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Reproductive Biology |
Department of Botany, University of Guelph, Guelph, Ontario, Canada N1G 2W1
Received for publication November 24, 2003. Accepted for publication April 29, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: female function • geitonogamy • male function • pollen discounting • pollen limitation
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; van Groenendael and de Kroon, 1990
). One consequence of clonal reproduction is that genetically identical individuals (ramets, Harper, 1977
; see Watson and Casper, 1984
; Callaghan et al., 1992
, for different definitions) become spatially clustered as the clone (genet) grows (Hutchings and Mogie, 1990
; Chung and Epperson, 1999
). Although such spatial structuring can increase both pollen and ovule production per genet, it can also have negative implications for both female and male function (Darwin, 1876
; Handel, 1985
; Charpentier, 2001
), due to the transfer of pollen between ramets within the same clone (e.g., geitonogamy and pollen discounting; Lloyd and Schoen, 1992
; de Jong et al., 1993
; Harder and Barrett, 1995
).
In self-compatible species, geitonogamous pollination in clones will cause a high rate of self-fertilization. As a result, seed and fruit production (female function) may be reduced through the effects of inbreeding depression (Charlesworth and Charlesworth, 1987
; Husband and Schemske, 1996
). Within-clone pollination may also affect paternal success by removing, from pollinators, pollen that would otherwise have been exported to stigmas of a different genet (= pollen discounting; Harder and Thomson, 1989
; Lloyd and Schoen, 1992
; Holsinger and Thomson, 1994
). As a result, reproductive success may not increase in proportion to clone size because paternal and maternal fitness per ramet is reduced.
Although self-incompatible (SI) species avoid selfing and thus the consequences of inbreeding depression, the effects of clonality and geitonogamy may still be significant in such species. Visits to peripheral ramets in a clone may remove pollen from incoming pollinators, creating pollen limitation for central ramets. Furthermore, peripheral ramets may also remove pollen from outgoing pollinators, causing pollen discounting and reduced paternal success of central ramets. Geitonogamy can be substantial in clonal species (e.g., Barrett et al., 1994
; LeClerc-Potvin and Ritland, 1994
; Back et al., 1996
; Eckert et al., 2000
; Reusch, 2001
). However, the relationship between clone size and geitonogamy is poorly understood. Furthermore, the influence of clone size on paternal function and pollen discounting has rarely been considered.
In this study, we investigated the effect of clone size on reproductive success in apples (Malus x domestica). Although it is a cultivated plant and clonal only in a horticultural setting, data from crops and orchards have been useful in the past for testing hypotheses applicable to natural populations (e.g., Handel, 1985
; Schoen and Stewart, 1986
). The domestic apple, in particular, provides several advantages germane to this study: (1) Varieties are SI, so that fruit is only produced from pollen transfer between varieties (Waite, 1899
; Free, 1993
). (2) Each tree of a variety is a ramet of the same genet and therefore genetically identical (genet level analysis; Eriksson, 1993
). (3) Varieties are often structured into single-variety clones, or blocks, of different sizes. (4) Previous work has developed diagnostic, genetic markers for many apple varieties for use in paternity estimation (Kron et al., 2001a
, b
).
Our research had three main objectives. (1) In simulations, estimate the theoretical effects of clone size on paternal siring success in neighboring clones and the potential for pollen limitation within clones. (2) Empirically determine the effect of clone size on outcross siring success in seeds of neighboring varieties (paternal reproductive success). (3) Empirically determine the effect of clone size on fruit and seed production (maternal reproductive success).
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) generated from the average of four separate dispersal curves, two of which were based on the "Idared" variety. This curve shows that a given pollen donor row sires 56% (SE ± 8) of seeds in the first adjacent row and declines to 8% (±2) by the seventh adjacent row. Because this curve was constructed for distances from one to seven rows within an orchard, all of our simulations are within this range. From this curve, we used two pieces of information: the proportion of ovules sired by a target row in a recipient row i rows away (
i) and its associated standard deviation (
i). We treated each siring-success estimate as a proxy for the amount of pollen exported. Consequently the proportion of a row's exported pollen (
i) that reached the ith recipient row was calculated as: 
i plus a normally distributed, random error term with a mean of zero and standard deviation of i. Then the percentage of pollen contributed from a clone of block size n was calculated as: 
The expected impact of clone size on pollen receipt was simulated in a manner analogous to the paternity simulations. Each recipient row in a given block was partitioned in half and pollen was imported from trees in the nearest seven rows (x = 1–7) on either side of the recipient row. For each row of a block, the ratio of compatible to incompatible pollen was calculated as:
Field sites
The qualitative predictions of the simulations were tested quantitatively at four commercial apple orchards in southern Ontario, Canada: Dwarf Tree; Eramosa; Farmer Jack's; and Versteigh (Table 1). At 900 trees/ ha, these orchards are classified as medium to high density (Wilson, 1990
). Trees are grafted to dwarf rootstock and arranged in rows (4.8–4.9 m between rows, 1.8–2.3 m between trees within rows), which are oriented north/south in all orchards. Each row in the study area comprises a single apple variety (genotype). While orchards contain from 11 to 17 different varieties, a given variety is often grown in adjacent rows, producing blocks of genetically identical trees.
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, b
) have provided genetic profiles of many different varieties of apple and have shown that the paternity of the Idared variety can be determined unambiguously. To measure reproductive success, 17 blocks of Idared trees were chosen from the four orchards with sizes ranging from one to five rows. Each row consisted of a minimum of 50 trees. Adjacent to each of these blocks was a row of trees of a variety other than Idared from which the paternal success of the blocks was estimated. Based on the availability of orchards, complete replication of all block sizes at each orchard was not possible (Table 1). Nevertheless, three different block sizes were replicated three times in the Farmer Jack's orchard. Consequently, in our statistical analyses, we analyzed all orchards combined and Farmer Jack's orchard alone to account for any confounding effects between block size and orchard. Maternal reproductive success was estimated for trees sampled within each block. The criteria for selecting a block were (1) it contained only Idared trees; (2) it was isolated from other Idared blocks by at least 15 rows; and (3) the adjacent row was a variety compatible with Idared with overlapping flowering time.
Sampling of fruit for paternal success
For each Idared block, two trees, one-third and two-thirds down the row immediately adjacent to the block, were chosen for sampling. A previous study (Kron et al., 2001b
) suggested that the variance in paternal contributions to trees in a row is low; thus, two recipient trees are sufficient to estimate the mean paternal siring success of a block. Paternal success was evaluated in a single row adjacent to the Idared block, rather than multiple rows. We chose this sampling strategy because we wished to test for an effect of clone size on mean siring success and had no a priori reason to expect the distribution of siring success among adjacent rows to change. Whenever possible, the row selected was on the east side of the block. For five blocks (two at Versteigh and three at Farmer Jack's), the selected row was on the west side. Eight apples were randomly chosen from each side of the trees (for a total of 16 per tree, 32 per row). Apples were selected by dividing the tree visually into quarters, selecting four evenly distributed branches in each quarter, and selecting one apple from each branch by counting in from the tip a random number of apples.
Sampling of fruit for maternal success
To estimate maternal success, we selected five trees evenly spaced along each row in each block. One branch was selected from each side of each tree and a segment containing approximately four trusses (cluster of 5–6 flowers) was marked. Between 14 and 18 May 2002, the number of trusses and flowers in the marked segments of each branch were counted. The number of developing fruit was counted in these segments at two intervals during the season. The first census, 24 and 30 May, was before natural and chemical thinning could affect fruit set. The second was at harvest, 14 and 15 August. Maternal success was then estimated by fruit set, calculated as the number of fruit produced divided by the number of flowers originally present on a branch, and seed set, calculated as the number of seeds harvested per apple averaged across apples within a branch. When no apples were produced on the marked branch, the nearest fruit to the marked area was collected and the seeds counted to provide a seed number measure for that branch. Each of these branch values was then averaged across all branches within a row for use in the statistical analyses.
Analysis of paternal success
Thirty seeds were randomly sampled from the 16 apples per tree (two seeds per fruit) in the rows adjacent to blocks, and these seeds were screened for Idared paternity. Paternity was estimated from isozyme profiles using cellulose-acetate-gel electrophoresis (Hebert and Beaton, 1989
). The seed coat was removed and the embryo and cotyledons were ground in 50 µL of "Decodon" extraction buffer (Eckert and Barrett, 1994
) after freezing in liquid nitrogen. The resulting homogenate was centrifuged for 10 min at 14 820 x g and the supernatant applied to the gel.
Gels were run for 45–60 min at 250 V and stained for acid phosphatase (
-ACP, EC 3.1.3.2.) and glutamic-oxaloacetic transaminase (GOT, EC 2.6.1.1.). Idared paternity was assigned to a seed if it possessed the "slow" GOT and "fast" -ACP alleles. Idared is homozygous for both of these alleles, while most other varieties do not have both alleles (Kron et al., 2001a
). The exception to this pattern is "Mutsu," which bears the "slow" GOT allele. Consequently, paternity of Mutsu fruit was assigned on the basis of -ACP alone. In these cases, none of the varieties, other than Idared, carried the "fast" -ACP allele within 23 rows of the target row. The percentage Idared paternity was then calculated for each tree as the number of Idared-sired seeds per 30 seeds per tree and then averaged across the two trees in a row to give a paternal-success estimate for each block.
We tested the effect of clone size on paternal success with an ANOVA of block size on percentage Idared paternity (all statistical analyses were performed using R software, R Development Core Team, 2003
). Orchard was included as a random effect and block size, nested within orchard, was a fixed effect. Under the hypothesis of no pollen discounting, each additional row in a block should contribute a proportional increase in siring success (i.e., a constant marginal gain; squares in Fig. 1). Conversely, as derived from the Monte-Carlo simulations described earlier, a decreasing marginal gain, and thus the absence of a monotonic increase, in siring success with block size is consistent with the effects of pollen discounting. Because the theoretical expectations are based on pollen dispersal across a random assortment of compatible varieties, any deviations from the shape of this null model represents an effect of the spatial structuring of varieties into blocks. If a clone has significantly higher siring success than expected at certain block sizes, it may be due to a tendency for pollen to exit a block more frequently than an equally sized set of multi-variety rows. Conversely, reduced siring success may be the result of a tendency for pollen to remain within a block. As described earlier, to eliminate any possibility of confounding effects of orchard, we also examined paternal success in Farmer Jack's orchard alone.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In the simulations of pollen import, the mean compatible/ incompatible pollen ratio declined as block size increased (Fig. 2). In addition to this effect of whole block size, within five row blocks the proportion of compatible pollen declined from peripheral to central rows (Fig. 3).
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10%. An ANOVA based on Farmer Jack's alone also found no significant effect of block size (F2,6 = 0.295, P > 0.75).
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1 seed. The separate analysis of Farmer Jack's also showed no significant effect of block size on either fruit or seed set (F2,31 = 1.79, P > 0.15 and F2,33 = 0.27, P > 0.75). Mean seed set, as depicted in Fig. 5, appears to decline in a step fashion with clone size; however, most of this variation was attributable to orchard effects.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Paternal success
If an increase in clone size (i.e., flower number) increases total pollen export, then we would expect to see a significant increase in male reproductive success in apples with increasing clone size. However, we detected no significant effect of block size on siring success. We consider three potential explanations for this lack of effect. First, if pollen discounting counteracts the increase in pollen production of large blocks, siring success would not increase with clone size (Fig. 1). This within-block pollen movement may be due to the tendency for pollinators to remain within single-variety blocks. The primary pollinators of apples, honeybees, and bumble bees often exhibit floral constancy (reviewed in Chittka et al., 1999
; Gegear and Laverty, 2001
) in which they sequentially visit one floral type while ignoring nearby alternatives. Second, we may simply have not had sufficient statistical power to detect changes in siring success. However, based on the observed within- and between-block variances, we should be able to detect siring success changes of 10%. The no-discounting model presented in Fig. 1 suggests that much larger increases in siring success should occur over our range of block sizes. Third, the range of block sizes used may have been insufficient to cause an increase in siring success. We cannot rule out this possibility entirely. However, our simulations suggest that this is not likely. Furthermore, from the biological perspective, if a greater than five-fold increase in flower production is required to accrue male fitness benefits such an effect would be relatively unimportant in the field.
To our knowledge, only one other study has investigated the influence of clonal growth on pollen export (Handel, 1985
). In this study, a cotyledon trait was used to track the siring success of a central genet of cultivated cucumber (Cucumis sativus) into surrounding genets. As the growing season progressed, the number of flowers per plant, area occupied per plant, and pollinator density increased. Handel (1985)
found that the average distance pollen traveled from the central genet decreased from 4.12 to 3.37 m between early- and late-season fruits. This reduction was attributed to increased within-genet pollen movement associated with the increase in clone size. In contrast, our study used replicate clone sizes and much larger variation in clone size to test for an effect of pollen dispersal. Moreover, the power of our experimental design was sufficient to detect a smaller magnitude of effect than the 18% reported by Handel (1985)
. In another study, Schoen and Stewart (1986)
estimated the influence of cone production on paternal success in the clonal, wind-pollinated white spruce. Although they found significant linear and quadratic increases in paternal success with increasing cone number, the ramets of genets were randomly arranged within seed orchards. The lack of evidence for pollen discounting in this study is not surprising because spatial structure of ramets contributes to within-clone pollinations.
Maternal success
Our simulations indicated that the proportions of incompatible pollen received by ramets in a block should increase, while compatible pollen will decrease with block size. If pollinator activity is limited, ramets within large blocks may experience reduced fruit and seed set due to pollen limitation. Further, the prevalence of incompatible pollen could trigger an SI reaction that disrupts the growth of compatible pollen tubes or ovule and fruit development. In fact, several studies have shown that SI species experience a substantial reduction in seed set when cross-pollination is preceded or accompanied by self-pollination (e.g., Ockendon and Currah, 1977
; Waser and Price, 1991
; Kellerhals and Wirther-Christinet, 1996
, but see Visser, 1984
).
In apple orchards, blocks of just two rows may receive up to 20% incompatible pollen. This value is likely to be an underestimate as it does not include contributions from ramets within the same row nor from geitonogamous pollinations among flowers within ramets. Unfortunately, we do not have sufficient information to quantitatively infer the impact of changes in the ratio of compatible to incompatible pollen on fruit set and maternal fitness. However, we detected no significant effect of block size or position within a block on fruit or seed set. These findings at least suggest that the amount of incompatible pollen present in large blocks was not sufficient to impair maternal success and pollinator activity was sufficiently high to prevent pollen limitation. Alternatively, our blocks may have been too small to detect an effect on maternal success. In our largest blocks (five rows), all trees are at most three rows from a compatible donor. The lack of a block effect on fruit set may reflect in part the effects of domestication on maternal function. If maternal traits such as large fruit size have been selectively favored, fruit set may be resource limited under a wide range of pollination conditions. As a result, the effects of block size, which should alter the quantity of compatible pollen, may be reduced in this species compared to non-domesticated species. Indeed, several studies of wild species have reported a negative relationship between genet size and seed set in self-incompatible species (e.g., Silander, 1985
; Eriksson and Bremer, 1993
; Free, 1993
). For example, seed set was reduced in the largest genet in a population of Linnaea borealis (Wilcock and Jennings, 1999
), and rare ramets of Calystegia collina were more likely to set seed than common genets (Wolf et al., 2000
). However, without information on male function, it is not clear what the relative sensitivities of male and female function are in these species.
Implications for the evolution of clonality
Variation in clonal growth form, exemplified by phalanx (dense clustering of ramets) and guerrilla (low density, wide ranging) types, are often interpreted as alternate foraging behaviors to maximize occupancy or discovery of resources (Sutherland and Stillmann, 1988
; Schmid, 1990
). Because of the differences in spatial clustering of ramets, these variants may also differ in the likelihood of geitonogamy and pollen discounting. Clonal organisms with a phalanx growth form are likely to experience frequent pollen flow among ramets within a genet, thus enhancing opportunities for pollen discounting. On the other hand, the guerrilla growth form has less spatial structure and therefore may experience less geitonogamy and smaller impacts of clone size on paternal function (Handel, 1985
). In ecological conditions that favor sexual reproduction (Bierzychudek, 1987
), selection may favor the guerrilla form over phalanx or the evolution of secondary modifications to floral display that can minimize the rates of geitonogamy, particularly in phalanx species. Ultimately, however, the growth form favored by selection will depend on the trade-off between the resource benefits of clonal growth and the costs to sexual reproduction (Reusch, 2001
).
Although domestic apples are not actually clonal, they are cultivated in orchards in a way that resembles a phalanx growth form. The effects of clone size on paternal function in this study are consistent with strong pollen discounting, which is expected with this growth form. What is less clear is the extent to which these data may also apply to other phalanx species. Because apples are not naturally clonal, they may lack some of the secondary modifications in allocation of resources and floral form that most phalanx species have. On the other hand, this may highlight an important advantage to using such a species, because we can separate the effects of discounting from other allocation adjustments that occur with increasing clone size in clonal organisms.
Implications for orchard design
Apple growers usually arrange their orchards in blocks of varieties to improve the efficiency of harvesting and variety-specific maintenance. However, this study and others (Kron et al., 2001a
, b
) demonstrate that the mating consequences of such clustering can be important. This is certainly true with respect to reduced pollen availability and maternal success; while we found no significant effects of block size on maternal success in blocks of up to five rows, several studies have observed reduced fruit set in the center of large blocks (Free and Spencer-Booth, 1964
; Maggs et al., 1971
; DeGrandi-Hoffman et al., 1984
; Milutinovic et al., 1995
). For apple growers, the effect of block size on paternal success may be less obvious, although growers recognize the importance of pollen transfer among varieties and invest heavily in the services of bees during the bloom to accomplish this. Our research suggests that increasing block sizes significantly reduces the contribution that each row makes as a pollen donor. As demonstrated by the nonsignificant change in siring success with block size, any further increase in block size has little benefit, as most of the additional pollen produced is deposited on flowers within the block. Any pollen that fails to reach a compatible recipient can have a substantial economic cost in terms of wasted effort of bees, which are often hired as colonies for the flowering period. This cost of large block size to effective pollen donation argues strongly for reduced block size and frequent interplantings of pollenizers such as crabapples in commercial orchards.
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FOOTNOTES |
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2 Current address: Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada T2N 1N4 (routley{at}ucalgary.ca
)
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