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Molecular Evidence for an African Origin of the Hawaiian Endemic Hesperomannia (Asteraceae)

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Molecular Evidence for an African Origin of the Hawaiian Endemic Hesperomannia (Asteraceae) Proc. Natl. Acad. Sci. USA Vol. 95, pp. 15440–15445, December 1998 Evolution Molecular evidence for an African origin of the Hawaiian endemic Hesperomannia (Asteraceae) HYI-GYUNG KIM*†,STERLING C. KEELEY‡,PETER S. VROOM‡, AND ROBERT K. JANSEN*§ *Department of Botany and Institute of Cellular and Molecular Biology, University of Texas, Austin, TX 78713; and ‡Department of Botany, University of Hawaii, Honolulu, HI 96822 Communicated by Peter H. Raven, Missouri Botanical Garden, St. Louis, MO, October 14, 1998 (received for review June 4, 1998) ABSTRACT Identification of the progenitors of plants en- Hawaiian plants are more complicated than those of plants of demic to oceanic islands often is complicated by extreme mor- other volcanic oceanic archipelagos. phological divergence between island and continental taxa. This We have been examining phylogenetic relationships of the is especially true for the Hawaiian Islands, which are 3,900 km Hawaiian endemic genus Hesperomannia, a member of the from any continental source. We examine the origin of Hespero- flowering plant family Asteraceae, one of the largest families in mannia, a genus of three species endemic to Hawaii that always the Hawaiian Islands (2). Previous workers considered this small have been placed in the tribe Mutisieae of the sunflower family. genus of three species to be a close relative of several South Phylogenetic analyses of representatives from all tribes in this American genera of the tribe Mutisieae (10–13). Hesperomannia family using the chloroplast gene ndhF (where ndhF is the ND5 was considered basal in the tribe, and its position was used to protein of chloroplast NADH dehydrogenase) indicate that Hes- support the thesis that the Asteraceae originated in South Amer- peromannia belongs to the tribe Vernonieae. Phylogenetic com- ica (12). Our DNA phylogenies disagree with all previous studies parisons within the Vernonieae using sequences of both ndhF and and clearly indicate that Hesperomannia is closely allied to the internal transcribed spacer regions of nuclear ribosomal African members of the tribe Vernonieae. This result confirms a DNA reveal that Hesperomannia is sister to African species of source area for the highly endemic and morphologically distinc- Vernonia. Long-distance dispersal northeastward from Africa to tive Hawaiian biota. southeast Asia and across the many Pacific Ocean island chains is the most likely explanation for this unusual biogeographic MATERIALS AND METHODS connection. The 17- to 26-million-year divergence time between DNA Sequencing. Phylogenetic analyses were conducted by African Vernonia and Hesperomannia estimated by the DNA using sequences of the chloroplast gene ndhF (ndhF is the ND5 sequences predates the age of the eight existing Hawaiian Is- lands. These estimates are consistent with an hypothesis that the protein of chloroplast NADH dehydrogenase) and the internal progenitor of Hesperomannia arrived at one of the low islands of transcribed spacer (ITS) region of nuclear ribosomal DNA. Total genomic DNA was isolated from fresh leaves (14), followed by the Hawaiian-Emperor chain between the late Oligocene and y mid-Miocene when these islands were above sea level. Subse- purification in cesium chloride ethidium bromide gradients. quent to its arrival the southeast Pacific island chains served as DNA extractions from herbarium specimens and silica-dried steppingstones for dispersal to the existing Hawaiian Islands. leaves were performed (15). Amplifications were performed in 50 ml with 1 ml of unquantified genomic DNA, 20 pmol of primer, 3 The Hawaiian Islands are 3,900 km from the closest continent and 1 Tfl polymerase buffer, 0.5 units of Tfl polymerase (Epicentre are one of the most remote land masses in the world. Despite this Technologies, Madison, WI), 10 mM of MgCl2, and 0.2 mM of distance the islands have an exceptionally diverse flora. Estimates each dNTP. The first thermal cycle consisted of 3 min denatur- of endemism for major archipelagos show that Hawaii has the ation at 94°C, 1 min of annealing at 50°C, and 1 min and 20 sec highest known (90%) compared with 40% for the Galapagos and of polymerization at 72°C. This cycle was followed by 34 cycles at 25% for the Canaries (1). It is estimated that the 1,000 species of 94°C for 1 min, 50°C for 1 min, and 72°C for 1 min and 20 sec, native Hawaiian flowering plants originated from 270–280 pro- followed by a final extension cycle of 72°C for 7 min. The genitors (2), all as waif elements brought by long-distance dis- amplified DNA was purified by electrophoresis in a 1% agarose persal. Identification of specific progenitors and source regions is gel and the GeneClean II system (Bio 101). The purified PCR difficult because of the disharmonic nature of the flora and product was sequenced by the snap-chill method (16) using number of possible source areas. Suggested floristic affinities SEQUENASE version 2.0 (United States Biochemical product no. include Malaysia, North America, northern South America, 70770) and 35S-dATP labeling. Australia, New Zealand, and pantropical or southern South Amplifications of the ITS region used primers ITS5 and ITS4 America (2–4). Recent molecular phylogenetic studies of Hawai- (17) as modified by Downie and Katz-Downie (18). Complemen- ian endemic plants have provided many new insights into the tary strands of the ITS region were sequenced by using primers origin and evolution of the flora, including the identification of P2, P3, P4, and P5 (17). For tribal level analyses, the chloroplast continental relatives from western North America (5, 6) and New gene ndhF was amplified by using two primers, 252 and 1607, Guinea (7) and both single (5, 8) and multiple colonizations (9) and sequenced with 12 forward primers (19). For intergeneric of the archipelago. The existence of a chain of Hawaiian islands comparisons within the Vernonieae, only the highly variable 39 for the past 70 million years (myr) adds to the complexity of end of ndhF was sequenced. determining the origin of the endemic flora. The affinities of the flora to disparate geographic regions and the large distances to Abbreviations: ITS, internal transcribed spacer; myr, million years; source areas suggests that the biogeographic histories of endemic ndhF, ND5 protein of chloroplast NADH dehydrogenase. Data deposition: The sequences reported in this paper have been The publication costs of this article were defrayed in part by page charge deposited in the GenBank database (accession nos. AF092584– AF092607 for ndhF and AF092608–AF092637 for ITS). payment. This article must therefore be hereby marked ‘‘advertisement’’ in †Present address: Laboratory of Molecular Systematics, Smithsonian accordance with 18 U.S.C. §1734 solely to indicate this fact. Institution, 4210 Silver Hill Road, Suitland, MD 20746. © 1998 by The National Academy of Sciences 0027-8424y98y9515440-6$2.00y0 §To whom reprint requests should be addressed. e-mail: rjansen@ PNAS is available online at www.pnas.org. utxvms.cc.utexas.edu. 15440 Downloaded by guest on September 26, 2021 Evolution: Kim et al. Proc. Natl. Acad. Sci. USA 95 (1998) 15441 DNA sequences were aligned manually in MACCLADE (20) for ymous differences by using the complete-deletion option for gaps both ndhF and ITS data. The ITS sequences also were aligned by and missing data because of different evolutionary rates at the using CLUSTAL V (21) followed by minor manual corrections. The different codon positions. Pairwise distance comparisons of boundaries of ITS-1 and ITS-2 were determined by comparing noncoding regions (ITS sequences) were calculated with the the aligned sequence with published sequences from other As- transitionytransversion ratio set to 1.03 by using the pairwise- teraceae (22). MACCLADE was used to calculate transitiony deletion option for gaps and missing data. The DNADIST program transversion ratios from the most parsimonious trees. of PHYLIP (27) was used to calculate nucleotide sequence diver- Phylogenetic Analyses. Phylogenetic analyses were conducted gence under Kimura’s two-parameter model (28) and with Jukes by using three data sets. The aligned sequences for all data sets and Cantor’s one-parameter method (29) for 534 bp of ITS and were deposited in TreeBASE (http:yyherbaria.harvard.eduy 804 bp of ndhF, respectively. To assess rate homogeneity between treebasey). The first data set examined the tribal position of different lineages, a relative-rate test (30, 31) was performed. Hesperomannia and it included the entire ndhF gene (2,235 bp) Vernonia populifolia was used as the reference taxon for both tests for 50 representative genera from eight tribes and all three because this lineage was sister to the rest of the taxa. Standard subfamilies of Asteraceae (see ref. 23 for voucher information). errors for estimated relative rate differences between the lineages Three genera of the subfamily Barnadesioideae were used as were calculated according to Li and Tanimura (31) and Kimura outgroups (19, 24). The two other data sets were designed to (28), and were used for significance tests to assess whether a examine the position of Hesperomannia within the Vernonieae molecular clock could be rejected. The average rate of nucleotide (Table 1). One data set included the 39 end of ndhF (804 bp) for substitutions between two clades was calculated by using per- two of the three species of Hesperomannia, 19 worldwide repre- centage change per site per unit time. sentatives of Vernonieae, and three genera of Liabeae as out- groups. The other used the ITS region and sampled the same two RESULTS taxa of Hesperomannia, 16 representatives of Vernonieae from Tribal Position of Hesperomannia. To investigate the tribal North and South America, Asia, and Africa, and one outgroup position of Hesperomannia, we compared the entire chloroplast from the Liabeae. Sampling was not identical for these two data gene ndhF from 50 representative genera of all of the currently sets because it was not possible to amplify both ndhF and ITS for recognized tribes of the Asteraceae, with more extensive sam- all available taxa.
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