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Reproductive Biology |
Department of Environmental, Population, and Organismic Biology, University of Colorado, Campus Box #334, Boulder, Colorado 80309 USA
Received for publication August 6, 2002. Accepted for publication December 6, 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: andromonoecy • architecture • development • phenotypic plasticity • sexual systems • Solanaceae • Solanum
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Whalen and Costich, 1986
; Anderson and Symon, 1989
; Spalik, 1991
; Diggle, 1993
, 1994
; Emms, 1996
; Emms et al., 1997
). Andromonoecy is widely thought to provide a mechanism to independently adjust allocation to male and female function; individuals are assumed to vary production of hermaphroditic and staminate flowers in response to changes in resource availability (reviewed in Bertin, 1982a
; but see Podolsky, 1993
). Thus, andromonoecy is often considered a form of phenotypic plasticity. Regardless of the particular advantages of andromonoecy, however, the evolution of this sexual system requires the innovation of developmental mechanisms that allow for the production of two distinct floral types. Comparative developmental and morphological analyses of closely related species that vary in the magnitude of andromonoecy (i.e., in the relative production of hermaphroditic and staminate flowers) can identify those features that have been modified in association with the evolution and diversification of this sexual system. Once we understand how complex phenotypes such as andromonoecy evolve, we can create and test more refined hypotheses for why they evolve.
In the plant family Solanaceae, andromonoecy is well documented in Solanum subgenus Leptostemonum and has been reported for 13 of 22 described sections (Whalen and Costich, 1986
). Lasiocarpa is a small section of 12 species, within subgenus Leptostemonum, that is strongly supported as monophyletic based on morphological, allozyme, karyotype, and chloroplast restriction site data (Heiser, 1972
, 1987
; Whalen and Caruso, 1983
; Bernardello et al., 1994
; Bruneau et al., 1995
). Although all members of Lasiocarpa are andromonoecious, the numbers of hermaphroditic and staminate flowers produced among species in this section varies considerably (Whalen et al., 1981). Some species are characterized as weakly andromonoecious (e.g., S. hirtum Vahl., Diggle, 1993
; S. stramonifolium Jacq., Whalen et al., 1981); that is, plants produce relatively few staminate flowers. In contrast, other species bear many staminate flowers and are described as strongly andromonoecious (e.g., S. quitoense Lam., Whalen and Costich, 1986
; S. vestissimum Dunal., Whalen et al., 1981). The diversity of sexual expression among species in section Lasiocarpa makes this an ideal group for comparative analyses.
Detailed investigation of Solanum hirtum (section Lasiocarpa) has shown that sexual expression is phenotypically plastic; fruit-bearing plants produce a greater proportion of staminate flowers than genetically identical plants that are prevented from producing fruit (Diggle, 1993
). Because fruit development poses a significant drain on resources available for continued development (Lloyd, 1980
), plasticity of sexual expression in S. hirtum is consistent with hypotheses for the evolution of andromonoecy that suggest that the production of staminate flowers is a mechanism for adjusting allocation to male and female function. As continued fruit production becomes resource-limited, subsequent production of staminate flowers allows reallocation of resources away from "costly" gynoecia toward increased male function, vegetative growth, or storage (reviewed in Bertin, 1982a
; Whalen and Costich, 1986
; Spalik, 1991
). These analyses of S. hirtum indicate that consideration of plasticity should be integral in comparative studies of the expression of andromonoecy in section Lasiocarpa.
To compare andromonoecy and developmental plasticity among species, sexual expression must be characterized at multiple levels of morphological organization. In S. hirtum the occurrence of staminate flowers varied both within and among inflorescences. All inflorescences on fruit-bearing plants produced both hermaphroditic and staminate flowers; however, the proportion of staminate flowers increased in successively developing inflorescences (Diggle, 1994
). We refer to this variation in sexual expression as an inter-inflorescence architectural effect. In addition, within inflorescences, flowers in basal positions were predictably hermaphroditic, that is, the phenotype of these flowers was fixed regardless of treatment. Only the phenotype of flowers in distal positions within inflorescences was plastic and varied with fruiting treatment. These flowers developed as hermaphroditic in the absence of fruit and as staminate on fruit-bearing plants (Diggle, 1994
). We refer to variation in the developmental potential of individual flowers within inflorescences as an intra-inflorescence architectural effect (sensu Diggle, 1995
). Both inter- and intra-inflorescence architectural effects varied among genotypes of S. hirtum and affected the magnitude of plasticity and the strength of andromonoecy. Therefore, we also ask how these architectural effects are expressed in other species in section Lasiocarpa and whether these effects contribute to the diverse expression of andromonoecy among species.
To investigate the potential roles of phenotypic plasticity and architectural effects in the diversification of andromonoecy, we studied sexual expression for four additional species in section Lasiocarpa: Solanum candidum Lindl., S. ferox var. lasiocarpum (Dunal) Miq., S. pseudolulo Heiser, and S. quitoense Lam. The four species were chosen to encompass wide variation in the degree of andromonoecy. Specifically, we consider four questions for each of these species. (1) What is the degree of andromonoecy and to what extent does andromonoecy vary among these closely related species? (2) Is sexual expression phenotypically plastic with respect to fruiting status (i.e., resource availability)? (3) How does inter-inflorescence variation affect whole plant sexual expression? (4) What is the distribution of hermaphroditic and staminate flowers within inflorescences, and is there a predictable architectural component of staminate flower production within inflorescences?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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1.5 m tall, with considerable lateral branching) to larger, treelike species (S. quitoense, >3 m tall, with minimal lateral branching). Flower size and production also varied considerably. Flower production ranged from 5 or 6 flowers per inflorescence for S. pseudolulo and S. ferox (Whalen et al., 1981; J. S. Miller and P. K. Diggle, unpublished data) to >10 flowers per inflorescence for S. candidum and S. quitoense. Flowers from S. quitoense were also 60–80% larger compared to the other species. Seed for S. candidum was obtained from L. Bohs (University of Utah, Salt Lake City, Utah, USA) and was collected from La Cangreja Reserve in Costa Rica (Bohs no. 98–104). Solanum ferox var. lasiocarpum was collected from Indonesia (M. Ansyar 9605), and seed was obtained from C. Heiser (University of Indiana, Bloomington, Indiana, USA). The Botanical Garden of Nijmegen, Netherlands, provided seed for S. pseudolulo (accession no. 824750021). Seed for S. quitoense was acquired in Quito, Ecuador by C. Heiser. Voucher specimens for all species are housed at the University of Colorado herbarium (COLO).
Experimental design
Plants were grown from seed and clonally replicated by vegetative cuttings to produce genetically identical plants. For Solanum candidum, S. pseudolulo, and S. quitoense, four replicate clones were produced from either six (S. pseudolulo) or eight (S. candidum, S. quitoense) genotypes for a total of 88 plants. For S. ferox, six genotypes were used, and eight replicate clones were produced per genotype (8 clones x 6 genotypes = 48 plants). All plants were grown in 11-L (3-gal) pots containing a 2 : 1 mix of Fafard Growing Mix #2 (Conrad Fafard, Agawam, Massachusetts, USA) to Persolite (Persolite Products, Florence, Colorado, USA) plus Osmocote 13-13-13 slow-release fertilizer (Scotts Company, Marysville, Ohio, USA). Plants were watered daily with 150–200 ppm of Excel Magnitrate fertilizer (Scotts Company). Two (S. candidum, S. pseudolulo, S. quitoense) or four (S. ferox) replicates for each genotype were randomly assigned positions in each of two greenhouse rooms (110 and 111), and within each room these replicates were randomly assigned a fruiting treatment: +Fruit or –Fruit.
An important determinant of plant resource status is fruit set; plants with developing fruit have fewer resources available for growth and continued reproduction than plants with no developing fruit (Lloyd, 1980
). Because inflorescences are produced continuously, fruits, flowers, and flower buds occur simultaneously on each branch, and experimental manipulation of plant fruiting status is an effective, biologically relevant way to manipulate resource status. For plants in the +Fruit treatment, all open hermaphroditic flowers were pollinated every other day using a mixture of pollen collected from several (
3 genotypes) conspecific pollen donors. Hermaphroditic flowers remained open for 2–3 d; therefore, most flowers were pollinated at least twice, thus maximizing the potential for successful fertilization. In contrast, no flowers were pollinated on plants in the –Fruit treatment and any autogamously produced fruits were removed shortly after their initiation. Autogamous fruit production was rare in S. ferox, S. pseudolulo, and S. quitoense, but occurred occasionally in S. candidum.
Plants of these species have a predictable architecture; branches are sympodial and produce inflorescences sequentially and continuously. Two branches on each plant were haphazardly selected and censused every other day. Inflorescences were numbered from the base of the branch such that basal, early-developing inflorescences were numbered first. Floral positions within inflorescences were numbered distally from the basal-most position. Inflorescence position, flower position, floral sexual phenotype (i.e., hermaphroditic or staminate), and fruit production (+Fruit treatment only) were recorded for all flowers on 10 inflorescences on each of two marked branches per individual. Hermaphroditic flowers are easily distinguished from staminate flowers by their larger size and long-exserted styles that exceed the anthers (Whalen et al., 1981; Whalen and Costich, 1986
; Diggle, 1991
; J. S. Miller and P. K. Diggle, unpublished data). The experiment continued from July 2000 until May 2001 for S. candidum, S. pseudolulo, and S. quitoense and from September 2001 to March 2002 for S. ferox.
Statistical analyses
To determine the effects of fruiting treatment and inter-inflorescence ontogeny on sexual expression, we first calculated the proportion of staminate flowers produced within each inflorescence for all inflorescences on marked branches. Proportions were arcsin-square-root transformed and analyzed as a repeated measures design using either PROC MIXED (S. candidum, S. ferox, and S. quitoense; Littell et al., 1996
) or PROC GLM (S. pseudolulo; Littell et al., 1991
) in SAS. Because inflorescence production occurred over time along branches, the repeated measure in these analyses was the proportion of staminate flowers produced within inflorescences, which were numbered from the earliest inflorescence (=1) to the last inflorescence (=10) along each branch. In the PROC MIXED analyses, effects included in the model were fruiting treatment (overall phenotypic plasticity), genotype, greenhouse room (overall block effect), inflorescence position (inter-inflorescence effect), and all interaction terms; the interactions of importance to our interpretation were genotype by treatment (genotypic variation for plasticity) and inflorescence by treatment (plasticity of inter-inflorescence variation). Because the PROC MIXED model was not appropriate for analysis of S. pseudolulo (i.e., the maximum likelihood model did not fit the observed data), we used PROC GLM to analyze data for this species. This model included fruiting treatment, genotype, greenhouse room, and all interactions as between-subject effects, as well as inflorescence position as the within-subjects effect. All of the interaction terms with inflorescence position were also included. Because PROC GLM excludes data from subjects with missing data, we included data from only the first eight inflorescences of S. pseudolulo.
For each species, we determined the effect of intra-inflorescence architectural variation on sexual expression by calculating the probability of producing a staminate flower at each floral position averaged over all inflorescence positions. Hermaphroditic flowers were assigned the number 0 and staminate flowers were assigned the number 1, and these values were averaged for each floral position within inflorescences. We used nonparametric Kendall rank correlations to determine if the probability of producing a staminate flower increased with increasing floral position within inflorescences.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plasticity of sexual expression and variation among genotypes
Plasticity of sexual expression differed among species. Solanum candidum and S. ferox were phenotypically plastic; individuals of S. candidum and S. ferox with developing fruit produced significantly more staminate flowers than genetically identical individuals lacking fruit (Fig. 1). The fruiting treatment by greenhouse room interaction was significant for S. candidum (F1,31 = 5.54, P = 0.025). This interaction reflects the difference between fruiting treatments in the two greenhouse rooms: the +Fruit plants produced 6% more staminate flowers than –Fruit plants in room 110 and 19% more in room 111. Nevertheless, when greenhouse rooms were analyzed separately for S. candidum, staminate flower production was significantly higher for the +Fruit treatment compared to the –Fruit treatment in each room (room 110, F1,15 = 17.01, P = 0.0009; room 111, F1,16 = 23.91, P = 0.0002). In contrast to S. candidum and S. ferox, S. pseudolulo and S. quitoense were not plastic; staminate flower production did not depend on fruiting status (Fig. 1).
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Inter-inflorescence effects
Inflorescence position had a strong and significant effect on staminate flower production for all four species. In S. candidum and S. ferox, the inflorescence effect depended on the fruiting treatment, and there was a significant inflorescence by treatment interaction for these species (S. candidum, F9,197 = 8.10, P = 0.0001; S. ferox, F9,535 = 3.99, P = 0.0001). Staminate flower production in the –Fruit treatment changed little (<15%) in successive inflorescences, whereas in the +Fruit treatment staminate flower production increased dramatically with inflorescence position (73% in S. candidum and 44% in S. ferox; Fig. 3A, B). For S. pseudolulo and S. quitoense, inflorescences in more distal positions produced significantly more staminate flowers (S. pseudolulo, F7,63 = 10.84, P = 0.0001; S. quitoense, F9,158 = 6.69, P = 0.0001; Fig. 3C, D); however, there were no significant interactions between inflorescence position and fruiting treatment for either species.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Andromonoecy in Solanum section Lasiocarpa
The degree of andromonoecy differs widely among species in Solanum section Lasiocarpa. Choice of the appropriate metric for quantitative comparison among the species, however, is problematic. Although the –Fruit treatment may not be realistic in natural populations, we argue that comparisons among species should be made using the –Fruit treatment because patterns of sexual expression using data from plants without fruit measures their inherent tendency to produce staminate flowers. In addition, the –Fruit treatment is equivalent across species, whereas the +Fruit treatment may differ among species due to differential fruit production or fruit size. It should be noted, however, that the rank order of the strength of andromonoecy is the same regardless of the measure used for comparison (Fig. 1).
In the absence of fruit production, S. candidum and S. ferox (this study) and S. hirtum (Diggle, 1993
) produce few staminate flowers (3%, 7%, and <1%, respectively; Fig. 1), and therefore should be considered weakly andromonoecious. In contrast, even in the absence of fruit production, S. quitoense is strongly andromonoecious and produces nearly 60% staminate flowers per inflorescence. Solanum pseudolulo is intermediate and produces 39% staminate flowers (Fig. 1). Although all of these species are typologically andromonoecious and are capable of producing both hermaphroditic and staminate flowers, they differ dramatically in the magnitude of expression of this sexual system, despite sharing a common origin of andromonoecy.
Plasticity in Solanum section Lasiocarpa
Plasticity of allocation to male and female function generally is thought to be an important component of the evolution of andromonoecy (reviewed in Bertin, 1982a
) and is clearly the mechanism by which staminate flower production occurs in S. hirtum (Diggle, 1993
). Yet, analyses of four additional species of Lasiocarpa reveal that staminate flower production is a phenotypically plastic response to fruit production in S. candidum and S. ferox, but is a fixed aspect of the phenotype in S. quitoense and S. pseudolulo (Fig. 1). Thus, andromonoecy and the production of staminate flowers in Lasiocarpa is not inevitably a plastic response to the presence of developing fruit.
The presence or absence of plasticity per se appears to be associated with differences in the strength of andromonoecy: plastic species are weakly andromonoecious, whereas staminate flower production is fixed in strongly andromonoecious species. Considering only the plastic species, we cannot determine whether variation in the magnitude of plasticity (the difference in staminate flower production between the two treatments) is associated with variation in the degree of andromonoecy; plasticity and the degree of andromonoecy are similar among S. ferox, S. candidum, and S. hirtum. Thus, although plasticity is a mechanism for staminate flower production by some taxa within Lasiocarpa, differences in plasticity do not underlie the observed variation in andromonoecy.
Our results demonstrate that analyses of phenotypic plasticity are always context specific. Although the four species differed in their capacity to respond to the fruiting treatment, they all responded plastically to the different environmental conditions of the two greenhouse rooms. All species produced more staminate flowers in greenhouse room 111 compared to room 110, significantly so for S. candidum, S. ferox, and S. pseudolulo. The two rooms are physically adjacent to each other and both maintained a mean temperature of 21°C. However, room 111 was significantly more shaded than room 110 (159.0 ± 13.0 µmol vs. 264.3 ± 33.4 µmol, respectively; F1,98 = 8.6, P = 0.004). Studies of other andromonoecious species have shown that decreased light is associated with staminate flower production (Aesculus pavia, Bertin, 1982b
; Solanum carolinense, Solomon, 1985
). In addition, population sex ratios in some diphasic orchids are female biased in open habitats and male biased in closed canopies (Gregg, 1975
, 1978
; Zimmerman, 1991
). The intuitive (but untested) explanation is that plants growing under increased light have greater photosynthate availability and thus an enhanced ability to mature fruit. It would be advantageous for plants under such conditions to produce hermaphroditic flowers. Whatever the proximate cue, staminate flower production differed significantly among rooms and represents a distinct form of plasticity in sexual expression.
Architectural effects on sexual expression in section Lasiocarpa
All species of Lasiocarpa investigated bear staminate flowers in a predictable pattern that encompasses both within- and among-inflorescence variation. At the level of branches, a greater proportion of staminate flowers are borne in later-produced inflorescences. For S. candidum and S. ferox, much of this pattern is the result of plastic changes in sexual expression in response to fruiting treatment. Staminate flower production in basal inflorescences of plants in the –Fruit treatment was near zero and remained less than 15% even in the distal-most inflorescences. Among inflorescences of plants in the +Fruit treatment, however, staminate flower production increased by over 40% from basal to distal inflorescences (Fig. 3A, B). A similar pattern of inter-inflorescence variation in association with plasticity occurred in S. hirtum (Diggle, 1993
). This pattern of increased staminate flower production in successive inflorescences is consistent with a plastic response by developing flowers to the presence of maturing fruit at earlier (more basal) inflorescence positions.
Staminate flower production in the nonplastic species, S. pseudolulo and S. quitoense, also increases in distal inflorescences (Fig. 3C, D); however, this pattern is not dependent on fruiting treatment, rather, it is a fixed aspect of the architecture of each branch. The pattern of inter-inflorescence increase in the proportion of staminate flowers in the nonplastic species is qualitatively similar to that of fruit-bearing plants of the plastic species (S. candidum and S. ferox; Fig. 3), though staminate flower production commences at earlier (more basal) inflorescences in the nonplastic species. For example, the first inflorescence bears 20% (S. pseudolulo) to 40% (S. quitoense) staminate flowers in nonplastic species compared to near zero in the plastic species (compare Fig. 3A, B to C, D). Strong andromonoecy exhibited by S. pseudolulo and S. quitoense is due, in part, to the onset of staminate flower production at early inflorescence positions.
Within inflorescences of each of the four species, staminate flowers can be produced at all floral positions; however, the probability is very low at basal positions and increases distally (Fig. 4). Thus, the general pattern is one of hermaphroditic flowers in basal positions, and staminate flowers, if produced, in terminal portions of each inflorescence. Although the pattern is qualitatively similar, there are quantitative differences in the average intra-inflorescence pattern of staminate flower production among the four species and between treatments of the plastic species. Two indices can be used for comparison: the flower position at which the probability of producing a staminate flower exceeds 50% (dotted line in Fig. 4) and the probability of staminate flower production in the distal-most positions. In inflorescences of the strongly andromonoecious species, S. quitoense and S. pseudolulo, staminate flower production occurs early (>50% probability by flower position 4–5) and, in the distal-most positions, the probability of staminate flowers exceeds 80% (Fig. 4C, D). In contrast, in weakly andromonoecious S. ferox, staminate flower production does not exceed 50% until flower position 7 in fruit-bearing plants and never exceeds 50% in nonfruiting plants (Fig. 4B). In S. candidum, despite a distal increase in staminate flower production, the average probability never exceeds 50% at any position in either treatment (Fig. 4A). Thus, within inflorescences, strong andromonoecy is associated with an earlier transition from hermaphroditic to staminate flower production and a greater probability of staminate flowers in distal-most positions.
The preceding analysis considers the intra-inflorescence pattern averaged across all 10 inflorescences per branch (Fig. 4). While this summary allows for explicit quantitative comparisons, it obscures the significant variation in staminate flower production among inflorescences. Figure 5 depicts the combined effects of both sources of variation in sexual expression: intra- and inter-inflorescence architectural effects. This representation confirms that staminate flowers are produced distally within inflorescences and that the transition from hermaphroditic to staminate flower development occurs at more basal floral positions within later, more distal inflorescences. Moreover, Fig. 5 emphasizes that strong andromonoecy is the result of an earlier transition from hermaphroditic to staminate flower production both within and among inflorescences. For example, the strongly andromonoecious S. quitoense bears staminate flowers on the first inflorescence, and within that inflorescence, the transition to staminate flowers occurs at flower position six (Fig. 5D). In contrast, the weakly andromonoecious species produce staminate flowers at later inflorescences (2 or 5) and later flower positions (8 or 11; S. ferox and S. candidum, respectively; Fig. 5A, B). These comparisons indicate that diversification of andromonoecy has occurred by quantitative variation in both inter- and intra-inflorescence positional effects on floral development.
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predicted that strong andromonoecy would not be associated with the production of excess staminate flowers. Comparisons among more closely related species shows this to be incorrect. Clearly, the addition of flowers, which are predominantly staminate, increases the degree of andromonoecy for S. quitoense (Fig. 5D).
Implications for andromonoecy in Solanum
Quantitative variation within an otherwise uniform architectural pattern appears to underlie differences in sexual expression within Solanum section Lasiocarpa. This model may be extended to other members of the genus. General branching architecture (sensu Hallé et al., 1978
) is quite uniform throughout the genus Solanum: branches grow sympodially with each sympodial unit bearing a characteristic number of leaves and terminating in an inflorescence (Child, 1979
; Child and Lester, 1991
). Thus, each leafy branch produces an indeterminate succession of inflorescences and typically bears fruits, flowers, and floral primordia simultaneously. Within the genus, andromonoecy has evolved and diversified within the context of this stereotypical morphology. In all described andromonoecious Solanum (belonging to different sections or even to different subgenera and likely representing more than one origin of andromonoecy), staminate flowers occur predominantly in distal positions within inflorescences (S. torvum, Hossain, 1973
; S. sodomeum and S. campanulatum, Symon, 1979
; S. marginatum, Dulberger et al., 1981
; section Lasiocarpa, Whalen et al., 1981; S. paliacanthum, Coleman and Coleman, 1982
; S. carolinense, Solomon, 1985
; references to additional species in Whalen and Costich, 1986
and Anderson and Symon, 1989
). Other patterns of staminate flower production, for example, basal staminate and distal hermaphroditic flowers within inflorescences or the production of exclusively hermaphroditic and exclusively staminate inflorescences within the same branch, have never been described for Solanum. Based on these observations, it is likely that what variation in sexual expression exists among andromonoecious species of the genus as a whole depends on the types of quantitative variation in architectural effects described here for section Lasiocarpa.
Architectural effects may also have played a critical role in the evolutionary transition from hermaphroditism to andromonoecy in Solanum. In many hermaphroditic species (regardless of taxon), fruit set is reduced or absent at distal positions within inflorescences (reviewed in Diggle, 1995
, 2002
); thus, many hermaphroditic taxa are functionally andromonoecious. Intra-inflorescence variation in female function has not been investigated explicitly in hermaphroditic species of Solanum; however, fruit size declines dramatically within inflorescences of cultivated tomato (Bertin, 1995
), and distal hermaphroditic flowers in species of section Lasiocarpa rarely set fruit (P. K. Diggle, personal observation). Within Solanum, intra-inflorescence declines in female function may be an evolutionary antecedent of andromonoecy. If so, then the transition from functional to morphological andromonoecy would require only the origin of a developmental mechanism for pre-anthesis termination of ovary development in flowers that are already functionally female-sterile.
Evolutionary dynamics of plasticity
Although variation in the magnitude of plasticity may not underlie species-level variation in andromonoecy, we found variation in plasticity per se. Within the small section Lasiocarpa, staminate flower production is a phenotypically plastic response to fruit production in some species and a fixed aspect of the phenotype in others. Interestingly, the architectural pattern of staminate flower production is qualitatively similar in nonplastic species and fruit-bearing plants of the plastic species. There is a transition from hermaphroditic to staminate flower production within each inflorescence, and this transition occurs earlier (at more basal positions) on successive inflorescences. Thus, it is qualitatively the same phenotype that is fixed in some species and produced as a plastic response to fruit set in others. The pressing issue for future research is to understand the sequence of evolutionary transitions between these phenotypes. Because andromonoecy is typically assumed to be a form of plasticity, traditional hypotheses would predict that andromonoecy arose in the ancestor of Lasiocarpa as a plastic response and has become a fixed developmental pattern in some species.
We also found an association between weak andromonoecy and plasticity and between strong andromonoecy and fixed phenotypes. The association between plasticity and the degree of andromonoecy may be related to developmental constraints imposed by the architecture of Solanum. Given that inflorescences invariably contain both hermaphroditic and staminate flowers, an effective way to increase staminate flower production is to produce staminate flowers at earlier (more basal) positions both within and among inflorescences. Moreover, for the plastic species, if initiation of fruit development is the proximate cue for staminate flower development, then the production of staminate flowers will not be possible until later in branch ontogeny after significant numbers of fruit producing hermaphroditic flowers have developed. Hence, plastic plants may necessarily produce more hermaphroditic flowers relative to staminate flowers and will be classified as weakly andromonoecious.
Conclusions
That flowering plants as a group possess an enormous diversity of sexual systems is well known (Darwin, 1877
). Surprisingly, the expression of a single sexual system can vary widely, even among members of a small clade. Andromonoecy has been defined typologically as a single phenotype, that is, the presence of both hermaphroditic and staminate flowers on individual plants. Analysis of Solanum section Lasiocarpa shows that andromonoecy clearly varies among species. The common ancestor of these species was likely andromonoecious, thus the variation documented here represents evolutionary diversification from a single "andromonoecious phenotype." At least three factors contribute to the diversification of sexual expression in this group, including the presence or absence of phenotypic plasticity in response to fruit set, intra- and inter-inflorescence architectural effects, and total flower production. Consideration of the stereotypical branching architecture of the genus Solanum and the recurring intra- and inter-inflorescence pattern of staminate flower production among all andromonoecious species indicates that these factors may also have been important in the evolutionary dynamics of andromonoecy in the genus as a whole.
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FOOTNOTES |
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2 Author for reprint requests, current address: Department of Biology, Amherst College, Amherst, Massachusetts USA (Tel. 413-542-2168; FAX 413-542-7955; jsmiller{at}amherst.edu
)
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LITERATURE CITED |
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Bernardello L. M. C. B. Heiser M. Piazzano 1994 Karyotypic studies in Solanum section Lasiocarpa (Solanaceae). American Journal of Botany 81: 95-103[CrossRef][ISI]
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Bertin R. I. 1995 Competition for assimilates and fruit position affect fruit set in indeterminate greenhouse tomato. Annals of Botany 75: 55-65
Bruneau A. E. E. Dickson S. Knapp 1995 Congruence of chloroplast DNA restriction site characters with morphological and isozyme data in Solanum sect. Lasiocarpa. Canadian Journal of Botany 73: 1151-1167[CrossRef]
Child A. 1979 A review of branching patterns in the Solanaceae. In J. G. Hawkes, R. N. Lester, and A. D. Skelding [eds.], The biology and taxonomy of the Solanaceae, 345–356. Academic Press, London, UK
Child A. R. N. Lester 1991 Life form and branching within the Solanaceae. In J. G. Hawkes, R. N. Lester, M. Nee, and N. Estrada [eds.], Solanaceae III: taxonomy, chemistry, evolution. Royal Botanic Gardens Kew and Linnean Society, London, UK
Coleman J. R. M. A. Coleman 1982 Reproductive biology of an andromonoecious Solanum (S. paliacanthum Dun). Biotropica 14: 69-75
Darwin C. 1877 The different forms of flowers on plants of the same species. Murray, London, UK
Diggle P. K. 1991 Labile sex expression in andromonoecious Solanum hirtum: pattern of variation in floral structure. Canadian Journal of Botany 69: 2033-2043[ISI]
Diggle P. K. 1993 Developmental plasticity, genetic variation, and the evolution of andromonoecy in Solanum hirtum (Solanaceae). American Journal of Botany 80: 967-973[CrossRef][ISI]
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