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- 1 Material and methods
- 2 Results
- 3 Discussion
Abstract The aim of the present study was to investigate the phylogeographic patterns of Spiraea alpina (Rosaceae) and clarify its response to past climatic changes in the climate-sensitive Qinghai-Tibetan Plateau (QTP). We sequenced a chloroplast DNA fragment (trnL–trnF) from 528 individuals representing 43 populations. We identified 10 haplotypes, which were tentatively divided into three groups. These haplotypes or groups were distributed in the different regions of the QTP. Only half the populations were fixed by a single haplotype, whereas the others contained two or more. In the central and eastern regions, adjacent populations at the local scale shared the same haplotype. Our phylogeographic analyses suggest that this alpine shrub survived in multiple refugia during the Last Glacial Maximum and that earlier glaciations may have trigged deep intraspecific divergences. Post-glacial expansions occurred only within populations or across multiple populations within a local range. The findings of the present study together with previous phylogeographic reports suggest that evolutionary histories of plants in the QTP are complex and variable depending on the species investigated.
As the largest and highest region, the Qinghai–Tibetan Plateau (QTP) has been considered the most sensitive to historical climate changes (Zheng, 1996; Zheng & Yao, 2004). Thus, it should be possible to trace climate changes as shifts in the distributional range of both the plants and animals that occur there (Zheng, 1996). These shifts can be detected from the genetic structure of current populations, especially with regard to glacial retreat (into refugia) and post-glacial recolonization since the Last Glacial Maximum (LGM; Hewitt, 1996, 2000, 2004; Avise, 2000, 2004). Such a pattern of retreat and recolonization has been found for several alpine species in the QTP (Zhang et al., 2005; Meng et al., 2007; Chen et al., 2008; Yang et al., 2008; Wu et al., 2010). These species retreated into the southeastern refugia and recolonized the platform during the interglacial ages or at the end of the LGM. However, others may have survived through the Quaternary glacial ages at high altitude (Wang et al., 2009a; Jia et al., 2011, 2012). These studies further suggest that although the LGM did not seriously affect the distributional range of the species and that they survived in multiple refugia, previous climatic changes may have led to deep intraspecific divergences (Gao et al., 2007, 2009; Wang et al., 2008a, 2008b, 2009a, 2009b; Opgenoorth et al., 2010; Sun et al., 2010; Wu et al., 2010; Jia et al., 2011). This is understandable given the fact that the massive ice sheet never developed on the QTP and that the coldest climate occurred between 1.2 and 0.4 Ma when the largest glaciation developed, rather than at the time of the LGM (Shi et al., 1998; Zhou et al., 2006). The available data also suggest that plant species with different habits or traits may show contrasting patterns of responses to Quaternary climatic oscillations. In the QTP, more than 1800 alpine species have been recorded at high altitude (i.e. >4500 m asl; Wu et al., 1995). However, the phylogeographic patterns of most species remain unknown.
Herein we report on the phylogeographic structure of Spiraea alpina Pall. (Rosaceae). This shrub is widely distributed at altitudes between 2000 and 4500 m asl in the QTP, with partial extensions to adjacent regions (Lu et al., 2003; Zhang et al., 2006; Potter et al., 2007; Fig. 1). Chloroplast (cp) DNA is maternally inherited in Rosaceae (Soltis & Soltis, 1998) and is therefore a good marker for tracing population or range expansion of the species through seed dispersal (e.g. Meng et al., 2008; Wang et al., 2008a; Weeks, 2008; Pan et al., 2009). In the present study, we examined the sequence variation of all samples using the cpDNA fragment trnL–trnF because this intergenic spacer region has been found to be highly variable within and between the other congeners (Zhang et al., 2006; Potter et al., 2007). We used these population genetic data to trace shifts in the range of this alpine shrub in response to past climatic changes. We were particularly interested in whether this shrub species survived in multiple refugia during the LGM as did other alpine shrubs that occur in the QTP (e.g. Wang et al., 2009b; Sun et al., 2010; Jia et al., 2011).
Figure 1. Map showing locations of the sampled populations of Spiraea alpina and haplotype distribution. a, Genealogical relationships of haplotypes based on the trnL–trnF intergenic spacer of the chloroplast (cp) DNA genome. The diameter of the circles is proportional to haplotype frequency; vertical dashed lines represent missing intermediate haplotypes. Different shading of circles indicates different haplotypes and these correspond to the shaded circles that appear on the map. b, Map of China showing the Qinghai–Tibetan Plateau. The map is reproduced with permission from the Data-Sharing Network of Earth System Science (http://www.geodata.cn, accessed 20 May 2009).
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- Top of page
- 1 Material and methods
- 2 Results
- 3 Discussion
The present study revealed a high level of population differentiation with GST= 0.737 and low genetic diversity within populations of S. alpina (Table 1). This was confirmed by AMOVA analyses, which indicated that 79.41% of the total genetic variation occurred among populations (Table 1). This high between-population differentiation has also been found for numerous other alpine species in the QTP (e.g. Zhang et al., 2005; Chen et al., 2008; Wang et al., 2008a, 2008b; Yang et al., 2008; Zeng et al., 2010). Such genetic structure may arise from strong bottlenecks and founder effects in favoring and/or fixing different alleles in isolated regions (Birky et al., 1989). In fact, the geographical distribution of the three tentative haplotype groups and each of the 10 haplotypes supports this hypothesis (Fig. 1). For example, one clade comprising three haplotypes (H4, H5, and H6) occurred exclusively in the central region westward, whereas another clade consisting of the H7 and H8 haplotypes was distributed more westward. The remaining five haplotypes occurred in the eastern, southern, or western regions. As suggested by Avise (2004), such a high genetic differentiation between populations is usually coupled with distinct phylogeographic structure. Our PERMUT analyses did suggest a distinct phylogeographic structure (GST= 0.737 < NST= 0.819; P < 0.05). This is also similar to that found in other alpine species (e.g. Zhang et al., 2005; Meng et al., 2007; Chen et al., 2008; Wang et al., 2008a, 2008b; Yang et al., 2008; Zeng et al., 2010). In some of these species, such as Juniperus przewalskii (Zhang et al., 2005), Picea crassifolia (Meng et al., 2007), and Pedicularis longiflora (Yang et al., 2008), this pattern resulted from founder effects due to the large-scale range recolonization from the edge refugia. However, for S. alpina (present study), Potentilla fruticosa (Sun et al., 2010), Potentilla glabra (Wang et al., 2009b), and Hippophae tibetana (Jia et al., 2011), the bottlenecks and small-scale range expansions within the local regions may have contributed more to such a high between-population differentiation and distinct phylogeographic structure.
The accurate mutation rate of the cpDNA in S. alpina or congeners remains unknown. However, cpDNA mutation rates in most plants are very low, varying between 1 × 10−9 and 3 × 10−9 substitutions per site per year (Wolfe et al., 1987; Demesure et al., 1996; Posada & Crandall, 2001). Even if the fast rate is assumed, each mutation that resulted in the haplotypes identified within our sequenced trnL–trnF intergenic spacer should have occurred before the LGM (approximately 16 000 years ago; Petit et al., 1997, 2004; Newton et al., 1999). Therefore, at least one refugium was maintained within the current distribution of each haplotype recovered during the LGM. Because some haplotypes (e.g. H9, H10, and H4) were restricted into one or two adjacent populations (Fig. 1), these populations can be considered as independent refugia during the LGM. In addition, some haplotypes (e.g. H1 and H2) were mainly fixed in adjacent populations of one region, but also disjunctly distributed in some population of another region (Fig. 1). The disjunct distributions of the same haplotype in different regions may also represent independent refugia, although we cannot rule out the possibility that long-distance dispersal may have also contributed to such a distribution pattern. However, in most populations recent expansion mainly occurred (monotypic in haplotype fixing, as shown in Fig. 1) or at the local scale (the same haplotype fixed in adjacent populations; Fig. 1). This pattern differs from that seen with large-scale range expansion (Zhang et al., 2005; Meng et al., 2007; Yang et al., 2008), in which the genetic diversity and the number of haplotypes gradually decrease with increasing distance to the recolonization region from the edge refugia (Hewitt, 2000; Heuertz et al., 2004; Petit et al., 2005; Latch et al., 2009). Instead, our results are largely consistent with phylogeographic patterns reported for other species (Wang et al., 2009b; Opgenoorth et al., 2010; Sun et al., 2010; Wu et al., 2010; Jia et al., 2011; Li et al., 2011). Similarly, these species survived the LGM in multiple refugia in the QTP and the post-glacial expansions occurred mostly within populations or across adjacent populations at the local scale.
It is interesting that the H4, H5, and H6 haplotypes comprised an independent group with two mutations from the H3 haplotype. This group may have originated earlier before the LGM; for example, due to earlier glaciations or climatic changes, as found in other alpine species occurring there (Wang et al., 2009a; Jia et al., 2011, 2012). This haplotype group was exclusively distributed in the high-altitude region, suggesting that S. alpina may have survived there even during the early glaciations. However, the early climatic changes may have caused deep intraspecific divergences in this species. In fact, these findings agree well with recent geological and climatic studies of the QTP (Shi et al., 1998). The largest glaciation in the QTP occurred between 1.2 and 0.4 Ma, and even during this stage the total plateau was not covered by the ice sheet. It is likely that a limited number of species may have survived this glaciation at high altitude, but developed the deeply diverged lineages in response to such a climatic change. However, the climatic changes of the LGM were much weaker and therefore had smaller effects on plant shifts.
In conclusion, we found that S. alpina may have survived in multiple refugia and been subjected to deep intraspecific divergences, while the recent expansions occurred mainly within populations or at a local scale if compared with phylogeographic patterns of other shrub or herb species (e.g. Yang et al., 2008; Wang et al., 2009a; Jia et al., 2011, 2012). Together, the results of the present study and these previous reports suggest that evolutionary histories of plants in the QTP are more complex than expected and are highly variable depending on the species studied.