Assessing the distribution of geographically restricted and evolutionarily unique species and their underlying drivers is key to understanding biogeographical processes and critical for global conservation prioritization. Here, we quantified the geographic distribution and drivers of phylogenetic endemism for ~320,000 seed plants worldwide and identified centers and drivers of evolutionarily young (neoendemism) and evolutionarily old endemism (paleoendemism). Tropical and subtropical islands as well as tropical mountain regions displayed the world's highest phylogenetic endemism. Most tropical rainforest regions emerged as centers of paleoendemism, while most Mediterranean-climate regions showed high neoendemism. Centers where high neo- and paleoendemism coincide emerged on some oceanic and continental fragment islands, in Mediterranean-climate regions and parts of the Irano-Turanian floristic region. Global variation in phylogenetic endemism was well explained by a combination of past and present environmental factors (79.8 to 87.7% of variance explained) and most strongly related to environmental heterogeneity. Also, warm and wet climates, geographic isolation, and long-term climatic stability emerged as key drivers of phylogenetic endemism. Neo- and paleoendemism were jointly explained by climatic and geological history. Long-term climatic stability promoted the persistence of paleoendemics, while the isolation of oceanic islands and their unique geological histories promoted neoendemism. Mountainous regions promoted both neo- and paleoendemism, reflecting both diversification and persistence over time. Our study provides insights into the evolutionary underpinnings of biogeographical patterns in seed plants and identifies the areas on Earth with the highest evolutionary and biogeographical uniqueness-key information for setting global conservation priorities.

Biodiversity Macroecology and Biogeography University of Göttingen Göttingen 37077 Germany

Campus Institute Data Science Göttingen 37077 Germany

Centre of Biodiversity and Sustainable Land Use University of Göttingen Göttingen 37077 Germany

Czech Academy of Sciences Institute of Botany Department of Invasion Ecology Průhonice 252 43 Czech Republic

Department of Biosciences Durham University Durham DH1 3LE United Kingdom

Department of Ecology Faculty of Science Charles University Prague 128 44 Czech Republic

Division of Bioinvasions Global Change and Macroecology University Vienna Vienna 1030 Austria

Ecology Department of Biology University of Konstanz Konstanz 78464 Germany

German Centre for Integrative Biodiversity Research Halle Jena Leipzig Leipzig 04103 Germany

School of Natural Sciences Macquarie University Sydney NSW 2109 Australia

Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation Taizhou University Taizhou 318000 China

Zobrazit více v PubMed

Sheth S. N., Morueta-Holme N., Angert A. L., Determinants of geographic range size in plants. New Phytol. 226, 650–665 (2020). PubMed

Enquist B. J., et al. , The commonness of rarity: Global and future distribution of rarity across land plants. Sci. Adv. 5, eaaz0414 (2019). PubMed PMC

Kier G., et al. , A global assessment of endemism and species richness across island and mainland regions. Proc. Natl. Acad. Sci. U.S.A. 106, 9322–9327 (2009). PubMed PMC

Myers N., Mittermeier R. A., Mittermeier C. G., da Fonseca G. A. B., Kent J., Biodiversity hotspots for conservation priorities. Nature 403, 853–858 (2000). PubMed

Pitman N. C. A., Jørgensen P. M., Estimating the size of the world’s threatened flora. Science 298, 989–989 (2002). PubMed

Purvis A., Agapow P.-M., Gittleman J. L., Mace G. M., Nonrandom extinction and the loss of evolutionary history. Science 288, 328–330 (2000). PubMed

Mace G. M., Gittleman J. L., Purvis A., Preserving the tree of life. Science 300, 1707–1709 (2003). PubMed

Gumbs R., et al. , The EDGE2 protocol: Advancing the prioritisation of evolutionarily distinct and globally endangered species for practical conservation action. PLoS Biol. 21, e3001991 (2023). PubMed PMC

Faith D. P., Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61, 1–10 (1992).

Veron S., et al. , High evolutionary and functional distinctiveness of endemic monocots in world islands. Biodivers. Conserv. 30, 3697–3715 (2021).

Rosauer D., Laffan S. W., Crisp M. D., Donnellan S. C., Cook L. G., Phylogenetic endemism: A new approach for identifying geographical concentrations of evolutionary history. Mol. Ecol. 18, 4061–4072 (2009). PubMed

Mishler B. D., et al. , Phylogenetic measures of biodiversity and neo- and paleo-endemism in Australian Acacia. Nat. Commun. 5, 4473 (2014). PubMed

Thompson J. D., Lavergne S., Affre L., Gaudeul M., Debussche M., Ecological differentiation of mediterranean endemic plants. Taxon 54, 967–976 (2005).

Hughes C. E., Atchison G. W., The ubiquity of alpine plant radiations: From the andes to the hengduan mountains. New Phytol. 207, 275–282 (2015). PubMed

Fernández-Mazuecos M., et al. , The radiation of Darwin’s giant daisies in the Galápagos Islands. Curr. Biol. 30, 4989–4998 (2020). PubMed

Losos J. B., Ricklefs R. E., Adaptation and diversification on islands. Nature 457, 830–836 (2009). PubMed

Weigelt P., et al. , Global patterns and drivers of phylogenetic structure in island floras. Sci. Rep. 5, 12213 (2015). PubMed PMC

Cronk Q. C. B., Relict floras of Atlantic islands: Patterns assessed. Biol. J. Linn. Soc. Lond. 46, 91–103 (1992).

Fjeldså J., Lovett J. C., Geographical patterns of old and young species in African forest biota: The significance of specific montane areas as evolutionary centres. Biodivers. Conserv. 6, 325–346 (1997).

Dynesius M., Jansson R., Evolutionary consequences of changes in species’ geographical distributions driven by Milankovitch climate oscillations. Proc. Natl. Acad. Sci. U.S.A. 97, 9115–9120 (2000). PubMed PMC

Davis M. B., Shaw R. G., Range shifts and adaptive responses to Quaternary climate change. Science 292, 673–679 (2001). PubMed

Jansson R., Global patterns in endemism explained by past climatic change. Proc. R. Soc. Lond. B Biol. Sci. 270, 583–590 (2003). PubMed PMC

Bennett K. D., Tzedakis P. C., Willis K. J., Quaternary refugia of north European trees. J. Biogeogr. 18, 103–115 (1991).

Jump A. S., Mátyás C., Peñuelas J., The altitude-for-latitude disparity in the range retractions of woody species. Trends Ecol. Evol. 24, 694–701 (2009). PubMed

Crisp M. D., Laffan S., Linder H. P., Monro A., Endemism in the Australian flora. J. Biogeogr. 28, 183–198 (2001).

Gillespie R. G., Roderick G. K., Arthropods on islands: Colonization, speciation, and conservation. Annu. Rev. Entomol. 47, 595–632 (2002). PubMed

Cronk Q. C. B., Islands: Stability, diversity, conservation. Biodivers. Conserv. 6, 477–493 (1997).

Lu L.-M., et al. , Evolutionary history of the angiosperm flora of China. Nature 554, 234–238 (2018). PubMed

Thornhill A. H., et al. , Continental-scale spatial phylogenetics of Australian angiosperms provides insights into ecology, evolution and conservation. J. Biogeogr. 43, 2085–2098 (2016).

Weigelt P., König C., Kreft H., GIFT – A global inventory of floras and traits for macroecology and biogeography. J. Biogeogr. 47, 16–43 (2020).

Govaerts R., Nic Lughadha E., Black N., Turner R., Paton A., The world checklist of vascular plants, a continuously updated resource for exploring global plant diversity. Sci. Data 8, 215 (2021). PubMed PMC

Smith S. A., Brown J. W., Constructing a broadly inclusive seed plant phylogeny. Am. J. Bot. 105, 302–314 (2018). PubMed

Hojsgaard D., Klatt S., Baier R., Carman J. G., Hörandl E., Taxonomy and biogeography of apomixis in angiosperms and associated biodiversity characteristics. CRC Crit. Rev. Plant Sci. 33, 414–427 (2014). PubMed PMC

Mishler B. D., Spatial phylogenetics. J. Biogeogr. 50, jbi.14618 (2023).

Rudbeck A. V., et al. , The darwinian shortfall in plants: phylogenetic knowledge is driven by range size. Ecography 2022, e06142 (2022).

Daru B. H., Farooq H., Antonelli A., Faurby S., Endemism patterns are scale dependent. Nat. Commun. 11, 2115 (2020). PubMed PMC

Weigelt P., Kreft H., Quantifying island isolation–insights from global patterns of insular plant species richness. Ecography 36, 417–429 (2013).

Takhtajan A. L., Floristic Regions of the World (University of California Press, 1986).

Gallagher R. V., et al. , Global shortfalls in threat assessments for endemic flora by country. Plants People Planet 5, ppp3.10369 (2023).

Cronk Q. C. B., The history of endemic flora of St Helena: A relictual series. New Phytol. 105, 509–520 (1987). PubMed

Clement W. L., et al. , Phylogenetic position and biogeography of Hillebrandia sandwicensis (Begoniaceae): A rare Hawaiian relict. Am. J. Bot. 91, 905–917 (2004). PubMed

Zhang L., et al. , The water lily genome and the early evolution of flowering plants. Nature 577, 79–84 (2020). PubMed PMC

Kisel Y., Barraclough T. G., Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175, 316–334 (2010). PubMed

Antonelli A., et al. , Madagascar’s extraordinary biodiversity: Evolution, distribution, and use. Science 378, eabf0869 (2022). PubMed

Yoder A. D., Nowak M. D., Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annu. Rev. Ecol. Evol. Syst. 37, 405–431 (2006).

Buerki S., Devey D. S., Callmander M. W., Phillipson P. B., Forest F., Spatio-temporal history of the endemic genera of Madagascar. Bot. J. Linn. Soc. 171, 304–329 (2013).

Procheş Ş, Ramdhani S., Perera S. J., Ali J. R., Gairola S., Global hotspots in the present-day distribution of ancient animal and plant lineages. Sci. Rep. 5, 15457 (2015). PubMed PMC

Fernández-Palacios J. M., et al. , Scientists’ warning – The outstanding biodiversity of islands is in peril. Glob. Ecol. Conserv. 31, e01847 (2021). PubMed PMC

Cai L., et al. , Global models and predictions of plant diversity based on advanced machine learning techniques. New Phytol. 237, 1432–1445 (2023). PubMed

Dagallier L. M. J., et al. , Cradles and museums of generic plant diversity across tropical Africa. New Phytol. 225, 2196–2213 (2020). PubMed PMC

Merckx V. S. F. T., et al. , Evolution of endemism on a young tropical mountain. Nature 524, 347–350 (2015). PubMed

Xing Y., Ree R. H., Uplift-driven diversification in the Hengduan Mountains, a temperate biodiversity hotspot. Proc. Natl. Acad. Sci. U.S.A. 114, E3444–E3451 (2017). PubMed PMC

Antonelli A., et al. , Geological and climatic influences on mountain biodiversity. Nat. Geosci. 11, 718–725 (2018).

Rahbek C., et al. , Building mountain biodiversity: Geological and evolutionary processes. Science 365, 1114–1119 (2019). PubMed

Flantua S. G. A., et al. , Snapshot isolation and isolation history challenge the analogy between mountains and islands used to understand endemism. Global Ecol. Biogeogr. 29, 1651–1673 (2020).

Sandel B., et al. , The influence of late quaternary climate-change velocity on species endemism. Science 334, 660–664 (2011). PubMed

Evans K. L., Warren P. H., Gaston K. J., Species–energy relationships at the macroecological scale: A review of the mechanisms. Biol. Rev. 80, 1–25 (2005). PubMed

Valente L. M., Savolainen V., Vargas P., Unparalleled rates of species diversification in Europe. Proc. R. Soc. B Biol. Sci. 277, 1489–1496 (2010). PubMed PMC

Storch D., Keil P., Jetz W., Universal species–area and endemics–area relationships at continental scales. Nature 488, 78–81 (2012). PubMed

Thornhill A. H., et al. , Spatial phylogenetics of the native California flora. BMC Biol 15, 96 (2017). PubMed PMC

Sandel B., et al. , Current climate, isolation and history drive global patterns of tree phylogenetic endemism. Glob. Ecol. Biogeogr. 29, 4–15 (2020).

Denelle P., Weigelt P., Kreft H., GIFT – an R package to access the Global Inventory of Floras and Traits. bioRxiv [Preprint] (2023). 10.1101/2023.06.27.546704 (accessed 22 October 2022). DOI

Chamberlain S. A., E., Szöcs, taxize: Taxonomic search and retrieval in R. F1000Res 2, 191 (2013). PubMed PMC

Majeský L., Krahulec F., Vašut R. J., How apomictic taxa are treated in current taxonomy: A review. Taxon 66, 1017–1040 (2017).

Sochor M., Vašut R. J., Sharbel T. F., Trávníček B., How just a few makes a lot: Speciation via reticulation and apomixis on example of European brambles (Rubus subgen. Rubus, Rosaceae). Mol. Phylogenet. Evol. 89, 13–27 (2015). PubMed

Tietje M., et al. , Global variation in diversification rate and species richness are unlinked in plants. Proc. Natl. Acad. Sci. U.S.A. 119, e2120662119 (2022). PubMed PMC

Pearse W. D., et al. , pez: Phylogenetics for the environmental sciences. Bioinformatics 31, 2888–2890 (2015). PubMed

Qian H., Ricklefs R. E., Thuiller W., Evolutionary assembly of flowering plants into sky islands. Nat. Ecol. Evol. 5, 640–646 (2021). PubMed

Qian H., Jin Y., Are phylogenies resolved at the genus level appropriate for studies on phylogenetic structure of species assemblages? Plant Divers. 43, 255–263 (2021). PubMed PMC

Hengl T., et al. , SoilGrids250m: Global gridded soil information based on machine learning. PLoS One 12, e0169748 (2017). PubMed PMC

Danielson J. J., Gesch D. B.. Global multi-resolution terrain elevation data 2010 (GMTED2010) (2011). 10.3133/ofr20111073. Accessed 02 May 2017. DOI

Karger D. N., et al. , Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017). PubMed PMC

Owens H. L., Guralnick R., climateStability: An R package to estimate climate stability from time-slice climatologies. Biodivers. Inform. 14, 8–13 (2019).

Brown J. L., Hill D. J., Dolan A. M., Carnaval A. C., Haywood A. M., PaleoClim, high spatial resolution paleoclimate surfaces for global land areas. Sci. Data 5, 1–9 (2018). PubMed PMC

Solt F., Y., Hu, interplot: Plot the effects of variables in interaction terms (2015). https://CRAN.R-project.org/package=interplot. Accessed 19 May 2022.

Dormann C., et al. , Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30, 609–628 (2007).

Crase B., Liedloff A. C., Wintle B. A., A new method for dealing with residual spatial autocorrelation in species distribution models. Ecography 35, 879–888 (2012).

Lim J. Y., Svenning J.-C., Göldel B., Faurby S., Kissling W. D., Frugivore-fruit size relationships between palms and mammals reveal past and future defaunation impacts. Nat. Commun. 11, 4904 (2020). PubMed PMC

Cai L., Data and codes for exploring global centers of neo- and paleoendemism in seed plants. figshare. 10.6084/m9.figshare.21909822. Deposited 17 January 2023. PubMed DOI

Environmental filtering, not dispersal history, explains global patterns of phylogenetic turnover in seed plants at deep evolutionary timescales