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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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).
The authors declare no competing financial interests.
Reviewer Information Nature thanks R. Colwell, V. Savolainen and the other anonymous reviewer(s) for their contribution to the peer review of this work.
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Extended data figures and tables
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.
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 × 10−33). e, Correlation of family ages between treePL and ref. 23 (n = 257; r = 0.55, P = 4.54 × 10−22). f, Correlation of family ages between ref. 22 and ref. 23 (n = 235; r = 0.75, P = 2.11 × 10−43). The solid line is y = x.
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.
Mean and median values of the divergence times are indicated.
Extended Data Figure 5 Histograms and distribution of skewness and kurtosis for divergence times in each grid cell.
a–c, Range of skewness for all genera (a), woody genera (b) and herbaceous genera (c). d–f, Range of kurtosis (computed as the fourth standardized moment) for all genera (d), woody genera (e) and herbaceous genera (f). g–i, Spatial distribution of skewness for all genera (g), woody genera (h) and herbaceous genera (i). j–l, 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.
a–i, Median ages for all genera, woody genera and herbaceous genera (from left to right), based on all sampled genera (a–c), the youngest 25% of genera (d–f), and the oldest 25% of genera (g–i) in each grid cell. j–l, 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).
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.
a–d, 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 Spearman’s 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 × 10−3), 0.59 (P = 1.21 × 10−87), 0.43 (P = 2.51 × 10−43) 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).
Extended Data Figure 8 Patterns of generic richness, phylogenetic diversity and phylogenetic structure for the Chinese angiosperm genera.
a–c, Richness for all genera (a), woody genera (b) and herbaceous genera (c). d–f, Phylogenetic diversity for all genera (d), woody genera (e) and herbaceous genera (f). g–i, SES-PD for all genera (g), woody genera (h) and herbaceous genera (i). j–l, NRI for all genera (j), woody genera (k) and herbaceous genera (l). m–o, 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).
Extended Data Figure 9 Patterns of species-level phylogenetic diversity for all Chinese angiosperms.
a–l, 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). m–o, 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; Spearman’s rank correlation coefficients, r > 0.99, P < 2.20 × 10−16. Maps adapted from National Administration of Surveying, Mapping and Geoinformation of China (http://www.sbsm.gov.cn; review drawing number: GS(2016)1576).
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Lu, L., Mao, L., Yang, T. et al. Evolutionary history of the angiosperm flora of China. Nature 554, 234–238 (2018). https://doi.org/10.1038/nature25485
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