Evolution of endemism on a young tropical mountain

Journal name:
Nature
Volume:
524,
Pages:
347–350
Date published:
DOI:
doi:10.1038/nature14949
Received
Accepted
Published online

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.

At a glance

Figures

  1. Map of the study area.
    Figure 1: Map of the study area.

    Inset left, location of the study area in the World and in Borneo. Inset middle, detail of the summit trail in Kinabalu Park. The eight expedition stations in Kinabalu Park and Crocker Range Park are indicated with red markers, ten additional sampling sites with blue markers. Not indicated separately are 15 sites along the summit trail, and four sites very close to Mahua, Gunung Alab, and Inobong.

  2. Examples of phylogenetic reconstructions.
    Figure 2: Examples of phylogenetic reconstructions.

    a, Centric endemism (Ptomaphaginus). b, Eccentric endemism (Impatiens). c, Centric endemism superimposed on eccentric endemism (detail of the Cortinarius phylogeny). Clades are coloured with the same colour scheme as in Fig. 1, by elevational zone at which they occur (see legend). High-elevation endemics in a and b are indicated in red. For support values and other details on these and other trees, see Extended Data Figs 1, 2, 3, 4.

  3. Elevations and ages for endemic species.
    Figure 3: Elevations and ages for endemic species.

    Elevations (mid-points, minima and maxima) and dates of origination derived from molecular dating (averages and 95% credible intervals) for endemic species; eccentric species (see main text) are indicated with a black circle. The vertical dashed line indicates the oldest possible date for Kinabalu to have reached its current elevation. For details, see Extended Data Figs 5 and 6.

  4. Phylogenetic reconstructions for Anura, Araneae, Athyriaceae, Balsaminaceae and Begoniaceae.
    Extended Data Fig. 1: Phylogenetic reconstructions for Anura, Araneae, Athyriaceae, Balsaminaceae and Begoniaceae.

    Details of materials and methods used are given in Supplementary Table 2.

  5. Phylogenetic reconstructions for Coleoptera, Dicranaceae, Diptera and Cortinariaceae.
    Extended Data Fig. 2: Phylogenetic reconstructions for Coleoptera, Dicranaceae, Diptera and Cortinariaceae.

    Details of materials and methods used are given in Supplementary Table 2.

  6. Phylogenetic reconstructions for Ericaceae, Gastropoda, Glomeraceae, Hemiptera and Hirudinea.
    Extended Data Fig. 3: Phylogenetic reconstructions for Ericaceae, Gastropoda, Glomeraceae, Hemiptera and Hirudinea.

    Details of materials and methods used are given in Supplementary Table 2.

  7. Phylogenetic reconstructions for Nepenthaceae, Odonata, Polygalaceae, Rubiaceae and Trombidiformes.
    Extended Data Fig. 4: Phylogenetic reconstructions for Nepenthaceae, Odonata, Polygalaceae, Rubiaceae and Trombidiformes.

    Details of materials and methods used are given in Supplementary Table 2.

  8. Chronograms for Athyrium, Begonia, Coeliccia, Dacrycarpus, Epirixanthes, Dendrochilum, Dicranoloma, Impatiens, Hygrobates, Hedyotis, Ilex and Myrmarachne.
    Extended Data Fig. 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.

  9. Chronograms for Euphrasia, Kalophrynus, Nepenthes, Paphiopedilum, Philalanka, Ptomaphaginus, Payena, Trichosanthes, Rhododendron, Ranunculus, Tritetrabdella and Weinmannia.
    Extended Data Fig. 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.

  10. Ancestral range estimations for Athyrium, Begonia, Coeliccia, Dacrycarpus, Dendrochilum, Dicranoloma, Epirixanthes, Euphrasia and Hedyotis.
    Extended Data Fig. 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.

  11. Ancestral range estimations for Hygrobates, Ilex, Impatiens, Kalophrynus, Myrmarachne, Nepenthes, Paphiopedilum, Payena and Philalanka.
    Extended Data Fig. 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.

  12. Ancestral range estimations for Ptomaphaginus, Ranunculus, Rhododendron, Teleopsis, Trichosanthes, Tritetrabdella and Weinmannia.
    Extended Data Fig. 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.

Tables

  1. Details for all studied endemic taxa
    Extended Data Table 1: Details for all studied endemic taxa

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Author information

  1. Deceased.

    • Phyau-Soon Shim

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

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 financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

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.

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Phylogenetic reconstructions for Anura, Araneae, Athyriaceae, Balsaminaceae and Begoniaceae. (262 KB)

    Details of materials and methods used are given in Supplementary Table 2.

  2. Extended Data Figure 2: Phylogenetic reconstructions for Coleoptera, Dicranaceae, Diptera and Cortinariaceae. (324 KB)

    Details of materials and methods used are given in Supplementary Table 2.

  3. Extended Data Figure 3: Phylogenetic reconstructions for Ericaceae, Gastropoda, Glomeraceae, Hemiptera and Hirudinea. (212 KB)

    Details of materials and methods used are given in Supplementary Table 2.

  4. Extended Data Figure 4: Phylogenetic reconstructions for Nepenthaceae, Odonata, Polygalaceae, Rubiaceae and Trombidiformes. (191 KB)

    Details of materials and methods used are given in Supplementary Table 2.

  5. Extended Data Figure 5: Chronograms for Athyrium, Begonia, Coeliccia, Dacrycarpus, Epirixanthes, Dendrochilum, Dicranoloma, Impatiens, Hygrobates, Hedyotis, Ilex and Myrmarachne. (496 KB)

    See Supplementary Table 5 for more details. Node colours represent posterior probabilities. Endemic species printed in red.

  6. Extended Data Figure 6: Chronograms for Euphrasia, Kalophrynus, Nepenthes, Paphiopedilum, Philalanka, Ptomaphaginus, Payena, Trichosanthes, Rhododendron, Ranunculus, Tritetrabdella and Weinmannia. (479 KB)

    See Supplementary Table 5 for more details. Node colours represent posterior probabilities. Endemic species printed in red.

  7. Extended Data Figure 7: Ancestral range estimations for Athyrium, Begonia, Coeliccia, Dacrycarpus, Dendrochilum, Dicranoloma, Epirixanthes, Euphrasia and Hedyotis. (281 KB)

    See Methods for further details. The trees are alphabetically ordered by genus name.

  8. Extended Data Figure 8: Ancestral range estimations for Hygrobates, Ilex, Impatiens, Kalophrynus, Myrmarachne, Nepenthes, Paphiopedilum, Payena and Philalanka. (268 KB)

    See Methods for further details. The trees are alphabetically ordered by genus name.

  9. Extended Data Figure 9: Ancestral range estimations for Ptomaphaginus, Ranunculus, Rhododendron, Teleopsis, Trichosanthes, Tritetrabdella and Weinmannia. (244 KB)

    See Methods for further details. The trees are alphabetically ordered by genus name.

Extended Data Tables

  1. Extended Data Table 1: Details for all studied endemic taxa (1,086 KB)

Supplementary information

PDF files

  1. Supplementary Tables (3.1 MB)

    This file contains Supplementary Tables 1, 3, 4, 6 and 7 (see separate files for Supplementary Tables 2 and 5).

  2. Supplementary Tables (591 KB)

    This file contains Supplementary Table 2.

Excel files

  1. Supplementary Tables (57 KB)

    This file contains supplementary Table 5.

Additional data