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Phylogenetics of the Florally Diverse Andean Clade Iochrominae (Solanaceae)1

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Phylogenetics of the Florally Diverse Andean Clade Iochrominae (Solanaceae)1 American Journal of Botany 93(8): 1140–1153. 2006. PHYLOGENETICS OF THE FLORALLY DIVERSE ANDEAN CLADE IOCHROMINAE (SOLANACEAE)1 STACEY DEWITT SMITH2,3 AND DAVID A. BAUM2 2Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 USA Recent molecular phylogenetic studies of Solanaceae have identified many well-supported clades within the family and have permitted the creation of a phylogenetic system of classification. Here we estimate the phylogeny for Iochrominae, a clade of Physaleae sensu Olmstead et al. (1999), which contains 34 Andean species encompassing an immense diversity of floral forms and colors. Using three nuclear regions, ITS, the second intron of LEAFY, and exons 2 to 9 of the granule-bound starch synthase gene (waxy), we evaluated the monophyly of the traditional genera comprising Iochrominae and assessed the extent of interspecific hybridization within the clade. Only one of the six traditionally recognized genera of Iochrominae was supported as monophyletic. Further, comparison of the individual nuclear data sets revealed two interspecific hybrid taxa and a third possible case. These hybrid taxa occur in the Amotape–Huancabamba zone, a region between the northern and central Andes that has the greatest diversity of Iochroma species and offers frequent opportunities for hybridization in areas of sympatry. We postulate that periodic hybridization events in this area coupled with pollinator-mediated selection and the potential for microallopatry may have acted together to promote diversification in montane Andean taxa, such as Iochrominae. Key words: floral evolution; granule-bound starch synthase; interspecific hybridization; LEAFY; phylogeny; pollination; reticulate evolution; speciation. The tropical Andes comprise the pre-eminent hotspot of e.g., hummingbirds (Bleiweiss, 1998), may explain the plant biodiversity, with approximately 15% of all plant species ‘‘explosive’’ speciation seen in some Andean groups (Gentry, native to that region (Myers et al., 2000). Many plant families, 1982; Luteyn, 2002). Here we investigate the phylogenetic though cosmopolitan, have centers of diversity in western history of Iochrominae, a group of Andean Solanaceae, which South America, for example, Ericaceae, Orchidaceae, and have radiated in floral morphology and pollination system Solanaceae (Dressler, 1981; D’Arcy, 1991; Luteyn, 2002). An (Cocucci, 1999) and which may serve as a model system for important contributor to the origin of this diversity is the other Andean radiations. topological and environmental variation resulting from the Recent phylogenetic analyses using plastid genes have uplift of the Andes (Gentry, 1982; Hooghiemstra et al., 2002). greatly clarified relationships within Solanaceae and allowed Phylogenetic studies support an association between the for the creation of a phylogenetic system of classification diversification of Andean plants (von Hagen and Kadereit, (Olmstead and Sweere, 1994; Olmstead et al., 1999; Martins 2003; Kay et al., 2005) and animals (Patton and Smith, 1992; and Barkman, 2005; Olmstead et al., University of Wash- Bates and Zink, 1994; Brower, 1994) and the major episodes of ington, personal communication). Iochrominae sensu Olmstead Andean uplift, beginning in the early Miocene (ca. 20 mya) and et al. (1999) is a clade of Physaleae comprising around 34 ending in the Pliocene (ca. 3 mya) (Hoorn et al., 1995; mainly Andean species traditionally assigned to six genera: Hooghiemstra and van der Hammen, 1998). Indeed, the Acnistus Schott, Dunalia H.B.K, Eriolarynx (Hunz.) Hunz., parallel invasions of higher elevations by numerous plant Iochroma Benth., Saracha R. and P., and Vassobia Rusby groups and the coincident radiations of pollinating animals, (Table 1). In the Olmstead et al. (1999; R. G. Olmstead, University of Washington, unpublished manuscript) scheme, 1 Manuscript received 7 December 2005; revision accepted 1 May 2006. Iochrominae together with Physalinae and Withaninae form the The authors thank S. Hall, O. Jadan, D. Neill, C. Padilla, W. Quizhpe, large clade Physaleae, which is sister to Capsiceae. Although A. Rodriguez, H. Vargas, V. Zak and in particular, S. Leiva G., for the phylogenetic classification was not accompanied by assistance during fieldwork and plant collection; N. W. Sawyer for a morphological reassessment, Iochrominae can be distin- determinations of Cuatresia and Larnax; M. Nee for determinations of guished from other subtribes in Physaleae by the fact that they Lycianthes and Capsicum; S. Keel for determination of Salpichroa;D.G. are all woody shrubs or small trees and often have showy Howarth for advice with LFY; R. G. Olmstead for providing DNA of Leucophysalis grandiflora and Tubocapsicum anomalum; L. Bohs for tubular flowers. In a recent morphological phylogenetic material of Dunalia brachyacantha, Saracha punctata, and Acnistus analysis (Sawyer, 2005), all Iochrominae genera except one, arborescens; G. van der Weerden for material of E. lorentzii; A. Tye for Acnistus, were found to be monophyletic, united most notably help in obtaining samples of I. ellipticum; P. E. Berry, L. Bohs, J. W. by the rounded-mucronate shape of the fruiting calyx margin Boughman, N. I. Cacho, M. Nee, R. G. Olmstead, D. M. Spooner, K. J. and the presence of sclerosomes in the fruit wall. Sytsma, and T. J. Theim for helpful discussion; two anonymous reviewers Although it contains only one-third the number of species in for useful comments; B. Larget for advice regarding Bayesian analyses; K. its probable sister group Physalinae, Iochrominae boasts Elliot for assistance with illustrations; and R. A. Smith for editing. Finally, a greater floral diversity, spanning all major flower colors the authors acknowledge financial support from the National Science Foundation grant DEB-0309310, the University of Wisconsin chapter of and forms found in the entire Solanaceae. Iochrominae flowers Graduate Women in Science, the Marie Christine Kohler Fellowship, the may be red, orange, yellow, green, blue, purple, or white, and American Society of Plant Taxonomists, the University of Wisconsin the corolla varies from rotate to tubular, with over eight-fold Tinker-Nave Fund, and the O. N. Allen Memorial Fund. variation in tube length across species (Shaw, 1998; Hunziker, 3 Author for correspondence (e-mail: [email protected]) 2001; Table 1). In contrast, a vast majority of taxa within 1140 August 2006] SMITH AND BAUM—PHYLOGENETICS OF IOCHROMINAE 1141 TABLE 1. Summary information for genera of Iochrominae. Number of species is from recent treatments and descriptions (Acnistus [Hunziker, 1982], Eriolarynx [Hunziker, 2000, 2001], Dunalia [Hunziker, 1960, 2001], Iochroma [Leiva, 1995; Leiva et al., 1998, 2003; Shaw, 1998], Saracha [Alvarez, 1996], Vassobia [Hunziker, 1984, 2001]). Genus No. species No. sampled Distribution Elevation (m a.s.l.) Distinctive features Acnistus 1 1 Southern Mexico, Central America, the 300–2000 Campanulate or funnel-shaped fragrant flowers; Caribbean, northern South America valvate bud aestivation; triangular corolla lobes; and eastern Brazil green markings inside corolla lobes; edible fruit Dunalia 5 5 Colombia to Argentina 1600–3700 Often spiny; a few dioecious or gynodioecious; tubular flowers with wing-like appendages of stapet (filament base) Eriolarynx 3 2 Bolivia and Argentina 1000–3000 Rotate or campanulate flowers with a dense ring of trichomes at base of corolla tube; stapet with small projections (‘‘auricles’’) Iochroma 21 þ 3 21 þ 3 Colombia to Peru, with one species 1100–3500 Tubular, often colorful flowers, with inflated calyces in undescribed taxa undescribed taxa in the Galapagos* some species Saracha 2 2 Venezuela to Bolivia 2700–4500 Occasionally spiny; coriaceous to subcoriaceous leaves; campanulate or funnel-shaped flowers; pyrenes in fruit Vassobia 2 2 Bolivia, Argentina, Paraguay, 300–2700 One spiny; campanulate flowers mostly glabrous; Uruguay and Brazil stapet with auricles Note: *The range for Iochroma excludes the two southern Andean species shown in this study not to belong in Iochroma. Physalinae, Withaninae, and Capsiceae have small, white or specific and generic relationships in Solanaceae (e.g., Marshall yellow, rotate flowers, and there are no instances of long, et al., 2001; Peralta and Spooner, 2001; Whitson and Manos, tubular, red or purple corollas in these three clades. Thus, the 2005). LFY introns are increasingly utilized for resolving brightly colored tubular flowers likely represent a derived interspecific relationships and identifying hybrid taxa (e.g., Oh feature that arose within or at the base of Iochrominae. and Potter, 2003; Howarth and Baum, 2005), although this is The great floral diversity of Iochrominae sensu Olmstead et the first study to use LFY in Solanaceae systematics. Our al. (1999) has misled classifications based on morphology. For specific objectives were to evaluate the monophyly of the six example, Hunziker’s (2001) morphologically delimited Iochro- traditional genera of Iochrominae and to assess the extent of minae included Oryctes S. Watson, a monotypic tubular- interspecific hybridization. We close by considering our results flowered genus native to California and Nevada. Oryctes has in a biogeographical context. since been shown to be nested within Physalinae, probably sister to Leucophysalis (Whitson and Manos, 2005; Olmstead et al., University of Washington, personal communication). MATERIALS AND METHODS Similarly, Sawyer’s (2005) morphological cladistic analysis of Physaleae
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