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Solanaceae): the Roles of Phenotypic Plasticity and Architecture1

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Solanaceae): the Roles of Phenotypic Plasticity and Architecture1 American Journal of Botany 90(5): 707±715. 2003. DIVERSIFICATION OF ANDROMONOECY IN SOLANUM SECTION LASIOCARPA (SOLANACEAE): THE ROLES OF PHENOTYPIC PLASTICITY AND ARCHITECTURE1 JILL S. MILLER2 AND PAMELA K. DIGGLE Department of Environmental, Population, and Organismic Biology, University of Colorado, Campus Box #334, Boulder, Colorado 80309 USA Quantitative analyses of sexual expression show extensive interspeci®c variation in the strength of andromonoecy (proportions of hermaphroditic and staminate ¯owers) among Solanum species in the monophyletic section Lasiocarpa. The roles of phenotypic plasticity and inter- and intra-in¯orescence architecture in the diversi®cation of andromonoecy within this small clade were analyzed. Four species that represent a range of expression of andromonoecy were examined. Staminate ¯owers produced within in¯orescences ranged from 3% (S. candidum)to7%(S. ferox) in weakly andromonoecious species and from 39% (S. pseudolulo) to 60% (S. quitoense) in more strongly andromonoecious species. Manipulation of fruit set on clonal replicates of multiple genotypes demonstrated variation among species for phenotypic plasticity. The strongly andromonoecious species, S. pseudolulo and S. quitoense, were not plastic and produced a large proportion of staminate ¯owers regardless of fruiting treatment, whereas S. candidum and S. ferox were phenotypically plastic and produced signi®cantly more staminate ¯owers in the presence of developing fruit. Staminate ¯ower production of all four species varied both within and among in¯orescences. A greater proportion of staminate ¯owers were produced in distal (later produced) in¯orescences. Within in¯orescences, hermaphroditic ¯owers occurred in basal positions, whereas staminate ¯owers, when produced, occurred more distally. This pattern of staminate ¯ower production is qualitatively the same in all species investigated; however, quantitative variation in the transition from hermaphroditic to staminate ¯ower production within and among in¯orescences is associated with variation in the strength of andromonoecy. At least three factors have contributed to the diversi®cation of andromonoecy in section Lasiocarpa including the presence or absence of phenotypic plasticity in response to fruit set, quantitative variation in intra- and inter-in¯orescence architectural effects, and total ¯ower production. Key words: andromonoecy; architecture; development; phenotypic plasticity; sexual systems; Solanaceae; Solanum. Andromonoecy has historically been de®ned as a sexual novation of developmental mechanisms that allow for the pro- system in which plants produce both hermaphroditic and fe- duction of two distinct ¯oral types. Comparative developmen- male-sterile (hereafter, staminate) ¯owers. Andromonoecy oc- tal and morphological analyses of closely related species that curs in approximately 4000 species of ¯owering plants from vary in the magnitude of andromonoecy (i.e., in the relative at least 33 families (21 listed in Yampolsky and Yampolsky, production of hermaphroditic and staminate ¯owers) can iden- 1922; references for additional families available on request) tify those features that have been modi®ed in association with and has clearly evolved independently in numerous plant lin- the evolution and diversi®cation of this sexual system. Once eages. Considerable attention has focused on the adaptive sig- we understand how complex phenotypes such as andromon- ni®cance of andromonoecy (Bertin, 1982a; Whalen and Cos- oecy evolve, we can create and test more re®ned hypotheses tich, 1986; Anderson and Symon, 1989; Spalik, 1991; Diggle, for why they evolve. 1993, 1994; Emms, 1996; Emms et al., 1997). Andromonoecy In the plant family Solanaceae, andromonoecy is well doc- is widely thought to provide a mechanism to independently umented in Solanum subgenus Leptostemonum and has been adjust allocation to male and female function; individuals are reported for 13 of 22 described sections (Whalen and Costich, assumed to vary production of hermaphroditic and staminate 1986). Lasiocarpa is a small section of 12 species, within sub- ¯owers in response to changes in resource availability (re- genus Leptostemonum, that is strongly supported as monophy- viewed in Bertin, 1982a; but see Podolsky, 1993). Thus, an- letic based on morphological, allozyme, karyotype, and chlo- dromonoecy is often considered a form of phenotypic plastic- roplast restriction site data (Heiser, 1972, 1987; Whalen and ity. Regardless of the particular advantages of andromonoecy, Caruso, 1983; Bernardello et al., 1994; Bruneau et al., 1995). however, the evolution of this sexual system requires the in- Although all members of Lasiocarpa are andromonoecious, the numbers of hermaphroditic and staminate ¯owers produced 1 Manuscript received 6 August 2002; revision accepted 6 December 2002. among species in this section varies considerably (Whalen et The authors thank C. Heiser, L. Bohs, and the Botanical Garden of Nij- al., 1981). Some species are characterized as weakly andro- megen for seed accessions; T. Lemieux for providing valuable advice and monoecious (e.g., S. hirtum Vahl., Diggle, 1993; S. stramon- support regarding greenhouse space; H. Bechtold and K. Ryerson for assisting with data collection; R. Khorsand, T. Forbis, C. McGraw, and M. Allsop for ifolium Jacq., Whalen et al., 1981); that is, plants produce rel- assistance in the greenhouse; V. Ebbert for the use of a light meter; the De- atively few staminate ¯owers. In contrast, other species bear partment of E. P. O. Biology at the University of Colorado for greenhouse many staminate ¯owers and are described as strongly andro- space; and R. A. Levin and members of the Diggle and Friedman laboratory monoecious (e.g., S. quitoense Lam., Whalen and Costich, group for comments on earlier drafts of the manuscript. This work was sup- 1986; S. vestissimum Dunal., Whalen et al., 1981). The diver- ported by grants from the University of Colorado and the National Science sity of sexual expression among species in section Lasiocarpa Foundation DEB 9982489 to P.K.D. 2 Author for reprint requests, current address: Department of Biology, Am- makes this an ideal group for comparative analyses. herst College, Amherst, Massachusetts USA (Tel. 413-542-2168; FAX 413- Detailed investigation of Solanum hirtum (section Lasio- 542-7955; e-mail: [email protected]). carpa) has shown that sexual expression is phenotypically 707 708 AMERICAN JOURNAL OF BOTANY [Vol. 90 plastic; fruit-bearing plants produce a greater proportion of Lasiocarpa of Solanum subgenus Leptostemonum. All members of section staminate ¯owers than genetically identical plants that are pre- Lasiocarpa are sexually reproducing, self-compatible, and andromonoecious, vented from producing fruit (Diggle, 1993). Because fruit de- producing both hermaphroditic and staminate ¯owers (Whalen et al., 1981). velopment poses a signi®cant drain on resources available for The four species included were chosen to incorporate variation within section continued development (Lloyd, 1980), plasticity of sexual ex- Lasiocarpa. For example, vegetative size ranged from small, bushy species pression in S. hirtum is consistent with hypotheses for the evo- (S. pseudolulo, ;1.5 m tall, with considerable lateral branching) to larger, lution of andromonoecy that suggest that the production of treelike species (S. quitoense, .3 m tall, with minimal lateral branching). staminate ¯owers is a mechanism for adjusting allocation to Flower size and production also varied considerably. Flower production male and female function. As continued fruit production be- ranged from 5 or 6 ¯owers per in¯orescence for S. pseudolulo and S. ferox comes resource-limited, subsequent production of staminate (Whalen et al., 1981; J. S. Miller and P. K. Diggle, unpublished data) to .10 ¯owers allows reallocation of resources away from ``costly'' ¯owers per in¯orescence for S. candidum and S. quitoense. Flowers from S. quitoense were also 60±80% larger compared to the other species. gynoecia toward increased male function, vegetative growth, Seed for S. candidum was obtained from L. Bohs (University of Utah, Salt or storage (reviewed in Bertin, 1982a; Whalen and Costich, Lake City, Utah, USA) and was collected from La Cangreja Reserve in Costa 1986; Spalik, 1991). These analyses of S. hirtum indicate that Rica (Bohs no. 98±104). Solanum ferox var. lasiocarpum was collected from consideration of plasticity should be integral in comparative Indonesia (M. Ansyar 9605), and seed was obtained from C. Heiser (Univer- studies of the expression of andromonoecy in section Lasio- sity of Indiana, Bloomington, Indiana, USA). The Botanical Garden of Nij- carpa. megen, Netherlands, provided seed for S. pseudolulo (accession no. To compare andromonoecy and developmental plasticity 824750021). Seed for S. quitoense was acquired in Quito, Ecuador by C. among species, sexual expression must be characterized at Heiser. Voucher specimens for all species are housed at the University of multiple levels of morphological organization. In S. hirtum the Colorado herbarium (COLO). occurrence of staminate ¯owers varied both within and among in¯orescences. All in¯orescences on fruit-bearing plants pro- Experimental designÐPlants were grown from seed and clonally replicated duced both hermaphroditic and staminate ¯owers; however, by vegetative cuttings to produce genetically identical plants. For Solanum the proportion of staminate ¯owers increased in successively candidum, S. pseudolulo,
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