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Systematics and Phytogeography |
Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650204, China
Received for publication August 19, 2005. Accepted for publication February 13, 2006.
ABSTRACT
Spiraea japonica, a diverse, perennial shrubby species complex widespread across E Asia, was a useful model in a first attempt to link specific phylogeny, floristic evolution, and historical environmental changes in E Asia. DNA-based phylogenetic reconstruction served as a framework to investigate whether the patterns of variation in alkaloids and nrITS from varieties of S. japonica reflect the geological history of China and the uplifting of the Himalaya-Tibet plateau, the most significant geological event in E Asia since the late Paleocene. The high geographical structure found in the phylogenetic trees was corroborated by the distribution of alkaloids. All populations from E China, with mainly hetisine-type alkaloids, formed a single clade, sister to a clade of all populations from SW China, with mainly atisine-type alkaloids. The distribution boundary between the two clades roughly matched the floristic division between the Sino-Japanese Forest and the Sino-Himalayan Forest subkingdoms, as well as the environmental division between SW and E China, suggesting a close link between specific phylogeny, floristic evolution, and geographical changes in E Asia. The divergence between lineages at variety and population level within the eastern clade was slightly older than those within the southwestern clade, supporting the hypothesis of a northeast–southwest migration of Spiraea since the Eocene. The uplift of the Himalaya-Tibet plateau and subsequent increase in geographical complexity in SW China, could facilitate divergence maintenance, thus accelerating the evolutionary rate.
Key Words: biological effects • East Asia • environmental heterogeneity • Himalaya-Tibet Plateau uplift • Rosaceae • Spiraea japonica
Spiraea japonica L. f. is a perennial shrubby species complex widespread across East Asia that has received considerable attention in China for its potential medicinal uses. Morphologically, the complex is very diverse with nine intraspecific varieties, discriminated by differences in leaf size and shape (Rehder, 1913
; Yu, 1974
; Wu and Raven, 2003
; Table 1, Fig. 3b). With respect to variation and distribution patterns, the complex seems to reflect some floristic characteristics of the plant flora in the East Asiatic kingdom (Wu and Wu, 1998
). The complex is morphologically most diversified in southwest China, with the majority of varieties occurring in this extremely narrow region. By contrast, only three varieties occupy central and eastern China, Japan, and south Korea, a combined area that is much larger than southwest China (Fig. 1c). From the perspective of dispersal and variation, the S. japonica complex represents a useful model to investigate the correlation between biodiversity patterns and environmental heterogeneity on a large, regional scale.
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; Fig. 1a). The physical environments in the western mountainous plateau and the eastern plains are relatively homogenous, compared with the complex mix of habitats in the transitional belt—these habitats are especially diverse in southwest China. This complexity of habitat types is mirrored by climatic complexity: the eastern plains are affected by the southeastern Pacific monsoon, the western mountainous plateau by the southwestern monsoon from the Indian Ocean, while the transitional belt (especially in southwest China) encounters both monsoons (Committee of Chinese Academy of Sciences for Physical Geography of China, 1985
; Wang, 1994
; Fig. 1a).
Botanical diversity is greatest in the eastern plains and the transitional belt, with fewer plant species in the high western regions. Moreover, bearing almost half of the total plant species in China, the transitional belt, especially the southwest China is an important center for biodiversity, with more than a third of its species being endemic (Wang, 1961
; Wu, 1980
; Wu and Wu, 1998
). Floristic studies (Wu, 1979
; Wu and Wu, 1998
) suggested that the forest area in the East Asiatic Kingdom could be divided into two subkingdoms, namely the Sino-Japanese Forest subkingdom and the Sino-Himalayan Forest subkingdom (Fig. 1b). The formation of these spatiotemporal patterns of biodiversity has long been suspected of correlating with physical environmental changes resulting from the Himalaya-Tibet Plateau uplifting (Chang, 1983
; Tanai, 1992
; Axelrod et al., 1998
). However, the nature and extent of this correlation remains a question. Intensive biological observations of widespread species at population levels may provide insights into the biogeography of this region. In this paper, we use DNA-based phylogenetic reconstruction as a framework to look at alkaloid variation in the S. japonica complex and to look for a correlation between the variation in molecular data (alkaloids, nrITS) from taxonomic varieties of S. japonica and the geological history of China and the Himalaya-Tibet plateau.
MATERIALS AND METHODS
Taxa and sampling
New sequences for Spiraea japonica were produced in present study, while all other sequences were from the databank in National Center for Biotechnology Information (http://www.ncbi.nlm.nih.gov/). The material resources are listed in Table 1 and distribution of the samples in Fig. 1c. All vouchers were deposited in the Herbarium of Kunming Institute of Botany, CAS [KUN]. A total of 14 populations representing eight varieties within the S. japonica complex and S. cantonensis Lour. were analyzed for ITS sequence variation. A total of 13 populations representing seven varieties within the S. japonica complex were analyzed for alkaloid polymorphisms. The sampling strategy was to allow both detection of variation at the intraspecific level and an estimation of variation at the interspecific level.
Producing a chronology of divergence events is essential to make any biogeographical inference in relation to historical events. However, phylogenetic calibrations of the rate of evolution within species have not been possible because of the difficulty in assigning fossils to specific lineages at the species level. As a result, most estimates of molecular evolution rates have been at the level of genera or higher (Drummond et al., 2003
). To provide calibration points in a divergence time analysis (explained later), we reconstructed a more inclusive phylogeny. A species of the closely related genera Sorbaria [S. sorbifolia (L.) A. Br.] was included in the phylogenetic reconstruction, and one species of each of the two genera Rosa L. and Rubus L. were used as distant outgroups. The inclusion of Sorbaria sorbifolia was based on reviews (Yu, 1984
; Lu, 1996
) of the subfamily Spiraeoideae, and the outgroup choice was based on phylogenetic placements in a rbcL analysis (Morgan et al., 1994
), as well as allowing inclusion of fossil information of Spiraea (Heer, 1869
; Knowlton, 1894
; Hollick, 1936
; Committee of Chinese Academy of Sciences for Plant of Cenozoic China, 1978
) and Sorbaria (Tao and Xiong, 1986
; Tao, 2000
) for data calibration in the divergence time analysis (described later).
Alkaloid extraction
Procedures for alkaloid extraction and isolation from 13 populations representing seven varieties within the Spiraea japonica complex followed Fan et al. (2004)
. Dried powder of whole plants was extracted with ethanol by reflux. The ethanol extracts were suspended in 5% hydrochloric acid and centrifuged. The supernatants were neutralized with aqueous ammonia solution to pH 10, and extracted with chloroform. After repeated column chromatography over silica gel (200–300 mesh, eluted with petroleum-ether–acetone–diethylamine [100 : 5 : 1, 100 : 10 : 2, 85 : 15 : 5, v/v/v]) and petroleum-ether–chloroform–diethylamine (100 : 3 : 1, 90 : 10 : 3, 80 : 20 : 5, 75 : 25 : 5, 60 : 40 : 5, v/v/v) and over Sephadex LH-20 reversed-phase C-18 silica gel, alkaloids were recrystallized from petroleum-ether–acetone. Structures of extracted alkaloids were determined by comparing spectroscopic data (mass spectrometry and 1H and 13C nuclear magnetic resonance) with those previously reported.
DNA extraction and sequencing
Total DNA was extracted from silica-gel-dried leaf tissue according to a modified CTAB procedure (Doyle and Doyle 1987
). Double-stranded DNA was directly amplified by symmetric PCR amplification with the ITS5 and ITS4 primers (White et al., 1990
). Reaction volumes were 20 µL and contained 1.5 units AmpliTaq (TaKaRa Biotechnology, Dalian, China) DNA polymerase, Replitherm buffer (TaKaRa Biotecnology), 1.5 mmol/L MgCl2, 0.4 mmol/L dNTPs, 0.1 µmol/L primer, 5% dimethyl sulfoxide, 25–60 ng sample DNA. PCR was performed in a GeneAmp 9600 thermal cycler (Perkin-Elmer, Applied Biosystems, Foster City, California, USA) and consisted of 30 cycles of 1.5 min at 94°C for template denaturation, 2 min at 55°C for primer annealing, 1 min at 72°C for primer extension, followed by a final extension of 7 min at 72°C. PCR products were purified with a purification kit (Promega, Madison, Wisconsin, USA) prior to being sequenced. Double-stranded purified PCR products were sequenced by the dideoxy chain termination method with an ABI PRISM BigDye Terminator Cycle Sequencing Ready Reaction kit (Applied Biosystem, Foster City, California, USA) with AmpliTaq DNA polymerase FS (Perkin-Elmer). Reactions and programs were chosen according to the recommendations of the manufacturer's handbook (Perkin-Elmer, Applied Biosystem). Samples were electrophoresed in an ABI310 automated sequencer.
Phylogenetic analysis
The DNA sequences were edited in Seqman (Lasergene, DNASTAR Inc., Madison, Wisconsin, USA). The ITS region limit was determined by referring to the published sequence of S. cantoniensis. Sequences were aligned in Megalign (DNASTAR Package) with minor manual adjustments where necessary.
The phylogenetic reconstruction was performed with PAUP* (Swofford, 2002
) using maximum-parsimony (MP) and maximum likelihood methods. For MP analysis, characters were weighted equally and gaps treated as missing data; a heuristic search strategy with stepwise data addition (1000 random replications) and tree-bisection-reconnection (TBR) branch swapping was applied to search trees; parsimony trees with equal length were summarized using the 50% majority rule as well as strict rule consensus method; bootstrap values were calculated from 1000 pseudoreplicate analyses with the same heuristic search strategy to assess the relative support for each clade. For ML analyses, the best-fitting model of nucleotide substitution (TrN + G) was selected based on likelihood ratio tests (LRTs) implemented in Modeltest version 3.06 (Posada and Crandall, 1998
). ML analyses were performed with PAUP* specifying the optimal model as reflected by the LRTs implemented in Modeltest v3.06. A heuristic search strategy with stepwise data addition (1000 random replications) and TBR branch swapping was used for searching trees, and bootstrap values were calculated from 1000 pseudoreplicate analyses applying a heuristic search strategy with stepwise data addition and TBR branch swapping.
Estimation of divergence time
Bayesian approaches are a valuable method for divergence time estimation without assuming a constant molecular mutation rate, albeit with methodologies still being refined (Kishino et al., 2001
; Thorne and Kishino, 2002
). Divergence times in the present study were estimated with Bayesian approaches using the software Multidivtime (Thorne and Kishino, 2002
) and PAML (Yang, 1997
). A chosen MP tree and the sequence data were input into the PAML package to estimate the maximum likelihood of the branch lengths of the tree and the variance–covariance matrix. The prior and posterior distribution of substitution rates and divergence times were approximated by performing a Bayesian Markov Chain Monte Carlo (MCMC) analysis in the Multidivtime package.
Specification of prior distributions for parameters is indispensable to the Bayesian method. The prior mean and standard deviation for gamma-distributed time of the ingroup root node (rttime and rttimesd) was set to 43 million years. The value was an estimate based on the split of Spiraea and Sorbaria. Fossil reports of Spiraea are much more abundant than that of Sorbaria, although fossil records are available for both genera. Over a long period, various authors (Heer, 1869
; Knowlton, 1894
; Hollick, 1936
) had identified oldest fossil Spiraea from within different Eocene sediments (53–33.7 myr). In contrast, essentially only one report (Tao and Xiong, 1986
; Tao, 2000
) indicated the existence of fossil Sorbaria in late Cretaceous sediment (96–65 myr). In addition, Tao and Xiong (1986)
pointed out that the analogues of the leaf fossils used as evidence of the existence of Sorbaria were very few; only two were found. Normally, the reliability of fossil information is dependent upon the number of available fossils and sediments to corroborate its existence and how many authors have identified these fossils. In this case, the minimum age of the split between Spiraea and Sorbaria was conservatively dated back to the Eocene (53–33.7 myr, with mean value c. 43 myr). Other data-dependent settings were also applied in the multidivtime control file according to recommendations in the manual: (1) Length, sampling frequency, and burn-in period of the Markov chain were set to 100 000 trees sampled every 100th generation, with a burn-in of 100 000 trees. (2) The priori rate at the root node (rtrate) was set to 0.005, calculated by dividing the median distance between the ingroup root and the ingroup tips obtained from estbranches by the time unit. (3) The prior for the Brownian motion parameter nu (brownmean), which determines the permitted rate change between ancestral and descendant nodes, was set to 0.023, following the manual's recommendation that the time units between root and tips to the power of nu be about 1; the standard deviation on nu was also set to 0.023. In addition, as stated previously, it is difficult to get appropriate calibration points in divergence time estimation at intra-specific level, although the Bayesian approach has the advantage of allowing multiple calibrations. We used only one calibration point in this study: the split of Spiraea and Sorbaria, which was calibrated at 53–33.7 myr.
RESULTS
Alkaloid polymorphism within the Spiraea japonica complex
The alkaloid survey indicated that the alkaloids were good indicators for geographical varieties or populations of the S. japonica complex. Two types of fundamental molecular skeletons (Fig. 3b) recognizable for the alkaloids (the atisine and hetisine types) were highly homologous. Although both comprised a skeleton of 20 C atoms C20 was connected to C7 by an O-bridge in the atisine type, while C20 was connected to C14 in the hetisine type. Accordingly, the alkaloids could be classified into two groups: alkaloids produced by populations from the southwest China were mainly the atisine type, while those by populations from the east China were mainly of hetisine type (Table 1, Fig. 3b).
Sequence characteristics and phylogenetic reconstruction
Characteristics of the ITS region of the S. japonica complex are shown in Table 2. The seven most parsimonious trees were recovered from the parsimony analysis with a length of 358 steps, a CI of 0.897, an RI of 0.908, an RC of 0.814, and a single ML tree (Fig. 2a) was recovered from the likelihood analysis with a –lnL being 2562.66024. The MP trees and the ML tree were similar. Both kinds of tree topology were highly geographically structured and matched the alkaloid distribution pattern (Figs. 2, 3). In the MP tree (Fig. 3a), which was most fully resolved and used in the Bayesian analysis, all populations (varieties) from the east formed a clade with 99% bootstrap support (for convenience, only bootstrap values under parsimony criterion are presented here), while all populations (varieties) from the southwest China formed another clade, also with high bootstrap support of 100%. However, phylogenetic structure within the two clades was ill-defined, with variable levels of bootstrap support. In a clade consisting of the western populations, the monophyletic nature of var. stellaris was supported with a bootstrap value of 94%. The close relationship of var. incisa and var. acuta was also supported, with the two varieties being sister to each other within a subclade with 88% bootstrap support. The monophyletic nature of var. ovalifolia was also weakly supported with a bootstrap value of 65%. Accessions of var. acuminata were unresolved at the base of this clade. In the clade consisting of the eastern populations, the monophyletic nature of var. glabra was supported with a bootstrap value of 86%. A clade containing populations of var. fortunei, the only tetraploid variety, had a lower bootstrap value (59%), and was sister to a weakly supported clade bearing the diploid varieties from the east (var. glabra and var. japonica).
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Biodiversity pattern displayed by the S. japonica complex
Four aspects of the revealed biogeographical patterns of the S. japonica complex deserve attention. First, the S. japonica complex is morphologically most diversified in southwest China, with the majority of the varieties occurring in this extremely narrow region. By contrast, only three varieties occupy the eastern part, which is much larger than the southwest region (Fig. 1). Second, the phylogeny of the S. japonica complex reconstructed by ITS sequences was corroborated by the distribution pattern of alkaloids (Table 1; Fig. 3), and the distribution boundary between the two major clades roughly matched the division line between the Sino-Japanese Forest Subkingdom and the Sino-Himalayan Forest Subkingdom, as well as the division of environmental heterogeneity between the east and the transitional belt (Table 1, Figs. 1, 3). Third, the only tetraploid variant (S. japonica var. fortunei) occurs around this division line suggesting a possible correlation between environmental changes and polyploidization (Fig. 1). Fourth, the average sequence divergence among populations within the southwestern group is slightly higher than that within the eastern group (Table 2), while divergence times estimated for the southwestern group are younger than that for the eastern clade (Table 3), suggesting a difference in the evolutionary rate between the east and the southwest.
General known picture of the natural history and presumed migration and dispersal of Spiraea in East Asia
During the early Tertiary, East Asia was rather even in geography, with the altitude gradually decreasing from the east to the west, while the continent was climatically dominated by a planetary wind belt (Committee of Chinese Academy of Sciences for Physical Geography of China, 1984
; Wang, 1984
; Liu and Ding, 1984
). Since the late Palaeocene (about 55myr), East Asia has changed greatly topographically and climatically; the western regions has undergone phased uplift with the development of the Himalaya, while the east has remained comparatively stable (Committee of Chinese Academy of Sciences for Physical Geography of China, 1984
; Sharma, 1984
; Harrison et al., 1992
; Molnar et al., 1993
). By the Miocene, the topological configuration of East Asia had been radically reshaped. The formerly lower western region had been uplifted higher than the east (Committee of Chinese Academy of Sciences for Physical Geography of China, 1984
; Chung et al., 1998
) and underwent further uplift (Sharma, 1984
; Molnar et al., 1993
). By the Early Quaternary, the present topography of East Asia had largely taken shape, with the three distinguishable regions of environmental heterogeneity (Committee of Chinese Academy of Sciences for Physical Geography of China, 1984
; Committee of Chinese Academy of Sciences for Collection of Articles on Tibet Plateau, 1999
; Fig. 1a, b). Meanwhile, this geographic evolution in East Asia was accompanied by climatic changes, including global cooling (Collinson et al., 1981
), and the formation of a monsoon system in East Asia (Quade et al., 1989
). The global cooling led to the southward movement of climate belts, and the development of different monsoon systems affected sites regionally (Guo, 1981
; Liu and Ding, 1984
). Presumably, this history of environmental changes has influenced floristic evolution in East Asia.
A hypothesis for the migration and dispersal of Spiraea in East Asia since the Eocene can be developed, given that fossils of Spiraea were found in Eocene, Oligocene, and Miocene sediments in Alaska, Europe, and East Asia, respectively (Heer, 1869
; Knowlton, 1894
; Hollick, 1936
; Committee of Chinese Academy of Sciences for Plant of Cenozoic China, 1978
). The origin of Spiraea can be dated back at least to the Eocene based on the fossil records. During the Eocene, the temperate zone was still located at higher latitudes (Committee of Chinese Academy of Sciences for Physical Geography of China, 1984
; Wang, 1984
; Liu and Ding, 1984
; Tanai, 1992
). At that time, therefore, occurrence of Spiraea as a temperate plant would be limited to the higher latitudes; this is corroborated by the fact that fossils of Spiraea have so far only been found at higher latitudes. With global cooling in the Cenozoic and the southwards movement of the climate belts, it is conceivable that ancestral Spiraea also migrated southward to reach its present occurrence latitude. During the southward migration of Spiraea, the development of an arid belt from northwest to southeast in central East Asia since the Paleogene (Wang, 1988
) would have prevented Spiraea from reaching southwest China directly from the north. Therefore, Spiraea in southwest China today may have migrated from the northeast China after the gradual retreat of the arid belt (Wang, 1988
).
Biogeography implications
The biodiversity patterns of the S. japonica complex and the approximate estimates of divergence times resulting from the Bayesian molecular dating are compatible with the environmental and floristic history of East Asia. The finding of two main clades in the ITS phylogeny and the agreement of the distribution pattern of alkaloidsin the S. japonica complex with the two clades suggest a divergence early in the evolution of S. japonica. This divergence between the two main lineages was dated to 19.87 mya, corresponding to the second stage of Himalayan movements. Thus, the divergence may be correlated with the hypsography transformation during this period.
During the Miocene, environmental conditions were suitable for temperate plants in southwest China (Committee of Chinese Academy of Sciences for Physical Geography of China, 1984
; Wang, 1984
; Liu and Ding, 1984
; Tanai, 1992
), and it was possible for an ancestral form of S. japonica to have migrated here from the northeast. It is conceivable that the two clades of S. japonica diverged from their common ancestor during this migration, adapting to the great environmental changes caused by the second phase of uplift of the Himalaya (Chung et al., 1998
). Since then, the two clades have been exposed to different environmental conditions, and divergence between varieties within the two major clades are estimated to have occurred within the last 10 myr. Although the eastern part of East Asia has been affected by geological events, the physical environment has remained relatively stable and homogenous (Committee of Chinese Academy of Sciences for Physical Geography of China, 1985
). Arguably, fewer geographical barriers, weaker divergent selection pressures, higher gene flow, and fewer bottleneck events could be expected for populations growing in this region. This is supported by the comparatively low morphological and genetic differentiation among populations for the eastern S. japonica group (Table 2). In contrast, a different evolutionary scenario can be envisaged for the southwestern clade. Southwest China is located at the boundary belt between Eurasia, the Indian subcontinent, and the Burma-Malaya Geoblock, with the interface being directly impacted by continental collision (Zhang et al., 1984
; Sengor and Natal'in, 1996
). With further development of the Himalaya movement, physical environmental heterogeneity in this region has increased continuously, with plateaus, mountains, basins, and gorges compressed within a narrow geographical mosaic (Committee of Chinese Academy of Sciences for Physical Geography of China, 1984
). This was intensified by the third phase of Himalayan movements during the early Quaternary, with extreme environments developing (Committee of Chinese Academy of Sciences for Physical Geography of China, 1985
). This increased environmental complexity could have resulted in more geographical barriers, higher selection pressures, greater isolation, and less gene flow between populations. All these factors might explain the higher divergence and diversification among S. japonica populations within the southwestern group. Moreover, the estimations of evolutionary rates at internal nodes within the southwestern clade are slightly higher than those for the eastern clade (Table 3). This suggests that higher evolutionary rates might have contributed to the diversification of the southwestern group and that the rate increase might be correlated with a large number of factors such as environmental stress, reduced population sizes, and strong, changing selection pressures.
It is a general principle that the higher the genetic divergence between two phylogenetic lines, the earlier the two lines diverged. This has been widely applied in the interpretation of biogeographical history using sequence data (for example Richardson et al., 2001
). Our observation of the S. japonica complex suggests caution in the use of this principle. As we stated earlier, a migration of S. japonica from the northeast to the southwest China is one hypothesis as to how S. japonica reached southwest China, and diversification of the southwest group could be related to the environmental heterogeneity associated with the relatively recent phase of the Himalayan movements. Therefore, we presume that the divergence of phylogenetic lines from each other in the eastern group might be prior to that in the southwest group. This point is corroborated by the Bayesian molecular dating (Table 3). However, the detected divergence among the supposedly younger phylogenetic lines in the southwest group was slightly higher than that for the eastern group (Table 2). A possible explanation might be that although molecular mutation of closely related taxa typically occurs at a similar rate, different areas with different environments will vary in mutation accumulation or divergence maintenance and consequently differ in detectable evolutionary rate. In effect, the increased environmental complexity in southwest China could facilitate different divergence maintenance compared with the homogenous environment in eastern China and hence contribute toward the observed patterns.
Summary
In terms of the distribution of East Asian flora, two of the most notable features are the rich biodiversity center of southwest China, and the east–west axial floristic divergence (Wu, 1979
; Wu and Wu, 1998
). In this paper, we conclude that the specific phylogeny of S. japonica is closely linked to the general floristic evolution and historical environmental changes in East Asia. More specifically, physical environmental changes stemming from the Himalaya-Tibet plateau uplifting might have played a key role in specific phylogeny and origination of polyploid variants. More generally, in the floristic evolution in the region, the increased environmental complexity that facilitated divergence maintenance might be a key reason for the high biodiversity in southwest China. However, further studies are required to assess the extent to which the Himalaya-Tibet uplifting is responsible for the formation of the present biodiversity patterns in East Asia.
FOOTNOTES
1 The authors thank M. Hollingsworth and two anonymous reviewers for critical comments that greatly improved the manuscript, X. Gong for kindly providing resources to keep the cultivated plants, Y. Y. Chen and L. M. Gao for experimental help, and D. Melick for improving the English. This study was financially supported by the National Natural Science Foundation of China Project 30270120, the Xibuzhiguang Project of CAS, and the Provincial Natural Science Foundation of Yunnan Project 2004C0021G. 
2 Author for correspondence (zhangzy{at}mail.kib.ac.cn
)
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