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Brief Communication |
Graduate School of Human and Environmental Studies, Kyoto University, Sakyo-ku, Kyoto 606-8501, Japan; 3Agricultural and Forestry Office, Hyogo Prefectural Government, Asago 669-5202, Japan; 4Division of Ecological Restoration, Museum of Nature and Human Activities, Hyogo, Sanda 669-1546, Japan; and 5Makino Herbarium, Tokyo Metropolitan University, Hachioji, Tokyo 192-0397, Japan
Received for publication January 25, 2006. Accepted for publication October 9, 2006.
ABSTRACT
Climate changes during glacial periods have had significant effects on the present geographic distribution of plant species. To elucidate the evolutionary history of a plant species with a disjunctive distribution, we investigated the geographic distribution patterns of cpDNA haplotypes in Photinia glabra (Rosaceae) growing in broadleaved evergreen forests in Japan. We examined cpDNA in 42 populations of P. glabra sampled over a geographic range that included Kinki and its surrounding areas and the disjunctive regions in the Amakusa Islands. Both areas had unique cpDNA haplotypes. Moreover, the AMOVA revealed that a large proportion of the total variance (51%, P < 0.001) could be explained by differences among these regions. These results suggest a past fragmentation of this plant species into two separate refugia: southwestern Kyushu and Kinki, including the surrounding area, during the Quaternary glacial periods. A particularly interesting result was that in the southern disjunct distribution in the Amakusa Islands, the genetic subdivision (
CT = 1.00, P < 0.001) appears to lie between the populations from nearly contiguous islands located across a fairway only approximately 80 to 150 m in width.
Key Words: biogeography • broadleaved evergreen forest • chloroplast DNA • glacial refugia • intraspecific variation • Japan • Photinia glabra • phylogeography
The current geographic distribution of living organisms is the result of both present and past ecological factors. The warm temperate and subtropical zones in Japan are now covered with forests dominated by broadleaved evergreen trees. The current geographic distribution of the component species of broadleaved evergreen forests is primarily the result of present climatic conditions such as temperature, precipitation, snowfall, and on-shore winds (Hattori, 1985
); in particular, the diversity of plant species in these forests has a high positive correlation with the monthly mean temperature of the coldest month (Hattori et al., 2002
). However, some component species have geographic distributions that do not coincide with the environmental conditions mentioned and cannot be accounted for by present environmental conditions alone. It has been reported that the glacial–interglacial cycles of the Quaternary period had a major influence on the current geographic distribution of these forests. Before the Quaternary period, broadleaved evergreen forests were dominant in the Japanese lowlands, and these forests underwent cold periods at least four times during the Quaternary (Tsukada, 1974
; Minato and Ijiri, 1976
). During glacial advances, climatic cooling caused southward and lower-land shifts in the geographic distribution of broadleaved evergreen forests. During the last period of cooling, approximately 20 000 years ago, these forest species were restricted to southern refugial populations, but after climate warming, these species spread to the present areas of distribution. We can account for the present geographic distribution of these forest species by considering the past geographic distribution (i.e., the respective regions where each species survived), together with present climatic conditions.
Phylogeography has become a powerful approach for investigating postglacial migration and dispersal and is especially useful for the study of plants that have not been preserved well in the palynological record (Avise, 2000
; Cruzan and Templeton, 2000
). Moreover, phylogeographic studies could provide a basis for identifying suitable units for conservation, evolutionarily significant units (ESUs) (Newton et al., 1999
). With respect to plant species, chloroplast DNA (cpDNA) is considered to be appropriate for the reconstruction of past migrational routes from many perspectives (Petit et al., 1993
). Numerous studies have reported the geographic distribution of intraspecific cpDNA variation (Demesure et al., 1996
; Dumolin-Lapègue et al., 1997
; Ferris et al., 1998
; Fujii et al., 2002
; Aoki et al., 2003
, 2004a
; Griffin et al., 2004
). It has become of interest to compare the intraspecific phylogeographic patterns among several taxa over the same area and to search for congruent geographic patterns of genetic variation, which would indicate the influence of common historical factors (Avise, 1992
; Fujii et al., 1997
; Soltis et al., 1997
; Taberlet et al., 1998
; Hewitt, 1999
, 2004
; Arbogast and Kenagy, 2001
; Stewart and Lister, 2001
; Brochmann et al., 2003
; Petit et al., 2003
; Stehlik, 2003
; Aoki et al., 2004b
; Seo et al., 2004
).
In our previous study we selected six plant species (Prunus zippeliana, Alpinia japonica, Daphne kiusiana, Elaeocarpus sylvestris var. ellipticus, Arachniodes sporadosora, and A. aristata) growing in Castanopsis-type broadleaved evergreen forests with a similar geographic distribution in Japan (along the Pacific coast up to the Boso Peninsula as the northern limit of distribution) and investigated their intraspecific cpDNA phylogeographic patterns (Aoki et al., 2004b
). The pollen record indicates that refugial populations of these forests existed in southern Kyushu and migrated northwards from this southern refugia after the last glacial maximum (Tsukada, 1974
, 1984
; Matsuoka and Miyoshi, 1998
). However, broadleaved evergreen forests may also have survived in multiple refugia along the Pacific coast during the glacial periods (Maeda, 1980
; Kamei and Research group for the biogeography from Würm Glacial, 1981
(fig. 5); Hattori, 1985
, 2002
). In our previous study (Aoki et al., 2004b
), we compared the intraspecific phylogeographic patterns among six plant species growing in these forests with respect to two parameters (i.e., cpDNA haplotype uniqueness and haplotype diversity) to test the single vs. multiple refugia hypotheses. We located the important refugia during glacial periods in the area from Muroto to Kii Peninsula in addition to the southern Kyushu area.
Most of the geographic distribution patterns of cpDNA haplotypes in the six plant species were not clearly structured. In this study, we selected Photinia glabra, which is disjunctively distributed in Japan, from the 14 species with relatively large intraspecific cpDNA variations (Aoki et al., 2003
). The geographic distribution patterns of cpDNA haplotypes in a plant with a disjunctive distribution might be much more clearly differentiated among populations than those in the six plant species with a continuous geographic distribution along the Pacific coast.
Photinia glabra (Thunb.) Maxim. (Rosaceae) is a tree species that grows in broadleaved evergreen forests in Japan. The species occurs primarily in Kinki and the eastern Shikoku and Chugoku regions. Disjunct populations are known in the Amakusa Islands in southwestern Kyushu. The present distribution area of the plant species is shown in Fig. 1.
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MATERIALS AND METHODS
Plant materials
A total of 129 individuals of Photinia glabra from 42 populations, comprising 1–7 individuals per population, were sampled over a geographic range from Kinki to Shikoku, and the Amakusa Islands (including both Kamishima and Shimoshima islands). A sample of P. serratifolia K. from Taiwan was also collected for the outgroup of P. glabra. Fresh or silica-gel-dried leaves were collected from these sites (Appendix 1).
Sequencing of noncoding regions of cpDNA
Total DNAs were extracted using a 2x CTAB (hexadecyltrimethyl ammonium bromide) buffer according to the method of Doyle and Doyle (1987)
. Ten noncoding regions of cpDNA were amplified using the universal primers designed by Taberlet et al. (1991)
, Chiang et al. (1998)
, and Nishizawa and Watano (2000)
(Appendix S1, see Supplemental Data with online version of this article). The polymerase chain reaction (PCR) products were purified using a QIAquick Gel Extraction Kit (Qiagen, Valencia, California, USA) after electrophoresis in 1.0% agarose gels, and they were then used as templates for direct sequencing.
The sequencing reactions were prepared using a Big Dye terminator cycle sequencing kit (Applied Biosystems, Foster City, California, USA). The reaction mixtures were analyzed with an Applied Biosystems model 3100 genetic analyzer. The sequences were aligned using Sequence Navigator software (Applied Biosystems) and SeqPup version 0.6 (Gilbert, 1996
).
Data analysis
Calculations of haplotype (gene) diversity (Nei, 1987
), nucleotide diversity (
), the average number of nucleotide differences per site between two sequences (Nei, 1987
), and the Watterson estimator (
), that is, the number of segregating sites per site (Watterson, 1975
), were carried out using DnaSP version 4.0 (Rozas et al., 2003
). Relatedness between haplotypes was represented by a statistical parsimony network, generated by the program TCS (Clement et al., 2000
). Interpopulation differentiation and partitioning of cpDNA variation was estimated to quantify the degree of genetic differentiation between the two separate regions under study (the Amakusa Islands and Kinki including its surrounding area) using -statistics (Weir and Cockerham, 1984
) within the analysis of molecular variance framework (AMOVA; Excoffier et al., 1992
). The significance of fixation indices was tested using a nonparametric approach (Excoffier et al., 1992
). All analyses were performed using the ARLEQUIN software package (version 2.0; Schneider et al., 2000
).
RESULTS AND DISCUSSION
Intraspecific cpDNA variation
Nucleotide sequences of the 10 noncoding regions of 129 Photinia glabra samples collected from 42 sites in Japan were determined. The total length of the 10 noncoding regions varied from 4062–4087 bp (Appendix S1, see Supplemental Data with online version of this article). The length after multiple alignment of the sequences was 4111 bp. Aligned sequences of polymorphic sites and sequence variability are summarized in Table 1. The obtained sequences have been deposited in the DNA Databank of Japan (DDBJ) database under accession numbers AB191050–AB191061 and AB235099–AB235114. We detected cpDNA variations based on indels, including mononucleotide repeat length variations as well as nucleotide substitutions. In P. glabra, four distinguishable cpDNA haplotypes were recognized. The network of cpDNA haplotypes showed that haplotypes B, C, and D were distinguished from haplotype A by one nucleotide substitution and two indels, three nucleotide substitutions and three indels, and three nucleotide substitutions and six indels, respectively (Fig. 1). The calculated values of haplotype (gene) diversity, nucleotide diversity (), and Watterson estimator () are given in Table 2.
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), we observed no clear relationships between genetic and geographic distances among the cpDNA haplotypes in the six plant species examined, Prunus zippeliana, Alpinia japonica, Daphne kiusiana, Elaeocarpus sylvestris var. ellipticus, Arachniodes sporadosora, and A. aristata. In this study, the geographic distribution of the recognized cpDNA haplotypes showed strong geographical structuring (Fig. 1). The analysis of molecular variance (AMOVA) showed that a large proportion of the total variance (51%, P < 0.001) was explained by differences among regions when comparing the Amakusa Islands and the rest of the northern region (i.e., Kinki to Kii Peninsula, and Shikoku) (Table 3). This result suggested that these two separately distributed groups have strong genetic differentiation.
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CT = 1.00, P < 0.001), though these two islands are located across a fairway only approximately 80 to 150 m wide. It is surprising that no sharing of haplotypes has been observed between the populations from two nearly contiguous islands in Amakusa. It has never been reported that a suture zone of Amakusa Island is important as a genetic boundary for other plant species. Seed dispersal of Photinia glabra seems to be by birds, considering that this species has small red pome fruits like other Rosaceae species. However, our results suggest that genetic exchange via seed by birds did not frequently take place over long periods between the northern and southern islands in the Amakusa Islands. In Europe, high genetic differentiation and a clear phylogeographical structure has been detected in a fleshy-fruited tree species (Hampe et al., 2003
). This and the present case indicate that the relation between bird-mediated seed dispersal and low levels of cpDNA differentiation may not be as straightforward as has sometimes been assumed. It may be that seed dispersal by birds is not always predictable. Some subtle differences in environment on Kamishima and Shimoshima islands may also result in such a genetic boundary. Regardless, the genetic boundary between the populations from the nearly contiguous islands found in this study would also provide valuable information for the careful design of conservation programs facilitating transplantation of wild plants between adjacent populations.
Phylogeographic patterns in P. glabra
The cpDNA haplotypes B and D were restricted to Kinki and surrounding areas, and haplotype C was distributed only in Amakusa. Thus, both areas had unique cpDNA haplotypes of P. glabra. Moreover, the extent of genetic differentiation between the two areas was high (CT = 0.51). These results suggest a past fragmentation of this plant species into two separate regions (i.e., around Kyushu and around Kinki). Within the northern region, haplotype A was found to be relatively abundant from Shikoku and was virtually absent from the Kii Peninsula. In contrast, haplotype D was absent from Shikoku and was abundant on the Kii Peninsula. Although the AMOVA revealed no significant differences (CT = 0.03) between the Shikoku (locality nos. 15–18) and the Kii Peninsula (locality nos. 32–42), these findings suggest that in the past, the populations from Shikoku and those from Kii Peninsula may have had different sources.
In our previous study (Aoki et al., 2004b
), we compared the intraspecific phylogeographic patterns among six plant species with respect to cpDNA haplotype uniqueness and haplotype diversity. Many rare haplotypes and the greatest numbers of haplotypes were observed in Kyushu, a finding that agreed with fossilized pollen data demonstrative of the past existence of refugia in southern Kyushu (Tsukada, 1974
). We have also hypothesized that additional important refugia existed during glacial periods in the area from Muroto to Kii Peninsula, where pollen records of broadleaved evergreen species are insufficient. The geographical distribution area of P. glabra is currently too narrow to compare with those of the six plant species and to locate its refugia in the past. However, the phylogeographic pattern of cpDNA in P. glabra in this study also supports the existence of two refugia, i.e., southern Kyushu and the Muroto to Kii Peninsula areas. The geographic distribution of P. glabra has probably been restricted to the two refugia with other component species of broadleaved evergreen forests during repeated glacial periods in the Quaternary period. After climate warming since the last glacial maximum approximately 20 000 years ago, these surviving populations may have expanded very slowly, and the populations still have not come into contact. In this study, the recognized cpDNA haplotypes were clearly geographically structured, though the data were based on the equivalent of a single gene locus. In future studies, a comparison of the genetic structures of cpDNA and nuclear genomic markers should provide more insight into the genetic consequences of postglacial migration. For the populations of the Amakusa Islands, further analyses of genetic structures using nuclear genomic markers such as allozymes or AFLP polymorphisms should reveal whether dispersal via pollen between two nearby populations from Kamishima and Shimoshima has occurred.
In conclusion, our study shows clear phylogeographic patterns among the cpDNA haplotypes in plant species from the broadleaved evergreen forests in Japan. A particularly interesting result was that in the southern disjunct distribution range, an unexpected genetic boundary was found between the populations from nearly contiguous islands. Future work investigating phylogeographic patterns in plant species with a similar geographic distribution as that of P. glabra would be valuable for determining whether the plants display similar migratory histories and gene flow restriction. Such studies would undoubtedly lead to a better understanding of the biogeographic history of broadleaved evergreen forests in Japan. In the future, by comparing the phylogeographic patterns among plant species growing in various climatic zones in Japan (for example, beech forests in a cool temperate zone), we may be able to discuss historical processes generating the present geographical distribution of plants in Japan.
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1 This study was partly supported by a grant from the Museum of Nature and Human Activities, Hyogo, by a Grant-in-Aid from the Japan Society for the Promotion of Science no. 1701416 to K.A. and no. 16405014 to N.M., and by a Grant-in-Aid for 21st Century COE Research Kyoto University (A14). 
2 Author for correspondence (e-mail: aoki{at}sys.bot.kyoto-u.ac.jp
)
101 This study was partly supported by a grant from the Museum of Nature and Human Activities, Hyogo, by a Grant-in-Aid from the Japan Society for the Promotion of Science no.1701416 to K.A. and no.16405014 to N.M. and by a Grant-in-Aid for 21st Century COE Research Kyoto University (A14).
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