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Viburnum Phylogeny Based on Combined Molecular Data: Implications for Taxonomy and Biogeography1

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Viburnum Phylogeny Based on Combined Molecular Data: Implications for Taxonomy and Biogeography1 American Journal of Botany 92(4): 653±666. 2005. VIBURNUM PHYLOGENY BASED ON COMBINED MOLECULAR DATA: IMPLICATIONS FOR TAXONOMY AND BIOGEOGRAPHY1 RICHARD C. WINKWORTH2 AND MICHAEL J. DONOGHUE Department of Ecology and Evolutionary Biology, Yale University, P.O. Box 208106, New Haven, Connecticut 06520-8106 USA We investigated Viburnum phylogeny using separate and combined analyses of DNA sequence data from two chloroplast and three nuclear loci. Separate analyses of nuclear and chloroplast data sets resulted in gene trees that were generally congruent with one another and with trees from two previous analyses. Our gene trees do differ in the position of section Pseudotinus, as well as in species relationships within sections Pseudotinus and Lentago. However, tests for incongruence indicate that differences between the nuclear and chloroplast data are not signi®cant. Furthermore, gene trees from combined analyses were highly similar to those found in separate analyses, suggesting that these localized differences do not affect other parts of the tree. Our analyses provide convincing support for numerous relationships, although there is still uncertainty at the base of the tree. To facilitate future study, we propose informal names for 12 well-supported species groups, as well as for several higher-level clades. We also discuss the biogeographic implications of our phylogeny, focusing on repeated, although apparently temporally incongruent, patterns of disjunction between the Old and New Worlds. Key words: biogeography; data combination; phylogeny; taxonomy; Viburnum. Viburnum (Adoxaceae, Dipsacales) is a clade of ca. 160 nized four subsections within Megalotinus, and Hara (1983) species of shrubs and small trees. Although broadly distributed proposed subsections within sections Odontotinus, Viburnum, around the Northern Hemisphere, Viburnum has centers of and Solenotinus. Regional treatments have dealt with the Asian species diversity in eastern Asia and Latin America (Rehder, (Hara, 1983; Rehder, 1908; Hsu et al., 1988), Malesian (Kern, 1908; Hara, 1983; Donoghue, 1983a), and its range extends 1951; Kern and van Steenis, 1951), South American (Killip into the Southern Hemisphere in the mountains of southeast and Smith, 1929, 1931), Mexican and Central American (Mor- Asia (Kern, 1951) and South America (Killip and Smith, ton, 1933; Donoghue, 1982), and North American species 1931). The group displays relatively little variability in ¯ower (McAtee, 1956). These have varied in scope, but mostly con- and fruit morphology, but conspicuous diversity in numerous tain only keys and descriptions; species relationships within or other characters; variation in endocarp shape, fruit color, leaf between regions have seldom been considered. morphology, bud morphology, and in¯orescence form is par- The monophyly and phylogenetic placement of Viburnum ticularly striking. are now clearly established (e.g., Wilkinson, 1948; Donoghue, Linnaeus (1753) originally erected Viburnum. A later revi- 1983b; Pyck et al., 1999; Bell et al., 2001; Donoghue et al., sion by Oersted (1861) clearly identi®ed the principal variable 2001, 2003). In contrast, despite an earlier morphological characters within the group, although his proposed subdivision study (Donoghue, 1983a) and several unpublished molecular into ®ve genera was never widely adopted. Since Oersted's data sets (see abstracts by Donoghue and Sytsma, 1993; Don- (1861) treatment, few botanists have considered the classi®- oghue and Baldwin, 1993; see also Baldwin et al., 1995) evo- cation of Viburnum as a whole. One exception was Rehder lutionary relationships within Viburnum have remained largely (1940), who, although concentrating on the Asian species, rec- unresolved. However, two recent molecular phylogenetic stud- ognized nine sections. More recently, Hara (1983) greatly clar- iesÐDonoghue et al. (2004) using chloroplast trnK intron and i®ed the subgeneric nomenclature with his review of the sec- nuclear ribosomal ITS DNA sequences, and Winkworth and tion-level classi®cation. This treatment recognized 10 sections Donoghue (2004) using sequences from the low-copy number (Table 1)Ðthe nine suggested by Rehder (1940) plus section nuclear gene GBSSIÐhave improved our understanding of re- Oreinotinus to accommodate the Latin American species, for lationships within Viburnum. In broad terms, they con®rm the which Morton (1933) had proposed 10 sections. There have monophyly of many section-level taxa. Section Odontotinus been few section level revisions. The exceptions include a was the most striking exception, being divided into (1) a pur- thorough treatment of the eastern North American species of ple-fruited North American lineage that also includes the Latin section Lentago (Jones, 1983) and a monograph of several species complexes in Mexico and Central America (Dono- American section Oreinotinus, and (2) a mostly red-fruited ghue, 1982). In other studies, Hsu (1975) segregated a new Asian lineage that also contains the North American purple- section (Platyphylla) from Megalotinus, Kern (1951) recog- fruited species, V. acerifolium. Sections Lentago, Solenotinus, and Viburnum were also found to be nonmonophyletic. How- 1 Manuscript received 5 June 2004; revision accepted 7 January 2005. ever, for each of these groups, a core clade contains all but The authors thank Bob Cook and the staff of the Arnold Arboretum for one representative of the section (see below). allowing us to make extensive collections on the grounds and for their general Perhaps more importantly, the studies of Donoghue et al. support. Lab groups at Harvard and Yale provided valuable feedback. We (2004) and Winkworth and Donoghue (2004) provided con- thank ValeÂry MaleÂcot for input on species numbers. We also thank Richard Olmstead and an anonymous reviewer for helpful comments on an earlier sistent resolution of relationships among the sectional-level version. lineages, identifying three well-supported suprasectional 2 (E-mail: [email protected]); Telephone: 203-436-4992. clades. The largest suprasectional lineage contains subclades 653 654 AMERICAN JOURNAL OF BOTANY [Vol. 92 TABLE 1. Traditionally recognized sections of Viburnum (e.g., Hara, 1983). Approximate number Section of species Generalized geographic range Lentago 7 Eastern North America, except V. elatum in Mexico Megalotinus 18 Southeast Asia, extending west to India and south to Indonesia Odontotinus 37 Temperate Asia and Eastern North America, except V. orientale in the Caucasus Mountains Opulus 5 Circumboreal Oreinotinus 38 Mexico, Caribbean, Central and South America Pseudotinus 4 Asia, except V. lantanoides in Eastern North America Solenotinus 26 Asia, extending west to India and south to Indonesia Tinus 7 Asia, except V. tinus in Europe Tomentosa 2 China, Japan Viburnum 14 Asia, except V. lantana in Europe corresponding to (1) section Opulus, (2) section Tinus, (3) the lationships within Viburnum by combining the data sets of New World Odontotinus plus Oreinotinus, and (4) the Old Donoghue et al. (2004) and Winkworth and Donoghue (2004) World Odontotinus±acerifolium lineage plus V. cylindricum of with sequences from an additional chloroplast marker, the section Megalotinus. Each of the two remaining suprasectional psbA-trnH intergenic spacer (IGS). For our analyses, we lineages consists of a well-supported pair of section level formed new data partitions. Speci®cally, a chloroplast data set clades. In one of these, V. plicatum (section Tomentosa)is that included trnK intron sequences from Donoghue et al. sister to the core of section Solenotinus; in both studies this (2004) and our psbA-trnH IGS sequences, and a nuclear par- grouping is weakly associated with V. urceolatum (tradition- tition that consisted of nrITS (Donoghue et al., 2004) and ally of section Viburnum). The third suprasectional lineage GBSSI (Winkworth and Donoghue, 2004) sequences. We used contains the core species groups of sections Lentago and Vi- gene trees from analyses of chloroplast, nuclear, and combined burnum. This lineage also includes V. nudum (traditionally of data sets to test phylogenetic hypotheses suggested by earlier section Lentago), although its exact relationship to these sec- studies, to investigate differences between the data sets, and tion-level clades remains unclear. to clarify relationships left unresolved in previous analyses. The most striking difference between the gene trees inferred The results provide a ®rm basis for reclassi®cation of Vibur- by Donoghue et al. (2004) and those of Winkworth and Don- num and for a preliminary biogeographic analysis. oghue (2004) relates to the duplication of the GBSSI paralogs in several Viburnum lineages. Speci®cally, V. erubescens, V. MATERIALS AND METHODS odoratissimum, and V sieboldii of section Solenotinus and the Oreinotinus±dentatum clade were represented twice on GBSSI Taxon samplingÐFor this study, we included the same set of taxa (i.e., 41 gene trees. These lineage-speci®c duplications of the GBSSI Viburnum species plus an outgroup, Sambucus canadensis) that were used by Winkworth and Donoghue (2004). This sample includes approximately one loci are consistent with karyological evidence for polyploidy quarter of all Viburnum species, but more importantly it includes represen- in these groups (Winkworth and Donoghue, 2004). Although tatives of all traditionally recognized sections and major species complexes. in these two lineages the placement of GBSSI homoeologues Although we broadly covered Viburnum diversity,
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