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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Accessions

Data deposits

GenBank accession numbers for newly determined sequences are: KF369344, KF492848, KF839944KF839949, KM378672KM378719, KM489525KM489544, KM982697KM982715, KP152323KP152394, KP978313KP979097, KR002164KR002181, KR030167KR030238 and KR232819KR232836. 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 Voucher specimens have been archived in public natural history collections.

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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.

Author information

Author notes

    • Phyau-Soon Shim

    Deceased.

Affiliations

  1. Naturalis Biodiversity Center, Darwinweg 2, 2333 CR Leiden, The Netherlands

    • Vincent S. F. T. Merckx
    • , Kasper P. Hendriks
    • , Kevin K. Beentjes
    • , Constantijn B. Mennes
    • , Leontine E. Becking
    • , Katja T. C. A. Peijnenburg
    • , Hugo de Boer
    • , Ping-Ping Chen
    • , Rory Dow
    • , Frida A. A. Feijen
    • , Hans Feijen
    • , Cobi Feijen-van Soest
    • , József Geml
    • , Barbara Gravendeel
    • , Peter Hovenkamp
    • , Heike Kappes
    • , Frederic Lens
    • , Luis N. Morgado
    • , Nico Nieser
    • , Rachel M. Schwallier
    • , Harry Smit
    • , Nicolien Sol
    • , Michael Stech
    • , Frank Stokvis
    • , Daniel C. Thomas
    • , Jan van Tol
    •  & Menno Schilthuizen
  2. Institute of Biology Leiden, Leiden University, Sylviusweg 72, 2333 BE Leiden, The Netherlands

    • Vincent S. F. T. Merckx
    • , József Geml
    • , Barbara Gravendeel
    • , Frederic Lens
    •  & Menno Schilthuizen
  3. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborg 7, 9747 AG Groningen, The Netherlands

    • Kasper P. Hendriks
  4. Wageningen University & Research centre, Marine Animal Ecology Group, PO Box 338, 6700 AH Wageningen, The Netherlands

    • Leontine E. Becking
  5. Department of Environmental Science, Policy, & Management, University of California Berkeley, 130 Mulford Hall #3114, Berkeley, California 94720, USA

    • Leontine E. Becking
  6. Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands

    • Katja T. C. A. Peijnenburg
  7. Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Sabah, Malaysia

    • Aqilah Afendy
    • , Nivaarani Arumugam
    • , Homathevi Rahman
    • , Anati Sawang
    • , Monica Suleiman
    • , Bakhtiar E. Yahya
    •  & Menno Schilthuizen
  8. Faculty of Earth Science, Universiti Malaysia Kelantan, Jeli Campus, Locked bag No.100, 17600 Jeli, Kelantan Darul Naim, Malaysia

    • Nivaarani Arumugam
  9. Department of Organismal Biology, Uppsala University, Norbyvägen 18D, 75236 Uppsala, Sweden

    • Hugo de Boer
  10. Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway

    • Hugo de Boer
  11. Sabah Parks, Lot 45 & 46, Level 1-5, Blok H, KK Times Square, 88806 Kota Kinabalu, Sabah, Malaysia

    • Alim Biun
    • , Matsain M. Buang
    • , Paul Imbun
    • , Phyau-Soon Shim
    • , Maipul Spait
    • , Sukaibin Sumail
    • , Fred Y. Y. Tuh
    • , Jamili Nais
    • , Rimi Repin
    •  & Maklarin Lakim
  12. Forest Research Centre, Sabah Forestry Department, P.O. Box 1407, 90175 Sandakan, Sabah, Malaysia

    • Arthur Y. C. Chung
    • , Eyen Khoo
    • , Richard J. Majapun
    • , Joan T. Pereira
    • , Suzana Sabran
    •  & John B. Sugau
  13. Wageningen University, Department of Plant Sciences, Laboratory of Molecular Biology, 6700AP Wageningen, The Netherlands

    • René Geurts
  14. University of Applied Sciences Leiden, Zernikedreef 11, 2333 CK Leiden, The Netherlands

    • Barbara Gravendeel
  15. Faculty of Resource Science and Technology, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia

    • Isa Ipor
  16. Botanic Garden Meise, Nieuwelaan 38, 1860 Meise, Belgium

    • Steven B. Janssens
  17. Royal Belgian Institute of Natural Sciences, Aquatic and Terrestrial Ecology, Vautierstraat 29, 1000 Brussels, Belgium

    • Merlijn Jocqué
  18. Rutgers, The State University of New Jersey, Department of Biological Sciences, 195 University Avenue, Boyden Hall, Newark, New Jersey 07102, USA

    • Merlijn Jocqué
  19. Zoological Institute, University of Cologne, Zülpicher Strasse 47b, D-50674 Cologne, Germany

    • Heike Kappes
  20. Natuurmuseum Fryslân, Schoenmakersperk 2, 8911 EM Leeuwarden, The Netherlands

    • Peter Koomen
  21. EEB Department, University of Connecticut, 75 N. Eagleville Road, Storrs, Connecticut 06269-3043, USA

    • Suman Neupane
  22. School of Biological Sciences, University of Hong Kong, Pok Fu Lam Road, Hong Kong, China

    • Daniel C. Thomas
  23. Singapore Botanic Gardens, 1 Cluny Road, 259569 Singapore, Republic of Singapore

    • Daniel C. Thomas

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Contributions

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.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Menno Schilthuizen.

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DOI

https://doi.org/10.1038/nature14949

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