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Ontogenetic Origins of Floral Bilateral Symmetry in Moringaceae (Brassicales)1

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Ontogenetic Origins of Floral Bilateral Symmetry in Moringaceae (Brassicales)1 American Journal of Botany 90(1): 49–71. 2003. ONTOGENETIC ORIGINS OF FLORAL BILATERAL SYMMETRY IN MORINGACEAE (BRASSICALES)1 MARK E. OLSON2 Instituto de Biologı´a, U.N.A.M., Departamento de Bota´nica, Circuito exterior s/n, Ciudad Universitaria, Copilco, Coyoaca´n, A.P. 70-367 Me´xico, D.F., C.P. 04510, Mexico Floral morphology of the 13 species of Moringa ranges from actinomorphic flowers with little hypanthium to highly zygomorphic flowers with well-developed hypanthia. Scanning electron and light microscopy were used to identify ontogenetic differences among two actinomorphic and eight zygomorphic species. All species show traces of zygomorphy between petal organogenesis and anther differentiation. At late organogenesis, zygomorphy is manifest by one petal being larger than the others, slight unidirectional maturation of the anthers, and in many species, some staminodes may be missing. At organ differentiation and beyond, the actinomorphic species show a trend toward increasing actinomorphy, whereas the zygomorphic features of early ontogeny are progressively accentuated throughout the ontogeny of the zygomorphic species. Because of the early traces of zygomorphy throughout the family, ontogeny in Moringa does not resemble that known from the sister taxon Caricaceae, which has flowers that are actinomorphic throughout ontogeny. Great intraspecific variation was found in floral plan in the actinomorphic-flowered species in contrast to the zygomorphic species. Each of the main clades in the family is distinguished by at least one feature of floral ontogeny. In general, ontogenetic differences that are congruent with deeper phylogenetic splits tend to occur earlier in ontogeny than those congruent with more recent divergences. Key words: Brassicales; development; evolution; floral symmetry; homology; Moringa; ontogeny; phylogeny. Bilateral floral symmetry (zygomorphy) has repeatedly aris- and intermediate ontogenetic stages are as common as modi- en from ancestors with radially symmetrical (actinomorphic) fications to the terminal phases of ontogeny. flowers (Endress, 1999) and is a character of major systematic The 13 species of Moringa span the range from small, ac- significance. Likewise, floral symmetry is one of the primary tinomorphic, cream-colored flowers with little hypanthium, to factors determining the spectrum of pollinators that a flower highly zygomorphic, intensely colored flowers with pro- attracts (Dafni and Kevan, 1996). As a result of the importance nounced hypanthia (Figs. 1–13). Recent field work in dry trop- of this character, the evolutionary processes leading to sym- ical Asia, Africa, and Madagascar has made it possible to in- metry differences have received attention from a variety of clude ten of the 13 species in a comparative study of floral perspectives, from molecular genetics (Theissen, 2000; Shep- ontogeny with the following aims: (1) document floral orga- ard and Purugganan, 2002) to comparative morphological nogeny, anatomy, and ontogeny in Moringa, the only genus studies of ontogeny (e.g., Tucker, 1984, 1997, 2000). The latter in Moringaceae; (2) test the expectation that actinomorphic approach is particularly valuable when a phylogenetic hypoth- flowers in Moringa are entirely so in all stages, as in the the esis for the group in question is available, because the phy- sister group Caricacae (Ronse Decraene and Smets, 1999), and logeny can be used to identify the polarity of evolutionary that zygomorphy becomes manifest in the later stages of on- transformations within a clade. For example, Hufford (1995) togeny; (3) examine the congruence of ontogenetic characters evaluated his studies of comparative ontogeny in the snap- with a previous phylogenetic reconstruction (Fig. 14); and (4) dragon relative Besseya in the context of a phylogeny esti- examine the correlation of the timing of ontogenetic diver- mated from nonfloral data and arrived at the counterintuitive gences between species groups with degree of phylogenetic conclusion that evolutionary inversions and deletions of early relationship. Because perturbations to early ontogeny may drastically affect subsequent events, numerous workers (e.g., 1 Manuscript received 26 February 2002; revision accepted 11 June 2002. Takhtajan, 1972; Tucker, 1984, 1997) have suggested that early The author thanks Jessica Ingram for her remarkable assistance; Peter Ra- stages should be more evolutionarily conserved while later ven, Barbara Schaal, Mick Richardson, Walter Lewis, Jim Rodman, Louis stages are more evolutionarily labile. Therefore, divergences Ronse Decraene, Shirley Tucker, Jennifer Thorsch, and Peter Stevens for their in early ontogeny should characterize deep phylogenetic splits, encouragement and guidance; Mike Veith of the Washington University Mi- croscopy Facility for generous donations of time and film; David Odee, Joseph and divergences at later stages should characterize more recent Machua, Gilfrid Powys, Ambia A. Osman and Mohammed, Abdiaziz ‘‘Jack’’ evolutionary branching. Bashir, Halima Abdi Mohammed and Ahmad Salat Omar, Geoffrey Muluvi, Moringa flowers (Figs. 1–13) have five sepals, five petals, Hassan A. Sheikh, Shahina Ghazanfar, Martin Fisher, Sylvain Razafimandim- five antesepalous staminodes, and five antepetalous stamens bison, V. Amalan Stanley, and Fr. K. M. Mathew for their collaboration; Peter with monothecal, bisporangiate anthers. The ovary is borne Raven and Avinoam Danin for material of M. peregrina; Herta Kolberg for atop a gynophore of varying length, and the style is hollow. material of M. ovalifolia. Barbara Alongi produced the exquisite illustrations of mature flowers. Field and laboratory work were supported by grant number The four actinomorphic-flowered species, all massive pachy- 6141-98 from the Committee for Research and Exploration of the National caul trees, form a paraphyletic assemblage at the base of the Geographic Society, United States National Science Foundation Doctoral Dis- Moringa phylogeny (Fig. 14; Olson, 2002). Flowers in this sertation Improvement Award DEB-9801128, the Andrew Mellon Foundation, group (the ‘‘actinomorphic grade’’) are cream-colored with un- the Missouri Botanical Garden, and Washington University in St. Louis. Jes- reflexed sepals and petals that may be reflexed at anthesis (M. sica’s participation was made possible by the Young Scientist Program of Washington University. Three reviewers and the editors provided many help- drouhardii, Fig. 1; M. ovalifolia, Fig. 4) or may project for- ful suggestions. ward (M. hildebrandtii, Fig. 2; M. stenopetala, Fig. 3). The 2 E-mail address: [email protected]. nine zygomorphic-flowered species form a monophyletic 49 50 AMERICAN JOURNAL OF BOTANY [Vol. 90 Figs. 1–7. Flowers of all species in the actinomorphic grade and slender tree clades of Moringa. Side views unless specified. 1–4. Members of the actinomorphic grade showing actinomorphic or nearly actinomorphic arrangement of parts. 1. Moringa drouhardii Jum., apical and side views, showing reflexed petals, and bud showing irregular shape at base. 2. Moringa hildebrandtii Engl., showing slightly unequal filaments 3. Moringa stenopetala (Baker f.) Cufod., with details showing shallow and deep lobing of style apex. 4. Moringa ovalifolia Dinter & A. Berger. 5–7. Members of the slender tree subclade of the zygomorphic clade. 5. Moringa concanensis Nimmo, flower with nonadhering filaments and reduced anthers, with detail of reduced anther. 6. Moringa oleifera Lam. with detail of three-tiered anther presentation. 7. Moringa peregrina (Forssk.) Fiori. group (the ‘‘zygomorphic clade’’ in Fig. 14). Zygomorphy is Like many taxa of the dry tropics, most species of Moringa apparent in the flowers of all of these species through differ- have been little studied. The flowers of M. ovalifolia and M. ential flexion of petals, sepals, the androecium, and the gy- ruspoliana are illustrated here for the first time (Figs. 4, 12), noecium. The three principally Asian species (Figs. 5–7) have and, of those that have been illustrated previously, M. arborea, mostly cream-colored flowers and form a clade of slender trees M. borziana, M. pygmaea, and M. rivae are illustrated for the (‘‘S’’ in Fig. 14). The slender trees are the sister group to a first time in their correct orientations (Figs. 8–11). Previous clade of tuberous trees and shrubs that have diversified in the studies of floral anatomy (e.g., Dutt, 1978; Dutt, Narayana, Horn of Africa (‘‘T’’ in Fig. 14). This tuberous clade is sub- and Parvathi, 1978; Ronse Decraene, De Laet, and Smets, divided into two subclades, the rivae clade (‘‘ri’’ in Fig. 14), 1998) have examined only M. oleifera and M. concanensis, consisting of four species with yellowish flowers often both members of the slender tree clade from the Indian sub- blotched with maroon (Figs. 8–11). The remaining two species continent. Studies of wood anatomy, which also focused on (Figs. 12, 13) have the only red flowers in the genus and are the slender tree clade (e.g., Metcalfe and Chalk, 1950; Dutt, designated the red-flowered clade (‘‘rf’’ in Fig. 14). Rao, and Rai, 1978), greatly under-represented the diversity of January 2003] OLSON—FLORAL ONTOGENY IN MORINGACEAE 51 Figs. 8–13. Flowers of all species of the tuberous subclade of the zygomorphic clade in Moringa. Side views unless specified. 8–11. Members of the rivae subclade. 8. Moringa arborea Verdc.; sepals may be entirely reflexed. 9. Moringa borziana Mattei, showing nearly actinomorphic calyx. 10. Moringa rivae Chiov. subsp. rivae; lateral views of flower from above
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