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Reproductive Biology |
Department of Biological Sciences and Behavioural Ecology Research Group, 8888 University Drive, Simon Fraser University, Burnaby, British Columbia V5A 1S6 Canada
Received for publication August 14, 2003. Accepted for publication February 13, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: Collinsia parviflora • flower size • mating system • pollen : ovule ratios • pollen size • Scrophulariaceae • sex allocation • trade-off
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Charnov, 1982
). For outcrossing plants, allocation to primary male characters should increase in response to competition for the fertilization of ovules. Competition for pollinator visits can also lead to increased allocation of resources to secondary attractive structures (e.g., the corolla) in entomophilous species. Conversely, for highly selfing plants, local mate competition should act to reduce resources allocated to the production of pollen for which ovules are unavailable. This predicted covariation of sex allocation with the mating system (the latter estimated in different ways) has been demonstrated in several studies that compared multiple hermaphroditic species (Cruden, 1977
; Thomas and Murray, 1981
; Cruden and Lyon, 1985
; McKone, 1987
; Ritland and Ritland, 1989
; Cruden, 2000
), but rarely within a single species that shows among-population variation in the selfing rate (e.g., Schoen, 1982
; Ramsey, 1993
).
Sex allocation theory for simultaneous hermaphrodites assumes that trade-offs between male and female functions are ubiquitous, yet trade-offs have been notoriously difficult to demonstrate. Primary sex allocation trade-offs have been shown in some studies (Bawa and Webb, 1983
; Mazer et al., 1999
; Sarkissian and Harder, 2001
), but other results are ambiguous. For example, Mazer and Hultgård (1993)
found correlations between primary male and primary female allocation in only two of the four Primula species studied. In one species, pollen grain volume (but not number) was negatively correlated with ovule number, while in another species, pollen number (but not volume) was positively correlated with ovule number. Many other studies have failed to detect trade-offs between primary allocation to the two sexes (Carr and Fenster, 1994
; Damgaard and Loeschcke, 1994
; Mossop et al., 1994
; Ågren and Schemske, 1995
; Delesalle and Mazer, 1995
; Mazer and Delesalle, 1996
; Campbell, 1997
; Elle, 1998
; Parra-Tabla and Bullock, 2000
; Mazer and Dawson, 2001
). Trade-offs within a primary sexual function are also possible; gamete size–number trade-offs have been documented for pollen (Vonhof and Harder, 1995
; Harder, 1998
), but to our knowledge ovule size–number trade-offs have not been examined, though seed and fruit size–number trade-offs have been well documented (e.g., Sakai and Sakai, 1995
; Leishman, 2001
).
Trade-offs may also be expressed between primary and secondary sexual characteristics and/or among secondary sexual characteristics. Secondary male traits include the attractive corolla and pollinator rewards (e.g., nectar), which are considered to contribute more to male fitness than female fitness because increased pollinator visitation should increase pollen export, whereas relatively few visits may be required to fertilize all available ovules (Bell, 1985
). Trade-offs between primary and secondary male allocation have been found between androecium mass (primary) and petal mass (secondary) in Ipomoea wolcottiana Rose (Parra-Tabla and Bullock, 2000
) and between stamen number (primary) and nectar production (secondary) in Muntingia calabura L. in wet, though not in dry, areas (Bawa and Webb, 1983
). Secondary female traits include seeds, fruit, and any structures that protect the developing fruit, such as the calyx (Grant, 1950
; Ritland and Ritland, 1989
; Delph et al., 1996
). Trade-offs between primary and secondary female allocation have rarely been studied. Significant correlations were found between gynoecium and sepal mass in I. wolcottiana, but correlations differed in direction in two years of study (Parra-Tabla and Bullock, 2000
). A correlation analysis we performed on data in Table 3 of Ritland and Ritland (1989)
indicated pistil and calyx mass were positively correlated across eight species of Mimulus. Evidence for between-sex trade-offs include those documented between pollen (primary male allocation) and seed (secondary female) production in Gladiolus spp. (Rameau and Gouyon, 1991
) and Thymus vulgaris L. (Atlan et al., 1992
), between tassel mass and seed yield in Zea mays L. (Garnier et al., 1993
), between stamen production and fruit production in Astilbe biternata (Vent.) Britton (Olson and Antonovics, 2000
), and between corolla size (secondary male) and ovule number (primary female) in Primula stricta Hornem. (Mazer and Hultgård, 1993
). A trade-off between secondary male and female allocation was found between petal mass and sepal mass in I. wolcottiana (Parra-Tabla and Bullock, 2000
). However, the ability of researchers to detect trade-offs appears to depend greatly on environmental conditions. Galen (2000)
found a trade-off between corolla size and fruit production only in Polemonium viscosum Nutt. plants that survived drought conditions, but watered plants or those that did not survive drought exhibited positive or no correlations between the same variables. In four years of study on Ipomopsis aggregata (Pursh) V. Grant, Campbell (1992)
found a negative correlation between pistil mass and corolla size one year, a positive correlation one year, and no correlations the other two years. Elle (1999)
found a trade-off between pistil length and corolla diameter in only one of five experimental plots in Solanum carolinense L. and positive genetic correlations among the sizes of pistils, anthers, and corollas measured under controlled conditions (Elle, 1998
). Many other studies have also documented positive correlations between corolla size and primary male (Stanton and Preston, 1988
; Campbell, 1992
, 1997
; Damgaard and Loeschcke, 1994
) and/or female allocation (Damgaard and Loeschcke, 1994
; Delesalle and Mazer, 1995
; Mazer and Delesalle, 1996
; Campbell, 1997
).
Positive correlations for allocation to different sex functions within hermaphroditic individuals suggest that the assumption of trade-offs, a cornerstone of sex allocation theory, is false. However, there are many explanations for why trade-offs are difficult to detect, including ambiguity in dividing any flower into male and female parts (Goldman and Willson, 1986
), choice of an appropriate allocation currency (Abrahamson and Caswell, 1982
; Goldman and Willson, 1986
), differential genetic variation at different levels in the hierarchy of resource allocation (de Laguerie et al., 1991
), and variability among individuals in resource acquisition ability (van Noordwijk and de Jong, 1986
). Environmental factors may influence the expression of floral traits (e.g., Elle and Hare, 2002
), also making it difficult to detect trade-offs among them. The environment, variation in acquisition ability, and the sequential nature of allocation are all likely to inflate correlations toward positive values, which can be dealt with experimentally (by taking measurements in a controlled environment and maximizing variability by studying species where allocation strategies differ among populations; de Laguerie et al., 1991
) and statistically (by controlling for resource status; van Noordwijk and de Jong, 1986
).
Collinsia parviflora Dougl. ex Lindl. (Scrophulariaceae, sensu lato) populations in British Columbia, Canada, differ in two secondary sexual characteristics: corolla size (in the field [Elle and Carney, 2003
], and growth chamber [Elle, 2004
]) and nectar production (in the growth chamber [E. Elle, unpublished data]). Under pollinator-free conditions, among-population correlations between corolla size and the autonomous selfing rate were negative (Elle, 2004
). In experimental arrays of plants with different-sized corollas, pollinators were rarely observed visiting plants with small corollas, and emasculated flowers on plants with small corollas set few or no seeds. In contrast, pollinators frequently visited plants with large corollas, which had full seed set even when emasculated (Elle and Carney, 2003
). Thus, in C. parviflora, variation in corolla size is expected to be a good indicator of the capacity for outcrossing, as in other members of the tribe Collinsieae (Armbruster et al., 2002
), but it is unclear how primary sex allocation covaries with secondary allocation to corollas and whether this species exhibits assumed allocation trade-offs within and between the sexes.
We measured allocation to primary (pollen grain number and size, androecium mass, ovule number, and gynoecium mass) and secondary (linear corolla size measurements and corolla and calyx mass) floral characters to determine whether C. parviflora populations with larger corollas (secondary male allocation) differ in secondary female allocation, primary male allocation, or primary female allocation, and whether there is evidence of sex allocation trade-offs within and/or among populations.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Unlike elsewhere in the range of this species, populations in British Columbia are tetraploid and differ significantly from one another in corolla size (Ganders and Krause, 1986
; Elle and Carney, 2003
), leading to some taxonomic uncertainty for the species in this part of its range. Pollinators include several species of Bombus and Osmia, and visitation rate at one large-flowered population was more than twice the visitation rate at two small-flowered populations (Elle and Carney, 2003
). The fruit is a dry capsule enclosed by the calyx; when ripe, the 3–8 seeds per fruit are passively dispersed.
Data collection
We measured floral traits on plants grown from seeds collected from six populations of C. parviflora from Vancouver Island, British Columbia, that differed in corolla size in 2001: Rathtrevor Beach (RB), Thetis Lake (TL), Kin Beach (KB), Jack Point (JP), Cowichan River (CR), and Elk Falls (EF). See Elle and Carney (2003)
for population information. Open-pollinated seeds were collected from approximately 20 maternal parent plants from each population and three seeds from each parent were randomly planted in standard potting soil in 48-well flats. Plants were grown in a growth chamber under short days (10 h 20°C days/14 h 10°C nights) for 8 wk before switching to longer days (16 h) to induce flowering. Germination and survival were uneven; only maternal families with two or more surviving offspring were retained for analysis, with total number of maternal families/plants measured per population as follows: RB = 11/28, TL = 10/22, KB = 13/36, JP = 13/33, and EF = 12/29. In CR, germination and survival was especially poor; only four maternal families had at least two offspring surviving, but all 11 families/15 individuals available were retained in the analysis, so results for CR must be interpreted with caution.
We attempted to harvest the first four flowers (two flowers and two buds) from each plant, but occasionally later-produced flowers were collected. On each flower, we took three linear corolla measurements: width of the two attached banner petals, length 1 from the join of the banner and wing petals to the saccate bend in the corolla tube, and length 2 from the bend to the base of the ovary. Corolla tube length was measured this way because of differences among populations in the amount of bend in the corolla (E. Elle, unpublished data), which would affect the accuracy of our estimates of corolla length if just one measurement had been taken. Harvested flowers were dissected into androecium, gynoecium, corolla, and calyx, and dried. The four parts of one flower per plant were weighed to the nearest 0.001 mg. Corolla mass was considered a secondary male trait because of its importance in pollinator attraction. Calyx mass was considered a secondary female trait because it is retained during fruit formation and protects the developing capsule.
Buds were collected from all plants prior to anthesis and stored in 95% ethanol. The number of ovules per bud was determined by dissection of the two buds collected. Pollen was counted for one bud from each plant and the pollen : ovule (P : O) ratio was determined. To count pollen, all four anthers were removed from ethanol and allowed to air dry. The anthers were crushed with a miniature pestle until there were no visible anther particles and suspended in a 25-µL solution of three parts lactic acid to one part glycerol. The solution was vortexed for 3 min to ensure even suspension of pollen grains. Two 5-µL drops were placed on a hemocytometer grid, and three 1 x 1 mm squares within the grid were counted for each drop. The same grid locations were counted for each sample. Because the volume contained in each 1 x 1 mm square of our hemocytometer is 10–4 mL, we multiplied the mean of the six pollen counts by 250 to estimate the count in the 25-µL solution (and therefore the total pollen grains in each flower). Seventeen of the 155 samples were missing one or more anthers, so we made the assumption that all anthers produce the same quantity of pollen and multiplied pollen counts by the appropriate scaling factor to estimate pollen quantity as if four intact anthers were present. Mean pollen diameter for each plant was calculated from measurements of three pollen grains located closest to three predetermined grid corners on the hemocytometer.
Statistical analyses
We averaged data from replicated flowers or buds on each individual when available (linear dimensions and ovule counts). Corolla dimensions (width, length 1 and length 2), corolla mass, gynoecium mass, and androecium mass were log transformed and pollen counts were cube-root transformed prior to analysis to reduce heteroscedasticity. All analyses were performed using SAS (SAS Institute, 1996
). We compared all floral characteristics among the six populations of C. parviflora using analysis of variance (ANOVA), with population as the main effect and maternal parent nested within population mean square as the error term. When the ANOVA indicated significant differences among populations, means were compared using the Ryan-Einot-Gabriel-Welsch multiple-range test (Ryan's Q; Day and Quinn, 1989
). To test the hypothesis that populations differed in relative maleness (i.e., that populations with larger linear corolla dimensions had greater total allocation to male function rather than exhibiting allometric scaling of the sizes of all floral parts), we performed an analysis of covariance testing for population differences in corolla + androecium mass using total flower mass (calyx + gynoecium + corolla + androecium) as a covariate.
Within-population trade-offs
Using maternal family means, we calculated correlations among biomass (four variables) and gamete (three variables) characters within the six populations. Within-population correlations using maternal families raised in a common environment approximate genetic correlations. We emphasize the preliminary nature of this analysis, however, because seeds were collected from open-pollinated plants from populations that likely differ in the selfing rate (affecting the relatedness among sibs) and our sample sizes (especially for CR) are small. In all correlation analyses, we determined significance after sequential Bonferroni adjustment (Rice, 1989
).
Across population trade-offs
Using the 70 maternal family means from the six populations, we calculated correlations among biomass and gamete characters. These correlations are essentially phenotypic correlations that control for environmental variation and the lack of independence of sibs within families and illustrate allocation trade-offs for the species. Some authors consider such correlations genetically based (e.g., Mazer and Delesalle, 1996
). As in the Mazer and Delesalle study, we expect our across-population analysis to yield stronger correlations than within-population analyses, both because of increased power and because of the greater range of phenotypes available across populations, which should increase our ability to detect trade-offs (de Laguerie et al., 1991
).
Within- and across-population correlations controlling for total floral allocation
Sex allocation trade-offs will be obscured if there is variation among individuals in resources available due to differences in acquisition ability (van Noordwijk and DeJong, 1986
); acquisition differences tend to lead to positive correlations. We did not measure vegetative size (considered the best correlate of resource status) in this study, but data from a separate study using these same populations showed that flower size (linear corolla width) was positively correlated with end-of-season vegetative biomass (Elle, 2004
). Here we controlled for differences among maternal families in total flower dry mass (calyx + gynoecium + corolla + androecium), which estimates reproductive allocation at the flowering stage, is highly correlated in the current data set with linear corolla width (R = 0.89, P < 0.0001, N = 70 maternal families), and should be correlated with vegetative size. We calculated partial correlations controlling for total flower mass on both the within- and across-population data.
Among-population trade-offs
If genetic trade-offs within populations persist during the process of population differentiation, we expect to find trade-offs among populations that reflect the correlations within populations. Using means of maternal families within populations, we performed three regressions to directly examine trade-offs of interest because power for a correlation analysis similar to those discussed earlier was limited by our sample size of six populations. In each case, we first regressed population means for the trait of interest on population means for total flower biomass, to control for differences among populations in total reproductive allocation, before performing the regression. These regressions included androecium mass vs. gynoecium mass, pollen grain number vs. ovule number, and pollen grain number vs. pollen grain size.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Armbruster et al., 2002
). Correlated shifts of both mating system and sex allocation were documented for six Gilia achilleifolia Benth. populations with selfing rates determined via allozyme electrophoresis (Schoen, 1982
) and for two Blandfordia grandiflora R. Br. populations for which self-fertility was estimated via hand pollination (Ramsey, 1993
), but we are unaware of other intraspecific studies of this kind in perfect-flowered hermaphrodites. Our assumptions about population differences in the degree of selfing are from field and growth-chamber estimates of pollinator visitation and autonomous selfing rates, respectively (Elle and Carney, 2003
; Elle, 2004
), which strongly suggest that selfing is negatively correlated with corolla size in C. parviflora.
Ritland and Ritland (1989)
calculated how proportional allocation to male function (corolla + androecium) is related to the different mating systems reviewed by Cruden and Lyon (1985)
: facultative autogamy is 38% male, facultative xenogamy 50.9%, and xenogamy 68.6%. In C. parviflora, proportional male biomass allocation ranged from 38% in RB to 70% in EF (Fig. 1), suggesting a range of mating systems across populations from facultative autogamy to xenogamy. It is worth noting that the Ritlands' eight Mimulus species ranged from 28% to 62% male allocation, variation similar in magnitude (34%) to the range of male allocation observed within our single, highly variable species (32%). Pollen : ovule ratios for C. parviflora (Fig. 2) all fall within the range for xenogamy suggested by Cruden and colleagues (1200–8000 pollen grains per ovule; Cruden, 1977
; Cruden and Lyon, 1989
; Cruden, 2000
). The prediction of xenogamy that results from sex allocation traits is in conflict with our documentation of high autonomous selfing rates (Elle, 2004
) and discrimination against small-flowered plants by pollinators (Elle and Carney, 2003
) in C. parviflora. One possible explanation is that pollen, in addition to nectar, serves as a pollinator reward; plant species that offer pollen rewards tend to have higher P : O ratios than plants with nectar rewards (Cruden, 2000
; and see later).
The presence of allocation trade-offs is a major assumption of sex allocation theory. Here, we provide evidence of male– female trade-offs for biomass allocation. It has been suggested that biomass is a poor currency (Goldman and Willson, 1986
; McKone, 1987
; Ashman, 1994
), and some studies that used absolute biomass did not detect trade-offs (e.g., Ågren and Schemske, 1995
; Campbell, 1997
). We also found positive correlations among the sizes of flower parts when using absolute biomass, which is expected if larger individuals have a greater ability to acquire resources and so allocate more to all flower parts (van Noordwijk and de Jong, 1986
). In some studies, controlling for differences in flower size changed the sign of correlations from positive to negative (e.g., Campbell, 1992
; O'Neil and Schmitt, 1993
). Similarly, we elucidated trade-offs between androecium mass and gynoecium mass within populations and across populations when total floral allocation was controlled statistically. Because we used maternal family means for this analysis, within-population results suggest negative genetic correlations between these traits.
Curiously, we found trade-offs between the number of male vs. female gametes when flower size was not controlled in the across-population analysis using maternal family means, and (marginally) in the among-population analysis controlling for flower size, but not in the across-population analysis controlling for flower size. This result may reflect the fact that while biomass of the four floral organs and pollen production were all significantly positively correlated with total flower biomass in the across-population analysis (i.e., greater allocation to flowers means larger size of all flower parts), ovule number was significantly negatively correlated with total flower biomass (data not shown). A similar result was found in the among-population analysis when regressing ovule number on total flower biomass. This result suggests a developmental constraint, such that increasing allocation to floral biomass precludes ovule formation.
Within populations, there were no genetic correlations between pollen number and ovule number, regardless of whether we controlled for total flower allocation, and no relationship between total flower biomass and ovule number except for KB (negative). All populations except JP and TL showed a significant positive correlation between floral biomass and pollen number. Populations may be at different optima for sex-specific gamete production, especially ovule production, but at this time we do not know if this is due to differences in their selection history, perhaps related to mating system evolution, or to founder effects coupled with low amounts of among-population gene flow.
Trade-offs within a sex have been more easily documented than between-sex trade-offs, for instance seed size–number trade-offs (Sakai and Sakai, 1995
; Leishman, 2001
) and pollen size–number trade-offs (Stanton and Young, 1994
; Vonhof and Harder, 1995
; Worley and Barrett, 2000
; Sarkissian and Harder, 2001
). We concentrated on initial allocation to flowers and so could not examine the former, but did find the latter trade-off in C. parviflora, both in the across-population analysis not controlling for flower size differences and in the among-population regression analysis. The lack of a relationship between these variables in the across-population analysis when flower size was controlled statistically may be due to similar reasons as those discussed for ovule number; pollen diameter, like ovule number, was negatively correlated with total flower biomass. Because pollen size is important for post-pollination processes (Harder, 1998
), plants are expected to optimize their investment in pollen grains so that individual grains are large enough to achieve fertilization of available ovules (Vonhof and Harder, 1995
). Larger pollen grains may have more resources and greater viability (Kelly et al., 2002
), allowing growth through longer stigmas. Although positive correlations between pistil length and pollen size are common (recently reviewed in Torres, 2000
; Aguilar et al., 2002
) and these traits are genetically correlated in one species where such correlations have been measured (Sarkissian and Harder, 2001
), in C. parviflora, populations with longer pistils (i.e., larger-flowered populations) have smaller pollen grain diameters and there are no genetic correlations between these traits in any of our populations. The lack of a positive relationship between flower size and pollen diameter suggests that post-pollination processes are not an important selective agent for pollen size variation in C. parviflora. However, the lack of genetic correlations between pollen size and number (the within-population analysis) suggests that pollen size differences are not due to a correlated response to selection on pollen number, as was found in Brassica rapa L. by Sarkissian and Harder (2001)
, although our ability to detect genetic correlations is not as strong as in their selection experiment.
If the apparent lack of genetic correlations between pollen size and number in C. parviflora is a robust result, it is necessary to consider alternative explanations for the trade-off between these traits in the among-population analysis. Previously, we hypothesized that pollen-collecting bees may have selected for excess pollen production, leading to extremely high P : O ratios in this taxon. Harder (1998)
examined and dismissed the hypothesis that pollen size variation among species could be due to divergent selection by different pollinators, i.e., pollen-collecting bees that select for small pollen size (small grains that escape being groomed into scopae are the ones available to fertilize ovules) vs. other pollinators that are unlikely to exert selection on pollen size (because pollen is passively accumulated and moved among flowers). Harder's data set does not include comparisons of self- and cross-fertilized taxa, however, and it is possible that differences in pollen diameter in C. parviflora are indeed due to divergent selection for small grains that escape grooming in populations where pollinator visits are common and for large grains that are highly effective at fertilizing ovules in relatively selfing populations where pollinator visits are uncommon. This hypothesis should be explored in more detail.
We have described significant among-population variation in floral traits in C. parviflora when plants were grown under controlled conditions. This variation may be due to local selection and adaptation, by both biotic agents (pollinators: Elle and Carney, 2003
) and abiotic agents (rainfall and growing season length: Elle, 2004
). If so, understanding within-population selection and constraint is essential, and more in-depth study of both selection in natural populations and the quantitative genetics of sex allocation in this species is in order.
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FOOTNOTES |
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2 Present address: Department of Botany, University of Guelph, Guelph, Ontario N1G 2W1 Canada. E-mail: aparachn{at}uoguelph.ca
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