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Comparative phylogeographic study of Hosta sieboldiana and Hosta albomarginata (Asparagaceae) in Japan Sangryong Lee & Masayuki Maki Botanical Gardens, Tohoku University, Kawauchi 12-2, Aoba-ku, Sendai 980-0862, Japan Keywords Abstract BARRIER, chloroplast DNA, Hosta albomarginata, Hosta sieboldiana, haplotype We analyzed variations in chloroplast DNA (cpDNA) in the widespread herba- diversity, Hosta, Japanese archipelago, NJ ceous species Hosta sieboldiana and Hosta albomarginata across large portions tree, phylogeography, SAMOVA. of their geographic ranges in the Japanese archipelago. Our objective was to compare the phylogeographic histories and phylogeographic structures of the Correspondence two congeneric species in the Japanese archipelago. The location of the study is Sangryong Lee, Botanical Gardens, Tohoku Japanese archipelago. We sequenced 1380 bp of noncoding cpDNA from 45 University, Aoba-ku, Sendai 980-0862, Japan. populations of H. sieboldiana (n = 362) and 55 populations of H. albomargi- Tel/Fax: +81-22-795-6789; = E-mail: [email protected] nata (n 436) to assess genetic variations within and among populations across almost the entire distributions of the species in Japan. Extant patterns of Funding Information geographic structure were analyzed using statistical parsimony networks and This study was partly supported by a Grant- spatial analysis of molecular variance (SAMOVA). We also used Monmonier’s in-Aid from the Japan Ministry of Education, algorithm to detect genetic barriers between regions. Relationships between the Science, Sports and Culture to M.M. populations were examined using a neighbor-joining (NJ) method. Four haplo- types were found for H. sieboldiana, whereas eight haplotypes were identified Received: 7 March 2013; Revised: 12 September 2013; Accepted: 16 September for H. albomarginata. Total genetic haplotype diversity (hT) and within-popula- 2013 tion haplotype diversity (hS) for H. sieboldiana were 0.352 and 0.040, respec- tively, while the values for H. albomarginata were 0.529 and 0.085, respectively. Ecology and Evolution 2013; 3(14): 4767– The population differentiations (GST) for H. sieboldiana and H. albomarginata 4785 were 0.839 and 0.886, respectively. The SAMOVA analysis revealed two clusters in H. sieboldiana and four clusters in H. albomarginata. Differentiations doi: 10.1002/ece3.838 between and among the clusters were supported by the BARRIER analysis and the NJ tree. We detected differences in the population genetic structure between the two species. We found that H. sieboldiana had lower haplotype diversity than H. albomarginata. These results may be partially explained by the differ- ence in ecological habitats and geographic distributions between the species. Hosta albomarginata is more widely distributed than H. sieboldiana in East Asia including Russia, and this large distribution range would enable more chances to intraspecific gene flow. Introduction (Bermingham and Moritz 1998; Moritz and Faith 1998; Avise 2000). Comparative phylogeography of woody Over the past decade, the geographic distributions of plants has been especially useful in reconstructing Quater- intraspecific cpDNA variations have been examined in a nary forest distributions, particularly in Europe and east- variety of plant species to elucidate their postglacial ern North America (Palme et al. 2003, 2004; Heuertz migration history (Petit et al. 2002; Mclachlan et al. 2005; et al. 2004; Grivet et al. 2006; Maliouchenko et al. 2007; Ikeda et al. 2009; Bai et al. 2010; Kikuchi et al. 2010; La- Saeki et al. 2011), and similar types of studies on Japa- fontaine et al. 2010; Chou et al. 2011; Higashi et al. 2012; nese plants have been performed on tree species (Okaura Sede et al. 2012; Cosacov et al. 2013). A principal goal of and Harada 2002; Kanno et al. 2004; Okaura et al. 2007; comparative phylogeography is to infer biogeographic Iwasaki et al. 2012) and alpine plants in temperate zones history from recurrent patterns in the geographic distri- (Ohi et al. 2003; Fujii and Senni 2006; Ikeda and Setogu- bution of genetic variation in co-distributed species chi 2006, 2007; Ikeda et al. 2006, 2008a,b). However, to ª 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 4767 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Comparative phylogeography of two Hosta species S. Lee & M. Maki date, few comparative phylogeographic studies have been refugia in Honshu during warmer postglacial periods. The conducted for herbaceous species in the Japanese archi- genus Hosta has probably diversified because of speciation pelago (Toyama and Yahara 2009). in the archipelago. Fujita (1976) classified 18 species and The Japanese archipelago was connected to the Eur- seven varieties in the genus Hosta. The congeneric species, asian continent by four landbridges as a result of the Hosta sieboldiana and H. albomarginata of the Hosta lower sea level during the last glacial era (18,000– genus, are the most common and widespread herbaceous 20,000 years ago): Sakhalin, the Kuriles, the Korean pen- species in the Japanese archipelago (Fig. 1). Hosta siebol- insula, and the Ryukyu Islands. These connections might diana and H. albomarginata are not so close species in have affect on the genetic structures and distributions of the genus Hosta. Hosta sieboldiana belongs to the section many plants (Hotta 1974). Phylogeographic studies on Helipteroides although H. albomarginata belongs to the the Japanese archipelago elucidated several genetic dis- section Nipponosta. However, the distributions of these junct distribution patterns. For example, genetic differen- two species are similar in Japan, and their overall mor- tiation exists between populations along the Sea of Japan phologies and life forms are also similar. So, we think and the Pacific Sea sides of Japan (Okaura and Harada that these two species are good materials for comparative 2002; Tsumura et al. 2007a,b; Hiraoka and Tomaru 2009; phylogeography. These two species are mostly pollinated Iwasaki et al. 2012). It might be thought that there are by bumblebee species. The flowers of H. sieboldiana are some mountain ranges from northeast to southeast in the self-compatible but require pollinators for seed produc- Japanese mainland, probably acting as physical barriers to tion (Takahashi et al. 1993). Those of H. albomarginata the migration or gene flow of many plant species (Tsuk- are also weakly self-compatible and a facultatively xenoga- ada 1980). The mountain ranges creates a climate bound- mous species (Suzuki et al. 2002). The seeds with wings ary, dividing the main Japanese islands into zones with of these two species are dispersed by wind. The common wet winter with heavy snow along the Japan Sea sides pollinator might visit the two species at the overlapping and with dry winter with small precipitation along the flowering seasons and the hybridization might occur. Pacific sides (Hiraoka and Tomaru 2009). Fagus crenata Although these species sometimes co-occur, they differ in and Cryptomeria japonica have shown the genetic diver- their habitat preferences; H. sieboldiana mostly occupies gence between the sides of Japan Sea and the sides of the cliffs around waterfalls and steep clines, whereas H. al- Pacific sea. Furthermore, a clearly phylogeographic break bomarginata widely inhabits wetlands. Furthermore, H. sie- exists between the northern and central parts and/or wes- boldiana is endemic to Japan, while H. albomarginata is tern parts of Japan (Tsuda and Ide 2005, 2010; Fujii and distributed in both Japan and Russia (Tamura and Fujita Senni 2006; Ikeda et al. 2006, 2008a; Tsumura et al. 2013). In addition to the Japanese archipelago, it occurs 2007a,b; Sugahara et al. 2011). The most likely explana- south of the Amurskaya and Primorsky Territories of the tion for this phylogeographic pattern might be the multi- Eurasian continent, Sakhalin, and the Kurils of Russia ple colonization events following different glacial episodes (Gage et al. 2006). with the Japanese archipelago, during repeated glacial and Because the morphologies of these two species are very interglacial cycles. Some alpine plants such as Pedicularis diverse, intraspecific taxa have been recognized. Popula- chamissonis and Primula cuneifolia have shown the diver- tions of H. sieboldiana along the Sea of Japan have been gence pattern between the northern parts and central treated as H. sieboldiana, although other populations were parts. Fujii and Senni (2006) concluded that these diver- regarded as another species, H. montana (Maekawa gence times corresponded to the period from the middle 1940). Maekawa (1972) suggested that H. sieboldiana and of the Pliocene (Tertiary) to the middle of the Pleistocene H. montana can be discriminated in the length of pedun- (Quaternary) in these two species. Some wood plants cle, the color of perianth, the opened angle of the corolla, such as Chamaecyparis obtuse and Aesculus turbinate have and the white powder of the back side of leaves. Hosta shown the possibility that there have been refugia of high albomarginata has also been regarded as more than one mountains in the western parts. Finally, phylogeographic species; the populations from the northern part of the divergence was detected between Hokkaido and Honshu Japanese archipelago have been treated as H. rectifolia islands (Aizawa et al. 2007; Hu et

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