Zygomorphy and Heteranthery in Solanum in a Phylogenetic Context

The majority of species in the large genus Solanum (ca. 1500 species) have five-merous, radially symmetrical flowers with equal stamens. However, some Solanum species and groups are characterized by four-merous and/or zygomorphic flowers, unequal stamens and enantiostyly (styles deflected to one side of the flower). Previous workers have used flower and seed coat morphology in these unusual Solanum species as a guide to interpreting their evolutionary relationships. However, the phylogenetic position of the zygomorphic and heterantherous solanums is only beginning to be examined using molecular data and cladistic methodology. DNA sequence data from both the chloroplast and nuclear genomes are used to infer the phylogenetic position of Solanum taxa with variously modified flowers. Zygomorphy and heteranthery have evolved multiple times within Solanum, and most frequently within the spiny solanums (Solanum subg. Leptostemonum). The phylogenies shed light on the disparate morphologies and geographical distributions encountered in the zygomorphic and heterantherous species and pinpoint the likely relatives of these taxa among the actinomorphic Solanum species with equal stamens. INTRODUCTION Solanum, with approximately 1500 species, is the largest genus in the Solanaceae and one of the largest genera of flowering plants (Frodin, 2004). In general, Solanum flowers are easily recognized by their five-merous, radially symmetrical flowers with equal (isantherous) stamens that dehisce by terminal pores. The flowers are adapted for buzz pollination by bees, which vibrate the anthers using their indirect flight muscles and in turn cause pollen to discharge in a stream from the pores (Buchmann, 1983). Within the Solanaceae, only the genus Lycianthes also exhibits poricidal anther dehiscence, and in most cases, it can be readily distinguished from Solanum by differences in calyx structure (D’Arcy, 1986). A number of Solanum taxa have modified the stereotypical Solanum flower ground plan to exhibit such unusual floral features as four-merous and/or zygomorphic flowers, unequal stamens, and enantiostyly (styles deflected to one side of the flower in a leftor right-handed arrangement). Heteranthery (the presence of highly unequal stamens in a single flower; also called heterandry in previous Solanum literature) is a particularly notable feature that occurs in many Solanum lineages. In Solanum, differences in overall stamen size can be due to differences in filament length, anther length, or both. In some cases, these morphological modifications are so striking that they have led previous taxonomists to exclude these species from Solanum. For example, species with highly heterantherous and often zygomorphic flowers were segregated into the genera Normania Lowe, Nycterium Venten., and Androcera Nutt. (Whalen, 1984; Lester et al., 1999; Francisco-Ortega et al., 1993), although these genera are now subsumed within Solanum (Whalen, 1979, 1984; Bohs and Olmstead, 2001). The occurrence of unusual floral features within various Solanum lineages and related genera is mapped onto a summary cladogram derived from Weese and Bohs (2007) in Fig. 1. The evolution of derived floral morphologies in Solanum was most comprehensively examined by Lester et al. (1999), who used SEM studies of pollen VI International Solanaceae Conference Eds.: D.M. Spooner et al. Acta Hort. 745, ISHS 2007 201 grains and seed surface features to determine whether the heterantherous Solanum species form a natural group, examined biogeographic patterns among the heterantherous solanums, and attempted to identify the sister groups to the heterantherous taxa. The work reported here focuses on the same key species groups identified in Lester et al. (1999) and builds on this foundation by analyzing most of these species in a phylogenetic framework using DNA sequence data. Our results are compared to those of Lester et al. (1999) and in some cases extend beyond their paper to suggest well supported sister relationships between heterantherous and isantherous Solanum species. We also evaluate the biogeographic patterns of the heterantherous species in a phylogenetic context and suggest further morphological and molecular studies that will elucidate evolutionary and developmental patterns in these taxa. TAXA STUDIED Within Solanum, several groups exhibit striking degrees of heteranthery, often accompanied by other floral modifications such as zygomorphy and enantiostyly. Lester et al. (1999) focused on four Solanum groups that show strong heteranthery: 1) the Normania group, 2) the Androceras group, 3) the Anisantherum and Monodolichopus group, and 4) the Nycterium group. In our study, we included representatives of as many of these groups as possible, along with isantherous species hypothesized to be their closest relatives. We also included S. thelopodium, a member of the S. thelopodium species group of Knapp (2000). Flowers in this group are highly heterantherous but these species were not examined by Lester et al. (1999). Floral morphologies, breeding systems (here defined as the presence of self-compatibility vs. self-incompatibility), and previous ideas of relationships are summarized below and in Table 1 for the five focal groups. Illustrations of representative flowers of heterantherous Solanum species and their relatives are given in Figs. 2 and 3. Focal Groups in the Non-Spiny Solanums 1. Solanum thelopodium Species Group. This group includes three non-spiny species of South American primary rainforest shrubs. These species were neglected until Knapp’s recent treatment, in which two of the three species were newly described (Knapp, 2000). Although these taxa are obviously closely related, they have not been properly placed in any of the published Solanum sections (see Knapp, 2000 for a summary of the taxonomic and nomenclatural history of the group). The flowers are five-merous with actinomorphic corollas. The androecium is highly heterantherous with a unique combination of stamen morphologies (Fig. 2A). The lowermost stamen is longest due to its very long anther and filament. The uppermost stamens are shortest and the middle two stamens are intermediate in length, with the length difference due mainly to differences in filament length (Knapp, 2000). The style is straight and extends through the groove between the anther thecae of the longest and lowermost stamen. There is no evidence of andromonoecy in this group, and breeding systems of the three species are unknown. 2. Normania Clade. This monophyletic group encompasses three species formerly placed in the genera Normania and Triguera. All were reinstated in or transferred to Solanum by Bohs and Olmstead (2001) when they were found to form a clade nested within the genus. Solanum trisectum and S. nava Webb & Berthel. (former members of genus Normania) are native to Macaronesia, whereas S. herculeum (former genus Triguera) is found in nearby areas of Spain and northwestern Africa. All are five-merous, with actinomorphic to slightly zygomorphic corollas and unusual floral morphologies, but the flowers of S. herculeum are quite different from those of the other two species. In this species, the anthers are equal or subequal and each is tipped by two small apical horns (Fig. 2E). They dehisce initially by two subapical pores that enlarge into longitudinal slits with age. Breeding systems and pollination biology have not been investigated in this species. In contrast, the androecium of Solanum trisectum and S. nava is highly heterantherous, with two long curved anthers, two medium-sized curved anthers, and one short relatively straight anther (Fig. 2D). The shortest stamen is lowermost in the flower,