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Tropical Biology |
2Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de Mexico, A. P. 21, San Patricio, Jalisco, Mexico 48980; and 3Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica
Received for publication July 25, 2000. Accepted for publication April 27, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Bombacaceae • Pachira quinata • paternity • pollen competition • pollen–pistil interactions • self-incompatibility • tropical dry forest
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Delph and Havens, 1998
; Winsor, Peretz, and Stephenson, 2000
). The size of the pollen load deposited onto a stigma may affect the number and size of seeds produced per fruit (Winsor, Davis, and Stephenson, 1987
; Stephenson, Devlin, and Horton, 1988
; Quesada, Winsor, and Stephenson, 1993
), the probability of seed and fruit abortion (Bawa and Webb, 1984
; Stephenson and Winsor, 1986
; Casper, 1988
; Lee, 1988
; Nakamura, 1988
; Niesenbaum and Casper, 1994
; Niesenbaum, 1999
), and the quality of the progeny produced (Mulcahy and Mulcahy, 1975
; McKenna and Mulcahy, 1983
; Ottaviano et al., 1988
; Richardson and Stephenson, 1992
; Quesada, Winsor, and Stephenson, 1993, 1996a, b
; Johannsson and Stephenson, 1997
; Winsor, Peretz, and Stephenson, 2000
; but see Snow, 1990
; Mitchell, 1997
).
The genetic composition of the pollen load is also known to affect the number and size of seeds produced per fruit. For example, when mixtures of self and cross pollen are deposited onto a stigma, the self pollen is less likely to achieve fertilization in species with cryptic, partial, or complete self-incompatibility systems (Bertin and Sullivan, 1988
; Lloyd, 1992
; Plitmann, 1993
; Cruzan and Barret, 1996
; Levin, 1996
; Stephenson, Good, and Vogler, 2000
). This may lead to reduced seed production if there is insufficient cross pollen to fertilize all of the ovules. In self-compatible species, self-fertilization and other forms of inbreeding are known to result in higher levels of seed abortion and/or smaller seeds, due to homozygosity of rare lethal and defective alleles (e.g., Darwin, 1876
; Charlesworth and Charlesworth, 1987
; Husband and Schemske, 1995
; Bosch and Waser, 1999
). Late-acting self-incompatibility (Seavey and Bawa, 1986
) and other forms of self-incompatibility (Bertin and Sullivan, 1988
; Becerra and Lloyd, 1992
) can also lead to reduced seed production following self-fertilization. Reduced seed production per fruit, in turn, adversely affects the probability of fruit maturation by reducing the sink strength of the developing fruit relative to developing fruits with a full complement of seeds (see Stephenson et al., 1995
).
Only a few studies have evaluated the implications of natural variation of pollen load size on the reproduction of plants and these have been mostly limited to herbaceous species of temperate regions (Cruzan, Neal, and Wilson, 1988
; Stephenson et al., 1995
; Delph and Havens, 1998
; Winsor, Peretz, and Stephenson, 2000
). In this study we evaluate the relationship between the number of microgametophytes per pistil, the incompatibility system, and the number of sires with respect to the production of fruits and seeds in a natural population of the tropical tree Pachira quinata. We specifically address the following questions: (1) What is the relationship between the amount of microgametophytes per pistil and the production of fruits and seeds under natural conditions? (2) What is the breeding system of Pachira quinata, based on experimental crosses and genetic analysis? (3) Is fruit set affected by the breeding system? (4) What is the relationship between the breeding system and the genetic relatedness of the progeny from the flowers that set fruit under natural conditions?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Study species
Pachira quinata (Bombacaceae) (Jacq.) Alverson [= Bombacopsis quinatum (Jacq. Dugand)] (Alverson, 1994
) is a Neotropical species that is distributed in the dry forest from Honduras to northern South America. It is an important timber species that has been heavily exploited because of its durable and resistant wood. Pachira quinata trees may grow up to 35 m in height and 2.5 m in diameter under natural conditions. Trees normally have big buttresses at the base, a gray, thorny bark, and a deep central root system. Leaves are digitate compound, with glabrous, oblong leaflets. Pachira quinata is deciduous: leaf drop occurs in late November and new leaves are produced in early May. The flowering period extends from January to March, immediately followed by the fruiting period, from April through May. Flowers are hermaphroditic, and protandrous, with multistaminate white filaments and a single central style. Anthesis takes place at 1900 and flowers last for one night. Flowers are pollinated by bats (Glossophaga soricina) and sphingid moths. Fruits are dehiscent, dry, and woody. Each ovary contains an average of 160 ovules and fruits mature an average of 20 seeds, which are small and wind dispersed. Pachira quinata has been classified as a self-incompatible species based on hand pollination experiments (Kane et al., 1993
).
Natural variation of pollen load size and fruit and seed production
Nine adult P. quinata trees were selected based on accessibility to flowers. To estimate the relationship between pollen load size on fruit and seed production, a sample of flowers from each tree was marked and followed until fruit maturation for the entire reproductive period of 1998. A total of 630 flowers, equally distributed on the nine trees sampled, were marked and followed to fruit maturation. Approximately 14 flowers were marked daily during 45 consecutive days from February to mid-March. Flowers were marked during the flowering peak of trees in the population to insure that the flowers most likely to be pollinated were sampled. To determine the flowering peak of the population, we followed the flowering phenology of 40 trees by counting the number of flowers produced by each individual daily during the entire reproductive season. Flower styles were excised 48 h after anthesis. Preliminary results showed that pollen tubes grow from the stigma to the ovary in <24 h. Therefore, even if flowers were pollinated at sunrise, the pollen tubes had sufficient time to grow into the ovary. Mature fruits produced by marked flowers were collected and seeds from each fruit were extracted and counted. Flower stigmas and fruits were collected using 4- to 9-m ladders.
All the styles from flowers that initiated fruits and later aborted and from flowers that developed into fruits were observed under the microscope. For each style, pollen grains and tubes were counted under a UV microscope (Zeiss, Germany) using Martin's (1959)
aniline blue technique. A subsample of ten flowers that did not develop into fruits (16% of the total sample) were randomly selected from each tree and observed under the microscope. Pollen grains and tubes were counted using the same technique described above. A logistic regression (LOGISTIC; SAS, 1995
) was used to determine the effect of pollen load size on fruit set. The number of pollen grains per stigma and the number of pollen tubes per style were used as the independent variables. Fruit set was used as the response variable with the following levels: (1) flowers that successfully developed into fruit, (2) flowers that initiated fruit development but aborted, and (3) flowers that did not develop into fruit. A regression analysis (REG; SAS, 1995
) was performed to determine the relationship between the number of seeds produced per fruit and the number of pollen grains found on stigmas. A square root transformation was used for seed number.
To assure that the style excision technique described above did not affect natural fruit set, we compared the overall fruit set of 17 unmanipulated trees with the fruit set of the 9 trees with sampled flowers (pollen load experiment). Total flower and fruit production was recorded for these 17 unmanipulated trees for 60 consecutive days.
To determine the relationship between the number and size of seeds from fruits produced from naturally pollinated flowers, we collected a sample of ten fruits from 20 trees in the same population as above. Seeds from each mature fruit were counted and classified as either aborted or potentially viable; aborted seeds are usually wrinkled, hollowed, and black, whereas potentially viable seeds are well rounded and brown. We selected a sample of five potentially viable seeds per fruit and each seed was individually weighed. Aborted seeds were excluded. A regression analysis (REG; SAS, 1995
) was conducted to determine the relationship between the number of seeds produced per fruit and seed mass.
Breeding system and number of sires
To determine the incompatibility system of P. quinata, 90 hand pollinations were performed on nine trees. Outcrossed flowers were obtained by artificially pollinating 45 pristine flowers using pollen from at least five different donors. Similarly, a total of 45 pristine flowers were self-pollinated using pollen from the same tree. An equal number of outcross and self-pollinations were performed on each tree. Flowers were marked and covered before anthesis with mosquito net bags to prevent pollinator visitation. Both self- and outcross pollen were collected in plastic cups 1 h after anthesis. Hand pollinations were performed by gently saturating the stigma with pollen (>500 pollen grains per stigma) using a soft paintbrush. Each marked flower was followed until fruit maturation.
To compare the performance of self- and outcross microgametophytes of P. quinata, a time series experiment was conducted to determine pollen tube growth rate of both types of pollen (GLM; SAS, 1995
). A total of 36 flowers from three trees were hand pollinated. Eighteen flowers were self-pollinated and 18 received pollen from at least four different donors. Six styles (two per tree) from both self- and outcross flower styles were excised at 2, 4, and 8 h after pollination. All styles were stained and observed under the UV microscope (Martin, 1959
). Pollen tubes were counted in four different regions of each style: the region near the stigma (region 1), the middle region of the style near the stigma (region 2), the middle region of the style near the base of the ovary (region 3), and the region at the base of the style near the ovary (region 4). A repeated measures two-way ANOVA (analysis of variance) was used to compare the pollen tube growth rate of outcross vs. self-pollen (GLM; SAS, 1995
). This model considered treatment (outcross vs. self-pollen tubes) and time intervals of style excision after pollination (2, 4, and 8 h) as the main effects of the analysis and region within each style (1–4) as the repeated factor. Region was used as the repeated factor because pollen tube counts were not independent of each other within the same style.
As an independent test to determine the breeding system of P. quinata, we conducted an allozyme genetic analysis using enzyme gel electrophoresis. We collected 20 fruits from each of 15 adult trees and randomly selected and genotyped four seeds from each fruit. Seeds were germinated in individual petri dishes. Enzymes were extracted from homogenized hypocotile tissue obtained 5 d after seed germination using extraction buffers, gel buffers, and staining protocols followed by Soltis and Soltis (1989)
procedures. Six polymorphic enzyme systems were analyzed: leucine aminopeptidase (LAP, EC 3.4.11.1), shikimate dehydrogenase (SKDH, EC 1.1.1.25), phosphoglucoisomerase (PGI, EC 5.3.1.9), aspartate aminotransferase (AAT, EC 2.6.1.1.), esterase (EST, EC 3.1.1.1.), and alcohol dehydrogenase (ADH, EC 1.1.1.1). The PGI enzyme system showed two polymorphic loci; therefore, seven polymorphic loci were used to determine the selfing rate and genetic relatedness within P. quinata progenies.
Two genetic parameters were calculated for the progeny produced by trees: an estimated multilocus outbreeding rate (tm) and paternity correlation (rp) within and between fruits (i.e., probability of full-sib progeny of seeds within and between fruits). These parameters were calculated using the genetic models proposed by Ritland (1989)
and the MLTR (multilocus mating system program) computer program (Ritland, 1996
). Standard errors were calculated using the method of bootstrapping with 1000 repetitions (Ritland, 1996
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 13.73; df = 1; P < 0.0002), the number of pollen tubes at the top of styles (Wald 2 = 12.99; df = 1; P < 0.0003), and at the base of styles (Wald 2 = 12.83; df = 1; P < 0.0003) (Fig. 1). There is a significant positive relationship between the number of pollen grains deposited onto a flower's stigma and the square root of the number of seeds produced in mature fruits (Fig. 2). There is also a significant positive relationship between the number of seeds per fruit and seed size (Fig. 3).
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= 0.6279; F = 2.445; df = 6,56; P < 0.03). The mean number of pollen tubes is significantly greater at 8 h in region 1 than at 2 h in the other regions of the style (LSMEANS [least square means]; GLM; SAS, 1995
) (Fig. 4). There are significantly more pollen tubes in the region near the stigma (region 1) than the middle regions of the style (regions 2 and 3), and significantly more in the middle regions than at the base of the style near the ovary (region 4).
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states that the paternity correlation is inversely related to the number of outcross parents (n), where rp = 1/n. A paternity correlation value of 1 indicates that the progeny are full-sibs and a value of 0 indicates that the progeny do not share sires. These results indicate that P. quinata is predominantly an outcrossing species. In general, the proportion of full-sib progeny was greater within fruits than between fruits. Seeds within fruits are sired by one or two donors (Table 1). The probability of common paternity is significantly greater within fruits than between fruits. The mean correlation of paternity (rp = 0.252, SE = 0.0814) shows that the genetic diversity within trees of P. quinata could be explained by three to five sires with equal contribution to the pollen pool.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Stephenson, 1981
; Sutherland and Delph, 1984
; Lee, 1988
; Stephenson et al., 1995
). The size of the pollen load deposited onto the stigma of flowers is an important factor in the production of fruit and seeds in P. quinata. The only flowers that successfully developed fruit received a mean load of 422 pollen grains (2.6 : 1 pollen grain : ovule) and an average of 23 pollen grains were deposited for each mature seed. Flowers that received <200 pollen grains on the stigma did not develop a fruit or aborted. In P. quinata, about half of the pollen grains transferred to a flower stigma germinated and developed pollen tubes to the base of the style. Only the flowers that set fruit received a sufficient number of microgametophytes at the base of the style to fertilize all the ovules in an ovary (Fig. 1). However, in these fruits only a mean of 14% of the ovules matured into seeds. One possible explanation for this result is that all the ovules are fertilized but only a few develop to maturity due to the limited resources of the maternal plant. Our study indicates that the number of seeds per fruit increases with the size of the pollen load (Fig. 2) and that seed mass increases with seed number (Fig. 3). Apparently, most fruits produced under natural conditions do not reach the maximum number and size of seeds a fruit of P. quinata could potentially produce. These results suggest that flowers that set fruit are primarily affected by the number of microgametophytes in the pistil, rather than the amount of resources provided by the plant. An alternative explanation is that pollen tube attrition occurs at the base of the style or at the ovary and fruit maturation occurs only after a large number of compatible microgametophytes achieve fertilization. Our results indicate that as the number of compatible microgametophytes increases, seed set increases (Fig. 2).
Few studies have established a direct quantitative relationship between the microgametophyte load (i.e., both pollen grains and tubes) received by a flower style and the production of fruit and seed under natural conditions. A review of the literature shows that most studies have analyzed this phenomenon by either establishing a relationship between the number of pollen grains deposited onto a flower's stigma and the number of ovules in the ovary (Snow and Roubik, 1987
; Uma Shaanker and Ganeshaiah, 1990
) or by establishing a relationship between the number of pollen grains (but not pollen tubes) deposited on a flower's stigma with respect to the production of fruits and seeds (Ornduff, 1971
; Bertin, 1982
; Snow, 1982, 1986
; Casper, 1983
; McDade, 1983
; McDade and Dadivar, 1984
; Galen, Zimmer, and Newport, 1987
; Snow and Roubik, 1987
; Spira et al., 1992
; Winsor, Peretz, and Stephenson, 2000
; but see Mulcahy, Curtis, and Snow, 1983
; Levin, 1990
; Niesenbaum and Casper, 1994
). In partially self-compatible or incompatible plants, it is difficult to interpret the significance of the size of the pollen load deposited under natural conditions by measuring only the number of pollen grains present on a stigma. In many tropical trees with self-incompatibility, including several species in the family Bombacaceae (Bawa, 1979
; Hamrick and Murawski, 1990
; Murawski et al., 1990
; Murawski and Hamrick, 1992
; Baum, 1995
), the incompatibility reaction occurs at the base of the flower style or at the ovary. The results of the hand pollination experiments and the genetic analysis (Table 1; Fig. 4), revealed that this population of P. quinata is predominantly outcrossing (tm = 0.918, SE = 0.0514), but that both self- and outcross pollen tubes can grow through flower styles. Therefore, the interaction of compatible and incompatible microgametophytes can potentially affect the performance of compatible pollen and its ability to sire seeds in P. quinata. Pollen–pollen and pollen–pistil interactions have been reported to affect pollen performance and the siring success of donors, due to factors associated with the maternal sporophyte and the microgametophyte (Cruzan, 1990
; Schlichting et al., 1990
; Quesada et al., 1991
; Mulcahy, Mulcahy, and Searcy, 1992
; Plitman, 1993
; Cruzan and Barrett, 1996
). Although our study could not detect the frequency in which self- or cross microgametophytes occur in the pistils, it is possible that the flowers that never set fruit are the result of mainly self-pollinations. In contrast, in the flowers that set fruit, both incompatible and compatible microgametophytes could have been found in similar proportions in the pistils but the cross-compatible pollen outcompeted the self-pollen, successfully siring seeds in the fruits that developed to maturity. An alternative explanation is that the pollen tube growth of compatible pollen is in fact not affected or even facilitated by incompatible pollen tubes. Flowers that set fruit received similar loads of compatible and incompatible pollen but the incompatible tubes were arrested at the base of the style without affecting the performance of cross-compatible microgametophytes. It is also possible that because our hand pollinations (Fig. 4) tested the performance of self- and cross microgametophytes separately, when mixed together only cross-pollen tubes grow through the style. However, this type of pollen–pollen interaction is rare, and it has not been reported for other Bombacaceous trees (Sukhada and Jayachandra, 1981
; Baum, 1995
). Even so, it is not clear whether the competitive ability of compatible pollen or pollen tube attrition (or both) are important mechanisms operating in the pistils of P. quinata; the only fruits that developed to maturity are the result of pollinations performed with large cross-compatible pollen loads.
The identity of pollen grains contained in naturally deposited pollen loads may also affect the probability of fruit development. Our study indicates that in P. quinata, seeds within fruits are sired mainly by one or two cross-compatible donors and that the total seed crop within trees is sired by three to five cross-compatible donors (Table 1). Outcross single-sired fruits are expected when pollinators deliver pollen to a flower stigma after previously visiting one pollen donor or when pollinators deliver pollen from many donors but only one donor successfully sires seeds. Because the P. quinata individuals sampled produced an average of 60 flowers per day (SE = 9.86) throughout the reproductive season, it is possible that the main pollinators, the long-tongued bat (Glossophaga soricina) and sphingid moths, visited and collected pollen from many flowers on one tree or only a few trees each night. It has been documented for some plant species that feeding rates of G. soricina may be as high as 1000 visits/h to a single plant and that individual bats showed feeding fidelity to individual plants over their flowering season (Lemke, 1984
). Glossophaga soricina may fly up to 2 km between foraging sties (Fleming, Hooper, and Wilson, 1972
) and sphingid moths up to several kilometers (Miller, 1981
; Haber and Frankie, 1989
); therefore, they have the capacity to move pollen relatively long distances and promote outcrossing (Heithaus, Fleming, and Opler, 1975
). However, if resources are abundant within a few individuals of P. quinata during peak flowering season, it might not be necessary for pollinators to visit many trees in one night, which could explain the relatively low number of sires we observed in the genetic analysis.
In conclusion, our study demonstrates, using natural pollinations rather than controlled hand crosses, that fruit and seed production in natural populations of P. quinata are directly related to size of the pollen load and that only a few cross-pollen donors sire seeds within fruits. Future studies on natural plant populations need to determine if the variation of microgametophyte performance is associated to the competitive ability of sires. These studies should also determine how pollen dispersal (via pollinator activity) and pollen–pistil interactions affect the ability of donors to sire seeds.
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FOOTNOTES |
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4 Author for reprint requests (mquesada{at}ibiologia.unam.mx
).
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= 0.682 + 0.00029(pollen grains); r2 = 0.34; P < 0.05]
