
; Marshall, 1991
, 1998
), (2) maternal condition is known to affect seed paternity (Marshall and Ellstrand, 1988
; Marshall and Fuller, 1994
; Marshall and Diggle, 2001
), and (3) a previous study of pollen availability and paternity showed that seed paternity was unchanged across a range of pollen load sizes (Marshall et al., 2000
).
Here we broadened the range of pollen load sizes used to include smaller pollen load sizes than used in the previous study. In addition, we altered maternal condition by changing water availability. We measured pollen donor performance under these conditions to ask the following questions: (1) Are the smallest pollen loads so small that not all ovules produce seeds? If so, the opportunity for nonrandom mating could be substantially reduced. (2) Does seed siring success vary with pollen availability? If so, (3) was the stress treatment strong enough such that altering maternal condition has an effect on seed siring success? If so, environmental variability in the field may alter plant mating patterns. (4) Was there an interaction between pollen load size and maternal condition that affects seed siring success? If so, some field conditions may severely limit the opportunity for nonrandom mating.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Stanton, 1987
; Stanton and Preston, 1988
).
Wild radish has several characteristics that facilitated our study. The plant has abundant flowers, so many crosses are possible. The fruits are multi-seeded, so a reduction in the number of seeds may be an indication of pollen donor success. Ovule number averages 6–10 per ovary. In the greenhouse, with large pollen loads seed set is very close to ovule number. The plants exhibit sporophytic self-incompatibility (Hinata and Nishio, 1980
; Pundir et al., 1983
), preventing complication of seed paternity by selfing. Seeds weigh on average 10 mg and can be genotyped without germination. Wild radish has high levels of isozyme polymorphism, making scoring paternity of seeds possible (Ellstrand, 1984
; Ellstrand and Marshall, 1986
; Devlin and Ellstrand, 1990
).
Enough is known about reproduction in the field to interpret our experimental pollinations. Pollen load size varies and multiple paternity of seeds within a fruit is known to occur (Ellstrand, 1984
; Ellstrand and Marshall, 1986
; Ashman et al., 1993
). Multiple paternity is likely the result of mixed pollen loads rather than the sequential deposition of pollen from different donors (Marshall and Ellstrand, 1985
). Thus, mixing pollen and varying pollen load size in greenhouse plants is likely representative of pollination events in the field.
Experimental design
Plant selection
Ninety seeds (two seeds each from 45 different plants) were planted. The two siblings will hereafter be called a family. The seeds came from two field sites in California. We chose families that were likely to include a substantial number of different S-alleles to ensure compatibility among pollen donors and pollen recipients and to reduce the possibility of using plants that were too closely related (see Karron et al., 1990
). Previous studies show that progeny from plants in these sites set as much seed from between-site as from within-site crosses (Marshall and Ellstrand, 1988
). Seeds were soaked in gibberellic acid (40 mg/100 mL) for 1 h and then were then planted in a 4 : 1 : 1 sand : peatmoss : perlite mixture in 3.79 L pots with two seeds per pot. The plants were watered 1–3 times daily until the stress treatment was started and fertilized twice weekly with Peter's 20 : 20 : 20 fertilizer (Scotts Company, Marysville, Ohio, USA) and once per week with micronutrients (Minor L, Albuquerque Chemical Company). Once the plants had their first true leaves they were thinned to one plant per pot.
Crosses were performed to assess the compatibility among the 45 families. Of these, 30 families were widely compatible with one another. From these 30 compatible families, four maternal families were selected based upon their general health, phosphoglucose isomerase (PGI) phenotype and flower morphology. We chose maternal plants that were easy to emasculate. From the remaining 26 families, three plants were chosen as pollen donors based on pollen viability of >95%, PGI phenotype, and compatibility with all maternal plants. Pollen viability was scored by collecting three representative pollen samples per potential donor and staining with Alexander's stain (Alexander, 1980
). Two hundred pollen grains per sample were counted and viability was then determined per sample and per potential donor.
So that each of the pollen donors could be used in mixed pollen loads, three additional pollen donors were chosen, one to pair with each of the earlier donors (Fig. 1). The three additional donors were grown from additional families known to be homozygous for a rare allele of PGI. None of the original pollen donors had the rare PGI allele, nor did any of the plants chosen to be maternal plants. The three additional donors were fully compatible with all of the maternal families. Using the six donors (three from the original 45 lineages and three with the rare PGI allele), we designated three pollen donor pairs. Each pair had one pollen donor that was homozygous for the rare PGI allele and one pollen donor that did not contain that allele. Thus, paternity of seeds from mixed pollinations was always distinguishable using the PGI phenotype.
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), and a pair of forceps wrapped in a tissue for the large load. Each cross was replicated five times. Prior to pollination, each maternal flower was emasculated with forceps.
To ensure that pollen load sizes were consistent over time, test stigmas were checked after every replicate of pollinations. This was done by performing either an emasculation alone or a pollination in the manner described earlier, then snipping the stigma off the maternal plant and staining with Alexander's stain (Alexander, 1980
). We then counted the amount of pollen on the stigmatic surface. Five test counts for each load size were made after each replicate of pollinations.
To account for differences in pollen number per flower among plants, three buds were collected from the paternal plants three times throughout the course of the experiment (prior to pollinations, after completion of the second replicate, and after completion of the fifth replicate). The buds were dried in microcentrifuge tubes for 2 wk then rehydrated with 500 µL of ethanol and one drop of Tween 80 (Fisher Scientific, Fair Lawn, New Jersey, USA). This solution was then added to 20 mL of 2% saline, sonicated, and the number of pollen grains per flower was scored using an Elzone model 280pc particle counter (Particle Data, Elmhurst, Illinois, USA). Four 1-mL readings were taken for each flower. The mean of these four readings was used in the analyses described next.
Stress treatments
To impose water stress, water was reduced for one plant from each maternal family for 1 wk prior to the start of pollinations and then throughout the course of the experiment. The other plant in that family was treated as a control, watered under normal conditions in the greenhouse environment. The low-water sibling received 450 mL water two times per day per 3.79-L pot, and the control sibling received 900 mL water two times per day per 3.79-L pot. The water-stressed plants visibly wilted daily and the control plants did not. These treatments mimic those used in three other experiments with wild radish (Marshall and Ellstrand, 1988
; Marshall and Fuller, 1994
; Marshall and Diggle, 2001
). In all of these cases, the treatments were sufficient to affect reproductive traits. All plants received 450 mL of fertilizer solution twice weekly.
Order of crosses
To minimize potential effects of maternal age, the order in which crosses were performed was carefully controlled. First, each of the five replicates consisted of three pollen load sizes for each of the three donor pairs. For each maternal plant, a random order of the three pollen donor pairs was produced. Once a pollen donor was designated, the large, medium, and small pollinations were performed for that pair before using the next donor pair in the random order. Different random orders were used for each replicate for each maternal plant. All pollinations for one replicate on a maternal plant were completed before the next replicate began. The duration of a replicate across all maternal plants was at most 8 d and all five of the replicates were completed in 47 d. A total of 360 pollinations was performed (four maternal families x two water treatments (stress and control) x three pollen donor pairs x three pollen load size treatments x five replicates) (see Fig. 1).
Data collection
Ten days after pollination, the fruits were scored as either aborted or developing. At maturity, the fruits were collected and number of seeds per fruit, seed position within fruits, and seed mass to the nearest 0.01 mg were recorded. The PGI phenotype was then scored for each seed (>1500) by starch gel electrophoresis (Ellstrand, 1984
) and seed paternity was assigned.
Data analysis
We performed an analysis of variance to determine whether the three pollen load sizes were distinct (PROC GLM, SAS Institute, 2000
). Pollen grains per stigma was the dependent variable and pollen load size was the independent variable. Additionally, we performed a one-tailed t test to determine whether the small pollen load size used in this study was distinct from the small pollen load used in a previous study of wild radish.
To address whether or not there were significant differences in pollen production among donors that might affect the percentage of seeds sired, we performed an analysis of variance (PROC GLM, SAS Institute, 2000
). The individual donor was the independent variable and pollen production per flower was the dependent variable. We analyzed each pollen donor pair separately.
To test whether mean seed mass, good seeds per fruit, and total seed mass per fruit were influenced by pollen load size and maternal stress, we performed ANOVAs (PROC GLM, SAS Institute, 2000
) using each of the three measurements of female reproductive fitness as dependent variables and maternal family, pollen donor pair, pollen load size, stress treatment, and their interactions as independent variables. In this and subsequent analyses, all variables were treated as fixed. While we considered treating maternal family as a random effect, we could not do so as our maternal families were not selected at random. They were chosen based upon health, flower morphology, compatibility with other plants, and PGI phenotype. Thus, our conclusions must be confined to the set of plants that were studied.
We compared the outcomes of pollination with different pollen loads using chi-square tests and with logistic regression. We first asked whether the frequencies of aborted and full fruits were different among pollen load sizes and stress treatments. Then we used a logistic regression to consider jointly the effects of maternal family, pollen load size, stress treatment, and their interactions. However, two of the maternal families had only 5–6% overall fruit abortion and could not be used in the logistic regression because they added too many empty cells in the model. Consequently, we used the remaining two families, which averaged about 20% fruit abortion.
We compared seed paternity across donors and treatments in two ways. First, chi-square tests were used to address whether the two donors in each pair sired equal numbers of seeds. We tested the observed frequencies of seed paternity against two expectations: an expectation that each donor in a pair had equal seed paternity and an expectation that the frequencies of seeds sired were equal to the relative amounts of pollen produced per flower. Second, we performed logistic regressions for each pollen donor pair to test whether frequency of seeds sired was affected by maternal family, pollen load size, stress treatment, and the interaction of pollen load size and stress treatment. Inclusion of the additional two-way interactions or the three-way interaction made the model unstable, so they were removed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) (t = 2.16, P < 0.02, one-tailed). Mean pollen production per flower was statistically indistinguishable among the members of each pollen donor pair (Table 1).
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), we first asked whether our results indicated the presence of a threshold. The number of good (mature and fully filled) seeds per fruit was significantly lower for the small pollen load than for the large or medium pollen loads (Table 2). This suggests that at the small pollen load size, there was insufficient pollen for full seed set. Therefore, we considered that a threshold in pollen availability occurred between the small and medium pollen load sizes, with nonrandom mating being less likely for the small pollen load where not all seeds were filled. As a result, we lumped the pollen loads into two categories in the remaining analyses: small and large. The large pollen load size is a combination of the medium and the large pollen load treatments, while the small pollen load size is composed solely of the small pollen load treatment. In figures, we continue to show all three pollen load sizes so that the possibility of a threshold effect can be examined further.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Marshall, 1991
; Marshall, 1998
) and other species (Mitchell and Marshall, 1998
), compatible pollen donors vary in seed siring success, supporting the hypothesis that pollen competition and mate choice can be important in plants. However, because greenhouse conditions may lack important sources of variability for field plants, questions remain about the interpretation of patterns of nonrandom mating seen only in the greenhouse. Therefore, to consider the range of conditions under which nonrandom mating might operate, we varied maternal condition and pollen availability and examined differences in seed siring success among pollen donors.
First, we asked whether we could produce pollen loads that were small enough to reduce the opportunity for nonrandom mating because insufficient variation in pollen load size would make the results difficult to interpret (Mitchell, 1997a
). The number of good seeds per fruit was significantly reduced in our smallest pollen load, suggesting that not all ovules were fertilized and that the potential for nonrandom mating was diminished. The smallest pollen load, 25.7 grains per stigma, was also smaller than we had achieved in a previous study (Marshall et al., 2000
). There were also significantly more aborted fruits at the small pollen load size than at the larger pollen load sizes (Fig. 2, Table 3). This pattern of fruit abortion suggests that abortion was selective based on seed quality or quantity per fruit (Stephenson and Winsor, 1986
; Winsor et al., 1987
; Stephenson et al., 1988
).
Second, we asked how a change in pollen availability would affect the proportion of seeds sired by pollen donors. Number of seeds sired became more similar at the small pollen load size for donors in pairs 2 and 3 (Fig. 3). This pattern was statistically significant (Table 6), supporting our prediction that reduction in pollen load size reduces opportunities for nonrandom mating. In contrast, in a previous study of wild radish, seed siring success was invariant across pollen load sizes (Marshall et al., 2000
). However, the smallest pollen load size in that study was significantly greater than the smallest pollen load here (44.2 ± 36.5 vs. 25.7 ± 10.8 pollen grains per stigma). Perhaps our smallest pollen load in this experiment crossed a threshold for which the opportunity for nonrandom mating was significantly reduced.
One explanation for the presence of this threshold may be changes in opportunity for pollen competition and mate choice. When pollen is abundant, offspring fitness is often increased; when pollen is limited, offspring fitness may decrease (Davis et al., 1987
; Winsor et al., 1987
; Stephenson et al., 1988
; Bjorkman, 1995
; Johannsson and Stephenson, 1997
; Niesenbaum, 1999
). However, not all studies of pollen load size showed a reduction in offspring growth when pollen load size was reduced (Ter-Avanesian, 1978
; Snow, 1990
, 1991
; Mitchell, 1997a
, b
; Németh and Smith-Huerta, 2003
). Perhaps these were cases in which the threshold was not crossed. However, in some of these studies, pollen grain number was sufficiently low to reduce seed set per fruit (e.g., Németh and Smith-Huerta, 2003
).
Third, we asked whether maternal stress affects the pattern of mating. The watering regime did not increase fruit abortion (Table 3), but it did reduce seed mass (Table 7). Maternal stress also significantly altered the mating pattern for pair 2; mating performance diverged more under stress (Fig. 5a). Interestingly, this is opposite of the effect of maternal stress in two previous studies of wild radish (Marshall and Fuller, 1994
; Marshall and Diggle, 2001
). In those studies, there was less discrimination among pollen donors when maternal plants were under stress (Marshall and Fuller, 1994
; Marshall and Diggle, 2001
).
One explanation for this difference in pollen donor performance may have to do with the timing of the stress treatment. In an earlier study of wild radish, maternal plants that were stressed early tended to show high fruit abortion and seed paternity was closer to random than in control fruits (Marshall and Ellstrand, 1988
). However, when maternal plants exposed to stress later in the life cycle, they were more likely to abort individual embryos within a given fruit and seed paternity became more distinct among donors (Marshall and Ellstrand, 1988
). For this experiment, stress was initiated just before pollination and continued throughout the experiment. The number of mature seeds per fruit was not reduced by stress, but fruit set was reduced. Perhaps the abortion of some fruits affected the mating pattern.
Finally, we asked whether pollen availability and maternal condition interacted to change the mating pattern. For pollen donor pair 1, there was a significant interaction effect of maternal stress and pollen load size on mating pattern (Table 6). Overall, seed paternity was indistinguishable among the two donors; however, examination of seed paternity across stress treatments and pollen load sizes revealed a fascinating pattern. The rank order of pollen donor performance reversed between the medium and small pollen load sizes for the control and stress treatments (Fig. 5a). The most successful donor at the large pollen load size was the least successful in the small pollen load size.
Overall results of this and a previous study (Marshall et al., 2000
) show that above 40 pollen grains per stigma, mating patterns were consistent across pollen load sizes. However, for the plants studied here, mating patterns became more random at a smaller pollen load size of about 26 grains per stigma. Thus, for very small pollen load sizes in the field, there may be little opportunity for nonrandom mating. For wild radish, for which mean pollen load size in the field can be above 90 grains per stigma (Ashman et al., 1993
), those very small pollen load sizes might not be common. Finally, our most intriguing observation was that, for one pollen donor pair, rank order of pollen donor performance reversed with a change in pollen load size and maternal condition. Although we found this for only one specific pair of pollen donors, it is interesting to speculate that this kind of condition-dependent variation in mating performance might help maintain variation in pollen donor ability in field populations. Thus, particular plants might fare better under specific mating conditions just as they might grow better under particular environmental conditions.
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FOOTNOTES |
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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