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Ecology |
Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1 Canada
Received for publication September 23, 2005. Accepted for publication January 31, 2006.
ABSTRACT
Many workers have demonstrated a genetic basis for variation in inflorescence traits, but this variation can also have an environmental component. Because flowering can incur significant water costs, I estimated plasticity of inflorescence traits of three populations of Lobelia siphilitica in response to drought. I manipulated soil water availability in the greenhouse and measured seven inflorescence traits. Under drought conditions, plants from one population flowered later and produced fewer flowers with shorter corollas and narrower landing pads. In contrast, the height of the flowering stalk decreased in response to drought in all three populations. Consequently, pollinator-mediated natural selection on these plastic traits may depend on soil water availability. Plastic responses differed between genotypes only for the height of the flowering stalk and the length of the corolla tube and only in one or two populations. This suggests that genotype x environment interactions would not limit the evolution of inflorescence traits in L. siphilitica. The strength and sign of phenotypic correlations among inflorescence traits did not respond plastically to drought, suggesting that indirect selection on inflorescence traits of L. siphilitica will not vary strongly with water availability. My results suggest that plasticity of inflorescence traits may influence their evolution, but the effects are population- and trait-specific.
Key Words: drought • inflorescence • Lobelia siphilitica • phenotypic plasticity
Phenotypic variation in plant traits is necessary for there to be natural selection on these traits. A genetic basis for variation in inflorescence traits is commonly detected (e.g., Conner and Via, 1993
; Campbell, 1996
; Ashman, 2003
; Caruso, 2004
), suggesting that these traits can evolve in response to natural selection. Variation in inflorescence traits can also have an environmental component. Plasticity of inflorescence traits has been documented in response to drought (Carroll et al., 2001
; Mal and Lovett-Doust, 2005
), nutrient availability (Dorken and Barrett, 2004
), light (Boose, 1997
; Vogler et al., 1999
; Weinig, 2002
), and intraspecific competition (Wolfe and Mazer, 2005
). However, inflorescence traits are generally less plastic than vegetative traits (Bradshaw, 1965
; Schlichting and Levin, 1984
; Frazee and Marquis, 1994
), and traits of individual flowers such as petal size are generally less plastic than plant-level traits, such as date of first flower and flower number (Berg, 1959
; Cresswell et al., 2001
; Dorken and Barrett, 2004
; Wolfe and Mazer, 2005
).
Phenotypic plasticity in inflorescence traits can influence their adaptive evolution by at least three mechanisms. First, if inflorescence traits are plastic, then the strength and direction of pollinator-mediated natural selection on these traits may be altered by the biotic or abiotic environment (Carroll et al., 2001
). For example, nectar production can respond plastically to the availability of water and light (Boose, 1997
; Carroll et al., 2001
), suggesting that pollinator services and consequently pollinator-mediated selection on this trait may differ between environments (Carroll et al., 2001
). Second, if the norm of reaction differs between genotypes (genotype x environment interaction), then the response to selection will be slowed (Via and Lande, 1985
). This is because the phenotypes favored by natural selection may be the same across environments, but the selected phenotypes are produced by different genotypes in each environment (Via and Lande, 1985
). Third, if phenotypic correlations among inflorescence traits are plastic (Schlichting, 1989
), then indirect selection on these traits may differ between environments (Bennington and McGraw, 1995
; Donohue and Schmitt, 1999
). This is because the strength and direction of indirect selection is dependent on the patterns of phenotypic correlations among a suite of traits. All things being equal, if phenotypic correlations among traits are weaker in one environment than another, then indirect selection on these traits will also be weaker (Lande and Arnold, 1983
).
Although inflorescence traits can respond plastically to many biotic and abiotic factors, they are particularly likely to respond to variation in soil water availability. Because flower maturation is largely the result of cell expansion rather than cell division, flowering can incur significant water costs (Galen et al., 1999
). For example, transpirational water loss from flowers can exceed that from leaves (Nobel, 1977
). Consequently, plants produce smaller flowers in response to drought (Elle and Hare, 2002
; Mal and Lovett-Doust, 2005
), and may potentially also produce fewer flowers and shorter inflorescences. Variation in soil water availability can also influence flowering phenology. For example, many plant species that are unable to tolerate drought instead accelerate flowering to escape drought (Ludlow, 1989
).
To determine if and how plasticity in inflorescence traits influences their adaptive evolution, I estimated plasticity of traits in Lobelia siphilitica L. in response to drought. Lobelia siphilitica is a short-lived perennial that experiences a range of soil water availabilities in the wild (Caruso et al., 2003
), suggesting that variation in soil water is ecologically relevant in this species. Responses of L. siphilitica to drought have not been measured, but inflorescence height responded to light availability (Pigliucci and Schlichting, 1995
), indicating that the inflorescence traits of this species can be plastic. Inflorescence traits of L. siphilitica are under natural selection in the wild (Johnston, 1991a
; Caruso et al., 2003
; Parachnowitsch, 2005
), and there is significant genetic variation for these traits (Caruso, 2004
), suggesting that inflorescence traits of L. siphilitica are undergoing adaptive evolution. However, any effect of phenotypic plasticity on this adaptive evolution is unknown. I experimentally manipulated water availability to L. siphilitica plants to answer the following questions: (1) Do inflorescence traits of L. siphilitica respond plastically to soil water availability? (2) Are traits of individual flowers less plastic than plant-level inflorescence traits? (3) If inflorescence traits of L. siphilitica are plastic, by what mechanism or mechanisms can this plasticity influence their evolution?
MATERIALS AND METHODS
Study species and seed sources
Lobelia siphilitica (Lobeliaceae) is a short-lived, herbaceous, perennial wildflower that grows in wet meadows and woods throughout eastern North America (Johnston, 1991a
and references therein). Its 3-cm long, blue flowers are primarily pollinated by Bombus spp. (Beaudoin Yetter, 1989
). In natural populations in Iowa, plants flower from early August until early October and fruits dehisce from mid-September through November (C. M. Caruso, personal observation). Lobelia siphilitica is gynodioecious, but the populations used in this study contain few (0–9%) females (C. M. Caruso, unpublished data). Hermaphroditic flowers are protandrous, and pollen is shed from a tube formed by the fused anthers and filaments (Johnston, 1991a
). Although L. siphilitica is self-compatible (Johnston, 1992
), the complete separation between staminate and pistillate phases of flower development prevents autogamous self-fertilization of hermaphrodites (Johnston, 1991b
). Consequently, pollinators are required for seed set, and phenotypic selection on inflorescence traits cannot be measured in their absence.
I measured plasticity of inflorescence traits of plants grown from seeds collected from three L. siphilitica populations (Conard Environmental Research Area [CERA], Krumm, and Reichelt) located in Jasper County, Iowa, USA and described in Caruso et al. (2003)
. These L. siphilitica populations occupied a variety of habitats, from saturated soils to dry soils that are virtually never saturated. Specifically, soil volumetric water content (VWC) was 60% higher in CERA and Reichelt relative to Krumm (Caruso et al., 2003
). Thus, variation in soil water availability may be an ecologically relevant type of environmental heterogeneity for L. siphilitica.
Experimental design
I germinated seeds from open-pollinated fruits collected from 10 plants per population. Lobelia siphilitica can produce clonal offshoots (Beaudoin Yetter, 1989
), but I attempted to sample fruits from only one ramet per genet. Seeds were rinsed with a dilute solution of bleach and ethanol to break dormancy (Dudle et al., 2001
). Approximately 20 seeds/pot were sown onto moist Pro-mix PGX (Premier Horticulture, Dorval, Quebec, Canada) and placed in standing water in the greenhouse at the University of Guelph, Guelph, Ontario, Canada. Two pots were planted for each maternal family. After 6 weeks, I transplanted six seedlings/family into 9 x 9 cm plastic pots. A total of 180 L. siphilitica seedlings were transplanted. Plants were watered as necessary, fertilized with Nutricote Total 13-13-13 (Plant Products, Brampton, Ontario, Canada), and exposed to supplemental light (16 h days).
After approximately 8 weeks of growth, I randomly assigned half of the plants in each of 30 families (10 per population) to the well-watered (wet) treatment and half to the drought (dry) treatment. I used a split-plot design (Wilkinson, 1997
), with treatment (wet vs. dry) as the between-plot effect and family as the within-plot effect. Consistent with this design, water availability was manipulated on a whole-plot level, with three wet "plots" (groups of seven trays) of plants and three dry "plots." The position of trays within plots was rotated weekly. Plants in the wet treatment were watered as necessary to ensure that they remained in standing water. To decide whether plants in the dry treatment needed to be watered, I measured soil moisture availability for 18 randomly chosen plants, evenly divided between the three dry plots, using a Lincoln soil moisture meter (Lincoln Irrigation Inc., Lincoln, Nebraska, USA) calibrated to a range of soil volumetric water contents (VWC). On days when the mean VWC was <15%, each tray of plants in the dry treatment received approximately 50 ml of water per plant. Mean (±1 SE) VWC was 40.04% (±0.02) within the wet treatment and 13.78% (±3.52 x 10–3) within the dry treatment. These treatments were maintained from 14 May 2003 until 7 October 2003, when the last plants were harvested.
Data collection
At flowering, I measured seven inflorescence traits per plant: corolla lobe length, corolla lobe width, corolla tube length, corolla tube width (Fig. 1), total flower number, height of the flowering stalk, and date of first flower. These traits were chosen because they are under significant natural selection in L. siphilitica populations (Johnston, 1991a
; Caruso et al., 2003
; Parachnowitsch, 2005
). Floral morphology was measured for three flowers/plant using handheld digital calipers. I estimated total flower number as the sum of the senescent flowers, open flowers, and unopened buds on each plant. The height of the flowering stalk was measured from the base of the stalk after the topmost flower had opened. To estimate date of first flower, I monitored plants every other day from 1 July 2003 until the end of the experiment. Because pollinators are necessary for L. siphilitica to reproduce, I was unable to measure seed or fruit set of greenhouse-grown plants. In addition, estimates of flower number may be inflated by the lack of pollination (Wolfe, 1992
).
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; Wilkinson, 1997
). Both treatment and family were fixed factors (Underwood, 1997
). A significant treatment term indicated that the trait responded plastically to soil water availability. Because split-plot ANOVAs are sensitive to unbalance, only families for which all six plants were measured were included in the analyses. All analyses were done separately for each population using SYSTAT 8.0 (SPSS, Chicago, Illinois, USA). Because variation among trays within plots did not have a significant effect on inflorescence traits (data not shown), tray effects were not included in any of the analyses. Each response variable was tested for the assumption of normality using Lilliefor's test (Wilkinson, 1997
). I tested the assumption of homogeneity of residual variance by examining variances for each treatment group.
To determine whether the magnitude of phenotypic plasticity varied among traits, I calculated the coefficient of variation (CV) for each combination of population, family, and trait (Schlichting and Levin, 1984
; Wolfe and Mazer, 2005
). Because the data were heteroscedastic, I used a nonparametric Kruskal–Wallis test to compare CVs among traits. All analyses were done separately for each population using SYSTAT 8.0 (SPSS).
To determine if correlations among inflorescence traits responded plastically to soil water availability, I calculated Pearson correlation coefficients (r) among inflorescence traits within each combination of population and treatment. Mantel's test (e.g., Bidart-Bouzat et al., 2004
) was used to compare these correlation matrices between treatments within each population. A significant (P < 0.05) positive Mantel's test indicates that the matrices were similar across treatments and therefore that correlations are not responding plastically to soil water availability. A significant (P < 0.05) negative Mantel's test indicates that the matrices were dissimilar across treatments and therefore that correlations are responding plastically to soil water availability. All Mantel's tests were done using XLSTAT-PRO (Addinsoft, New York, New York, USA).
RESULTS
Plasticity of inflorescence traits
All inflorescence traits except corolla lobe length and corolla tube width responded plastically to soil water availability in at least one population (Table 1; Fig. 2). Within Reichelt, plants produced 39% more flowers (Fig. 2O), flowered 4 days earlier (Fig. 2U), had 5.3% wider corolla lobes (Fig. 2F), and produced 5.8% longer corolla tubes (Fig. 2I) in the wet than in the dry treatment. In contrast, the height of the flowering stalk responded plastically to soil water availability in all three L. siphilitica populations. Plants from CERA (Fig. 2P), Krumm (Fig. 2Q), and Reichelt (Fig. 2R) produced respectively, 43.6, 47.7, and 39.0%, taller flowering stalks in the wet treatment than in the dry.
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Plasticity of individual flowers vs. plant-level traits
The mean coefficient of variation differed significantly among inflorescence traits. Coefficients of variation for flower size measures (length and width of corolla lobe, length and width of corolla tube) were lower than CVs for the three plant-level traits (flower number, height of flowering stalk, and date of first flower) in all populations (Fig. 3). In CERA, CVs for plant-level traits were 2.9 times larger than CVs for flower size measures (Kruskal-Wallis test statistic = 46.15; P < 0.001; df = 6; Fig. 3A). In Krumm, CVs for plant-level traits were 3.8 times larger than CVs for flower size measures (Kruskal–Wallis test statistic = 54.18; P < 0.001; df = 6; Fig. 3B). Finally, CVs for plant-level traits were 3.4 times larger than CVs for flower size measures in Reichelt (Kruskal–Wallis test statistic = 55.30; P < 0.001; df = 6; Fig. 3C).
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DISCUSSION
Five of seven inflorescence traits responded plastically to variation in soil moisture availability (Table 1), but not all traits were plastic in every population, suggesting that any effect of plasticity on inflorescence evolution of L. siphilitica will be population-specific. Interpopulation variation in plasticity of inflorescence traits is common (e.g., Schlichting and Levin, 1990
; Pigliucci et al., 1995
) and may be the result of selection for different types of plastic responses in different environments or a non-adaptive consequence of genetic drift (Schlichting, 1986
). Natural selection on corolla lobe length, corolla tube length, and flower number of L. siphilitica does vary significantly among CERA, Krumm, and Reichelt (Caruso et al., 2003
). This suggests that differences in plasticity among these populations might be the result of differences in natural selection between populations. However, measurements of selection on plasticity itself (e.g., Stinchcombe et al., 2004
) would be necessary to test whether interpopulation variation in plasticity of inflorescence traits in L. siphilitica is the result of selection. Alternatively, costs (sensu DeWitt et al., 1998
) may constrain the evolution of plasticity in inflorescence traits in some L. siphilitica populations. Although the costs of plasticity in inflorescence traits of L. siphilitica have not been measured, a recent review (van Kleunen and Fischer, 2005
) found little evidence that plasticity in plant traits is costly.
The significant plastic responses to drought for five of seven inflorescence traits of L. siphilitica suggest that the strength and direction of natural selection by pollinators on these traits may be altered by the soil moisture environment (Carroll et al., 2001
). For example, some pollinator taxa prefer to visit plants with more open flowers, whereas others have no preference (Conner and Rush, 1996
; Strauss et al., 1996
). If L. siphilitica's pollinators also differ in their preferences, then their visitation rates may differ between wet years, when plants would have relatively large inflorescences, and dry years, when plants would have relatively small floral displays. Any differences between pollinator taxa in visitation rate could, in turn, lead to differences in natural selection (e.g., Aigner, 2005
). Consistent with this hypothesis, natural selection on flower number of L. siphilitica plants did differ between 1999 and 2000, which were relatively wet and dry years, respectively (Caruso et al., 2003
). However, these data were collected from CERA and Krumm, populations in which flower number did not respond plastically to drought (Table 1), and pollinator visitation was not measured. Measuring variation in natural selection on and pollinator visitation to L. siphilitica from plastic populations would be necessary to definitively test whether selection on plastic traits depends on soil water availability. If pollinator-mediated selection depends on soil water availability, then the relationship between floral traits and an estimate of pollination such as the amount of pollen deposited on L. siphilitica stigmas should differ between dry and wet conditions.
The rarity of significant genotype x environment interactions for inflorescence traits of L. siphilitica (Table 1) suggests that variation in the response of different genotypes to drought is unlikely to be a significant limit on their adaptive evolution. Specifically, inflorescence phenotypes of L. siphilitica that are favored by selection will be produced by the same genotypes in different soil moisture environments. This result is consistent with most other studies of genotype x environment interactions for inflorescence traits (reviewed by Vogler et al., 1999
), in which there are either few or no significant genotype x environment interactions. Significant genotype x environment interactions for inflorescence traits may be more common in longer-lived, iteroparous perennials such as Campanula rapunculoides (Vogler et al., 1999
) and Epilobium canum (Boose, 1997
) than in short-lived perennials such as L. siphilitica. This is because longer-lived, iteroparous perennials may experience more variation in environmental conditions, such as soil water availability, both within and across years and therefore more selection for plasticity (Vogler et al., 1999
).
The matrix of phenotypic correlations did not differ significantly between treatments in any population (Table 2), suggesting that indirect selection on inflorescence traits of L. siphilitica would not be strongly influenced by the soil moisture environment. This result contrasts with the results of at least two other studies (Bennington and McGraw, 1995
; Donohue and Schmitt, 1999
), in which plasticity in the strength and direction of phenotypic correlations resulted in differences in indirect selection between environments. Although the overall correlation matrix did not differ between treatments for any L. siphilitica population, some of the individual correlations among inflorescence traits were significant in one soil moisture environment but not in the other (Table 2). For example, the correlation between corolla tube width and flower number in CERA was significant and negative in the dry treatment, but not in the wet treatment (Table 2). This suggests that the strength of indirect selection on specific traits may be influenced by soil moisture, even if the overall correlation matrix does not differ between environments.
Consistent with other studies (Berg, 1959
; Cresswell et al., 2001
; Dorken and Barrett, 2004
; Wolfe and Mazer, 2005
), traits of individual flowers were less plastic than plant-level traits. Not only did flower size respond plastically to drought in only one L. siphilitica population (Table 1), but the coefficients of variation for flower size were significantly lower than CVs for flower number, date of first flower, and height in all three populations (Fig. 3). Traits of individual flowers may be less plastic than whole-plant traits because they are under stabilizing selection that favors canalized rather than plastic genotypes (Wolfe and Mazer, 2005
). If this hypothesis is correct, then L. siphilitica families that are more plastic for flower size should have lower average fitness across environments, whereas families that are more plastic for flower number, date of first flower, and height of flowering stalk should have higher average fitness across environments; because L. siphilitica is insect-pollinated, I was unable to estimate fitness for my greenhouse-grown plants to test the prediction that plasticity in flower size is not adaptive. Alternatively, traits of individual L. siphilitica flowers may be less plastic than whole-plant traits because variation in traits of individual flowers has a larger genetic component (e.g., Campbell, 1996
, 1997
; Elle, 1998
). I did detect significant family effects more frequently for flower-level than plant-level traits of L. siphilitica (Table 1), supporting the hypothesis that flower-level traits are less plastic because they are under stronger genetic control.
Lobelia siphilitica plants growing in the dry treatment either took longer to flower than plants in the wet treatment (Reichelt; Table 1; Fig. 2U) or flowered at the same time (CERA and Krumm; Table 1; Figs. 2S, T), suggesting that this species does not accelerate flowering to escape drought (e.g., Ludlow, 1989
). Instead, L. siphilitica may acclimate to dry conditions by avoiding tissue dehydration (reviewed in Chaves et al., 2003
). For example, L. siphilitica growing in dry conditions were more water-use efficient in their photosynthesis than those in wet conditions (C. Caruso and H. Maherali, University of Guelph, unpublished data). An increase in water-use efficiency, the ratio of carbon fixed by photosynthesis to water lost via transpiration, is considered an adaptation to avoid dehydration (e.g., Geber and Dawson, 1997
; McKay et al., 2003
).
In conclusion, inflorescence traits of L. siphilitica do respond plastically to variation in soil moisture availability. This plasticity may influence the evolution of inflorescence traits in L. siphilitica by altering relationships between L. siphilitica and its pollinators. In addition to influencing patterns of natural selection, plasticity in inflorescence traits can also influence plant breeding systems (Elle and Hare, 2002
) and patterns of sex allocation (Dorken and Barrett, 2004
). My results therefore highlight the importance of measuring plastic responses of inflorescence traits, rather than assuming that these responses are not biologically significant.
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1 The author thanks H. Maherali and two anonymous reviewers for comments on this manuscript; L. Mottl for permission to collect seeds at CERA; T. Suwa, J. Thompson, A. Turnbull, and M. Yungblut for assistance in the greenhouse; and S. Ventis for the illustrations for Fig. 1. This work was supported by an operating grant from the Natural Science and Engineering Research Council of Canada to C.M.C. 
2 Author for correspondence (carusoc{at}uoguelph.ca
)
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