Boletín de la Sociedad Botánica de México 56: 77-88, 1995 DOI: 10.17129/botsci.1466 Bol. Soc. Bot. México 56: 77-88 (1995) Systematics and character evolution of the genus Yucca L. (Agavaceae): Evidence from morphology and molecular analyses KAREN H. CLARY AND BERYL B. SIMPSON. Department of Botany, The University ofTexas, Austin, Texas, 78713-7640 Abstract. Yucca L. (the Desert Soaptree, Agavaceae) consists of 45 perennial species distributed primarily in the deserts of Mexico and the United States. Although severa! taxonomic treatments of yuccas exist; the-phylogeny of the group is poorly known. It is unclear which taxa retain primitive characters and how characters have evolved. In addition, relationships oftaxa within the genus are uncertain. We compare our phylogeny based upon reproductive characters with a chloroplast phylogeny (Hanson and Rieseberg, 1991 ; Hanson, 1993) and with data from the ITS region of the nuclear genome (Bogler, this volume). The molecular analyses of the chloroplast genome by Hanson and Rieseberg (1991) led to a phylogeny on ly partially congruent with the traditional morphology-based phylogeny (McKelvey, 1938, 1947) because the cpDNA analysis indicated that chloroplast capture among distantly related, sympatric/parapatric species has been a factor in the evolution of the group. Our results indicate that Yucca in the traditional sen se is paraphyletic, that sect. Chaenocarpa is more basal than sect. Yucca ( =Sarcocarpa), and that Yucca (=Hesperoyucca) whipplei falls outside of Yucca. Key words: Agavaceae, evolution, molecular phylogeny, systematics, Yucca. Resumen. Yucca L. (Agavaceae) se compone de 45 especies perennes distribuidas principalmente en los desiertos de México y los Estados Unidos. Aunque existen varios tratamientos taxonómicos de Yucca, la filogenia del género es aún poco conocida. No está claro qué taxa retienen caracteres primitivos y cómo han evolucionado los caracteres. Además, las relaciones entre los taxa del genero son inciertas. En éste artículo, comparamos la filogenia basada en caracteres reproductivos con una filogenia del ADN del cloroplasto (cpADN) (Hanson y Rieseberg, 1991; Hanson, 1993) y con los datos de la region ITS del genoma nuclear (Bogler, este volumen). Los análisis moleculares del genoma del cloroplasto (Hanson y Rieseberg, 1991) produjeron una filogenia solo parcialmente congruente con la filogenia tradicional basada en morfología (McKelvey, 1938, 1947) porque la filogenia basada en cpADN indica que la captura del cloroplasto entre especies genéticamente distantes (simpátricas o parapátricas) ha influido en Ja evolución del grupo. Nuestros resultados indican que Yucca tal como se conoce tradicionalmente es parafilética, y que la seccción Chaenocarpa es más basal que la sección Yucca ( =Sarcocarpa), y que Yucca ( = Hesperoyucca) whipplei se encuentra fuera de los límites del genero Yucca. Palabras clave: Agavaceae, evolución, filogenia molecular, sistemática, Yucca. INTRODUCTION Indeed, substantial convergence of characters among of distantly related taxa appears to have obscured species The genus Yucca is composed of approximately 45 New relationships. Since the evolution of Yucca likely parallels World species, most of the which grow in the arid regions the climatic diversity of the New World deserts of the ofMexico and the western United States. The genus, one of Northern Hemisphere, this group is of special interest. Our the most widespread of ali the North American desertmonocots, research thus focuses on the evolution of characters in exhibits a high leve! of endemism where it occurs. Striking response to increasing aridity. We thereforeexamine characters in appearance with sword-shaped lea ves and massive, creamy, such as plant habit (tree, shrub, rosette (=acaulescent)), fruit whiteflowers,plants ofthis genus arean importantcomponent succulence (dry, fleshy), leaf rigidity (rigid, flaccid), and of desert habitats. They provide animals with food and shelter and are an integral part of the Iives of traditional, leaf margination (denticulate, smooth) which vary not only desert-dwelling American peoples. The budding stalks, and across species of Yucca, but also within other New World later, blossoms and fruits, are harvested and eaten. The monocot genera such as Agave, Nolina, Hesperaloe and leaves are a traditional source of cordage for rope and twine Dasylirion. Yucca is of particular importance in assessing and the hardened, woody flower stalks are used forconstruction changes of these features across aridity gradients because it purposes. is the only genus in which the en tire suite of characters listed Although these plants have obviously been used by abo ve is fo un d. Tracing the pattern of morphological features people since before the Conquest, little is understood about correlated with increased aridity might provide evidence the relationships between species or the patterns of speciation. abouthistorical specialization in all these genera. In unraveling ________________________ Clary KH, Simpson BB. 1995. Systematics and character evolution of the genus Yucca (Agavaceae): Evidence from morphology and molecular analyses. Boletín de la Sociedad Botánica de México 56: 77-88. 78 KAREN H. CLARY AND BERYL B. SIMPSON the evolution we need to answer whether the ancestors of In dealing with the evolutionary history of Yucca, we Yucca were fleshy-fruited, tropical trees, or small herb-like first ask whether the genus as traditionally circumscribed rosettes with dry fruits. (Trelease, 1902; McKelvey, 1938, 1947; Webber, 1953; Our analyses assess whether the traditional Matuda and Piña, 1980) is monophyletic. Specifically, we circumscription of the genus is natural. Taxonomists have question if Y. whipplei (sect. Hesperoyucca) is a «true» tended to define the genus based upon reliance on its major yucca. Y. whipplei has been placed both within (McKelvey, pollinator, the Yu cca moth (Tegeticula), fruit type, and 194 7; Webber, 1953) and outside of Yucca (Trelease, 1902) stigma morphology (Table 1). (Two monotypic sections, by various taxonomists. Trelease considered it a genus Hesperoyucca and Clistocarpa are pollinated, respectively, (Hesperoyucca) closely allied to both Yucca and Hesperaloe. by two distinct species of Tegeticula moths. Ali of the «Y. whipplei» shares reproductive characters with both Yucca species of the two remaining sections (Chaenocarpa and andHesperaloe (Table 2). (In both these genera, Hesperaloe, Yucca [ =Sarcocarpa}) are poll inated by the species complex, stamen characters are similar: the filaments reflex towards Tegeticula yuccasella). the ovary, they are the same length as the pistil, and the TABLE l. Morphological characters and pollinators which define traditional Yucca sections (sensu McKelvey, 1938, 1947). Yucca Section Hesperoyucca Clistocarpa Sarcocarpa Chaenocarpa Cha rae ter ha bit shrub/rosette tree/shrub tree/shrub tree/shru b/rosette stigma capitate cleft deeply cleft deeply cleft fruit dry spongy fle shy dry lf. margin denticulate denticulate denticulate/ denticulate/ smooth smooth pollinator T. maculata T. synthetica T. yurcasella T. yuccasel/a Table 2. Shared reproductive characters of Yucca, Hesperoyucca and anthers dehisce laterally, not apically. Besides pollination Hespera/oe. by a Yucca moth, it shares with Yucca a micro-reticulate pollen exine (Palacios-Chávez, 1978; Álvarez and Kohler, 1987), a large paniculate display and large, campanulate Character Yucca Hesperoyucca Hesp era/oe creamy-whitish flowers. Yucca whipplei possess time autapomorphies, a capitate stigma, tufted anthers and pallen Filaments reflex which is shed in a gelatinous mass rather than as dry toward ovary X X individual grains). Filaments sa me Ata higher taxonomic leve! we consider whether or len gth as ovary X X not the sections, based on fruit types, are monophyletic. An thers dehiscc Does fruit type reflect common ancestry or is it the result of apically X X homoplasy? Does fruit type correlate with habit? Most Yucca moth fleshy-fruited taxa are arboreal, most dry-fruited taxa are pollinator X X Poli en small shrubs or rosettes. Based upon the distribution of morphology X X these two characters among species, researchers (Trelease Large panicle 1902; Tidwell and Parker, 1990) hypothetized that the genus display X X arase as sizeable tropical trees (sect. Clistocarpa) and was Campan ulat e, widespread during the warmer, climatically equitableperiods pendan! flowers X X of the Eocene and Miocene (Tidwell and Parker, 1990; Dott Capitale stigma X and Prothero, 1994). Subsequent genetic diversification Pollen shed as occurred in response to the complex development of North gelatinous mass X American deserts. The Sonaran Desert of the Mexican SYSTEMATICS AND CHARACTER EVOLUTION OF THE GENUS YUCCA (AGAVACEAE) 79 Platea u is thought to have been a refugium during the last Ice the southern Mohave, while sect. Clistocarpa (trees with Age (Van Devender, 1990) and subsequently a center of spongy fruits) occurs entirely within the Mojave. substantial radiation afterwards (Trelease, 1902; Piña, 1980). Determining the ancestral morphology of Yucca is Present-day diversity and distributional patterns are thought speculative. The oldest Yucca-like fossils date from the to be the result of Holocene warming and drying trends Miocene of Nevada, USA (Tidwell and Parker, 1990). The which stimulated range expansion northward, where subsequent ancient fossils of the extinct Protoyucca shadishii are most diversification and reduction of the tree form