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Viola, Violaceae): Arctic Origins, Herbaceous Ancestry and Bird Dispersal

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Viola, Violaceae): Arctic Origins, Herbaceous Ancestry and Bird Dispersal Evolution, 54(5), 2000, pp. 1521±1532 EVOLUTION AND BIOGEOGRAPHY OF THE WOODY HAWAIIAN VIOLETS (VIOLA, VIOLACEAE): ARCTIC ORIGINS, HERBACEOUS ANCESTRY AND BIRD DISPERSAL HARVEY E. BALLARD,JR.1 AND KENNETH J. SYTSMA2 1Department of Environmental and Plant Biology, Ohio University, Porter Hall, Athens, Ohio 45701 E-mail: [email protected] 2Department of Botany, University of Wisconsin, 132 Birge Hall, 430 Lincoln Drive, Madison, Wisconsin 53706 E-mail: [email protected] Abstract. Specialists studying the genus Viola have consistently allied the Hawaiian violets comprising section NosphiniumÐmost of which are subshrubs or treeletsÐwith putatively primitive subshrubs in certain South American violet groups. Hawaiian violets also possess in¯orescences, a ¯oral disposition otherwise found only in other genera of the Violaceae, thus strengthening the hypothesis of a very ancient origin for the Hawaiian species. A survey of phylogenetic relationships among infrageneric groups of Viola worldwide using nuclear rDNA internal transcribed spacer (ITS) sequences revealed a dramatically different biogeographic origin for the Hawaiian violets: A monophyletic Hawaiian clade was placed in a close sister relationship with the amphi-Beringian tundra violet, V. langsdorf®i s. l., in a highly derived position. This remarkable and unforeseen relationship received strong clade support values across analyses, and monophyly of the Hawaiian lineage was further indicated by a unique 26-base-pair deletion in section Nosphinium. The high polyploid base chromosome number (n . 40) in the Hawaiian violets relates them to Alaskan and eastern Siberian populations in the polyploid V. langsdorf®i complex. More than 50 species of the 260 allochthonous birds wintering in the Hawaiian Islands are found to breed in the Arctic, occupying habitats in which individual birds might have encountered ancestral V. langsdorf®i populations and served as dispersers to the central Paci®c region. Acquisition of derived morphological traits (e.g., arborescence and in¯orescences), signi®cance of a con®rmed Arctic origin for a component of the Hawaiian ¯ora, and the likelihood of other ``cryptic'' Arctic elements in the Hawaiian ¯ora deserving independent molecular phylogenetic corroboration are discussed. Key words. Biogeography, bird dispersal, insular adaptations, internal transcribed spacers, molecular phylogeny. Received February 24, 1999. Accepted April 2, 2000. Extraordinary geographic isolation of the Hawaiian archi- 1997). Such misleading growth forms hamper identi®cation pelago (more than 3500 km from the nearest continent), a of homologous structures and may misdirect efforts to infer diverse ¯ora of nearly 1000 native angiosperm and approx- relationships between island endemics and continental imately 180 pteridophyte species, and an unparalleled 86% groups. The references cited above con®rm this phenomenon endemism in angiosperms and about 70% in pteridophytes and raise doubts about using macromorphological features (Wagner et al. 1990; Sakai et al. 1995; Wagner and Funk alone in insular groups, especially where characters have not 1995) make the Hawaiian ¯ora one of the most tantalizing been investigated carefully and rigorously examined through foci for evolutionary inquiry. Earlier explicit inferences on appropriate explicit methods, that is, cladistics. Macromor- the minimum number of successful colonizations responsible phological changes resulting from an adaptive radiation may, for the modern-day Hawaiian vascular ¯ora (Fosberg 1948; even after rigorous scrutiny, prove problematic as indicators Carlquist 1970) have recently been updated to 291 putative of phylogenetic relationship. Indeed, several morphological events for angiosperms and an additional 115 for pterido- and ecological traits such as stem woodiness and dioecy are phytes (Wagner 1991; Sakai et al. 1995). The Hawaiian ¯ora recurrent and well-known adaptations of island plants (Dar- thus offers unique opportunities for biogeographic and evo- win 1859; Carlquist 1970, 1974; Givnish 1998). Thus, es- lutionary studies of oceanic island systems (Carlquist 1965, pecially in insular settings, molecular data can provide an 1974; Wagner and Funk 1995; Givnish 1998). Comprehen- escape from the possible circularity of using morphological sive higher-level phylogenetic studies including endemic Ha- characters to reconstruct phylogenetic relationships and then waiian plants have the potential to elucidate the biogeograph- to infer patterns of evolution with the same charactersÐa ic origins of those plant groups and reevaluate previous hy- problem argued to be most severe in such cases of adaptive potheses of dispersal and character evolution. Well-estab- radiation (Sytsma et al. 1991; Givnish et al. 1995, 1997; lished geologic dates pinpoint the time of origin of islands Givnish and Sytsma 1997b,c). Phylogenetic analyses of mo- that formed ``conveyor-belt'' fashion (Carson and Clague lecular data provide an ideal framework for testing hypoth- 1995), permitting the coupling of island age with dispersal eses of morphological and biogeographic relationship and events to the islands, diversi®cation, and interisland dispersal clarifying patterns of character evolution. The use of mor- (e.g., Givnish et al. 1995; Baldwin 1997). phological and molecular data in examining evolution in is- Adaptive radiation in island ¯oras may yield dramatically land taxa has increased in recent years (see chapters in Wag- different-looking sister taxa and, conversely, morphologi- ner and Funk 1995; Givnish and Sytsma 1997a; Grant 1998), cally similar species of similar habitats on different islands and hypothesis testing of relationships and evolutionary sce- that are not phylogenetic sister taxa (Givnish et al. 1995; narios has become more rigorous with the application of ex- BoÈhle et al. 1996; Baldwin 1997; Francisco-Ortega et al. plicit (e.g., cladistic and other) analytical methods. Never- 1521 q 2000 The Society for the Study of Evolution. All rights reserved. 1522 H. E. BALLARD, JR. AND K. J. SYTSMA FIG.1. (a)Viola langsdorf®i: herbaceous, amphi-Beringian, bog and meadow species revealed by ITS sequences as sister to Hawaiian violets; (b) V. kauaensis; sprawling, herbaceous, bog species on Kauai; (c) V. chamissoniana ssp. tracheliifolia: spindly, dry forest treelet on Kauai, Oahu, and Molokai; (d) V. helenae: subshrub of stream banks on Kauai; (e) V. stipularis: semishrub of Mesoamerican and Andean cloud forests, previously allied with Hawaiian violets; (f) V. rubella: semishrub of Chilean coastal forests, member of basal section in Viola based on ITS sequence data. Scale bar 5 1 cm. Photo credits: (a) J. Pojar; (b±d) R. Gustafson; (e) H. Ballard; (f) T. Hashimoto. theless, few molecular phylogenetic studies have unambig- most recent treatment of the Hawaiian ¯ora recognizes seven uously con®rmed the biogeographic origins of insular plant species and three subspecies (Wagner et al. 1990), whereas groups (e.g., Baldwin et al. 1991; Kim et al. 1996; Mes and a nearly simultaneously published monograph recognizes 14 Hart 1996; Mes et al. 1996; Francisco-Ortega et al. 1997; species (St. John 1989). Differing taxonomic viewpoints Howarth et al. 1997). aside, taxonomists have interpreted certain morphological The genus Viola, a moderate-sized and largely herbaceous traits in the Hawaiian violets as putatively primitive features group of about 550 species worldwide, includes approxi- shared with Latin American sections (Fig. 1e, f) and argued mately 10 Hawaiian species and infraspeci®c taxa (Wagner that Hawaiian Viola represent an ancient lineage in the genus. et al. 1990). The entirely woody stems of most Hawaiian taxa Specialists disagree, however, over whether the Hawaiian are highly unusual in the genus, and their few-¯owered cy- violets are monophyletic (Becker 1917; Skottsberg 1940; mose in¯orescences are unique. The genus has undergone a Wagner et al. 1990) with all taxa in section Nosphinium or modest adaptive radiation (Givnish 1997; see also for review polyphyletic with woody taxa in Nosphinium and herbaceous of de®nitions) in the Hawaiian archipelago, yielding diver- taxa in Leptidium (St. John 1989). Proponents of a mono- gent morphological phenotypes occupying different habitats phyletic Hawaiian violet group do not agree on whether it is at high elevations on the islands. Taxa include the decumbent, derived from or related to Latin American section Leptidium herbaceous V. kauaensis with reniform leaves (Fig. 1b); the or section Rubellium (Becker 1917; Wagner et al. 1990) or tall, spindly treelet V. chamissoniana ssp. tracheliifolia with represents the most basal and most isolated group in the genus hastate leaves (Fig. 1c); and the knee-high, woody shrub V. (Skottsberg 1940). helenae with lance-linear to ovate-lanceolate leaves (Fig. 1d). A genuswide phylogenetic study of Viola was undertaken Taxonomic treatments of the group vary considerably. The using nuclear rDNA internal transcribed spacer (ITS) se- EVOLUTION OF HAWAIIAN VIOLETS 1523 quences (Ballard 1996; Ballard et al. 1998). Availability of gaps where needed. Data for the 18S and 26S coding regions new molecular data for most species and subspecies of Ha- ¯anking the ITS region and the 5.8S coding region between waiian violets in addition to sequences for most infrageneric the ITS1 and ITS2 spacers were excluded prior to analysis groups worldwide and those distributed around the Paci®c due to the dearth of informative characters and lack of com- basin
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