Rapid in situ diversification rates in Rhamnaceae explain the parallel evolution of high diversity in temperate biomes from global to local scales

Tian, Qin; Stull, Gregory W.; Kellermann, Jürgen; Medan, Diego; Nge, Francis J.; Liu, Shui‐Yin; Kates, Heather R.; Soltis, Douglas E.; Soltis, Pamela S.; Guralnick, Robert P.; Folk, Ryan A.; Onstein, Renske E.; Yi, Ting‐Shuang

doi:10.1111/nph.19504

Title: Rapid in situ diversification rates in Rhamnaceae explain the parallel evolution of high diversity in temperate biomes from global to local scales

Journal Article · 16 January 2024 · New Phytologist

DOI: https://doi.org/10.1111/nph.19504 · OSTI ID:2281619

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^[3]; Medan, Diego ^[4];

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^[6]; Kates, Heather R. ^[7];

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Germplasm Bank of Wild Species, Yunnan Key Laboratory of Crop Wild Relatives Omics, Kunming Institute of Botany Chinese Academy of Sciences Kunming 650201 China, University of Chinese Academy of Sciences Beijing 101408 China, Key Laboratory of Plant Diversity and Specialty Crops Chinese Academy of Sciences Beijing 100093 China, Naturalis Biodiversity Center Darwinweg 2 2333CR Leiden the Netherlands
Germplasm Bank of Wild Species, Yunnan Key Laboratory of Crop Wild Relatives Omics, Kunming Institute of Botany Chinese Academy of Sciences Kunming 650201 China
State Herbarium of South Australia, Botanic Gardens and State Herbarium Hackney Road Adelaide SA 5000 Australia, School of Biological Sciences The University of Adelaide Adelaide SA 5005 Australia
Cátedra de Botánica General, Facultad de Agronomía Universidad de Buenos Aires Ave San Martín 4453 C1417DSE Buenos Aires Argentina
State Herbarium of South Australia, Botanic Gardens and State Herbarium Hackney Road Adelaide SA 5000 Australia, School of Biological Sciences The University of Adelaide Adelaide SA 5005 Australia, IRD – Institut de Recherche pour le Développement Ave Agropolis BP 64501 Montpellier 34394 France
Germplasm Bank of Wild Species, Yunnan Key Laboratory of Crop Wild Relatives Omics, Kunming Institute of Botany Chinese Academy of Sciences Kunming 650201 China, University of Chinese Academy of Sciences Beijing 101408 China, Key Laboratory of Plant Diversity and Specialty Crops Chinese Academy of Sciences Beijing 100093 China
Florida Museum of Natural History University of Florida Gainesville FL 32611 USA
Florida Museum of Natural History University of Florida Gainesville FL 32611 USA, Department of Biology University of Florida Gainesville FL 32611 USA
Department of Biological Sciences Mississippi State University Mississippi MS 39762 USA
Naturalis Biodiversity Center Darwinweg 2 2333CR Leiden the Netherlands, Evolution and Adaptation German Centre for Integrative Biodiversity Research (iDiv) Halle–Jena–Leipzig Puschstrasse 4 Leipzig 04103 Germany, Leipzig University Leipzig 04013 Germany

Summary The macroevolutionary processes that have shaped biodiversity across the temperate realm remain poorly understood and may have resulted from evolutionary dynamics related to diversification rates, dispersal rates, and colonization times, closely coupled with Cenozoic climate change. We integrated phylogenomic, environmental ordination, and macroevolutionary analyses for the cosmopolitan angiosperm family Rhamnaceae to disentangle the evolutionary processes that have contributed to high species diversity within and across temperate biomes. Our results show independent colonization of environmentally similar but geographically separated temperate regions mainly during the Oligocene, consistent with the global expansion of temperate biomes. High global, regional, and local temperate diversity was the result of high in situ diversification rates, rather than high immigration rates or accumulation time, except for Southern China, which was colonized much earlier than the other regions. The relatively common lineage dispersals out of temperate hotspots highlight strong source‐sink dynamics across the cosmopolitan distribution of Rhamnaceae. The proliferation of temperate environments since the Oligocene may have provided the ecological opportunity for rapid in situ diversification of Rhamnaceae across the temperate realm. Our study illustrates the importance of high in situ diversification rates for the establishment of modern temperate biomes and biodiversity hotspots across spatial scales.

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Research Organization:: Univ. of Florida, Gainesville, FL (United States)

Sponsoring Organization:: USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: SC0018247

OSTI ID:: 2281619

Journal Information:: New Phytologist, Journal Name: New Phytologist Journal Issue: 4 Vol. 241; ISSN 0028-646X

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

References (95)

High‐throughput methods for efficiently building massive phylogenies from natural history collections Folk, Ryan A.; Kates, Heather R.; LaFrance, Raphael Applications in Plant Sciences, Vol. 9, Issue 2 https://doi.org/10.1002/aps3.11410	journal	February 2021
WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas: NEW CLIMATE SURFACES FOR GLOBAL LAND AREAS Fick, Stephen E.; Hijmans, Robert J. International Journal of Climatology, Vol. 37, Issue 12 https://doi.org/10.1002/joc.5086	journal	May 2017
Rhamnaceae Medan, D.; Schirarend, C. Flowering Plants · Dicotyledons https://doi.org/10.1007/978-3-662-07257-8_37	book	January 2004
OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes Hopper, Stephen D. Plant and Soil, Vol. 322, Issue 1-2 https://doi.org/10.1007/s11104-009-0068-0	journal	July 2009
Radiation in the Cape flora and the phylogeny of peacock irises Moraea (Iridaceae) based on four plastid DNA regions Goldblatt, P. Molecular Phylogenetics and Evolution, Vol. 25, Issue 2 https://doi.org/10.1016/S1055-7903(02)00235-X	journal	October 2002
Centres of neo- and paleo-endemism for Chinese woody flora and their environmental features Wang, Qing; Huang, Jihong; Zang, Runguo Biological Conservation, Vol. 276 https://doi.org/10.1016/j.biocon.2022.109817	journal	December 2022
Global Patterns and Drivers of Bee Distribution Orr, Michael C.; Hughes, Alice C.; Chesters, Douglas Current Biology, Vol. 31, Issue 3 https://doi.org/10.1016/j.cub.2020.10.053	journal	February 2021
Historical biogeography, ecology and species richness Wiens, John J.; Donoghue, Michael J. Trends in Ecology & Evolution, Vol. 19, Issue 12 https://doi.org/10.1016/j.tree.2004.09.011	journal	December 2004
The Latitudinal Diversity Gradient: Novel Understanding through Mechanistic Eco-evolutionary Models Pontarp, Mikael; Bunnefeld, Lynsey; Cabral, Juliano Sarmento Trends in Ecology & Evolution, Vol. 34, Issue 3 https://doi.org/10.1016/j.tree.2018.11.009	journal	March 2019
Historical biogeography of Pomaderris (Rhamnaceae): Continental vicariance in Australia and repeated independent dispersals to New Zealand Nge, Francis J.; Kellermann, Jürgen; Biffin, Ed Molecular Phylogenetics and Evolution, Vol. 158 https://doi.org/10.1016/j.ympev.2021.107085	journal	May 2021
The radiation of the Cape flora, southern Africa Linder, H. P. Biological Reviews, Vol. 78, Issue 4 https://doi.org/10.1017/S1464793103006171	journal	November 2003
Biodiversity hotspots for conservation priorities Myers, Norman; Mittermeier, Russell A.; Mittermeier, Cristina G. Nature, Vol. 403, Issue 6772 https://doi.org/10.1038/35002501	journal	February 2000
Phylogenetic biome conservatism on a global scale Crisp, Michael D.; Arroyo, Mary T. K.; Cook, Lyn G. Nature, Vol. 458, Issue 7239 https://doi.org/10.1038/nature07764	journal	February 2009
Speciation gradients and the distribution of biodiversity Schluter, Dolph; Pennell, Matthew W. Nature, Vol. 546, Issue 7656 https://doi.org/10.1038/nature22897	journal	June 2017
Evolutionary history of the angiosperm flora of China Lu, Li-Min; Mao, Ling-Feng; Yang, Tuo Nature, Vol. 554, Issue 7691 https://doi.org/10.1038/nature25485	journal	January 2018
Recent accelerated diversification in rosids occurred outside the tropics Sun, Miao; Folk, Ryan A.; Gitzendanner, Matthew A. Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-17116-5	journal	July 2020
The rise of grasslands is linked to atmospheric CO2 decline in the late Palaeogene Palazzesi, Luis; Hidalgo, Oriane; Barreda, Viviana D. Nature Communications, Vol. 13, Issue 1 https://doi.org/10.1038/s41467-021-27897-y	journal	January 2022
Extant timetrees are consistent with a myriad of diversification histories Louca, Stilianos; Pennell, Matthew W. Nature, Vol. 580, Issue 7804 https://doi.org/10.1038/s41586-020-2176-1	journal	April 2020
A phylogenetic perspective on the distribution of plant diversity Donoghue, M. J. Proceedings of the National Academy of Sciences, Vol. 105, Issue Supplement 1 https://doi.org/10.1073/pnas.0801962105	journal	August 2008
Contemporaneous and recent radiations of the world's major succulent plant lineages Arakaki, M.; Christin, P. -A.; Nyffeler, R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 20 https://doi.org/10.1073/pnas.1100628108	journal	May 2011
Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot Xing, Yaowu; Ree, Richard H. Proceedings of the National Academy of Sciences, Vol. 114, Issue 17 https://doi.org/10.1073/pnas.1616063114	journal	April 2017
Are there many different routes to becoming a global biodiversity hotspot? Hughes, Colin E. Proceedings of the National Academy of Sciences, Vol. 114, Issue 17 https://doi.org/10.1073/pnas.1703798114	journal	April 2017
Rates of niche and phenotype evolution lag behind diversification in a temperate radiation Folk, Ryan A.; Stubbs, Rebecca L.; Mort, Mark E. Proceedings of the National Academy of Sciences, Vol. 116, Issue 22 https://doi.org/10.1073/pnas.1817999116	journal	May 2019
Speciation across the Earth driven by global cooling in terrestrial orchids Thompson, Jamie B.; Davis, Katie E.; Dodd, Harry O. Proceedings of the National Academy of Sciences, Vol. 120, Issue 29 https://doi.org/10.1073/pnas.2102408120	journal	July 2023
Explaining Species Richness from Continents to Communities: The Time‐for‐Speciation Effect in Emydid Turtles Stephens, Patrick R.; Wiens, John J. The American Naturalist, Vol. 161, Issue 1 https://doi.org/10.1086/345091	journal	January 2003
On the Generality of the Latitudinal Diversity Gradient Hillebrand, Helmut The American Naturalist, Vol. 163, Issue 2 https://doi.org/10.1086/381004	journal	February 2004
Adaptation, Niche Conservatism, and Convergence: Comparative Studies of Leaf Evolution in the California Chaparral Ackerly, David D. The American Naturalist, Vol. 163, Issue 5 https://doi.org/10.1086/383062	journal	May 2004
Environment, Area, and Diversification in the Species‐Rich Flowering Plant Family Iridaceae Davies, T. Jonathan; Savolainen, Vincent; Chase, Mark W. The American Naturalist, Vol. 166, Issue 3 https://doi.org/10.1086/432022	journal	September 2005
Diversification ofCeanothus(Rhamnaceae) in the California Floristic Province Burge, Dylan O.; Erwin, Diane M.; Islam, Melissa B. International Journal of Plant Sciences, Vol. 172, Issue 9 https://doi.org/10.1086/662028	journal	November 2011
Convergence, Consilience, and the Evolution of Temperate Deciduous Forests Edwards, Erika J.; Chatelet, David S.; Chen, Bo-Chang The American Naturalist, Vol. 190, Issue S1 https://doi.org/10.1086/692627	journal	August 2017
SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry Journal of Computational Biology, Vol. 19, Issue 5 https://doi.org/10.1089/cmb.2012.0021	journal	May 2012
APE: Analyses of Phylogenetics and Evolution in R language Paradis, E.; Claude, J.; Strimmer, K. Bioinformatics, Vol. 20, Issue 2 https://doi.org/10.1093/bioinformatics/btg412	journal	January 2004
Picante: R tools for integrating phylogenies and ecology Kembel, S. W.; Cowan, P. D.; Helmus, M. R. Bioinformatics, Vol. 26, Issue 11 https://doi.org/10.1093/bioinformatics/btq166	journal	April 2010
The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell Junier, T.; Zdobnov, E. M. Bioinformatics, Vol. 26, Issue 13 https://doi.org/10.1093/bioinformatics/btq243	journal	May 2010
treePL: divergence time estimation using penalized likelihood for large phylogenies Smith, Stephen A.; O’Meara, Brian C. Bioinformatics, Vol. 28, Issue 20 https://doi.org/10.1093/bioinformatics/bts492	journal	August 2012
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, Alexandros Bioinformatics, Vol. 30, Issue 9 https://doi.org/10.1093/bioinformatics/btu033	journal	January 2014
Trimmomatic: a flexible trimmer for Illumina sequence data Bolger, Anthony M.; Lohse, Marc; Usadel, Bjoern Bioinformatics, Vol. 30, Issue 15 https://doi.org/10.1093/bioinformatics/btu170	journal	April 2014
Phyx: phylogenetic tools for unix Brown, Joseph W.; Walker, Joseph F.; Smith, Stephen A. Bioinformatics, Vol. 33, Issue 12 https://doi.org/10.1093/bioinformatics/btx063	journal	February 2017
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability Katoh, K.; Standley, D. M. Molecular Biology and Evolution, Vol. 30, Issue 4 https://doi.org/10.1093/molbev/mst010	journal	January 2013
Phylogenetic Inference of Reciprocal Effects between Geographic Range Evolution and Diversification Goldberg, Emma E.; Lancaster, Lesley T.; Ree, Richard H. Systematic Biology, Vol. 60, Issue 4 https://doi.org/10.1093/sysbio/syr046	journal	May 2011
Model Selection in Historical Biogeography Reveals that Founder-Event Speciation Is a Crucial Process in Island Clades Matzke, Nicholas J. Systematic Biology, Vol. 63, Issue 6 https://doi.org/10.1093/sysbio/syu056	journal	August 2014
Unparalleled rates of species diversification in Europe Valente, Luis M.; Savolainen, Vincent; Vargas, Pablo Proceedings of the Royal Society B: Biological Sciences, Vol. 277, Issue 1687 https://doi.org/10.1098/rspb.2009.2163	journal	January 2010
Darwin review: angiosperm phylogeny and evolutionary radiations Soltis, Pamela S.; Folk, Ryan A.; Soltis, Douglas E. Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1899 https://doi.org/10.1098/rspb.2019.0099	journal	March 2019
Macroevolutionary pattern ofSaussurea(Asteraceae) provides insights into the drivers of radiating diversification Zhang, Xu; Landis, Jacob B.; Sun, Yanxia Proceedings of the Royal Society B: Biological Sciences, Vol. 288, Issue 1962 https://doi.org/10.1098/rspb.2021.1575	journal	November 2021
Did succulents diversify in response to aridity? Evolutionary analyses of major succulent lineages around the world Thompson, Jamie; Ramirez-Barahona, Santiago; Priest, Nicholas bioRxiv https://doi.org/10.1101/2023.05.23.541957	journal	May 2023
Beyond climate: convergence in fast evolving sclerophylls in Cape and Australian Rhamnaceae predates the mediterranean climate Onstein, Renske E.; Linder, H. Peter Journal of Ecology, Vol. 104, Issue 3 https://doi.org/10.1111/1365-2745.12538	journal	February 2016
phyloregion: R package for biogeographical regionalization and macroecology Daru, Barnabas H.; Karunarathne, Piyal; Schliep, Klaus Methods in Ecology and Evolution, Vol. 11, Issue 11 https://doi.org/10.1111/2041-210X.13478	journal	September 2020
Fossils and a Large Molecular Phylogeny show that the Evolution of Species Richness, Generic Diversity, and Turnover Rates are Disconnected Xing, Yaowu; Onstein, Renske E.; Carter, Richard J. Evolution, Vol. 68, Issue 10 https://doi.org/10.1111/evo.12489	journal	August 2014
Do Mediterranean-type ecosystems have a common history?-Insights from the Buckthorn family (Rhamnaceae) Onstein, Renske E.; Carter, Richard J.; Xing, Yaowu Evolution, Vol. 69, Issue 3 https://doi.org/10.1111/evo.12605	journal	February 2015
The latitudinal diversity gradient in New World swallowtail butterflies is caused by contrasting patterns of out-of- and into-the-tropics dispersal Owens, Hannah L.; Lewis, Delano S.; Dupuis, Julian R. Global Ecology and Biogeography, Vol. 26, Issue 12 https://doi.org/10.1111/geb.12672	journal	November 2017
Historical biogeography of Australian Rhamnaceae, tribe Pomaderreae Ladiges, Pauline Y.; Kellermann, Jürgen; Nelson, Gareth Journal of Biogeography, Vol. 32, Issue 11 https://doi.org/10.1111/j.1365-2699.2005.01347.x	journal	September 2005
Centres of plant endemism in China: places for survival or for speciation? López-Pujol, Jordi; Zhang, Fu-Min; Sun, Hai-Qin Journal of Biogeography, Vol. 38, Issue 7 https://doi.org/10.1111/j.1365-2699.2011.02504.x	journal	April 2011
Rapid diversification of Tragopogon and ecological associates in Eurasia Bell, C. D.; Mavrodiev, E. V.; Soltis, P. S. Journal of Evolutionary Biology, Vol. 25, Issue 12 https://doi.org/10.1111/j.1420-9101.2012.02616.x	journal	November 2012
Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography Mittelbach, Gary G.; Schemske, Douglas W.; Cornell, Howard V. Ecology Letters, Vol. 10, Issue 4 https://doi.org/10.1111/j.1461-0248.2007.01020.x	journal	April 2007
VEGAN, a package of R functions for community ecology Dixon, Philip Journal of Vegetation Science, Vol. 14, Issue 6 https://doi.org/10.1111/j.1654-1103.2003.tb02228.x	journal	April 2003
`Diversitree` : comparative phylogenetic analyses of diversification in R FitzJohn, Richard G. Methods in Ecology and Evolution, Vol. 3, Issue 6 https://doi.org/10.1111/j.2041-210X.2012.00234.x	journal	August 2012
Stochastic Processes and Population Growth Kendall, David G. Journal of the Royal Statistical Society: Series B (Methodological), Vol. 11, Issue 2 https://doi.org/10.1111/j.2517-6161.1949.tb00032.x	journal	July 1949
Estimation Methods for Evolutive Processes Moran, P. A. P. Journal of the Royal Statistical Society: Series B (Methodological), Vol. 13, Issue 1 https://doi.org/10.1111/j.2517-6161.1951.tb00078.x	journal	January 1951
Bayesian estimation of the global biogeographical history of the Solanaceae Dupin, Julia; Matzke, Nicholas J.; Särkinen, Tiina Journal of Biogeography, Vol. 44, Issue 4 https://doi.org/10.1111/jbi.12898	journal	November 2016
Mountains, climate and niche heterogeneity explain global patterns of fern diversity Suissa, Jacob S.; Sundue, Michael A.; Testo, Weston L. Journal of Biogeography, Vol. 48, Issue 6 https://doi.org/10.1111/jbi.14076	journal	February 2021
Spatial phylogenetics of the Chinese angiosperm flora provides insights into endemism and conservation Zhang, Xiao‐Xia; Ye, Jian‐Fei; Laffan, Shawn W. Journal of Integrative Plant Biology, Vol. 64, Issue 1 https://doi.org/10.1111/jipb.13189	journal	January 2022
Evolutionary history of the flora of Mexico: Dry forests cradles and museums of endemism Sosa, Victoria; De‐Nova, J. Arturo; Vásquez‐Cruz, Marilyn Journal of Systematics and Evolution, Vol. 56, Issue 5 https://doi.org/10.1111/jse.12416	journal	May 2018
Phylogenomic analysis of the hemp family (Cannabaceae) reveals deep cyto‐nuclear discordance and provides new insights into generic relationships Fu, Xiao‐Gang; Liu, Shui‐Yin; van Velzen, Robin Journal of Systematics and Evolution, Vol. 61, Issue 5 https://doi.org/10.1111/jse.12920	journal	December 2022
The contrasting nature of woody plant species in different neotropical forest biomes reflects differences in ecological stability Pennington, R. Toby; Lavin, Matt New Phytologist, Vol. 210, Issue 1 https://doi.org/10.1111/nph.13724	journal	November 2015
Functional biogeography of angiosperms: life at the extremes Zanne, Amy E.; Pearse, William D.; Cornwell, William K. New Phytologist, Vol. 218, Issue 4 https://doi.org/10.1111/nph.15114	journal	March 2018
What explains high plant richness in East Asia? Time and diversification in the tribe Lysimachieae (Primulaceae) Yan, Hai‐Fei; Zhang, Cai‐Yun; Anderberg, Arne A. New Phytologist, Vol. 219, Issue 1 https://doi.org/10.1111/nph.15144	journal	April 2018
Increased diversification rates are coupled with higher rates of climate space exploration in Australian Acacia (Caesalpinioideae) Renner, Matt A. M.; Foster, Charles S. P.; Miller, Joseph T. New Phytologist, Vol. 226, Issue 2 https://doi.org/10.1111/nph.16349	journal	January 2020
Angiosperms at the edge: Extremity, diversity, and phylogeny Folk, Ryan A.; Siniscalchi, Carolina M.; Soltis, Douglas E. Plant, Cell & Environment, Vol. 43, Issue 12 https://doi.org/10.1111/pce.13887	journal	September 2020
Multiple macroevolutionary routes to becoming a biodiversity hotspot Igea, J.; Tanentzap, A. J. Science Advances, Vol. 5, Issue 2 https://doi.org/10.1126/sciadv.aau8067	journal	February 2019
Trends, Rhythms, and Aberrations in Global Climate 65 Ma to Present Zachos, J. Science, Vol. 292, Issue 5517 https://doi.org/10.1126/science.1059412	journal	April 2001
Out of the Tropics: Evolutionary Dynamics of the Latitudinal Diversity Gradient Jablonski, D.; Roy, K.; Valentine, J. W. Science, Vol. 314, Issue 5796 https://doi.org/10.1126/science.1130880	journal	October 2006
Ancient orogenic and monsoon-driven assembly of the world’s richest temperate alpine flora Ding, Wen-Na; Ree, Richard H.; Spicer, Robert A. Science, Vol. 369, Issue 6503 https://doi.org/10.1126/science.abb4484	journal	July 2020
Biome Shifts and Niche Evolution in Plants Donoghue, Michael J.; Edwards, Erika J. Annual Review of Ecology, Evolution, and Systematics, Vol. 45, Issue 1 https://doi.org/10.1146/annurev-ecolsys-120213-091905	journal	November 2014
Ecological Opportunity and Adaptive Radiation Stroud, James T.; Losos, Jonathan B. Annual Review of Ecology, Evolution, and Systematics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-ecolsys-121415-032254	journal	November 2016
Mediterranean Biomes: Evolution of Their Vegetation, Floras, and Climate Rundel, Philip W.; Arroyo, Mary T. K.; Cowling, Richard M. Annual Review of Ecology, Evolution, and Systematics, Vol. 47, Issue 1 https://doi.org/10.1146/annurev-ecolsys-121415-032330	journal	November 2016
Phylogenies and Community Ecology Webb, Campbell O.; Ackerly, David D.; McPeek, Mark A. Annual Review of Ecology and Systematics, Vol. 33, Issue 1 https://doi.org/10.1146/annurev.ecolsys.33.010802.150448	journal	November 2002
BLAST+: architecture and applications Camacho, Christiam; Coulouris, George; Avagyan, Vahram BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-421	journal	January 2009
Automated generation of heuristics for biological sequence comparison Slater, Guy St C.; Birney, Ewan BMC Bioinformatics, Vol. 6, Issue 1 https://doi.org/10.1186/1471-2105-6-31	journal	February 2005
Exploring power and parameter estimation of the BiSSE method for analyzing species diversification Davis, Matthew P.; Midford, Peter E.; Maddison, Wayne BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-38	journal	January 2013
ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees Zhang, Chao; Rabiee, Maryam; Sayyari, Erfan BMC Bioinformatics, Vol. 19, Issue S6 https://doi.org/10.1186/s12859-018-2129-y	journal	May 2018
Plastid phylogenomic insights into relationships of all flowering plant families Li, Hong-Tao; Luo, Yang; Gan, Lu BMC Biology, Vol. 19, Issue 1 https://doi.org/10.1186/s12915-021-01166-2	journal	October 2021
Phylogenetic relationships within the cosmopolitan buckthorn family (Rhamnaceae) support the resurrection of Sarcomphalus and the description of Pseudoziziphus gen. nov. Hauenschild, Frank; Matuszak, Sabine; Muellner-Riehl, Alexandra N. TAXON, Vol. 65, Issue 1 https://doi.org/10.12705/651.4	journal	November 2015
BEAST 2: A Software Platform for Bayesian Evolutionary Analysis Bouckaert, Remco; Heled, Joseph; Kühnert, Denise PLoS Computational Biology, Vol. 10, Issue 4 https://doi.org/10.1371/journal.pcbi.1003537	journal	April 2014
Adaptive Radiation in Mediterranean Cistus (Cistaceae) Guzmán, Beatriz; Lledó, María Dolores; Vargas, Pablo PLoS ONE, Vol. 4, Issue 7 https://doi.org/10.1371/journal.pone.0006362	journal	July 2009
C4 Photosynthesis Promoted Species Diversification during the Miocene Grassland Expansion Spriggs, Elizabeth L.; Christin, Pascal-Antoine; Edwards, Erika J. PLoS ONE, Vol. 9, Issue 5 https://doi.org/10.1371/journal.pone.0097722	journal	May 2014
Where on Earth are the “tropics”? Feeley, Kenneth J.; Stroud, James T. Frontiers of Biogeography, Vol. 10, Issue 1-2 https://doi.org/10.21425/F5101-238649	journal	August 2018
Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing Matzke, Nicholas Joseph Frontiers of Biogeography, Vol. 5, Issue 4 https://doi.org/10.21425/F55419694	journal	December 2013
Lineages through space and time plots: Visualising spatial and temporal changes in diversity Skeels, Alex Frontiers of Biogeography, Vol. 11, Issue 2 https://doi.org/10.21425/F5FBG42954	journal	July 2019
Phylogenetic analysis of Phylica L. (Rhamnaceae) with an emphasis on island species: evidence from plastid trnL‐F and nuclear internal transcribed spacer (ribosomal) DNA sequences Richardson, James E.; Weitz, Frans M.; Fay, Michael F. TAXON, Vol. 50, Issue 2 https://doi.org/10.2307/1223889	journal	May 2001
Endemism and Speciation in the California Flora Stebbins, G. Ledyard; Major, Jack Ecological Monographs, Vol. 35, Issue 1 https://doi.org/10.2307/1942216	journal	January 1965
A phylogenetic analysis of Rhamnaceae using rbcL and trnL‐F plastid DNA sequences Richardson, James E.; Fay, Michael F.; Cronk, Quentin C. B. American Journal of Botany, Vol. 87, Issue 9 https://doi.org/10.2307/2656724	journal	September 2000
A Revision of the Tribal Classification of Rhamnaceae Richardson, J. E.; Fay, M. F.; Cronk, Q. C. B. Kew Bulletin, Vol. 55, Issue 2 https://doi.org/10.2307/4115645	journal	January 2000
HybPiper: Extracting Coding Sequence and Introns for Phylogenetics from High-Throughput Sequencing Reads Using Target Enrichment Johnson, Matthew G.; Gardner, Elliot M.; Liu, Yang Applications in Plant Sciences, Vol. 4, Issue 7 https://doi.org/10.3732/apps.1600016	journal	July 2016
Updated world map of the Köppen-Geiger climate classification Peel, M. C.; Finlayson, B. L.; McMahon, T. A. Hydrology and Earth System Sciences, Vol. 11, Issue 5 https://doi.org/10.5194/hess-11-1633-2007	journal	January 2007
The Major Features of Evolution Simpson, George Gaylord https://doi.org/10.7312/simp93764	book	December 1953

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Title: Rapid in situ diversification rates in Rhamnaceae explain the parallel evolution of high diversity in temperate biomes from global to local scales

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