Abstract
Tropical mountains are hot spots of biodiversity and endemism1,2,3, but the evolutionary origins of their unique biotas are poorly understood4. In varying degrees, local and regional extinction, long-distance colonization, and local recruitment may all contribute to the exceptional character of these communities5. Also, it is debated whether mountain endemics mostly originate from local lowland taxa, or from lineages that reach the mountain by long-range dispersal from cool localities elsewhere6. Here we investigate the evolutionary routes to endemism by sampling an entire tropical mountain biota on the 4,095-metre-high Mount Kinabalu in Sabah, East Malaysia. We discover that most of its unique biodiversity is younger than the mountain itself (6 million years), and comprises a mix of immigrant pre-adapted lineages and descendants from local lowland ancestors, although substantial shifts from lower to higher vegetation zones in this latter group were rare. These insights could improve forecasts of the likelihood of extinction and ‘evolutionary rescue’7 in montane biodiversity hot spots under climate change scenarios.
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Accession codes
Primary accessions
GenBank/EMBL/DDBJ
Data deposits
GenBank accession numbers for newly determined sequences are: KF369344, KF492848, KF839944–KF839949, KM378672–KM378719, KM489525–KM489544, KM982697–KM982715, KP152323–KP152394, KP978313–KP979097, KR002164–KR002181, KR030167–KR030238 and KR232819–KR232836. A large portion of the data is also publicly available on BOLD (http://www.boldsystems.org), as dataset DS–KINA (http://dx.doi.org/10.5883/DS-KINA). Voucher specimens have been archived in public natural history collections.
References
Körner, C. & Spehn, E. M. Mountain Biodiversity: a Global Assessment (Parthenon, Boca Raton, 2002)
Chen, I. C. et al. Elevation increases in moth assemblages over 42 years on a tropical mountain. Proc. Natl Acad. Sci. USA 106, 1479–1483 (2009)
La Sorte, F. A. & Jetz, W. Projected range contractions of montane biodiversity under global warming. Proc. R. Soc. Lond. B 277, 3401–3410 (2010)
Graham, C. H. et al. The origin and maintenance of montane diversity: integrating evolutionary and ecological processes. Ecography 37, 711–719 (2014)
Cadena, C. D. et al. Latitude, elevational climatic zonation and speciation in New World vertebrates. Proc. R. Soc. Lond. B 279, 194–201 (2012)
Rodríguez-Castañeda, G. et al. Tropical forests are not flat: how mountains affect herbivore diversity. Ecol. Lett. 13, 1348–1357 (2010)
Schiffers, K., Borne, E. C., Lavergne, S., Thuiller, W. & Travis, J. M. J. Limited evolutionary rescue of locally adapted populations facing climate change. Phil. Trans. R. Soc. Lond. B 368, 20120083 (2013)
Hoorn, C., Mosbrugger, V., Mulch, A. & Antonelli, A. Biodiversity from mountain building. Nat. Geosci. 6, 154 (2013)
Warren, B. H. et al. Islands as model systems in ecology and evolution: prospects fifty years after MacArthur–Wilson. Ecol. Lett. 18, 200–217 (2015)
Watson, D. M. A conceptual framework for studying species composition in fragments, islands and other patchy ecosystems. J. Biogeogr. 29, 823–834 (2002)
Ornelas, J. F. et al. Comparative phylogeographic analyses illustrate the complex evolutionary history of threatened cloud forests of northern Mesoamerica. PLoS ONE 8, e56283 (2013)
Madriñán, S., Cortés, A. J. & Richardson, J. E. Páramo is the world’s fastest evolving and coolest biodiversity hotspot. Front. Genet. 4, 192 (2013)
Barkman, T. J. & Simpson, B. B. Origin of high-elevation Dendrochilum species (Orchidaceae) endemic to Mount Kinabalu, Sabah, Malaysia. Syst. Bot. 26, 658–669 (2001)
Gawin, D. F. et al. Patterns of avian diversification in Borneo: the case of the endemic Mountain Black-eye (Chlorocharis emiliae). Auk 131, 86–99 (2014)
Cottam, M. A. et al. Neogene rock uplift and erosion in northern Borneo: evidence from the Kinabalu granite, Mount Kinabalu. J. Geol. Soc. Lond. 170, 805–816 (2013)
Whitehead, J. Exploration of Mount Kina Balu, North Borneo (Gurney & Jackson, London, 1893)
Wong, K. M. & Phillips, A. Kinabalu, Summit of Borneo (Sabah Society & Sabah Parks, Kota Kinabalu, 1996)
van Steenis, C. G. G. J. Plant geography of the mountain flora of Mt. Kinabalu. Proc. R. Soc. Lond. B 161, 7–38 (1964)
Kitayama, K. An altitudinal transect study of the vegetation on Mount Kinabalu, Borneo. Vegetatio 102, 149–171 (1992)
Grubb, P. J. Interpretation of Massenerhebung effect on tropical mountains. Nature 229, 44–45 (1971)
Favre, A. et al. The role of the uplift of the Qinghai–Tibetan Plateau for the evolution of Tibetan biotas. Biol. Rev. Camb. Philos. Soc. 90, 236–253 (2015)
Schwery, O. et al. As old as the mountains: the radiations of the Ericaceae. New Phytol. 207, 355–367 (2015)
Price, T. D. et al. Niche filling slows the diversification of Himalayan songbirds. Nature 509, 222–225 (2014)
Crisp, M. D. et al. Phylogenetic biome conservatism on a global scale. Nature 458, 754–756 (2009)
Culmsee, H. & Leuschner, C. Consistent patterns of elevational change in tree taxonomic and phylogenetic diversity across Malesian mountain forests. J. Biogeogr. 40, 1997–2010 (2013)
Geml, J. et al. Large-scale fungal diversity assessment in the Andean Yungas forests reveals strong community turnover among forest types along an altitudinal gradient. Mol. Ecol. 23, 2452–2472 (2014)
Posada, D. & Crandall, K. A. Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818 (1998)
Ronquist, F. & Huelsenbeck, J. P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574 (2003)
Rambaut, A. & Drummond, A. J., Tracer v1.5. http://beast.bio.ed.ac.uk/Tracer (2009)
Zwickl, D. J. Genetic Algorithm Approaches for the Phylogenetic Analysis of Large Biological Sequence Datasets under the Maximum Likelihood Criterion (The University of Texas, Austin, 2006)
Bouckaert, R. et al. BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Comput. Biol. 10, e1003537 (2014)
Matzke, N. J. Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. Front. Biogeogr. 5, 242–248 (2013)
Meade, A. & Pagel M. BayesTraits, version 2.0. http://www.evolution.rdg.ac.uk (2015)
Hall, R. et al. The Geology of Mount Kinabalu (Sabah Parks, 2008)
Acknowledgements
We acknowledge the mountain guides of Sabah Parks for their help with material collection, ongoing assistance to continuing research in the area, and recent efforts following the 5 June 2015 earthquake. R. Butôt, M. de Jong, and B. Driessen carried out DNA extractions and PCRs. P. Wilkie provided a tissue sample for Payena. For the fungi, T. Semenova extracted DNA from the soil samples and E. Duijm generated the reads on the Ion Torrent sequencer. B. Blankevoort and E. J. Bosch prepared Fig. 1. J. Holloway (Natural History Museum, London, UK), I. Das (Universiti Malaysia Sarawak), and T. S. Liew (Naturalis, UMS) provided background on Kinabalu endemism, and R. Hall (University of London) on its geological history. R. Etienne (University of Groningen), R. Hall (University of London) and F. Bossuyt (Free University Brussels) read a draft of the paper. Collection and export permits were supplied by the Sabah Biodiversity Centre. Besides institutional support via Netherlands FES-funding, this project received funding via grants 821.01.002 and 825.12.007 of the Netherlands Organization for Scientific Research, the Alberta Mennega Foundation, the Ecology Fund of the Royal Netherlands Academy of Sciences, the Uyttenboogaart-Eliasen Foundation, and Pro Acarologia Basiliensis. G. van Uffelen, R. van Vugt, and P. Kessler (Botanic Gardens, Leiden) and T. de Winter, G. Thijsse, B. Hoeksema, H. Dautzenberg, J. Mols, and E. van Nieukerken (Naturalis) gave advice on transportation of specimens. Artist I. Kopelman and Naturalis general director E. van Huis (Naturalis) accompanied the expedition participants in the field. J. Gunsalam and P. Jilan (Sabah Parks Board of Trustees) officiated the opening and closing ceremony, respectively. P. Basintal, E. van Huis and E. Smets supervised the expedition as directors for the organizing institutions. Media coverage and communications were facilitated by J. van Alphen, A. Mohd. R. P. Dahlan, K. de Greef, A. Kromhout, J. Schilthuizen, E. E. Soudi, L. Stek, A. Taminiau, and M. Z. Abdul Wahab. Sabah Parks staff members L. Apin, B. Busin, B. Butit, J. Gampoyo, G. Gangko, B. Gangku, S. Gangku, P. Gimpiton, M. Gunggutou, T. Gunggutou, G. Gunsalam, J. Guntabid, I. Isnain, K. Ag. Jalil, Y. Johalin, R. M. Karim, Y. Kumin, D. Laban, A. Lahi, J. Lapidin, M. Latim, N. Maidin, N. Majuakim, R. Miadin, Y. Miki, M. Moguring, H. Mujih, F. Simin, K. C. Sion, D. Sumbin, D. Tingoh, E. Yakin, were invaluable for all manner of logistics and other support before, during, and after the expedition, in the field and at the stations and administrative offices. For the Forest Research Centre researchers, J. B. Dawat, M. Gumbilil, A. J. Jaimin, Jei. Jumian, Jem. Jumian, J. L. Yukang, P. J. Miun, M. A. T. Mustapha, and B. Saludin assisted in the field. T. Siew of Borneo Indah Sdn. Bhd. was the local supplier for consumables and field equipment. We thank the ESEB Outreach Fund and the Treub Foundation for funding outreach activities in Kinabalu Park and the Crocker Range Park. N. Raes helped with the niche modelling.
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M. Sch., V.S.F.T.M., M.Sp., M.M.B., C.B.M., L.E.B., K.T.C.A.P., J.N., R.R., and M.L. conceived and guided the study. M.Sch. and V.S.F.T.M. wrote the paper. K.H., F.S. and K.B. administrated all samples and sequences. K.H. and L.E.B. were responsible for DNA sampling in the field. V.S.F.T.M., A.A., N.A., A.B., P.-P.C., A.Y.C.C., R.D., H.F., C.F.-v.S., J.G., R.G., P.H., P.I., I.I., M.J., H.K., E.K., P.K., F.L., R.J.M., L.N.M., N.N., J.T.P., H.R., S.S., A.S., R.M.S., P.-S.S., H.S., N.S., J.B.S., M.Sul., S.Sum., J.v.T., F.Y.Y.T., B.E.Y., C.B.M., R.R. and M.Sch. collected material in the field and identified it following current taxonomy. K.H., V.S.F.T.M., H.d.B., F.A.A.F., J.G., B.G., P.H., S.B.J., S.N., M.St., D.C.T. and M.Sch. conducted the analyses.
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Extended data figures and tables
Extended Data Figure 1 Phylogenetic reconstructions for Anura, Araneae, Athyriaceae, Balsaminaceae and Begoniaceae.
Details of materials and methods used are given in Supplementary Table 2.
Extended Data Figure 2 Phylogenetic reconstructions for Coleoptera, Dicranaceae, Diptera and Cortinariaceae.
Details of materials and methods used are given in Supplementary Table 2.
Extended Data Figure 3 Phylogenetic reconstructions for Ericaceae, Gastropoda, Glomeraceae, Hemiptera and Hirudinea.
Details of materials and methods used are given in Supplementary Table 2.
Extended Data Figure 4 Phylogenetic reconstructions for Nepenthaceae, Odonata, Polygalaceae, Rubiaceae and Trombidiformes.
Details of materials and methods used are given in Supplementary Table 2.
Extended Data Figure 5 Chronograms for Athyrium, Begonia, Coeliccia, Dacrycarpus, Epirixanthes, Dendrochilum, Dicranoloma, Impatiens, Hygrobates, Hedyotis, Ilex and Myrmarachne.
See Supplementary Table 5 for more details. Node colours represent posterior probabilities. Endemic species printed in red.
Extended Data Figure 6 Chronograms for Euphrasia, Kalophrynus, Nepenthes, Paphiopedilum, Philalanka, Ptomaphaginus, Payena, Trichosanthes, Rhododendron, Ranunculus, Tritetrabdella and Weinmannia.
See Supplementary Table 5 for more details. Node colours represent posterior probabilities. Endemic species printed in red.
Extended Data Figure 7 Ancestral range estimations for Athyrium, Begonia, Coeliccia, Dacrycarpus, Dendrochilum, Dicranoloma, Epirixanthes, Euphrasia and Hedyotis.
See Methods for further details. The trees are alphabetically ordered by genus name.
Extended Data Figure 8 Ancestral range estimations for Hygrobates, Ilex, Impatiens, Kalophrynus, Myrmarachne, Nepenthes, Paphiopedilum, Payena and Philalanka.
See Methods for further details. The trees are alphabetically ordered by genus name.
Extended Data Figure 9 Ancestral range estimations for Ptomaphaginus, Ranunculus, Rhododendron, Teleopsis, Trichosanthes, Tritetrabdella and Weinmannia.
See Methods for further details. The trees are alphabetically ordered by genus name.
Supplementary information
Supplementary Tables
This file contains Supplementary Tables 1, 3, 4, 6 and 7 (see separate files for Supplementary Tables 2 and 5). (PDF 3236 kb)
Supplementary Tables
This file contains Supplementary Table 2. (PDF 591 kb)
Supplementary Tables
This file contains supplementary Table 5. (XLSX 57 kb)
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Merckx, V., Hendriks, K., Beentjes, K. et al. Evolution of endemism on a young tropical mountain. Nature 524, 347–350 (2015). https://doi.org/10.1038/nature14949
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DOI: https://doi.org/10.1038/nature14949
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