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Evolution of Biogeographic Disjunction Between Eastern Asia and Eastern North America in Phryma (Phrymaceae)1

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Evolution of Biogeographic Disjunction Between Eastern Asia and Eastern North America in Phryma (Phrymaceae)1 American Journal of Botany 93(9): 1343–1356. 2006. EVOLUTION OF BIOGEOGRAPHIC DISJUNCTION BETWEEN EASTERN ASIA AND EASTERN NORTH AMERICA IN PHRYMA (PHRYMACEAE)1 ZE-LONG NIE,2,3 HANG SUN,2 PAUL M. BEARDSLEY,4 RICHARD G. OLMSTEAD,5 AND JUN WEN6,7,8 2Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650204, China; 3Graduate School of Chinese Academy of Sciences, Beijing 100039, China; 4Department of Biological Sciences, Idaho State University, Campus Box 8007, Pocatello, Idaho 83209 USA; 5Department of Biology, Box 355325, University of Washington, Seattle, Washington 98195-5325 USA; 6Department of Botany, National Museum of Natural History, MRC 166, Smithsonian Institution, Washington, D.C. 20013-7012 USA; and 7Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Beijing 100093, China This study examines molecular and morphological differentiation in Phryma L., which has only one species with a well-known classic intercontinental disjunct distribution between eastern Asia (EA) and eastern North America (ENA). Phylogenetic analysis of nuclear ribosomal ITS and chloroplast rps16 and trnL-F sequences revealed two highly distinct clades corresponding to EA and ENA. The divergence time between the intercontinental populations was estimated to be 3.68 6 2.25 to 5.23 6 1.37 million years ago (mya) based on combined chloroplast data using Bayesian and penalized likelihood methods. Phylogeographic and dispersal-vicariance (DIVA) analysis suggest a North American origin of Phryma and its migration into EA via the Bering land bridge. Multivariate analysis based on 23 quantitative morphological characters detected no geographic groups at the intercontinental level. The intercontinental populations of Phryma thus show distinct molecular divergence with little morphological differentiation. The discordance of the molecular and morphological patterns may be explained by morphological stasis due to ecological similarity in both continents. The divergence of Phryma from its close relatives in the Phrymaceae was estimated to be at least 32.32 6 4.46 to 49.35 6 3.18 mya. Key words: biogeography; intercontinental disjunction; eastern Asia; eastern North America; morphological stasis; Phryma; Phrymaceae; phylogeography. Patterns of intercontinental disjunction in the northern ENA. Molecular and fossil data suggest a divergence time for hemisphere usually involve four well-known areas, eastern the two species of 10–16 million years ago (mya). This long- Asia (EA), eastern North America (ENA), western North term morphological stasis observed in Liriodendron was America (WNA), and Europe (Milne and Abbott, 2002; subsequently proposed for the EA and ENA species of Aralia Donoghue and Smith, 2004). The EA–ENA disjunction is sect. Dimorphanthus (Wen, 2000), Liquidambar (Hoey and a well-known classic biogeographic pattern (Li, 1952) that has Parks 1991; Shi et al., 1998), Magnolia sect. Rytidospermum received considerable attention in the last decade (Xiang et al., (Qiu et al., 1995a, b), and Osmorhiza (Wen et al., 2002). 1996, 1998, 2000; Wen, 1999, 2001; Manos and Donoghue, Morphologically similar species from these two areas in 2001). Morphological similarity has been observed in many Aralia, Magnolia,andOsmorhiza form paraphyletic or disjunct species, and some were originally described as polyphyletic groups, suggesting that the morphological a single intercontinental species with distributions in both similarities in these groups may be attributable to symplesio- EA and ENA (Halenius, 1750; Li, 1952). Parks and Wendel morphy or convergence, respectively (Wen, 1999, 2001). Most (1990) reported a high level of allozyme and cpDNA of the studies on species with disjunct distributions in these divergence in the morphologically similar Liriodendron two areas have focused on estimating phylogenetic relation- chinense (Hemsl.) Sargent from EA and L. tulipifera L. from ships among EA and ENA taxa and estimating divergence times, yet few have rigorously analyzed patterns of 1 Manuscript received 3 December 2005; revision accepted 30 May 2006. morphological variation among the disjunct taxa. This study was supported by grants from the Natural Science Phryma L. is distinctive in having a pseudomonomerous Foundation of China (NSFC 40332021 to H.S.), the Xibuzhiguang (Light gynoecium (two-carpellate with one carpel reduced de- in western China) project of the Chinese Academy of Science (to Z.L.N.), velopmentally). It has a synsepalous calyx with three upper the Innovation Project of the Chinese Academy of Sciences (KSCX2-1-09 to H.S.), Institute of Botany of the Chinese Academy of Sciences (to lobes subulate and hooked and a one-seeded achene enclosed J.W.), the Pritzker Laboratory for Molecular Systematics and Evolution of in an accrescent calyx (Thieret, 1972; Chadwell et al., 1992). the Field Museum, the Laboratory of Analytical Biology of Smithsonian The familial placement of Phryma has been controversial, Institution, and the U.S. National Science Foundation (DEB0108536 to having been placed in Scrophulariaceae, Acanthaceae, J.W.; DEB0105048 to R.G.O. and P.M.B.). The authors thank T.S. Yi, K. Lamiaceae, Verbenaceae, and its own monotypic family Feldkeim, S. Ickert-Bond, and J. Hunt for laboratory assistance, E. Haug, Phrymaceae (Holm, 1913; Engler and Prantl, 1936; Rao, J.P. Yue, and Y. Meng for field assistance, S. Manchester for advice on Lamiales fossils, K. Pigg, B. Archibald, and R. Dillhoff for helpful 1952; Hutchinson, 1959; Thieret, 1972; Whipple, 1972; discussions on the age of the Republic fossil, and the curators of A, CAS, Dahlgren, 1980; Cronquist, 1981; Takhtajan, 1987; Lu, CDBI, F, KUN, PE, and US for permission to examine their herbarium 1990; Chadwell et al., 1992). Phrymaceae has recently been collections. recircumscribed to include six genera previously placed in 8 Author for correspondence (e-mail: [email protected]) tribe Mimuleae (Berendtiella, Hemichaena, Lancea, Leuco- 1343 1344 AMERICAN JOURNAL OF BOTANY [Vol. 93 carpus, Mazus, and Mimulus), Phryma, Elacholoma, Glossos- MATERIALS AND METHODS tigma, Microcarpaea, and Peplidium based on chloroplast trnL-F and nuclear ribosomal ITS and ETS sequence data Molecular analysis—Sequences from 22 accessions of Phryma and three (Beardsley and Olmstead, 2002; Beardsley and Barker, 2005). related taxa were used in the study (Fig. 1; Appendix 1). Genomic DNA was extracted from 15 mg of dried leaf material using the modified CTAB method Oxelman et al. (2005), however, questioned the placement of of Doyle and Doyle (1987). The nuclear ribosomal ITS and the chloroplast Lancea and Mazus in Phrymaceae sensu Beardsley and trnL-F regions (including the trnL intron and the trnL-trnF spacer) and the Olmstead (2002). rps16 intron were used, because a large number of sequences were already Phryma is one of a few monotypic and taxonomically available for the Lamiales in GenBank to enable our biogeographic analysis in isolated genera with a high level of morphological similarity in the phylogenetic framework of the Lamiales. The ITS and trnL-F regions were amplified and sequenced following Beardsley and Olmstead (2002), and the intercontinental populations (Li, 1952; Hara, 1969; Thieret, rps16 intron sequences were obtained according to the protocol in Nie et al. 1972; Whipple, 1972; Ramana et al., 1983). In flowering (2005). Sequences were aligned with ClustalX, version 1.83 (PC version, plants, only Phryma leptostachya L. and Toxicodendron Thompson et al., 1997), followed by manual adjustments. radicans (L.) Kuntze include disjunct intercontinental pop- Phylogenetic analyses were performed using maximum parsimony (MP), ulations in both EA and ENA that are considered to be varieties maximum likelihood (ML), and Bayesian inference (Rannala and Yang, 1996). Mimulus aurantiacus and Lancea tibetica of Phrymaceae were used as or subspecies of the same species. Hara (1966) pointed out that outgroups because they are close relatives of Phryma in the recircumscribed disjunct populations of Phryma were identical in most Phrymaceae (Beardsley and Olmstead, 2002). Because of the relatively small morphological features, cytology, and ecological habitats, such number of terminals included in this analysis, the branch and bound search as flowers erect in bud but later spreading or becoming algorithm was used with PAUP* version 4.0b10 (Swofford, 2003). Gaps were deflexed, equal numbers of chromosomes (2n ¼ 28; Lo¨ve and scored as missing data. Bootstrap values (BV) are based on 1000 replicates Lo¨ve, 1982; Rudyka, 1995; Sun et al., 1996), and similar using parsimony and the branch and bound search algorithm (Felsenstein, 1985). The appropriate model of DNA substitution for the maximum likelihood habitats of deciduous or mixed forests. Plants from the two analysis was determined using Modeltest, version 3.6 (Posada and Buckley, different regions differ slightly in leaf size, shape of upper lip 2004). Once the best-fit model was determined, maximum likelihood searches of the corolla, and length of the upper spinulose calyx-lobes were performed for the data set with a heuristic research, each with 10 random (Hara, 1962, 1966, 1969; Li, 2000). The EA and ENA sequence additions. Bayesian inference was conducted using MrBayes, version populations were thus generally treated as two varieties (Hara, 3.0 (Huelsenbeck and Ronquist, 2001) with the model as estimated previously. The MCMC algorithm
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