Journal of
Plant Ecology
VOLUME 3, NUMBER 1,
PAGES 9–15
MARCH 2010
doi: 10.1093/jpe/rtp022
Advanced Access published
on 31 December 2009
available online at
www.jpe.oxfordjournals.org
Phylogeography of Potentilla
fruticosa, an alpine shrub on the
Qinghai-Tibetan Plateau
Cui Li1,2,*, Ayako Shimono1, Haihua Shen1 and Yanhong Tang1
1
Environmental Biology Division, National Institute for Environmental Studies, Onogawa 16-2, Tsukuba 305-8506, Japan
Faculty of Environment and Economics, Shanxi University of Finance and Economics, Taiyuan 030006, Shanxi, China
*Correspondence address: Faculty of Environment and Economics, Shanxi University of Finance and Economics,
Taiyuan 030006, Shanxi, China. Tel: +86-351-7666149; E-mail: [email protected]
2
Abstract
Aims
Our objectives were (i) to elucidate the phylogeography of chloroplast DNA (cpDNA) in Potentilla fruticosa in relation to Quaternary
climate change and postglacial colonization, (ii) to infer historical
population range expansion using mismatch distribution analyses
and (iii) to locate the refugia of this alpine species on the QinghaiTibetan plateau during glacial–interglacial periods.
Methods
Potentilla fruticosa is a widespread species distributed on the
Qinghai-Tibetan Plateau. We sampled leaves of P. fruticosa from
10 locations along a route of ;1 300 km from the northeastern plateau (Haibei, Qinghai) to the southern plateau (Dangxiong, Tibet).
We examined the cpDNA of 15 haplotypes for 87 individuals from
the 10 populations based on the sequence data from ;1 000 base
pairs of the trnS–trnG and rpl20–rps12. Phylogenetic relationship
of haplotypes was analyzed using the Phylip software package
and the program TCS. The diversity of populations indices was
obtained using the program ARLEQUIN.
INTRODUCTION
The present distribution of plant species reflects both historical
and contemporary environments (Hewitt 2000, 2004). Examination of the genetic structure of current plants can provide
insights not only into our understanding of the evolutional
history of plant species but also into the distributional process
of the species in the past. Based on this concept, many studies
have been conducted to locate refugia of plant species during
glacial periods and to elucidate the recolonization routes and
process after glacial periods (Bennett 1997; Bennett et al. 1991;
Hewitt 1996; Stehlik et al. 2001).
In the Quaternary ;2 million years ago, the climatic oscillations resulted in glacial and interglacial cycles (Shackleton
Important Findings
With the limited samples, we found that (i) higher nucleotide diversity often occurs in high-altitude populations, (ii) the ancestral haplotypes distribute in the populations with higher nucleotide diversity
than recent haplotypes, (iii) the expansion time of population in the
high altitudes was estimated to be approximately at 52–25 ka BP
(1000 years Before Present, where ‘‘Present’’ is AD 1950) and that
in the low altitudes to be ;5.1–2.5 ka BP and (iv) the source location
of P. fruticosa is at the high altitudes, which might provide refugia for
the species during the interglacial warm periods. The species expanded from the high-elevated locations on the Tanggula Mountains
during the Holocene.
Keywords: alpine plants
Qinghai d Tibet
d
climatic changes
d
cpDNA
Received: 25 September 2009 Revised: 26 October 2009 Accepted:
3 November 2009
and Dyke 1973). In Europe, it is suggested that the alpine
plants expanded their geographical distribution during relatively
warmer interglacial period but retreated to some high altitudinal
area, i.e. refugia during the glacial periods when large area of
glacial ice sheets were developed (e.g. Schönswetter 2002,
2005). However, in Asia, some recent studies have suggested
that the alpine plant species could experience range contraction during interglacial/postglacial periods and range expansion
during glacial periods (Ikeda and Setoguchi 2007). This may be
ascribed to the no-large-scale ice sheet developed in the areas.
It is considered that the Qinghai-Tibetan Plateau had reached
mean altitudes in the range of 4 000–5 000 m perhaps by the
end of the Lower Pleistocene (Kwan et al. 1996). The pollen
fossil studies have also suggested that there were glacial and
Ó The Author 2009. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
All rights reserved. For permissions, please email: [email protected]
d
10
interglacial cycles on the plateau (Tang and Shen 1996a, 1996b).
The current distribution of plants on the Qinghai-Tibetan Plateau is strongly affected by glaciations and paleoenvironments
during the Quaternary (Fort 1996; Hewitt 2000; Kwan et al.
1996; Zhang and Jing 2006). It is suggested that the mountain
glaciers developed without unified ice sheet existed on the
plateau in the late Pleistocene and Quaternary periods (Kwan
et al. 1996; Shi 2002).
The rapid change of topography combining with the plateau
elevation and climate changes should have greatly contributed
to the current spatial pattern and genetic diversity of plant species. The vegetations changed thus alternatively between tundra and forest on the plateau in response to the ice ages (Shi
et al. 1998; Tang and Shen 1996a, 1996b). Since the late Pleistocene, alpine shrubbery steppe and coniferous forest were
found in most parts of the Tibetan Plateau, whereas the
desert-steppe and meadow were found during cold periods.
During the last glaciations, permafrost and desert steppe occupied most areas of the plateau, with sparsely scattered forests
(Shi et al. 1998; Tang and Shen 1996b).
The sequences of chloroplast DNA (cpDNA) noncoding
regions contain variable informative sites, which can be used
for better understanding the introgression and evolutionary history of organisms (Afzal-Rafii and Dodd 2007; Bartish et al. 2006;
Demesure et al. 1996; Du et al. 2009; Fujii et al. 2002; Hewitt
2004). Due to the maternal inheritance, the variation of cpDNA
reflects more geographical structure than nuclear DNA (Grivet
and Petit 2003; Vendramin et al. 1999). Chloroplast DNA is thus
widely used to trace colonization routes in geographical distribution of plant species (Heuertz et al. 2004; King and Ferris
1998). With this property of cpDNA, the current geographical
patterns of cpDNA markers should provide insights to locating
the refugia and elucidating the colonization process of plant species with the change of climate and geology of the plateau.
In this study, we thus analyzed the cpDNA haplotypes and
their geographical structure of P. fruticosa to elucidate its refugia
location and expanding process. P. fruticosa can be widely found
in the temperate Northern Hemisphere. This species is common
to the Qinghai-Tibetan Plateau, in particular to the eastern area
of the plateau where it is a dominant species in the alpine shrublands. The species therefore can provide a good tool to examine
the phylogeography of the plant species on the Qinghai-Tibetan
Plateau. Shimono et al. (submitted for publication) first proposed
that the demographic history of P. fruticosa on the plateau involved population expansion during periods of climatic cooling,
alternating with warmer periods when the population contracted to the interior region. They have found this evidence
from a phylogeographical analysis using matK cpDNA region
of the species. Evidences, however, are still needed to further ensure their findings. We thus tried to use different sample sets as
well as different cpDNA noncoding regions. The sampling area in
the current study covered almost the major distribution area of
the species on the plateau across ;10° latitude and 8° longitude.
Our main objectives were (i) to elucidate the phylogeography of P. fruticosa likely associated to Quaternary climate
Journal of Plant Ecology
change and postglacial colonization, (ii) to infer historical population range expansion using mismatch distribution analyses
and (iii) to locate the refugia of organisms on the QinghaiTibetan plateau during glacial–interglacial periods.
MATERIALS AND METHODS
Sampling and sequencing
Leaf samples were collected from 10 populations across the
Qinghai-Tibetan Plateau (Fig. 1; Table 1). We sampled 4–10
individuals for each population and a total of 87 individuals.
Considering the altitude and topography, the strategies of sampling were designed according to the number sequence
marked as in Fig. 1. The leaf samples were dried and stored
in silica gel after sampling.
Total DNA was extracted using the modified cetyltrimethyl
ammonium bromide method (Murray and Thompson 1980).
The extracted DNA samples were dissolved in 100 ll of TE
buffer (10mM Tris-HCl, 1mM EDTA, pH = 8.0) and analyzed
using the polymerase chain reaction (PCR). Two pairs of primers were used to amplify trnS–trnG and rpl20–rps12, respectively (Hamilton 1999). All fragments were amplified in a total
volume of 15-ll reaction mixture containing 103 buffer, 0.2
mM dNTP (mix of dATP, dGTP, dCTP and dTTP, deoxyribonucleoside triphosphate), 2.5 mM MgCl2, 0.2 lM of each primer
and ;100 ng of 1 U AmpliTaq Gold DNA polymerase (Applied
Biosystems). The PCR condition was as follows: initial denaturation at 94°C for 5 min; followed by 35 cycles of denaturation
at 94°C for 30 s, annealing at 55°C for 1 min and extension at
72°C for 1 min. The PCR products were visualized on 1.0%
Tris-acetate-EDTA agarose gels stained with ethidium bromide.
The products were purified using a QIAquick Kit (Qiagen),
Figure 1: the location of sampled populations. JSJ River, Jinshajing
River; HD Mt, Hengduan Mountains; HMLY Mt, Himalaya Mountains;
KL Mt, Kunlun Mountains; NQTGL Mt, Nianqing Tanggula Mountains; TGL Mt, Tanggula Mountains; YL River, Yellow River; YLZBJ,
Yaluzengbujing River. The numbers circled represent the location
number. The pie chart adjacent to the circled number indicates the
haplotype composition of the corresponding sample. The color square
frames represent the haplotypes.
Li et al.
|
Phylogeography of Potentilla fruticosa
following the protocols. We carried out 20-ll BigDye (Applied
Biosystems) sequencing reactions using 20 ng of purified DNA
following standard protocols, and sequencing was conducted
on an ABI PRISM 3730 Genetic Analyzer (Applied Biosystems)
automatic sequencer with both forward and reverse primers.
The primers used for sequencing were the same as those for
PCR amplification. These chloroplast fragment sequences have
been deposited in the GenBank under the following accession
numbers: GU002403 to GU002423.
Data analysis
Sequences were edited and aligned using BioEdit software
(Hall 1999). Molecular genetic variations such as Haplotype
diversity (h) and nucleotide diversity (p) were calculated using
the ARLEQUIN software version 2.000 (Schneider et al. 2000).
Phylogenetic relationships between the cpDNA haplotypes
were reconstructed using the neighbor-joining (NJ) method
using Phylip version 3.6 software package (Felsenstein
2004). We used bootstrap analysis with 1 000 replicates to
evaluate support for phylogenetic relationships and, in addition, used one sample of Potentilla nivea as an out-group to determine the ancestral haplotype, which was a species in the
same genus with P. fruticosa in the Qinghai-Tibetan Plateau.
The haplotypes networks were constructed using TCS1.06
(Clement et al. 2000). This program uses statistical parsimony
to connect haplotypes based on a 95% confidence interval.
Historic demographic expansions were investigated with the
distributions of pairwise differences between haplotypes (mismatch distributions). The concordance of the observed with
the expected distributions under a sudden-expansion model
was tested with the sum of squared deviations and Harpending’s (1994) raggedness index (HRag). If the sudden-expansion
model was not rejected, the expansion parameter (s) was converted to an estimate of time (T, in number of generations)
since expansion began using T = s/2u (Rogers 1995; Rogers
and Harpending 1992), where u is the neutral mutation rate
for the entire sequence (i.e. haplotype) per generation. The
value for u was calculated as u = lkg, where l is the substitution rate in substitutions per site per year (s/s/y), k the average
sequence length of the DNA region under study (here 908 base
pairs; see Results) and g the generation time in years (i.e. age of
first reproduction). The value for g was approximated as 10
years. An appropriate rate is necessary for estimating expansion time, but no well-documented cpDNA evolutionary rate
has been reported for P. fruticosa. So in this study, we took the
rate as 1–2 3 10 8 s/s/y. Mismatch analysis were carried out in
ARLEQUIN software version 2.000 (Schneider et al. 2000).
RESULTS
Geographic distribution of haplotypes
We detected 15 haplotypes based on 908 base pairs of sequence
data from the two noncoding regions of cpDNA, trnS–trnG and
rpl20–rps12 (Table 1; Fig. 2). The most common and wide-
11
spread haplotype A occurred in 32 individuals sampled from
the seven populations (37% of all samples), except for the populations in Xidatan 2 and 3, and Dangxiong 2. Haplotypes B, C,
D, G and K were shared among the populations with isolated
local areas or in two to three contiguous populations. Haplotypes M, N and P were private haplotypes, which were represented by a single sequence in the sample. Each of the
remaining six haplotypes was found in a single population
but occurred in a number of individuals in each population
(Table 1).
Haplotype relationships
Phylogenetic relationships among the haplotypes are shown in
the NJ tree (Fig. 3), which is constructed using the 15 haplotypes and one related species of P. nivea as the out-group. These
haplotypes break into two major evolutionary clades (Group 2
and Group 3), with moderate bootstrap-support values (73%)
in 1 000 replicates. The sister branches contained haplotypes
occurring in all populations (low altitudes) and some individuals for those from the high altitudes of Tanggula, Tuotuohe
and Dangxiong 1. Group 1 is close to the out-group P. nivea
and is more primal than the other groups. These Group 1 haplotypes were ancestral and were found only in the population
from Tanggula, Tuotuohe and Dangxiong 1. In particular, the
highest frequency was observed in the population of Tanggula
(70%). The most ancestral haplotype G was found in the population of Tanggula.
The haplotypes network was used to infer genealogical relationships among haplotypes and to assess haplotype frequencies in all samples (Fig. 3). Haplotype A occupied the basal
position of these haplotypes and was found in most populations. Haplotypes in Groups 2 and 3 were derivable from haplotype A by one to four steps mutations, reflecting that the
recent types have insufficient time to attain more variation
and to create networks structure. In contrast, haplotypes in
Group 1 represent deep divergence. The most diverged pair differed by nine substitutions. The network contained several extinct or not detected haplotypes.
Genetic diversity and history of each group
Haplotype diversity (h) and nucleotide diversity (p) within
populations of P. fruticosa ranged 0.0000–0.8000 and
0.0000–0.0076, respectively (Table 1). The diversity indices
are higher in the high-altitude populations of Tanggula, Tuotuohe and Dangxiong 1. Relationship between nucleotide diversity and altitude showed that these populations can be
divided into the ancestral group and the derived group. NJ tree
also indicates that the high-altitude populations have ancestral
haplotypes (Figs 3 and 4).
We carried out mismatch distribution analysis for ancestral
and derived groups. The observed values of the age expansion
parameter (s) were 8.88 and 0.87, which are ;52–25 and 5.1–
2.5 ka BP, respectively (Table 2). The observed HRag for each
of the two groups was not significantly different from that
expected under the population expansion model (P > 0.05).
12
Journal of Plant Ecology
Table 1: details of sampling sites, haplotype composition, haplotype diversity (h) and nucleotide diversity (p) in the investigated groups of
Potentilla fruticosa
Coordinates
Location
North East
Haplotype
Altitude (m) n
A B C D E F G H I
J
K L M N P
h
p
Derived groups
1. Haibei 1
37.61
101.32 3 200
10 6
3
1
0.600 6 0.00022 0.00078 6 0.00073
2. Haibei 2
37.61
101.32 3 500
10 2
6
2
0.622 6 0.00039 0.00103 6 0.00089
3. Dulan
36.47
98.22 3 800
10 8
2
0.356 6 0.00039 0.00041 6 0.00049
4. Xidatan 1
35.79
94.34 4 000
10 6
4
0.533 6 0.00059 0.00062 6 0.00060
5. Xidatan 2
35.75
94.29 4 400
8
8
6. Xidatan 3
35.7
94.28 4 670
7
2
7. Dangxiong 2
30.16
90.43 4 400
4
0.000 6 0.00000 0.00000 6 0.00000
1
4
0.667 6 0.00063 0.00133 6 0.00111
4
0.000 6 0.00000 0.00000 6 0.00000
Ancestral groups
8. Tuotuohe
34.11
92.37 4 740
9 5
1
9. Tanggula
32.84
91.91 5 150
10 1
4 3
10. Dangxiong 1 30.54
91.05 5 150
9 4
2
1
1
2 3
0.694 6 0.00274 0.00380 6 0.00244
1 0.800 6 0.00592 0.00765 6 0.00446
0.722 6 0.00133 0.00374 6 0.00241
Figure 2: relationship between the 15 cpDNA haplotypes and variable sites based on alignment. Only 69 variable positions in 980 base pairs are
shown. The dots indicate identical bases with the haplotype A; the numbers indicate variable sites.
The derived group had strictly unimodal distributions, indicating recent demographic expansion, or through a range expansion with high levels of migration between neighboring demes.
The ancestral group had a multimodal pattern indicating a long
population history with some population.
DISCUSSION
The NJ tree obtained in this study indicates that the haplotypes
G, I, F and L found in 12 individuals may be the primal haplotypes among the 87 individuals of P. fruticosa. These older and
primal haplotypes were all found in the high altitudes such as
Tanggula, Tuotuohe and Dangxiong 1. Especially, they showed
the highest frequency in the population from Tanggula, which
was located at one of the highest sites in this study. The
older haplotypes are also found in high altitudes in other
studies. Haplotype A may be basal to other haplotypes because of its highest occurrence among 87 individuals and
in all the populations. The most basal haplotype is not necessarily the oldest. From the NJ tree it seems that haplotype
G is the oldest among the sampled populations. Moreover, the
haplotype G was also found in the population of Tanggula
(Table 1). The high haplotype diversity (h) and nucleotide diversity (p) in the ancestral group imply that P. fruticosa had
spread and persisted in the high-altitude area for a long time.
The estimated absolute time since the expansion of the ancestral and the derived groups was approximately the last glacial
period (52–25 ka BP) and middle–late Holocene (5.1–2.5 ka BP),
respectively (Table 2). This estimation was similar to that from
the study on population expansion of Pedicularis longifolra
Li et al.
|
Phylogeography of Potentilla fruticosa
13
Figure 3: phylogenetic relationships of the 15 cpDNA haplotypes in Potentilla fruticosa shown in NJ tree (left) and haplotype networks (right). In
the NJ tree, one accession of Potentilla nivea is used as the out-group, and the result is obtained using the Phylip software based on 1 000 replicates.
The bootstrap support values are indicated in the branches. The population number is indicated in the parentheses. In the haplotypes networks,
each circle represents a haplotype, proportional to the haplotype’s frequency in the population. The small black circles on the branches indicate
how many steps each haplotype differs from its neighbor. The gray white circles show ancestral haplotypes.
Figure 4: relationship between nucleotide diversity and the altitudes
of the sampled populations. Circles represent the ancestral groups and
derived groups.
(Orobanchaceae) on the Qinghai-Tibetan Plateau (Yang et al.
2008). All these evidences suggest that the ancestral population of P. fruticosa might be located around the Tanggula
Mountains in the center of the Qinghai-Tibetan Plateau. Populations had expanded and dispersed northward from the
south of the Tanggula Mountains under more favorable climate conditions. The loss of diversity during expansion
leads to the low genetic diversity in northern populations
at present.
There is a long-standing debate concerning the origin of the
floristic history of the Qinghai-Tibetan Plateau. The evidence
from analysis of Potentilla genus has suggested that many temperate plants have originated from adjacent southeast moun-
tains area (Yü et al. 1984). Others have suggested that the
present flora have originated from in situ flora of the Tertiary
period on the Qinghai-Tibetan Plateau (Ward 1935; Wu 1979).
Phylogeographical studies also indicate that the flora in Qinghai is younger than in Tibet (Zhang et al. 2005).
Ancestral haplotypes are located in the center part of the
plateau, whereas the most derived haplotypes are located in
the northern part of the plateau. If ancestral and derived haplotypes do not overlap but are located in different regions, then
the ancestral haplotypes should be found close to refugia,
whereas the derived haplotypes are more likely to occur at
the leading edge of the range expansion (Rowe et al. 2004).
The refugia for P. fruticosa may thus be located at the highaltitude area around the Tanggula Mountains. We also propose
that the refugia for P. fruticosa were restricted to the highelevated mountains. This hypothesis can well explain the distribution of haplotypes in the three populations in Xidatan
and the two populations in Dangxiong. Particular attention
should be paid to the population of Dangxiong 1. For example,
ancestral haplotypes are distributed in Dangxiong 1 with high
altitude, despite of only derived haplotypes in Dangxiong 2
with low altitude. The conclusion is consistent with the results
of the previous study of P. fruticosa and Japanese alpine plant
Phyllodoce nipponica. The refugia were located at high elevations
and used for retreat during the interglacial warm periods due
to forest development (Ikeda and Setoguchi 2007; Shimono
et al., submitted for publication). Wang et al. (2009) reached
a similar conclusion from the species Aconitum gymnandrum
(Ranunculaceae), endemic to the Qinghai-Tibetan Plateau.
The strong summer monsoon climate in the high mountains
14
Journal of Plant Ecology
Table 2: mismatch distribution analysis for derived and ancestral groups of Potentilla fruticosa
Time (T) since expansion began, ka BP
Groups
Expansion
parameter, s
Derived
0.87 (0.0–3.5)
5 023
3 349
2 512
Ancestral
8.88 (2.4–20.6)
51 347
34 231
25 673
1 3 10
8
1.5 3 10
8
2.0 3 10
8
SSD
P
HRag
P
0.000072
0.92
0.087
0.84
0.061
0.26
0.137
0.24
SSD, sum of squared deviation.
both on the Qinghai-Tibetan Plateau and in Japan may have
contributed to the floristic evolution (Shi 2002). However, further evidences are needed to test the aforementioned hypothesis in the future.
At similar altitudes, the haplotypes were similar among the
populations from close geographical area. For example, the
haplotypes were similar to each other in the populations
from Haibei 1 and Haibei 2, or in the populations of Dulan
and Xidatan 1 (Table 1). In contrast, even within a small horizontal distance, the elevation of population seems to have
a large influence on the composition of haplotypes. For example, the populations of Xidatan 1, 2 and 3 were located close to
each other within a valley, but the composition of haplotypes
in Xidatan 1 located within the bottom of the valley was markedly different from that in other two populations, which were
located on the slope of the mountains (Table 1; Fig. 2). These
evidences indicate the importance of elevation in the genetic
variation of local populations. With increase of horizontal distance, topographical influence may play a more important
role. Multimodal pattern of P. fruticosa was confined to both
elevations and geographical area. The topographical diversity
of the Qinghai-Tibetan Plateau might have created both the
networks for refugia during glaciations and the complex barriers to subsequent expansion of populations (Hewitt 2004;
Qu et al. 2005; Zhang and Jing 2006).
FUNDING
Scientific Research Foundation for Returned Scholars (200846),
Shanxi Scholarship Council of China; the project ‘Early Detection and Prediction of Climate Warming Based on the LongTerm Monitoring of Alpine Ecosystems on the Tibetan Plateau’,
Ministry of the Environment, Japan.
ACKNOWLEDGEMENTS
Conflict of interest statement. None declared.
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