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Evolutionary history of the angiosperm flora of China

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High species diversity may result from recent rapid speciation in a ‘cradle’ and/or the gradual accumulation and preservation of species over time in a ‘museum’1,2. China harbours nearly 10% of angiosperm species worldwide and has long been considered as both a museum, owing to the presence of many species with hypothesized ancient origins3,4, and a cradle, as many lineages have originated as recent topographic changes and climatic shifts—such as the formation of the Qinghai–Tibetan Plateau and the development of the monsoon—provided new habitats that promoted remarkable radiation⁵. However, no detailed phylogenetic study has addressed when and how the major components of the Chinese angiosperm flora assembled to form the present-day vegetation. Here we investigate the spatio-temporal divergence patterns of the Chinese flora using a dated phylogeny of 92% of the angiosperm genera for the region, a nearly complete species-level tree comprising 26,978 species and detailed spatial distribution data. We found that 66% of the angiosperm genera in China did not originate until early in the Miocene epoch (23 million years ago (Mya)). The flora of eastern China bears a signature of older divergence (mean divergence times of 22.04–25.39 Mya), phylogenetic overdispersion (spatial co-occurrence of distant relatives) and higher phylogenetic diversity. In western China, the flora shows more recent divergence (mean divergence times of 15.29–18.86 Mya), pronounced phylogenetic clustering (co-occurrence of close relatives) and lower phylogenetic diversity. Analyses of species-level phylogenetic diversity using simulated branch lengths yielded results similar to genus-level patterns. Our analyses indicate that eastern China represents a floristic museum, and western China an evolutionary cradle, for herbaceous genera; eastern China has served as both a museum and a cradle for woody genera. These results identify areas of high species richness and phylogenetic diversity, and provide a foundation on which to build conservation efforts in China.
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00 MONTH 2018 | VOL 000 | NATURE | 1
LETTER doi:10.1038/nature25485
Evolutionary history of the angiosperm flora
of China
Li-Min Lu1*, Ling-Feng Mao2*, Tuo Yang1*, Jian-Fei Ye1,3,4*, Bing Liu1,5*, Hong-Lei Li6,7*, Miao Sun8,9*, Joseph T. Miller10,11,
Sarah Mathews10, Hai-Hua Hu1,3, Yan-Ting Niu1,3, Dan-Xiao Peng1,3, You-Hua Chen12, Stephen A. Smith13, Min Chen14,
Kun-Li Xiang1,3, Chi-Toan Le1,3, Viet-Cuong Dang1,3, An-Ming Lu1, Pamela S. Soltis9§, Douglas E. Soltis8,9§, Jian-Hua Li15§ &
Zhi-Duan Chen1,5§
High species diversity may result from recent rapid speciation in
a ‘cradle’ and/or the gradual accumulation and preservation of
species over time in a ‘museum’
1,2
. China harbours nearly 10% of
angiosperm species worldwide and has long been considered as both
a museum, owing to the presence of many species with hypothesized
ancient origins
3,4
, and a cradle, as many lineages have originated
as recent topographic changes and climatic shifts—such as the
formation of the Qinghai–Tibetan Plateau and the development of
the monsoon—provided new habitats that promoted remarkable
radiation5. However, no detailed phylogenetic study has addressed
when and how the major components of the Chinese angiosperm
flora assembled to form the present-day vegetation. Here we
investigate the spatio-temporal divergence patterns of the Chinese
flora using a dated phylogeny of 92% of the angiosperm genera for
the region, a nearly complete species-level tree comprising 26,978
species and detailed spatial distribution data. We found that 66% of
the angiosperm genera in China did not originate until early in the
Miocene epoch (23million years ago (Mya)). The flora of eastern
China bears a signature of older divergence (mean divergence
times of 22.04–25.39Mya), phylogenetic overdispersion (spatial
co-occurrence of distant relatives) and higher phylogenetic diversity.
In western China, the flora shows more recent divergence (mean
divergence times of 15.29–18.86Mya), pronounced phylogenetic
clustering (co-occurrence of close relatives) and lower phylogenetic
diversity. Analyses of species-level phylogenetic diversity using
simulated branch lengths yielded results similar to genus-level
patterns. Our analyses indicate that eastern China represents a
floristic museum, and western China an evolutionary cradle, for
herbaceous genera; eastern China has served as both a museum
and a cradle for woody genera. These results identify areas of
high species richness and phylogenetic diversity, and provide a
foundation on which to build conservation efforts in China.
Species composition within a geographic area is the result of
historical processes including speciation, extinction, migration
6
and
ongoing ecological interactions. The extent to which each process has
contributed to spatial and temporal patterns of biodiversity, as well
as community assembly, varies across the landscape. The biodiversity
patterns within a region may result from a recent increase in the rate
of speciation that has generated a cradle of biodiversity. Alternatively,
biodiversity may derive from the presence of numerous surviving
ancient lineages, together forming a museum region. The process
of speciation and the maintenance of ancient lineages need not be
mutually exclusive, and some regions have features of both cradles
and museums.
The evolutionary history of regional floras has typically been
addressed using specific taxa as exemplars7–9 or by examining the
entire flora at various taxonomic levels10–12. These investigations
provide insights into historical factors, including geological history,
climatic shifts and evolutionary processes, that might have contri buted
to modern geospatial patterns of biodiversity13,14. Concomitantly,
these studies lay the foundation for decision-making in conserving
biodiversity. However, few studies have explored the biodiversity
patterns of a large region incorporating dated phylogenies and detailed
distribution data.
China, which is home to 30,000 of the approximately 350,000
400,000 species of vascular plants
15
, is ideal for investigating patterns
of biodiversity because of its large size, range of habitats, considerable
biological diversity and heterogeneous physical geography. Whether
areas within China serve as cradles or museums remains unclear, as
floristic components of putative ancient origin
3,4
and of recent diversi-
fication
5
have both been discovered. It has previously been suggested
16
on the basis of comparisons between the taxonomic richness of vascular
plants in China and the United States, that the greater species diversity
in China reflects the regions complex topography and long connections
with tropical South-East Asia. On the basis of patterns in species rich-
ness (using 555 endemic seed plant species), mountainous regions of
central and southern China have been identified as the main centres
of plant endemism17. Previous studies have attributed most of the
geographic variation in species richness of woody plants in China to
temperature seasonality18 and the extent of winter cold19. Notably, to
our knowledge, no previous study has incorporated both phylogenetic
and spatial components to address the evolutionary history of the
Chinese flora.
We conducted a broad assessment of spatio-temporal divergence
patterns and of the assembly of the Chinese angiosperm flora, using
a robustly dated phylogeny as well as species distribution data (i) to
document the relative proportions of ancient and recent divergences
that shaped the extant Chinese angiosperm flora in various geographic
regions; (ii) to investigate the differential spatio-temporal divergence
patterns of woody and herbaceous genera and their relationships with
1State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. 2Co-Innovation Center for Sustainable Forestry in Southern
China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China. 3University of Chinese Academy of Sciences, Beijing 100049, China. 4Beijing Botanical
Garden, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China. 5Sino-Africa Joint Research Center, Chinese Academy of Sciences, Wuhan 430074, China. 6Chongqing Key
Laboratory of Economic Plant Biotechnology/Institute of Special Plants, Chongqing University of Arts and Sciences, Yongchuan 402160, China. 7Fairylake Botanical Garden, Shenzhen & Chinese
Academy of Sciences, Shenzhen 518004, China. 8Department of Biology, University of Florida, Gainesville, Florida 32611-7800, USA. 9Florida Museum of Natural History, University of Florida,
Gainesville, Florida 32611, USA. 10CSIRO National Research Collections, Australian National Herbarium, Canberra, Australian Capital Territory 2601, Australia. 11Office of International Science
and Engineering, National Science Foundation, Alexandria, Virginia 22314, USA. 12Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China. 13Department of Ecology
and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan 48109, USA. 14Institute of Botany, Jiangsu Province & Chinese Academy of Sciences, Nanjing 210014, China. 15Biology
Department, Hope College, Holland, Michigan 49423, USA.
*These authors contributed equally to this work.
§These authors jointly supervised this work.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
2 | NATURE | VOL 000 | 00 MONTH 2018
Letter
reSeArCH
environmental variables; and (iii) to compare genus- and species-level
measures of phylogenetic diversity and explore their conservation
implications for the Chinese flora.
Our phylogeny resolved evolutionary relationships among all major
angiosperm lineages in China (Extended Data Fig. 1), yielding topolo-
gies that are highly similar to those for angiosperms as a whole20,21.
Our estimates of divergence times based on penalized likelihood and
PATHd8 are congruent with one another, and agree with those obtained
in recent studies of angiosperms on a global basis22,23 (Extended
Data Fig. 2). Divergence time estimates show that 66% of Chinese
angiosperm genera originated during the Neogene and Quaternary
periods; the remaining genera diverged in the Palaeogene (29%) and
Cretaceous (5%) periods. Additionally, the herbaceous genera have
diversified much more rapidly than the woody genera during the past
30 million years (Extended Data Fig. 3).
We divided China into 100-km × 100-km grid cells, evaluated age
variance within grid cells (Extended Data Figs 4, 5), and calculated
mean divergence times (MDTs) and median divergence times of genera
within each grid cell (Fig. 1; Extended Data Figs 6, 7; Supplementary
Information). Mapping the MDTs of all genera revealed a transition belt
None
Ancient
Recent
l
N
None
Ancient
k
N
None
Ancient
Recent
j
N
i
N
34.15–37.54
37.55–39.85
39.86–41.57
41.58–43.20
43.21–44.81
44.82–46.49
46.50–48.22
48.23–50.02
50.03–51.95
51.96–58.38
h
N
18.63–35.02
35.03–41.60
41.61–46.52
46.53–51.05
51.06–54.52
54.53–57.37
57.38–60.16
60.17–62.86
62.87–66.99
67.00–73.32
g
N
34.80–38.85
38.86–41.41
41.42–43.45
43.46–45.32
45.33–47.07
47.08–49.05
49.06–51.48
51.49–54.54
54.55–57.53
57.54–61.02
fN
0.67–1.46
1.47–1.74
1.75–1.92
1.93–2.09
2.10–2.28
2.29–2.54
2.55–2.82
2.83–3.15
3.16–3.55
3.56–4.92
eN
1.98–2.85
2.86–3.57
3.58–3.95
3.96–4.36
4.37–4.87
4.88–5.48
5.49–6.21
6.22–7.06
7.07–7.84
7.85–9.46
dN
0.73–1.43
1.44–1.88
1.89–2.20
2.21–2.42
2.43–2.61
2.62–2.82
2.83–3.07
3.08–3.36
3.37–3.70
3.71–5.11
c
N
15.17–16.55
16.56–17.51
17.52–18.13
18.14–18.72
18.73–19.31
19.32–19.99
20.00–20.64
20.65–21.28
21.29–21.91
21.92–23.45
b
N
6.40–14.63
14.64–18.66
18.67–20.82
20.83–22.04
22.05–23.07
23.08–24.08
24.09–25.15
25.16–26.19
26.20–27.58
27.59–30.99
15.29–16.83
16.84–18.13
18.14–18.86
18.87–19.47
19.48–20.09
20.10–20.94
20.95–22.03
22.04–23.14
23.15–24.15
24.16–25.39
a
N
Null model (herbaceous genera)Null model (woody genera)Null model (all genera)
25%-oldest MDT (herbaceous genera)25%-oldest MDT (woody genera)25%-oldest MDT (all genera)
25%-youngest MDT (herbaceous genera)25%-youngest MDT (woody genera)25%-youngest MDT (all genera)
MDT (herbaceous genera)MDT (woody genera)MDT (all genera)
Figure 1 | Patterns of the MDTs for Chinese angiosperm genera.
ai, MDT for all genera, woody genera and herbaceous genera (from left
to right), based on all sampled genera (ac), the youngest 25% of genera
(df), and the oldest 25% of genera (gi) in each grid cell. jl, Null-
model test to recognize recent (blue grid cells) and ancient (red grid
cells) divergence centres. The analyses included 2,592 angiosperm
genera (woody genera, n = 925; herbaceous genera, n = 1,501; genera
with both woody and herbaceous species, n = 166). Maps adapted from
National Administration of Surveying, Mapping and Geoinformation
of China (http://www.sbsm.gov.cn; review drawing number:
GS(2016)1576).
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
00 MONTH 2018 | VOL 000 | NATURE | 3
Letter reSeArCH
that coincides with the modern 500-mm isoline of annual precipitation,
which marks the boundary between humid–semi-humid and arid–
semi-arid areas
24
(eastern China versus western China, Fig. 2). Both
MDT and null-model analyses indicate that eastern China has older
lineages (red grid cells, Fig. 1a, j), particularly in central to southern
China. By contrast, western China, and especially the Qinghai–Tibetan
Plateau, contains taxa that have diverged more recently (blue grid cells,
Fig. 1a, j). Furthermore, our genus-level analyses demonstrate that
eastern China is phylogenetically overdispersed with higher phylo-
genetic diversity, and that western China shows phylogenetic clustering
with lower phylogenetic diversity (Extended Data Fig. 8). These
findings are also observed in analyses of phylogenetic diversity based
on multiple species-level trees, in which taxa that lacked target DNA
sequences were provided with meaningful branch lengths using a
birth–death clock model (see Methods; Extended Data Fig. 9). The flora
of the Cape of South Africa likewise shows phylogenetic structure—the
western region is phylogenetically clustered, and the eastern region is
overdispersed10. However, taxon richness is decoupled from phylo-
genetic diversity in the Cape of South Africa; in China, taxon richness
and phylogenetic diversity are positively correlated.
Western China includes the arid north-western portion of the
country and most of the Qinghai–Tibetan Plateau (Fig. 2). A funda-
mental climate shift may have occurred in western China as recently
as the early Miocene, owing to the uplift of the Qinghai–Tibetan
Plateau and subsequent development of the Asian monsoon
24,25
. Of
the 111 genera that occur only in western China, 76% originated in
the past 20 million years and only 24% originated before this time. In
western China, a much higher percentage of herbaceous than woody
genera has originated since 30Mya (Fig. 3a). Moreover, genera that
occur only in western China are predominantly members of only a
few clades (Apiales, Asterales and Brassicales), most of which have
much younger divergence times than the major clades of eastern China
(Fig. 2; Extended Data Table 1). MDTs calculated from the youngest
25% of herbaceous genera in each grid cell also indicate that western
China—in particular the Qinghai–Tibetan Plateau—has younger
lineages (Fig. 1f ) than eastern China, which further suggests that
western China represents a cradle for herbaceous angiosperms.
Mountainous areas of eastern China have been proposed as
refugia for plants that originated in the early Cretaceous or late
Jurassic periods26,27 because their geological environment and
climate (including orogenic movements, annual temperature and
annual precipitation) may have experienced little change since the
Cretaceous
28
. Of the 1,026 genera that occur only in eastern China, 39%
originated before 20Mya and 61% arose more recently than this. Both
herbaceous and woody genera diverged at similar rates throughout
geological time (Fig. 3a). The 20 major clades with the largest number
of genera occurring only in eastern China are distributed throughout
the ordinal-level time-tree from early-diverging clades (for example,
Alismatales, Asparagales, Magnoliales and Ranunculales) to later-
diverging lineages (for example, Asterales, Gentianales and Lamiales)
(Fig. 2; Extended Data Table 1). MDTs based on the youngest 25% and
oldest 25% of genera in each grid cell reveal that eastern China has
old herbaceous lineages (Fig. 1f, i), but has both old and young woody
lineages (Fig. 1e, h). Eastern China may have served as a museum for
herbaceous genera, but as both a museum and a cradle for woody
genera.
112
46
29
24
18
32
45
15
102
29
19
23
16
81
98
30
25
8
18
10
23
26 Asterales
Oxalidales
Ceratophyllales
Icacinales
Petrosaviales
Vitales
Poales
Alismatales
Pandanales
Solanales
Fagales
Cucurbitales
Boraginales
Dipsacales
Crossosomatales
Piperales
Ranunculales
Arecales
Geraniales
Liliales
Asparagales
Escalloniales
Myrtales
Zingiberales
Garryales
Chloranthales
Gentianales
Santalales
Laurales
Malpighiales
Fabales
Caryophyllales
Malvales
Magnoliales
Acorales
Celastrales
Dilleniales
Huerteales
Nymphaeales
Sabiales
Brassicales
Saxifragales
Rosales
Commelinales
Aquifoliales
Apiales
Austrobaileyales
Metteniusales
Zygophyllales
Sapindales
Lamiales
Dioscorales
Buxales
Ericales
Cornales
Proteales
Trochodendrales
MagnoliidsSuperasterids MonocotsSuperrosids Basal eudicots
0
25
50
75
100
125
150
b
54
72
17
a
500 mm
500 mm
N
My
a
Figure 2 | Spatio-temporal divergence
patterns of the Chinese angiosperm flora.
a, Patterns of MDTs adapted from Fig. 1a.
The dark line represents the 500-mm annual
precipitation isoline adapted from ref. 24
(reprinted from ref. 24, with permission from
Elsevier). b, Ordinal time-tree with the major
clades of angiosperms indicated. The top five
orders with genera occurring only in western
China and top 20 orders with genera occurring
only in eastern China are indicated on the
tree with blue and red boxes, respectively.
The number of genera distributed in western
or eastern China from each order is shown
within the corresponding box. Map adapted
from National Administration of Surveying,
Mapping and Geoinformation of China
(http://www.sbsm.gov.cn; review drawing
number: GS(2016)1576).
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
4 | NATURE | VOL 000 | 00 MONTH 2018
Letter
reSeArCH
The mean annual precipitation (MAP) and mean annual temperature
(MAT) have higher explanatory power for the MDTs of the herbaceous
genera (Fig. 4c, f) than of the woody genera (Fig. 4b, e). These patterns
may reflect the heterogeneity in rates of evolution between herba-
ceous and woody lineages. Herbaceous plants are well known to have
higher substitution rates owing to their shorter generation times, which
perhaps allows them to respond more quickly to environmental change
through increased genetic divergence and speciation rates23,29.
The spatial divergence and diversity patterns of angiosperms
detected here do not precisely reflect the latitudinal gradient in China;
MDT and phylogenetic diversity decrease from south-east to north-
west (Fig. 2a; Extended Data Fig. 8d, g). Our results show the impor-
tance of water and temperature in limiting the dispersal of species from
humid and warm regions to drier and colder areas. The effects of topo-
graphy, with a pronounced altitudinal gradient increasing from east to
west, and the monsoon climate in eastern Asia are so extensive that the
decreasing temperature and precipitation gradients from south-eastern
to north-western China are not consistent with the latitudinal gradient,
as might be expected in flatter regions.
On the basis of a species-level phylogenetic tree and distribution
data with ‘county’ as the basic unit, we inferred that the species richness
and phylogenetic diversity in protected areas cover approximately 88%
and 96%, respectively, of the total species richness and phylogenetic
diversity in China. For conservation planning, these values may be over-
estimates that result from the coarse scale of our distributional data, as
most nature reserves are smaller in size than Chinese counties. Notably,
areas with the top 5% highest phylogenetic diversity and standard
effective size of phylogenetic diversity (SES-PD) are mainly located
in several provinces of eastern China (Fig. 3b): Guangdong, Guangxi,
Guizhou and Hainan for genus-level phylogenetic diversity hotspots,
and Yunnan for species-level phylogenetic diversity. These areas are
also hotspots for threatened plants in China
30
. However, in contrast
N
a b
Yunnan
Guangxi
Hainan
Guangdong
Guizhou
0%
5%
10%
15%
20%
25%
Miocene
Oligocene
Eocene
Palaeocene
Plio
.
Plt.
Late CretaceousEarly Cretaceous
015 10 52035 30 254055 50 456075 70 658095 90 85100115 110 105120
135
130 125 Mya
500 mm
500 mm
Genera (western China)
Genera (eastern China)
Woody genera (western China)
Herbaceous genera (western China)
Woody genera (eastern China)
Herbaceous genera (eastern China)
Western
China
Eastern
China
00
mm
500
Western
Chin
a
Eastern
China
Figure 3 | Angiosperm divergence pattern and conservation priorities
in western and eastern China. a, Percentage of genera occurring only in
western (n = 111) or eastern China (n = 1,026) during geological time.
Western China has a higher percentage of herbaceous genera (purple
dashed line) than woody genera (purple solid line) that have originated
since 20Mya. Western and eastern China are divided by the 500-mm
isoline of annual precipitation. Plio., Pliocene epoch; Plt., Pleistocene
epoch. b, Grid cells with the top 5% highest phylogenetic diversity and
SES-PD at genus (pink) and species (blue) levels. Protected areas are
highlighted in green. Maps adapted from National Administration of
Surveying, Mapping and Geoinformation of China (http://www.sbsm.gov.
cn; review drawing number: GS(2016)1576).
MDT of herbaceous genera
(
Mya
)
M
AT
(
°C)
5
10
1
5
20
25
R
2
=
0
.
46
16
18
20
2
2
2
4
f
M
DT of woody genera (Mya)
MAT
(
°C
)
e
–5
0
5
10
15
20
2
5
R
2
=
0
.
20
10
1
5
20
2
5
30
d
MDT of all
g
enera
(
Mya
)
MAT (
°
C
)
5
0
5
10
1
5
20
2
5
R
2
=
0
.
60
16
22
24
2
6
c
MDT of herbaceous genera
(
Mya
)
R
2
=
0
.
63
MAP
(
mm
)
0
5
00
1
,
000
1
,5
00
2
,
000
2
,5
00
16
18
20
2
2
24
b
=
0
.
26
MDT of woody genera (Mya
)
MAP
(
mm
)
0
5
00
1
,
000
1
,5
00
2
,
000
2
,5
00
10
1
5
2
5
30
a
MDT of all
g
enera
(
Mya
)
R
2
=
0
.7
4
MAP
(
mm
)
0
500
1
,
000
1
,5
00
2
,
000
2
,5
00
24
26
Figure 4 | Regression analyses between MDT
and two environmental variables for the
Chinese angiosperm genera. ac, MDT
and MAP. df, MDT and MAT. From left to
right, patterns for all genera (a, d), woody
genera (b, e) and herbaceous genera (c, f).
The analyses were conducted across all grid
cells (n = 943) and used the non-spatial linear
regression model.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
00 MONTH 2018 | VOL 000 | NATURE | 5
Letter reSeArCH
to western China, protected areas in eastern China are fragmented
(Fig. 3b), largely as a result of urbanization and administrative division.
Our data suggest the need to establish more connections between
existing nature reserves and national parks that span provincial borders
to conserve plant lineages of ancient and recent origins in eastern
China, as well as the other organisms that depend on these floristic
elements. These findings should be of broad interest to evolutionary
and conservation biologists, and serve to stimulate better-informed
conservation planning and research.
Online Content Methods, along with any additional Extended Data display items and
Source Data, are available in the online version of the paper; references unique to
these sections appear only in the online paper.
Received 26 January; accepted 22 December 2017.
Published online 31 January 2018.
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Supplementary Information is available in the online version of the paper.
Acknowledgements We thank J.-Y. Fang, D.-Z. Li, K.-P. Ma, S.-Z. Zhang, H. Sun,
J.-Q. Liu, Z.-H. Wang, X.-Q. Wang and H.-Z. Kong for help initiating this study.
This research was supported by the National Key Basic Research Program of
China (2014CB954100), the National Natural Science Foundation of China
(31590822), the Chinese Academy of Sciences International Institution
Development Program (SAJC201613), the National Natural Science Foundation
of China and US National Science Foundation Dimensions Collaboration Project
(31461123001), the US National Science Foundation (Open Tree of Life:
DEB-1207915, DEB-1208428; ABI DBI-1458466 and DBI-1458640; iDigBio:
EF-1115210 and DBI-1547229; US–China Dimensions of Biodiversity: DEB-
1442280) and the Priority Academic Program Development of Jiangsu Higher
Education Institutions (PAPD).
Author Contributions Z.-D.C., P.S.S., D.E.S and J.-H.L. conceived the paper.
L.-M.L., L.-F.M., T.Y., J.-F.Y., B.L., H.-L.L. and M.S. analysed the data. L.-M.L., L.-F.M.,
T.Y., J.-F.Y., B.L., J.T.M., S.M., P.S.S., D.E.S., J.-H.L. and Z.-D.C. wrote the first draft
and finalized the manuscript. H.-H.H., Y.-T.N., D.-X.P., M.C., K.-L.X., C.-T.L. and
V.-C.D. contributed data. J.T.M., A.-M.L., Y.-H.C., S.A.S., P.S.S., D.E.S., J.-H.L. and
Z.-D.C. contributed substantially to revisions. All authors commented on the
manuscript.
Author Information Reprints and permissions information is available at
www.nature.com/reprints. The authors declare no competing financial
interests. Readers are welcome to comment on the online version of the paper.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional
claims in published maps and institutional affiliations. Correspondence and
requests for materials should be addressed to Z.-D.C. (zhiduan@ibcas.ac.cn).
Reviewer Information Nature thanks R. Colwell, V. Savolainen and the other
anonymous reviewer(s) for their contribution to the peer review of this work.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter
reSeArCH
METHODS
Phylogeny reconstruction. Sequences of four plastid genes (atpB, matK, ndhF and
rbcL) and one mitochondrial gene (matR) were used to reconstruct the phylogeny
of Chinese vascular plants31. Generic circumscriptions were based on ref. 15. We
sampled one species for the 1,173 genera with only one species in China. For the
1,736 genera with 2–30 species in China, two species were sampled from each
genus. For the 267 genera with more than 30 species in China, approximately 10%
of the species of each genus were sampled, reflecting intrageneric diversity. We
downloaded all available sequences for the target DNA regions from GenBank; if
more than one sequence was available for the same locus for a species, the longest
one of good quality was selected. For genera with sequences that were unavailable
in the public database (781 genera in total), we generated new sequences from
leaf materials, collected from the field for 513 genera and from specimens from
the Chinese National Herbarium (PE) for 47 genera. There are 231 genera that
remain unavailable because we failed to obtain the materials or amplify the target
sequences. Details of DNA extraction, PCR, sequencing, alignment, accession
numbers of sequences and phylogeny reconstruction have previously been
published31.
Divergence time estimation. We used the penalized likelihood method as imple-
mented in treePL
32
(https://github.com/blackrim/treePL) to date divergence times
of Chinese angiosperms based on the optimal maximum likelihood phylogram
obtained with RAxML 8.0.2233 in the CIPRES Science Gateway34, after excluding
the outgroups (for example, lycophytes, ferns and gymnosperms). Our dated
phylogeny included 5,864 species native to China, representing 2,665 genera
from 273 families or approximately 92% of the angiosperm genera of China. We
validated the available fossils and selected 138 calibrations for dating analyses
(Supplementary Table 1 in Supplementary Information). The ‘prime’ option was
applied to identify the best optimization parameters, and a ‘thorough’ analysis was
then carried out with the optimal parameters determined above (opt = 1, optad = 1
and optcvad = 4). To identify the best smoothing parameter that affects the penalty
for rate variation over the phylogram, a ‘random subsample and replicate cross-
validation’ was conducted with treePL. Confidence intervals for each node were
calculated following previously published methods22. To accommodate for
variation in branch length estimates, we calculated 100 bootstrap replicates with
topology fixed to the above maximum likelihood phylogram but with varying
branch lengths. We then conducted treePL on these 100 replicates. Age statistics
for all nodes were summarized with TreeAnnotator v.1.8.435.
We also used an alternative dating method, PATHd8
36
, to estimate divergence
times of Chinese angiosperms. The calibrations for the PATHd8 analysis were
identical to those used for the treePL analysis, except that the crown age of angio-
sperms was set to 138Mya instead of a maximum of 140Mya and a minimum
of 136Mya (as in treePL) because PATHd8 requires one fixed calibration. Both
treePL and PATHd8 are rate-smoothing methods, but PATHd8 sequentially
takes averages over path lengths from an internode to all its descending termi-
nals, one pair of sister groups at a time37, where smoothing is done stepwise for
each node separately; by contrast, smoothing in treePL is done simultaneously
over the tree. The correlation between ages at all nodes based on the treePL
and PATHd8 analyses was assessed with Spearmans rank correlation analysis
in R v.3.2.038.
To evaluate whether dates for this regional time-tree are biased owing
to the geographic sampling, we used a correlation analysis to compare our
estimated divergence times with recent global-scale angiosperm time-tree
reconstructions
22,23
; one of these represents a family-level time-tree with multiple
fossil calibration points22, and the other is a species-level time-tree with dense
taxon sampling (32,223 species) and fewer calibrations
23
. The stem age of each
family was extracted for the Spearman’s rank correlation analyses. Only the family
ages were compared (circumscription of families, following ref. 20), because
different genera and species were included in the three studies. Ages of genera
were extracted from our dichotomous time-tree estimated by treePL for the down-
stream analyses. For monophyletic genera, stem ages were extracted directly by
tracing their stem node. For genera that are polyphyletic or paraphyletic (380 out
of 2,665), the stem age of each monophyletic lineage was extracted and the oldest
one was selected as the age of the genus. The numbers of angiosperm genera that
originated during specified geological timespans are provided in Extended Data
Fig. 3, with the global temperature changes since 65Mya39 indicated.
Distribution of angiosperm species in China. The spatial distribution data and
information on growth form were assembled from nearly all published national
and provincial floras, as well as some local floras, checklists and herbarium records.
The spatial distribution data are at the county level (2,377 counties) with an average
county-size of approximately 4,000km
2
. To minimize the sampling bias of unequal
sampling areas, we divided the map of China into 100-km × 100-km grid cells, and
grid cells on the border that cover less than 50% of the area of a grid cell (that is,
5,000 km2) were excluded from the analyses. Maps of China used in this study were
adapted from standard maps released by the National Administration of Surveying,
Mapping and Geoinformation of China (http://www.sbsm.gov.cn; review drawing
number: GS(2016)1576). The gridded distribution database contained 1,409,239
occurrence records for 26,978 angiosperm species from 2,845 genera. After match-
ing with the phylogeny, the final dataset included a total of 2,592 angiosperm
genera (woody genera, n = 925; herbaceous genera, n = 1,501; genera with both
woody and herbaceous species, n = 166).
Spatial distribution of MDTs and null-model test for divergence hotspots.
To explore the spatial divergence patterns of Chinese angiosperm genera, we
calculated the weighted MDTs of all genera in each grid cell by integrating spatial
distribution data with our dated phylogenetic tree. AGE
i
represented the age of a
genus i (i = 1, …, n) in a grid cell, and Si the species number in genus i in this grid
cell. From this, MDT was calculated as:
=
×+ ×+ ×+
+++ +
MDT
(AGE S) (AGE S) (AGE S) (AGE S)
SSSS
nn
n
112233
123
We further divided the genus dates in each grid cell into quartiles and calculated
MDTs on the basis of the youngest and oldest quartiles, separately, in each grid cell.
The MDTs based on the youngest quartile allowed us to recognize centres of recent
divergence, whereas MDTs based on the oldest quartile detected ancient centres
of divergence. To avoid potential bias from grid cells that had either relatively old
or young genera, we ranked all genera from youngest to oldest, partitioned them
into quartiles based on their ages, computed MDT in each cell for the absolute
youngest 25% and the absolute oldest 25% of genera, and then mapped the results
across China.
We designed a null model to identify ancient and recent divergence hotspots for
the angiosperm flora of China. The mean ages of the youngest and oldest quartiles
in each grid cell were selected as the observed values for the null models, and
then we shifted the genera randomly using all genera investigated in China as a
sampling pool to obtain the null distributions of ages for the youngest and oldest
quartiles for each grid cell. The standardized effect size of the mean divergence time
(SES-MDT) of genera for each grid cell was calculated as:
=
..
SESMDT
MDTMDT
sd(MDT )
observed random
random
where MDT
observed
is the observed MDT; MDT
random
is the expected MDT of the
randomized assemblages (n = 999); and s.d.(MDTrandom) is the s.d. of the MDT for
the randomized assemblages. Grid cells with values of SES-MDT for the youngest
quartile below 1.96 were identified as notable hotspots of recent divergence,
whereas grid cells with SES-MDT for the oldest quartile above 1.96 were identi
-
fied as notable hotspots of ancient divergence. Considering that the evolutionary
history of herbaceous and woody plants may differ
40
, the above analyses were also
conducted separately for herbaceous and woody genera. Analyses of MDT were
implemented in R and ArcGIS 10.1 (http://www.esri.com/).
Previous studies have demonstrated that the overall species richness patterns
of birds are largely determined by the geographically wide-ranging species
41–43
,
indicating that patterns may be driven by a subset of taxa and may not be
representative of an entire biota. To explore whether MDT patterns for China are
influenced largely by values for widespread species, we ranked genera from the
most restricted to most widespread in China, partitioned the genera into quartiles
on the basis of their range size and mapped MDT for each quartile following a
previously published description41.
Spatial distribution of median divergence times. Age variation within grid cells
was evaluated by plotting divergence times in each grid cell (Extended Data Fig. 4)
and calculating the skewness and kurtosis of divergence times (Extended Data Fig. 5).
To verify the results of MDT, we also investigated the distribution patterns of the
Chinese angiosperm genera by mapping the median divergence times (medianDT)
based on all genera, and the youngest and oldest quartiles in each grid cell. The null
model for the median divergence time applied a modified effective-size statistic44–46
and was calculated as:
=
>SESmedianDT
medianDT medianDT
14826 MAD
,ifMAD 0
observed random
random
random
=
=SESmedianDT
medianDT medianDT
12553 meanAD
,ifMAD 0
observed random
random
random
where medianDT
observed
is the observed median divergence time; medianDT
random
is the expected median divergence time of the randomized assemblages (n = 999);
MADrandom is the median absolute deviation of the divergence times for the
randomized assemblages; and meanAD
random
is the mean absolute deviation of
the divergence times for the randomized assemblages.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter reSeArCH
Richness and phylogenetic diversity. We calculated the generic richness, Faiths
phylogenetic diversity
47
and SES-PD of the Chinese angio sperm genera on the
basis of our ultrametric chronogram using the ‘picante’ package in R. Faith’s phylo-
genetic diversity is the sum of all phylogenetic branch lengths that connect species
in a community. We calculated phylogenetic diversity as the length of the subtree
that joins the genera in each grid cell to the root of the chronogram. SES-PD was
calculated because phylogenetic diversity is usually positively correlated with spe-
cies richness
48
. We first obtained a null distribution of the expected phylogenetic
diversity values by shuffling taxa labels across the tips of the tree 999 times for
each grid cell. SES-PD was then calculated by dividing the difference between the
observed (PDobserved) and expected phylogenetic diversity (PDrandom) by the s.d.
of the null distribution (s.d.(PDrandom)):
=
..
SESPD
PD PD
sd(PD)
observed random
random
Phylogenetic structure. The net relatedness index (NRI) and the nearest taxon
index (NTI) were calculated to investigate the phylogenetic structure (clustering
or overdispersion) of angiosperm genera across China
49
. NRI is based on the mean
phylogenetic distance (MPD), an estimate of the average phylogenetic relatedness
between all possible pairs of taxa within a grid cell, and primarily reflects structure
at deeper parts of the phylogeny. NTI is based on mean nearest taxon distance
(MNTD), an estimate of the mean phylogenetic relatedness between each pair of
taxa in a grid cell and its nearest relative in the phylogeny, and reflects shallower
parts of the phylogeny. NRI and NTI were calculated as follows:
=− ×
..
NRI1
MPDMPD
sd(MPD )
observed random
random
=− ×
..
NTI1
MNTD MNTD
sd(MNTD)
observed random
random
where MPDobserved and MNTDobserved are the observed MPD and MNTD;
MPD
random
and MNTD
random
are the averages of the expected MPD and MNTD of
the randomized assemblages (n = 999); and s.d.(MPDrandom) and s.d.(MNTDrandom)
are the standard deviation of MPD
random
and MNTD
random
for the randomized
assemblages. The null distributions of MPD and MNTD were created by randomly
selecting the observed number of genera in each grid cell 999 times, with all genera
in the phylogeny as a sampling pool. Positive values of NRI and NTI indicate
phylogenetic clustering, whereas negative values indicate phylogenetic overdisper-
sion in a grid cell. NRI and NTI for woody and herbaceous genera were calculated
separately to compare their phylogenetic structures across China.
Regression analyses between MDT and two climatic variables. To explore the
underlying mechanisms of spatial divergence patterns of the Chinese angiosperms,
MDT in each grid cell was regressed against the respective mean values of MAP
and MAT in each grid cell using the linear regression model in R. The adjusted R
2
was used to indicate the explanatory power of each variable, although it is clear that
these associations do not necessarily indicate causation of the climatic variables in
determining MDT. Climatic data were downloaded from the WorldClim database
Version 1.4 (http://www.worldclim.org/) with a spatial resolution of 10 min50.
Species tree reconstruction and conservation implications. With our dated
genus-level chronogram as the backbone, a species-level tree including 26,978
Chinese angiosperm species was generated by inserting species that were not
sampled in our generic tree within the genera to which they belong using the
R package ‘S.PhyloMaker51. Our species-level tree included approximately 96%
of all known angiosperm species native to China; 1,098 aquatic species were not
sampled. To mitigate the effect of polytomies on the calculation of phylogenetic
diversity, we resolved polytomies in the reconstructed tree with a birth–death clock
model
52
. We constructed constraints based on the tree constructed with molecular
data, and unresolved taxa were then placed within the relevant constraints. Node
heights for each constraint were fixed on the basis of divergence time estimates.
We then conducted a Bayesian analysis using MrBayes v.3.253 with the topological
and node height constraints and with the birth–death (speciation and extinction)
priors as uniform (0.0, 10.0). Two analyses were run for 2,500,000 generations,
sampling every 500 generations, to ensure convergence and mixing; the first
750,000 generations were discarded as burn-in, and 1,000 of the post-burn-in
trees were retained for further analyses. The species-level phylogenetic diversity
and SES-PD were calculated on the basis of 10 trees randomly selected from the
1,000 trees. The Spearman’s rank correlation was used to assess the consistency
of phylogenetic diversity or SES-PD patterns based on different trees. Grid cells
with the top 5% highest values of both phylogenetic diversity and SES-PD were
identified as hotspots of phylogenetic diversity (Fig. 3b). MDT analyses were not
conducted on the species tree as the missing data rendered the variation between
replicates uninformative. Once additional molecular information is collected for
these species, further analyses can be performed.
Spatial data of protected areas in China were compiled from two sources:
(i) a previous publication
30
that digitized nature reserves in mainland China, which
included 334 national, 857 provincial and 1,431 prefectural or county-level nature
reserves (provided by Z.-Y. Tang); and (ii) 92 protected areas in Taiwan, down-
loaded from the Database of Protected Areas (https://www.protectedplanet.net/;
accessed August 2017). Considering that most of the nature reserves were designed
according to administrative units, we calculated richness and phylogenetic diversity
in the protected areas with ‘county’ as the basic unit rather by than dividing China
into grid cells. Each conservation area was intersected with the map of China to
produce the protected areas in ArcGIS. Species occurring in these counties are
supposed to be protected, but counties with protected areas that covered less than
10% of the area of a county were excluded to reduce sampling bias.
Statistics and reproducibility. No statistical methods were used to predetermine
sample size. Spearmans rank correlation and linear regression analyses were
conducted in R. Precise P values are provided to show statistical significance.
Null-model tests (999 random replicates) were used to assess the significance of
spatial diversity and divergence distributions with 1.96 and 1.96 as significant
boundaries.
Code availability. Example code used to conduct null-model test (written in R)
can be found at Dryad: http://datadryad.org/resource/doi:10.5061/dryad.p89m3.
Data availability. Sequences for phylogenetic analyses have previously been
published
31
and deposited in GenBank. The dated phylogeny is archived in Dryad:
http://datadryad.org/resource/doi:10.5061/dryad.p89m3. The spatial distribu-
tion data are available from: http://www.darwintree.cn/resource/spatial_data. All
other additional data are available from the corresponding author upon reasonable
request.
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© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter
reSeArCH
Extended Data Figure 1 | Dated megaphylogeny of the Chinese angiosperms. Major clades, including magnoliids, monocots, superrosids and
superasterids, as well as the basal eudicot grade, are indicated with different colours. Divergence times were estimated using treePL.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter reSeArCH
Extended Data Figure 2 | The 95% confidence intervals of divergence
times and the Spearman’s rank correlation between our dating and
those of recent publications. a, b, Plots of divergence times and 95%
confidence intervals (grey bars) for each family (a, n = 273) and genus
(b, n = 2,909). The centre values are ages calculated based on the optimal
maximum likelihood tree. c, Correlation of nodal ages between treePL and
PATHd8 in this study (n = 5,863; r = 0.94, P = 0). d, Correlation of family
ages between treePL and ref. 22 (n = 236, r = 0.68, P = 1.17 × 1033).
e, Correlation of family ages between treePL and ref. 23 (n = 257; r = 0.55,
P = 4.54 × 1022). f, Correlation of family ages between ref. 22 and ref. 23
(n = 235; r = 0.75, P = 2.11 × 1043). The solid line is y = x.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter
reSeArCH
Extended Data Figure 3 | Number of angiosperm genera that originated
during specified geological timespans. Column with three colours shows
the number of woody (grey), herbaceous (yellow) and mixed genera (light
blue) that originated within a specific geological timespan. Number of
woody genera, n = 995; number of herbaceous genera, n = 1,569; mixed
genera (genera with both woody and herbaceous species), n = 101. The
dashed line indicates the accumulated percentage of genera that have
originated since the Early Cretaceous. Global temperature changes that
have occurred since the Palaeogene are shown by the red curve (from
ref. 39; reprinted with permission from AAAS). The x axis indicates the
geological period and time in millions of years. The left y axis shows the
total number of genera that have originated by any given time period;
the right y-axis represents the accumulated percentage of genera that
originated within a geological time period.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter reSeArCH
Extended Data Figure 4 | Plot of divergence times of the Chinese angiosperm genera in each grid cell. Mean and median values of the divergence
times are indicated.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter
reSeArCH
Extended Data Figure 5 | Histograms and distribution of skewness and
kurtosis for divergence times in each grid cell. ac, Range of skewness for
all genera (a), woody genera (b) and herbaceous genera (c). df, Range of
kurtosis (computed as the fourth standardized moment) for all genera (d),
woody genera (e) and herbaceous genera (f). gi, Spatial distribution of
skewness for all genera (g), woody genera (h) and herbaceous genera (i).
jl, Spatial distribution of kurtosis for all genera (j), woody genera (k) and
herbaceous genera (l). Skewness values in most grid cells are positive and
around 1–2, which implies that divergence times of genera are slightly
right-skewed (there are more young ages in each grid cell). Kurtosis values
in most grid cells are within a range of 4–8, larger than the value (3) for
a normal distribution, which implies that the distribution of divergence
times has more extreme outliers than the normal distribution. For eastern
China, kurtosis values of approximately 4 for all genera are consistent with
grid cells having a range of divergence times—including very young and
very old ages—as expected for an area that is both a cradle and a museum.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter reSeArCH
Extended Data Figure 6 | Geographic patterns of median ages for the
Chinese angiosperm genera. ai, Median ages for all genera, woody
genera and herbaceous genera (from left to right), based on all sampled
genera (ac), the youngest 25% of genera (df), and the oldest 25% of
genera (gi) in each grid cell. jl, Null-model test to identify recent (blue
grid cells) and ancient (red grid cells) divergence centres for all genera (j),
woody genera (k) and herbaceous genera (l). The analyses include
2,592 angiosperm genera (woody genera, n = 925; herbaceous genera,
n = 1,501; genera with both woody and herbaceous species, n = 166).
Maps adapted from National Administration of Surveying, Mapping
and Geoinformation of China (http://www.sbsm.gov.cn; review drawing
number: GS(2016)1576).
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter
reSeArCH
Extended Data Figure 7 | Spatial distribution of MDTs based on
geographic range-size quartiles and the youngest 25% and oldest 25% of
genera in China. ad, MDT patterns of the first (a), second (b), third (c)
and fourth quartiles (d) of the sampled Chinese angiosperm genera.
The first, second, third and fourth quartiles range from the narrowest
to the widest geographic distribution, and represent 0.6%, 3.5%, 13.7%
and 82.1% of 1,409,239 records, respectively. The Spearmans rank
correlation coefficients between the overall MDT (including all genera)
and MDT of the first, second, third and fourth geographic quartile are
0.12 (P = 1.46 × 103), 0.59 (P = 1.21 × 1087), 0.43 (P = 2.51 × 1043) and
0.99 (P = 0), respectively. e, MDT pattern of the youngest 25% of genera in
China, showing that there are young genera in both western and eastern
China. f, MDT pattern of the oldest 25% of genera in China, confirming
that older genera mainly occur in eastern China. Maps adapted from
National Administration of Surveying, Mapping and Geoinformation of
China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter reSeArCH
Extended Data Figure 8 | Patterns of generic richness, phylogenetic
diversity and phylogenetic structure for the Chinese angiosperm
genera. ac, Richness for all genera (a), woody genera (b) and herbaceous
genera (c). df, Phylogenetic diversity for all genera (d), woody genera (e)
and herbaceous genera (f). gi, SES-PD for all genera (g), woody genera (h)
and herbaceous genera (i). jl, NRI for all genera (j), woody genera (k) and
herbaceous genera (l). mo, NTI for all genera (m), woody genera (n)
and herbaceous genera (o). The analyses include 2,592 angiosperm
genera (woody genera, n = 925; herbaceous genera, n = 1,501; genera
with both woody and herbaceous species, n = 166). Maps adapted from
National Administration of Surveying, Mapping and Geoinformation of
China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter
reSeArCH
Extended Data Figure 9 | Patterns of species-level phylogenetic diversity
for all Chinese angiosperms. al, Observed phylogenetic diversity for
all species (a, d, g, j), woody species (b, e, h, k) and herbaceous species
(c, f, i, l) based on species trees 210, 30, 174 and 461 (species trees were
randomly selected from 1,000 post-burn-in trees). mo, SES-PD for
all species (m), woody species (n) and herbaceous species (o) based on
species tree 461. The analyses include 26,978 angiosperm species (woody,
n = 10,169; herbaceous, n = 16,809). Phylogenetic diversity and SES-PD
based on 10 species trees produce similar patterns; Spearmans rank
correlation coefficients, r > 0.99, P < 2.20 × 1016. Maps adapted from
National Administration of Surveying, Mapping and Geoinformation of
China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Letter reSeArCH
Extended Data Table 1 | Number of genera that occur only in western or eastern China, with the number of woody, herbaceous and mixed
genera in each order indicated
Mixed, genera with both woody and herbaceous species.
© 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
1
nature research | life sciences reporting summary June 2017
Corresponding author(s):
Pamela S. Soltis, Douglas E. Soltis, Jian-
Hua Li, Zhi-Duan Chen
Initial submission Revised version Final submission
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` Experimental design
1. Sample size
Describe how sample size was determined. 1. Our dated phylogeny included 5,864 species representing 2,665 genera native to
China (2,665/2,884, ca. 92% of angiosperm genera in China) from 273 families.
2. Our gridded distribution data included 1,409,239 occurrence records for 26,978
angiosperm species representing 2,845 genera. After matching with the phylogeny,
the final data set included a total of 2,592 angiosperm genera.
3. Our species-level time tree included 26,978 Chinese angiosperm species,
covering ca. 96% of all angiosperm species native to China.
2. Data exclusions
Describe any data exclusions. 1. We divided the map of China into 100-km × 100-km grid cells, and grid cells on
the border covering less than 50% of the area of a grid cell were excluded from the
analyses to minimize the sampling bias of unequal sampling areas. The criteria
were pre-established.
2. Our species tree excluded 1,098 aquatic species because phylogenetic diversity
and the environmental driving factors of terrestrial plants usually differ from those
of aquatic plants. The criteria were pre-established.
3. We inferred richness and PD in protected areas based on a species-level
phylogenetic tree and distribution data with “county” as the basic unit.
Considering that most nature reserves are smaller in size than Chinese counties,
we did not count counties with protected areas covering less than 10% of the area
of a county.
3. Replication
Describe whether the experimental findings were
reliably reproduced.
1. We conducted the dating analysis of Chinese angiosperms based on the
penalized likelihood and PATHd8 methods. Divergence times estimated with
treePL and PATHd8 are highly congruent with each other (Extended Data Fig. 2c).
Furthermore, a range of age estimates was computed using treePL based on 100
maximum likelihood bootstrap trees to better account for errors around the ages
(Extended Data Fig. 2a, b). We then compared these age estimates to those
inferred in recent papers by other authors.
2. To explore the spatial divergence patterns of Chinese angiosperms, we mapped
the mean and median divergence times of all genera in each grid cell and designed
null-model analyses to identify the ancient and recent divergence hotspots (Fig. 1;
Extended Data Fig. 6). We also mapped the mean age for the relative and absolute
25% youngest and oldest genera in each grid cell over the entire map (Extended
Data Fig. 7e–f vs. Fig. 1d, g), and both analyses show similar patterns and support
our conclusion.
3. We generated 1,000 post-burnin trees using the birth-death model to account
for alternative resolutions of polytomies in our species tree (see Methods for
details). The species-level PD and SES.PD were calculated based on 10 trees
randomly selected from the 1,000 trees, which indicate that the patterns of
phylogenetic diversity are robust to variation of trees generated by the birth-death
model (Extended Data Fig. 9).
4. Randomization
Describe how samples/organisms/participants were 1. To identify the best smoothing parameter that affects the penalty for rate
2
nature research | life sciences reporting summary June 2017
allocated into experimental groups. variation over the phylogram, a random subsample and replicate cross-validation
were conducted with treePL.
2. A randomized assemblage (n = 999) was used when we calculated SES.MDT,
SES.MedianDT, SES.PD, NRI and NTI (see Methods for details).
5. Blinding
Describe whether the investigators were blinded to
group allocation during data collection and/or analysis.
Not applicable
Note: all studies involving animals and/or human research participants must disclose whether blinding and randomization were used.
6. Statistical parameters
For all figures and tables that use statistical methods, confirm that the following items are present in relevant figure legends (or in the
Methods section if additional space is needed).
n/a Confirmed
The exact sample size (n) for each experimental group/condition, given as a discrete number and unit of measurement (animals, litters, cultures, etc.)
A description of how samples were collected, noting whether measurements were taken from distinct samples or whether the same
sample was measured repeatedly
A statement indicating how many times each experiment was replicated
The statistical test(s) used and whether they are one- or two-sided (note: only common tests should be described solely by name; more
complex techniques should be described in the Methods section)
A description of any assumptions or corrections, such as an adjustment for multiple comparisons
The test results (e.g. P values) given as exact values whenever possible and with confidence intervals noted
A clear description of statistics including central tendency (e.g. median, mean) and variation (e.g. standard deviation, interquartile range)
Clearly defined error bars
See the web collection on statistics for biologists for further resources and guidance.
` Software
Policy information about availability of computer code
7. Software
Describe the software used to analyze the data in this
study.
RAxML 8.0.22, treePL, TreeAnnotator 1.8.4, PATHd8, R 3.2.0, ArcGIS 10.1, MrBayes
3.2
For manuscripts utilizing custom algorithms or software that are central to the paper but not yet described in the published literature, software must be made
available to editors and reviewers upon request. We strongly encourage code deposition in a community repository (e.g. GitHub). Nature Methods guidance for
providing algorithms and software for publication provides further information on this topic.
` Materials and reagents
Policy information about availability of materials
8. Materials availability
Indicate whether there are restrictions on availability of
unique materials or if these materials are only available
for distribution by a for-profit company.
No restrictions. Most of the data that support the findings of this study are
available within the paper (and its Extended Data and Supplementary Information).
Sequences for phylogenetic analyses and divergence time estimation have been
deposited in GenBank. Detailed phylogenetic relationships within each major clade
are provided in Chen et al. (reference 31). Information on 138 calibrations used for
divergence time estimates of Chinese angiosperms is provided in Supplementary
Table 1. We also include a statement on data availability in our manuscript, as
required by Nature policy.
9. Antibodies
Describe the antibodies used and how they were validated
for use in the system under study (i.e. assay and species).
Not applicable
3
nature research | life sciences reporting summary June 2017
10. Eukaryotic cell lines
a. State the source of each eukaryotic cell line used. Not applicable
b. Describe the method of cell line authentication used. Not applicable
c. Report whether the cell lines were tested for
mycoplasma contamination.
Not applicable
d. If any of the cell lines used are listed in the database
of commonly misidentified cell lines maintained by
ICLAC, provide a scientific rationale for their use.
Not applicable
` Animals and human research participants
Policy information about studies involving animals; when reporting animal research, follow the ARRIVE guidelines
11. Description of research animals
Provide details on animals and/or animal-derived
materials used in the study.
Not applicable
Policy information about studies involving human research participants
12. Description of human research participants
Describe the covariate-relevant population
characteristics of the human research participants.
Not applicable
... Species composition of an ecological community reflects the interplay between ecological and evolutionary processes (Ricklefs, 1987). Numerous studies have shown that evolutionary histories of individual lineages have played important roles in governing species composition in ecological assemblages across geographic and ecological gradients (e.g., Voskamp et al., 2017 for birds;Safi et al., 2011 for mammals;Fritz & Rahbek, 2012 for amphibians; Qian et al., 2020 for fishes; Lu et al., 2018 andSandel, 2017 for plants). Evolutionary histories at different depths of a phylogenetic tree might have played different roles in assembling species into communities. ...
... Accordingly, knowledge of how deep evolutionary histories can affect the ecological assembly of angiosperms can help understand the mechanisms generating heterogeneous patterns of biodiversity across the globe. In this study, we take advantage of comprehensive data sets for Chinese angiosperm plants (Lu et al., 2018;Qian et al., 2020) to explore geographic and ecological patterns of family stem and crown ages and family phylogenetic fuses, all of which represent deep evolutionary histories of angiosperms relative to divergence times of genera and species, for angiosperm assemblages across China. These data sets have been used to address questions about geographic and ecological patterns of taxonomic and phylogenetic diversity of plants in China (e.g., Lu et al., 2018;Ye et al., 2019;Qian et al., 2020Qian et al., , 2021a. ...
... The primary goals of the present study are (i) to investigate geographic and ecological patterns of crown age, stem age, and phylogenetic fuse at the family level for angiosperm assemblages across China, using complete or nearly complete angiosperm floras, and (ii) to investigate geographic patterns of phylogenetic dispersion (relatedness) of angiosperms at the family level, which extents Lu et al.'s (2018) study by exploring patterns of phylogenetic dispersion for angiosperms in China at a deeper evolutionary depth (i.e., genus-level analysis in Lu et al.'s study versus family-level analysis in the present study). Regardless of whether the results of these two analyses are similar or different, knowledge of patterns of phylogenetic dispersion at both taxonomic levels is important to better understand the evolutionary history of angiosperms in China. ...
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Deep evolutionary histories can play an important role in assembling species into communities, but few studies have explored the effects of deep evolutionary histories on species assembly of angiosperms (flowering plants). Here we explore patterns of family divergence and diversification times (stem and crown ages, respectively) and phylogenetic fuses for angiosperm assemblages in 100 × 100 km grid cells across geographic and ecological gradients in China. We found that both family stem and crown ages of angiosperm assemblages are older in southeastern China with warm and humid climates than in northwestern China with cold and dry climates; these patterns are stronger for family stem ages than for family crown ages; families in colder and drier climates are more closely related across the family‐level angiosperm phylogeny; and family phylogenetic fuses are, on average, longer for angiosperm assemblages in warm and humid climates than in cold and dry climate. We conclude that the fact that deep evolutionary histories, which were measured as family stem and crown ages and family phylogenetic fuses in this study, have shown strong geographic and ecological patterns suggests that deep evolutionary histories of angiosperms have profound effects on assembling angiosperm species into ecological communities. This article is protected by copyright. All rights reserved.
... These patterns are consistent with the tropical niche conservatism hypothesis, which predicts phylogenetic relatedness increases with increasing environmental stress (Wiens & Donoghue, 2004). Increasing phylogenetic clustering with decreasing temperature and precipitation is commonly observed in assemblages of native angiosperms in China (e.g., Lu et al., 2018;Qian et al., 2019) and elsewhere (e.g., North America; Qian & Sandel, 2017); it was also observed in regional assemblages of naturalized angiosperms in eastern North America (Qian & Sandel, 2022). ...
... Thus, to better understand the relationship between invasiveness and phylogenetic relatedness for naturalized species, it is necessary to use a phylogeny-based approach to determine the relationships, as we did here.Some limitations in this study should be mentioned. For example, although the phylogenetic tree used in this study was resolved at a much higher degree than most of studies on species assembly phylogenetics for plants in the literature, including those on Chinese plants (e.g., about 22% and 39% of species were resolved in the phylogenetic trees used inLu et al. (2018) andQian et al. (2019), respectively, whereas 77% ...
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We test (1) whether invasive angiosperm (flowering plant) species are a phylogenetically clustered subset of all naturalized angiosperm species within an angiosperm assemblage, (2) whether more harmful invasive species are more strongly, or less strongly, related to each other, (3) whether the result of the first test is consistent with those for geographic regions distributed in substantially different climatic conditions, and (4) whether patterns of phylogenetic relatedness for invasive species in regions across climatic gradients are consistent with those for overall naturalized species. China. Current. Angiosperms (flowering plants). We recognized 28 province‐level regions in China and collated naturalized and invasive species lists of angiosperms for each region. Two phylogenetic metrics (i.e., net relatedness index and nearest taxon index), which represent different depths of evolutionary history, were used to quantify phylogenetic relatedness of angiosperms in China and in each region. Values of the metrics of phylogenetic relatedness were related to temperature and precipitation. At the national scale, invasive assemblage is a phylogenetically clustered subset of the naturalized species pool. More harmful invasive species are more strongly clustered. At the regional scale, both naturalized and invasive species are phylogenetically clustered subsets of the national naturalized species pool. Furthermore, invasive species in regional floras are also phylogenetically clustered subsets of their respective regional naturalized species pools. Invasive angiosperm species are a phylogenetically clustered subset of naturalized angiosperm species. More harmful invasive species are more strongly clustered with respect to their naturalized species pools, compared to less harmful invasive species. Our findings have significant implications to predicting and controlling invasive species based on phylogenetic relatedness among naturalized species.
... Tropical and subtropical Asia are major orchid diversity centers [15,16]. These regions are characterized by their high plant diversity and endemism [17,18] and have also been considered both a "Cradle" and a "Museum" for vascular plants since the Cretaceous [17,19,20]. During the Cenozoic, the Asian mainland experienced a series of complex geological and climate changes, such as the uplift of the Himalaya-Tibetan Plateau [21] and the establishment and intensification of the Asian monsoon [22]. ...
... Recent studies reported that both South and East Asian Summer monsoons played a decisive role in the landscape evolution of the Himalayas and the adjoining areas in the Indo-Malayan Realm [90]. The intensifications of the EASM during the Late Cenozoic brought abundant rainfall and, therefore, significantly promoted the survival and differentiation of plants in tropical and subtropical Asian mainland [19,[28][29][30]91]. During the dynamic evolutionary processes of Gastrochilus, five of eight migration events occurred from the East Asiatic region to Indo-Chinese region in the Pliocene to the early Pleistocene (4.70-2.15 ...
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Tropical and subtropical Asia are major orchid diversity and endemism centers. However, the evolutionary dynamics of orchids in these areas remain poorly studied. Gastrochilus D. Don, a species-rich orchid genus from tropical and subtropical Asian forests, was employed to investigate the issue. We firstly used eight DNA regions to reconstruct the phylogeny and estimate the divergence times within Gastrochilus. We inferred the ancestral ranges and conducted a diversification analysis based on empirical and simulated data. Subsequently, we assessed the ancestral niche state and tested for phylogenetic signals in the evolution of niche conditions. Our results suggested that the most recent common ancestor of Gastrochilus occurred in the subtropical area of the East Asiatic region in the late Miocene (8.13 Ma). At least eight dispersal events and four vicariant events were inferred to explain the current distribution of Gastrochilus, associated with the global cooling from the Plio-Pleistocene. The genus experienced a slowly decreasing diversification rate since its origin, and no significant correlation between current niches and phylogenetic relatedness was observed. The diversification of Gastrochilus was attributed to accumulation through time, integrated with the intensification of the Asian Monsoon system during the Plio-Pleistocene, pollination, and epiphytism.
... This may be resolved by rarefaction (Sandel, 2018), but at the expense of a loss of information and resulting increase in uncertainty in the phylogenetic metric (Qian et al., 2020). Accordingly, we followed recently published studies on phylogenetic dispersion (e.g., Lu et al., 2018;Park et al., 2020;Qian et al., 2020;Qian & Sandel, 2022) to use the non-rarefied values of MPD ses and MNND ses . ...
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The introduction of alien species may be influenced by the phylogenetic structure of the native assemblage, while at the same time altering that structure. Understanding these effects sheds light on both the factors influencing naturalization of introduced species and their impacts. Considering regional angiosperm assemblages across China, we ask the following questions: (a) Do geographic patterns and climate relationships of alien species richness and phylogenetic structure mirror those of natives? (b) Has the addition of alien species resulted in stronger phylogenetic clustering as predicted by Darwin's preadaptation hypothesis? (c) To what degree does the answer to these questions depend on phylogenetic scale? China. Current. Angiosperms (flowering plants). We divided China into 28 province‐level regions and collated native and naturalized alien species lists of angiosperms for each region. For each region, we computed two types of phylogenetic structure metrics [mean phylogenetic distance (MPD) and mean nearest neighbour distance (MNND), and their standardized effect sizes] for the native, alien and combined assemblages, and for angiosperms as a whole, 5 major clades and 10 well‐represented families. We then related these to climatic factors using correlation analyses. Richness of alien angiosperms is highest in regions with species rich and phylogenetically dispersed native assemblages. The standardized effect size of mean phylogenetic distance (MPDses) for aliens was positively correlated with that for natives. The introduction of alien species generally increased phylogenetic clustering of the combined assemblage compared to the natives for large phylogenetic extents, but effects within plant families were mixed. The MPDses was positively correlated with temperature and precipitation for both natives and aliens. The phylogenetic relationships at a lower level of phylogenetic scale may differ substantially from those at a higher level of phylogenetic scale. At the broadest phylogenetic extents, alien species tend to recapitulate the biogeographic patterns of natives, showing similar spatial patterns of species richness and phylogenetic structure, and tending to represent the same major angiosperm clades. This is highly consistent with Darwin's preadaptation hypothesis. Across narrower swaths of the phylogeny, these patterns are less clear, with a substantial number of plant families showing support for the biogeographic barrier hypothesis.
... In northeast China, southeast China, and the eastern Himalayas, high vegetation community complexity cells are mainly contributed by woody plants, while the high vegetation community complexity cells in the Mongolian Plateau, the Tibetan Plateau, and northwest China are mainly contributed by herbaceous plants ( Figure S6 in Supporting Information S1). Herbaceous plants have a generally higher vegetation community complexity than woody plants (Lu et al., 2018;Su et al., 2020), which may lead to the relatively high vegetation community complexity in northwest China and the Mongolian Plateau ( Figure 3 and Figure S6 in Supporting Information S1). ...
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Vegetation community complexity is a critical factor influencing terrestrial ecosystem stability. China, the country leading the world in vegetation greening resulting from human activities, has experienced dramatic changes in vegetation community composition during the past 30 years. However, how China's vegetation community complexity varies spatially and temporally remains unclear. Here, we examined the spatial pattern of China's vegetation community complexity and its temporal changes from the 1980s to 2015 using two vegetation maps of China as well as more than half a million field samples. Spatially, China's vegetation community complexity distribution is primarily dominated by elevation, although temperature and precipitation can be locally more influential than elevation when they become the factors limiting plant growth. Temporally, China's vegetation community complexity shows a significant decreasing trend during the past 30 years, despite the observed vegetation greening trend. Prevailing climate warming across China exhibits a significant negative correlation with the decrease in vegetation community complexity, but this correlation varies with biogeographical regions. The intensity of human activities have an overall negative influence on vegetation community complexity, but vegetation conservation and restoration efforts can have a positive effect on maintaining vegetation composition complexity, informing the critical role of vegetation management policies in achieving the sustainable development goal.
... Importantly, the least phylogenetically well-known regions are tropical and subtropical biodiversity hotspots with high concentration of threatened species, particularly due to habitat destruction (Myers et al. 2000, Baillie et al. 2004, Vamosi and Vamosi 2008. The paucity of phylogenetic data in these areas is a serious concern, as conservation efforts may benefit significantly from phylogenetic data (Lu et al. 2018, Velazco et al. 2020. Conversely, local and global extinction of species in those areas will make completing the plant Tree of Life increasingly difficult. ...
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The Darwinian shortfall, i.e. the lack of knowledge of phylogenetic relationships, significantly impedes our understanding of evolutionary drivers of global patterns of biodiversity. Spatial bias in the Darwinian shortfall, where phylogenetic knowledge in some regions is more complete than others, could undermine eco‐ and biogeographic inferences. Yet, spatial biases in phylogenetic knowledge for major groups – such as plants – remain poorly understood. Using data for 337 023 species (99.7%) of seed plants (Spermatophyta), we produced a global map of phylogenetic knowledge based on regional data and tested several potential drivers of the observed spatial variation. Regional phylogenetic knowledge was defined as the proportion of the regional seed plant flora represented in GenBank's nucleotide database with phylogenetically relevant data. We used simultaneous autoregressive models to explain variation in phylogenetic knowledge based on three biodiversity variables (species richness, range size and endemism) and six socioeconomic variables representing funding and accessibility. We compared observed patterns and relationships to established patterns of the Wallacean shortfall (the lack of knowledge of species distributions). We found that the Darwinian shortfall is strongly and significantly related to the macroecological distribution of species' range sizes. Small‐ranged species were significantly less likely to have phylogenetic data, leading to a concentration of the Darwinian shortfall in species‐rich, tropical countries where range sizes are small on average. Socioeconomic factors were less important, with significant but quantitatively small effects of accessibility and funding. In conclusion, reducing the Darwinian shortfall and smoothen its spatial bias will require increased efforts to sequence the world's small‐ranged (endemic) species.
... One of the most important questions on the evolution of plant diversification concerns when modern plant diversity first appeared and, specifically, the pinpointing of the earliest occurrence of a flora that is floristically comparable to present vegetation in the same region. Until recently, it was thought that many taxa in southwestern China originated during the Miocene, evidenced by molecular analyses using fossil records for calibration [7]. Previously, most fossil floras in southwestern China were dated using stratigraphic or floristic comparison [8], which were limited by their low resolution and reasoning circularity. ...
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Biodiversity hotspots are key regions for understanding the evolutionary history of biodiversity as well as the processes initiating and maintaining it [...]
... This area contains various vegetation types ranging from tropical rainforests to shrubs in alpine screes, while evergreen broadleaved forest is the dominant type (WGCV, 1980;Zhou and Chen, 2021). Molecular studies have inferred that most of the essential elements of the evergreen broadleaved forest originated near the beginning of the Miocene (Yu et al., 2017;Chen et al., 2018;Lu et al., 2018). However, increasing fossil evidence with well-constrained ages tells a different story. ...
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Quantifying the interactions between topography, climate and plant diversity within one of the world's biodiversity hotspots, the southeastern margin of the Tibetan Plateau, remains elusive due to few reliable quantitative paleoelevation reconstructions, precise geological age constraints and well-preserved plant fossils. The Lühe Basin, on the southeastern margin of Tibetan Plateau has yielded abundant plant fossils with a U-Pb age of 33–32 Ma, providing an opportunity to estimate the elevation of this region and plant diversity at that time. Fossil leaf physiognomy was used to reconstruct the paleoclimate and the paleoelevation of the basin was derived from moist enthalpy. The results show that the Lühe Basin, had attained it's present elevation (1.7 ± 0.9 km) by the early Oligocene and, compared to now, experienced a humid subtropical climate with a wetter dry season and lower precipitation seasonality in an overall wetter precipitation regime (1748.5 ± 606 mm). This was accompanied by a greater seasonal range in temperature, although the mean annual temperature (14.9 ± 2.3 °C) was similar to that of today (15.6 °C). Combined with previous studies, we conclude that the appearance of the modern flora across the southeastern margin of the Tibetan Plateau had started by the early Oligocene, corresponding with the establishment of modern topography at that time.
... The Sino-Japanese floristic region holds one of the oldest floras in the North Hemisphere with high species richness (Chen et al., 2018b;Lu et al., 2018). Climatic oscillations and geological events have greatly influenced the genetic pattern and distributional range of many plant species, particularly during the Quaternary glacial-interglacial cycles. ...
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Characterizing genetic diversity and structure and identifying conservation units are both crucial for the conservation and management of threatened species. The development of high-throughput sequencing technology provides exciting opportunities for conservation genetics. Here, we employed the powerful SuperGBS method to identify 33, 758 high-quality single-nucleotide polymorphisms (SNP) from 134 individuals of a critically endangered montane shrub endemic to North China, Lonicera oblata. A low level of genetic diversity and a high degree of genetic differentiation among populations were observed based on the SNP data. Both principal component and phylogenetic analyses detected seven clusters, which correspond exactly to the seven geographic populations. Under the optimal K = 7, Admixture suggested the combination of the two small and geographically neighboring populations in the Taihang Mountains, Dongling Mountains, and Lijiazhuang, while the division of the big population of Jiankou Great Wall in the Yan Mountains into two clusters. High population genetic diversity and a large number of private alleles were detected in the four large populations, while low diversity and non-private alleles were observed for the remaining three small populations, implying the importance of these large populations as conservation units in priority. Demographic history inference suggested two drastic contractions of population size events that occurred after the Middle Pleistocene Transition and the Last Glacial Maximum, respectively. Combining our previous ecological niche modeling results with the present genomic data, there was a possible presence of glacial refugia in the Taihang and Yan Mountains, North China. This study provides valuable data for the conservation and management of L. oblata and broadens the understanding of the high biodiversity in the Taihang and Yan Mountains.
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A common hypothesis for the rich biodiversity found in mountains is uplift-driven diversification-that orogeny creates conditions favoring rapid in situ speciation of resident lineages. We tested this hypothesis in the context of the Qinghai-Tibetan Plateau (QTP) and adjoining mountain ranges, using the phylogenetic and geographic histories of multiple groups of plants to infer the tempo (rate) and mode (colonization versus in situ diversification) of biotic assembly through time and across regions. We focused on the Hengduan Mountains region, which in comparison with the QTP and Himalayas was uplifted more recently (since the late Miocene) and is smaller in area and richer in species. Time-calibrated phylogenetic analyses show that about 8 million y ago the rate of in situ diversification increased in the Hengduan Mountains, significantly exceeding that in the geologically older QTP and Himalayas. By contrast, in the QTP and Himalayas during the same period the rate of in situ diversification remained relatively flat, with colonization dominating lineage accumulation. The Hengduan Mountains flora was thus assembled disproportionately by recent in situ diversification, temporally congruent with independent estimates of orogeny. This study shows quantitative evidence for uplift-driven diversification in this region, and more generally, tests the hypothesis by comparing the rate and mode of biotic assembly jointly across time and space. It thus complements the more prevalent method of examining endemic radiations individually and could be used as a template to augment such studies in other biodiversity hotspots.
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We reconstructed a phylogenetic tree of Chinese vascular plants (Tracheophyta) using sequences of the chloroplast genes atpB, matK, ndhF, and rbcL and mitochondrial matR. We produced a matrix comprising 6098 species and including 13 695 DNA sequences, of which 1803 were newly generated. Our taxonomic sampling spanned 3114 genera representing 323 families of Chinese vascular plants, covering more than 93% of all genera known from China. The comprehensive large phylogeny supports most relationships among and within families recognized by recent molecular phylogenetic studies for lycophytes, ferns (monilophytes), gymnosperms, and angiosperms. For angiosperms, most families in Angiosperm Phylogeny Group IV are supported as monophyletic, except for a paraphyletic Dipterocarpaceae and Santalaceae. The infrafamilial relationships of several large families and monophyly of some large genera are well supported by our dense taxonomic sampling. Our results showed thattwo species of Eberhardtia are sister to a clade formed by all other taxa of Sapotaceae, except Sarcosperma. We have made our phylogeny of Chinese vascular plants publically available for the creation of subtrees via SoTree (http://www.darwintree.cn/flora/index.shtml), an automated phylogeny assembly tool for ecologists.
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