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Evolution of endemism on a young tropical mountain

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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Figure 1: Map of the study area.
Figure 2: Examples of phylogenetic reconstructions.
Figure 3: Elevations and ages for endemic species.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

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 Voucher specimens have been archived in public natural history collections.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

Affiliations

Authors

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.

Corresponding author

Correspondence to Menno Schilthuizen.

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Competing interests

The authors declare no competing financial interests.

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.

Extended Data Table 1 Details for all studied endemic taxa

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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