Cover Page. The handle holds various files of this Leiden University dissertation

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1 Cover Page The handle holds various files of this Leiden University dissertation Author: Schwallier, Rachel Marie Title: Evolutionary diversification of Nepenthes (Nepenthaceae) Issue Date:

2 Chapter Two 27

3 Modified from NATURE (25) 524: Evolution of endemism on a young tropical mountain Vincent S. F. T. Merckx, asper P. Hendriks, evin. eentjes, Constantijn. Mennes, Leontine E. ecking, atja T. C. A. Peijnenburg, Aqilah Afendy, Nivaarani Arumugam, Hugo de oer, Alim iun, Matsain M. uang, Ping-Ping Chen, Arthur Y. C. Chung, Rory Dow, Frida A. A. Feijen, Hans Feijen, Cobi Feijen-van Soest, Jo zsef Geml, René Geurts, arbara Gravendeel, Peter Hovenkamp, Paul Imbun, Isa Ipor, Steven. Janssens, Merlijn Jocqué, Heike appes, Eyen hoo, Peter oomen, Frederic Lens, Richard J. Majapun, Luis N. Morgado, Suman Neupane, Nico Nieser, Joan T. Pereira, Homathevi Rahman, Suzana Sabran, Anati Sawang, Rachel M. Schwallier, Phyau-Soon Shim, Harry Smit, Nicolien Sol, Maipul Spait, Michael Stech, Frank Stokvis, John. Sugau, Monica Suleiman, Sukaibin Sumail, Daniel C. Thomas, Jan van Tol, Fred Y. Y. Tuh, akhtiar E. Yahya, Jamili Nais, Rimi Repin, Maklarin Lakim & Menno Schilthuizen Tropical mountains are hotspots of biodiversity and endemism, but the evolutionary origin of their unique biotas are poorly understood. Mountains may either act as museums where older lineages persist through evolutionary time, or as cradles where new species continue to be generated. e traced the evolutionary origins of endemism in 28 genera of plants, animals, and fungi on Mount inabalu (Malaysian orneo), one of the richest biodiversity hotspots on earth. e demonstrate that most of its unique biota is younger than the mountain itself and evolved from a mixture of immigrant and local lowland ancestors. According to the molecular clock analyses, Nepenthes show centric endemism. Speciation of the four Nepenthes species endemic to Mount inabalu, N. edwardsiana, N. rajah, N. villosa and N. x kinabaluensis, appears to coincide with the timing of mountain formation. eywords: Nepenthes systematics, tropical ecology. Tropical mountains are hot spots of biodiversity and endemism (orner & Spehn, 22; Chen et al., 29; Graham et al., 24), but the evolutionary origins of their unique biotas are poorly understood (Graham et al., 24). In varying degrees, local and regional extinction, long-distance colonization, and local recruitment may all contribute to the exceptional character of these communities (Cadena et al., 2). 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 elsewhere (Rodriguez-Castaneda et al., 2). Here we investigate the evolutionary routes to endemism by sampling an entire tropical mountain biota on the 4,95-metre-high Mount inabalu in Sabah, East Malaysia. e discover that most of its unique biodiversity is younger than the mountain itself (6 28

4 Chapter Two 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 (Schiffers et al., 23) in montane biodiversity hot spots under climate change scenariosin mountainous areas of the humid tropics, steep environmental gradients coincide with high primary productivity and relative climatic stability to sustain large numbers of species, often with striking degrees of endemism at higher elevations (orner & Spehn, 22; Hoorn et al., 23). It has therefore been recognized that tropical mountains are biodiversity hot spots of great conservation value (orner & Spehn, 22), especially because endemics on mountain tops are vulnerable to becoming trapped and then annihilated as a result of global warming (Chen et al., 29; La Sorte & Jetz, 2). The evolutionary origins of these unique biotas, however, are poorly understood (Graham et al., 24). Like other insular habitats (arren et al., 25), the endemic biota of an isolated mountain results from complex dynamics among colonization, in situ speciation, and local extinction. Each of these factors is dependent on the age and size of the habitat, and on the environmental contrast between the insular habitat and its matrix (atson, 22). In the case of a tropical mountain top, an added complication is the fact that climate fluctuations may have widened and restricted the geographic range over which the montane conditions have extended in the past, meaning that parts of the endemic biota may be relicts, and other components may be novel in character (Cadena et al., 2; Graham et al., 24). Disentangling these possibilities for a single tropical montane biodiversity hot spot requires molecular phylogenetic study of a large number of fauna and flora elements. However, with only few exceptions (Madriñán et al., 23; Ornelas et al., 23), evolutionary studies in such hot spots have been limited to single taxa (arkman & Simpson, 2; Gawin et al., 24). This precludes broad understanding of the evolutionary and biogeographic origins of an endemic biota as a whole (Graham et al., 24). e investigated the evolutionary routes to endemism by sampling an entire tropical mountain biota on the UNESCO orld Heritage site of Gunung inabalu in Sabah, East Malaysia. Included in this are the iconic carnivorous plant genera Nepenthes (Table 3 & Figure 6). e demonstrate that most of its unique biodiversity is younger than the mountain itself and comprises a mix of immigrant pre-adapted lineages as well as descendants from local lowland ancestors. 29

5 Evolution of Endemism TALE 3. Nepenthes collected from the inabalu Park and Crocker Range Park expedition stations and their distribution. Species Nepenthes chaniana Nepenthes edwardsiana Nepenthes fusca Nepenthes gracilis Nepenthes lowii Nepenthes mirabilis Nepenthes rajah Nepenthes tetaculata Nepenthes villosa Nepenthes x kinabaluensis Distribution orneo Endemic to Mount inabalu & neighboring Mount Tambyukon orneo ide distribution across SE Asia orneo ide distribution across SE Asia Endemic to Mount inabalu & neighboring Mount Tambyukon ide distribution across orneo & Sulawesi Endemic to Mount inabalu & neighboring Mount Tambyukon Endemic to Mount inabalu & neighboring Mount Tambyukon FIGURE 6. Nepenthes endemic to Mount inabalu & neighboring Mount Tambyukon. From left to right, N. edwardsiana, N. rajah, N. villosa, N. x kinabaluensis. Photos courtesy of Rogier van Vugt. At 4,95 m, inabalu is the tallest mountain between the Himalayas and New Guinea. It is a solitary sky island, having emerged during the Pliocene and early Pleistocene as a granite pluton within the surrounding sandstone of the Crocker Range, the latter having formed much earlier, between the Eocene and the early Miocene (Cottam et al., 23). ecause of the area s tectonic activity, as well as Pleistocene sea level changes, the exact historical progression of its elevation above sea level is not known, but it is likely that a major rise, even beyond today s elevation, of inabalu, as well as the central spine of the Crocker Range, took place between 6 million years ago and today (for more geological background see Methods). Since the early days of its exploration (hitehead, 893), inabalu has been famous for its extremely high biological diversity, especially its richness in endemic species, with endemism proportions reaching 25 3% for some taxa (ong, 996). 3

6 Chapter Two To unravel the origins of the exceptionally rich inabalu biota, we mounted a Malaysian Dutch expedition in which 47 taxonomists worked at 37 localities, spanning the full range of elevations (Fig. 7). e used Sanger sequencing to sequence one or more fast-evolving loci for,852 individuals, belonging to 8 genera representing gastropods, annelids, insects, arachnids, vertebrates, pteridophytes, bryophytes, and angiosperms. e also obtained 3.7 million basidiomycete and glomeromycete ITS2 rdna sequences from soil cores with ion semiconductor sequencing. In addition, we retrieved data from eight previously published single-taxon studies on vascular plants. FIGURE 7. Map of the study area. Inset left, location of the study area in the orld and in orneo. Inset middle, detail of the summit trail in inabalu Park. The eight expedition stations in inabalu Park and Crocker Range Park are indicated with red markers, ten additional sampling sites with blue markers. Not indicated separately are 5 sites along the summit trail, and four sites very close to Mahua, Gunung Alab, and Inobong. e analyzed all data within a phylogenetic framework to estimate the times of origin of endemic species, and to determine whether endemic species had descended from local or distant congeners (Methods, see web based publication online Fig. 2, Figs 8-). Note that we define endemic as restricted to the area in which our expedition took place. Although the present study offers the most comprehensive evolutionary analysis of any mountain biota to date, the taxa covered are, by necessity, an uneven and fragmentary sampling of the full diversity. Nonetheless, we expect that our results are representative for the inabalu biota as a whole, as our selected taxa encompass organisms with a wide variety of phylogenetic backgrounds, ecologies, and life history traits. Similar to Mesoamerican endemic cloud forest seed plants and vertebrates (Ornelas et al., 23), our molecular dating results show that the estimated mean stem-node ages of 33 endemic species span a wide range, from.2 million years to 4.6 million years (Figs. 8,9 and web-based publication Extended data Figs. 7-9). However, 76% of these fall within the past 6 million 3

7 Evolution of Endemism years, the time span during which inabalu is likely to have reached its present elevation. Only two endemics, the frog alophrynus baluensis and the flowering plant Ilex kinabaluensis, are markedly older than the mountain itself. These may be explained as artefactual if we failed to identify the closest non-endemic sister lineage, thereby inflating their reconstructed age, or if these species are actually not endemics, but more widespread. Alternatively, they may truly be old endemics that evolved during cooler periods at lower elevations in orneo before inabalu s formation. Our phylogenetic and biogeographic analyzes (Extended Data Online Table and Figs 4, 7 9) suggest the existence of two categories of endemics (van Steenis, 964): eccentric (2 taxa) and centric (25 taxa). The eccentric type of endemic has sister taxa that occur either in temperate climates (seven cases) or in other tropical mountains outside of orneo (five cases). To this group belong all bryophytes, pteridophytes, some of the fungal lineages and also the endemics in the flowering plant groups Hedyotis, Ilex, Impatiens, Ranunculus and Euphrasia, and the animals Coeliccia and Tritetrabdella. Eccentric endemics predominantly occur at high elevations (mean lower elevational boundary, 2,22 m; s.d., 837 m), they are strict inabalu endemics (they do not occur on nearby, lower mountains), and are further characterized by high dispersal capacities (one, two and seven clades with eccentric endemism have small, medium and large dispersal, respectively). elevation (m) 4, 4! 3,5 35! 3, 3! 2,5 25! 2, 2!,5 5! frogs insects arachnids snails leeches conifers ferns mosses flowering plants,! 5!!! 5!! 5! 2! 25! 3! divergence time (My) FIGURE 8. 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 inabalu to have reached its current elevation. For details, see Extended Data Online Figs 5 and 6. 32

8 Chapter Two iogeoears DEC+J on Nepenthes M_unconstrained ancstates: global optim, 3 areas max. d=.74; e=; j=.56; LnL= Nepenthes_northiana Nepenthes_x_kinabaluensis Nepenthes_rajah Nepenthes_lowii Nepenthes_chaniana Nepenthes_glandulifera Nepenthes_maxima Nepenthes_boschiana Nepenthes_vogelii Nepenthes_fusca Nepenthes_hurrelliana Nepenthes_villosa Nepenthes_edwardsiana2 Nepenthes_peltata Nepenthes_truncata Nepenthes_campanulata Nepenthes_alata Nepenthes_ventricosa Nepenthes_gymnamphora Nepenthes_bongso Nepenthes_insignis Nepenthes_specatabilis Nepenthes_reinwardtiana Nepenthes_benstonei Nepenthes_macfarlanei Nepenthes_singalana Nepenthes_kongkandana Nepenthes_andamana Nepenthes_vieillardii Nepenthes_bokorensis Nepenthes_albomarginata Nepenthes_ramispina Nepenthes_alba Nepenthes_sanguinea Nepenthes_gracillima Millions of years ago FIGURE 9. Ancestral range estimations for Nepenthes. 33

9 Evolution of Endemism The centric type of endemic has sister taxa that occur locally, in the orneo lowlands. Six out of the eight endemic animal species, some of the fungal lineages, the conifers, and 7 of the 2 flowering plants belong to this type. Centric endemics occur on average at lower elevations (mean lower elevational boundary,,724 m; s.d., 728 m) and tend to have lower dispersal capacities than the eccentric endemics (eight, seven and ten clades with centric endemism have small, medium and large dispersal, respectively). Some centric endemics, including Nepenthes, are not strict inabalu endemics, as they are also found on other mountains in inabalu s vicinity. Our ancestral state reconstructions (Supplementary Table 6 online) confirm a pattern of altitudinal bottom-up cladogenesis in the centric endemics, with 8 out of species ranging partially or entirely outside of the 95% credibility interval for the reconstructed elevation of the most recent common ancestor, and the remaining 3 out of falling entirely within this interval. hen we performed the same analysis with itayama s (992) seven vegetation zones, rather than elevation, we found that only three of these eight elevation shifts may represent a shift towards a higher vegetation zone. This suggests that, even in highelevation centric endemics, substantial niche shifts are rare. Niche conservatism is probably even underestimated, since the Massenerhebung effect causes an Nepenthaceae - Nepenthes L N. chaniana L N. chaniana L N. tentaculata L N. lowii.99 L N. lowii L N. lowii L N. lowii L N. fusca L N. fusca L N. fusca L N. fusca L.4499 N. tentaculata L.4492 N. tentaculata L.4495 N. tentaculata L.449 N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L.449 N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L N. tentaculata L.4494 N. mirabilis L.4493 N. mirabilis L.4492 N. mirabilis L.4498 N. mirabilis L N. mirabilis L N. mirabilis L N. mirabilis L N. mirabilis L N. mirabilis L N. gracilis L N. gracilis L.4499 N. gracilis.99 L N. mirabilis L N. mirabilis L N. gracilis L N. gracilis.99 L.4498 N. gracilis L.4499 N. gracilis L N. gracilis L N. gracilis L N. x hookeriana L N. ampullaria L N. ampullaria L N. ampullaria L N. ampullaria L.4496 N. edwardsiana L N. x kinabaluensis L N. x harryana L N. villosa L N. villosa.99 L N. x kinabaluensis L N.villosa L N. x kinabaluensis L N. villosa SNP34297 N. rajah L.4497 N. villosa L.4497 N. edwardsiana.98 L N. edwardsiana L N. edwardsiana AF35885 N. pervillei (Seychelles) FIGURE. Phylogenetic reconstructions for Nepenthaceae. 34

10 53,5 32,43 28,48 29,56 Microhyla_heymonsi Glyphoglossus_molossus Paradoxophyla_palmata Scaphiophryne_calcarata 2,4 47,98 Otophryne_pyburni 2,4 46,69 Nepenthes (ITS) Nepenthes (ITS) 36,2 36,2 53,45 53,45 Nepenthes (mat) Nepenthes (mat) 32, 32, Anodonthyla_boulengerii 24,2 Anodonthyla_montana 29,63 Platypelis_grandis,98 Chapter Two 27,7 Plethodontohyla_brevipes,7,98 24,54 Rhombophryne_alluaudi 6,95,99 Rhombophryne_testudo,7 2,6 Stumpffia_psologlossa 4,32,99 Stumpffia_pygmaea,6,6,5 Drosophyllum_lusitanicum,66,5 Ancistrocladus_tectorius 27, Triphyophyllum_peltatum Drosophyllum_lusitanicum 4,3,66 Dioncophyllum_thollonii Ancistrocladus_tectorius 27, Nepenthes_ampullaria Triphyophyllum_peltatum 4,3 Nepenthes_rafflesiana 7,9 Dioncophyllum_thollonii 2,93 Payena Nepenthes_hemsleyana Nepenthes_ampullaria 8,84 Nepenthes_gracilis2 Nepenthes_rafflesiana 7,9 5,7 2,93 Payena Nepenthes_mirabilis Nepenthes_hemsleyana 8,84,48 Nepenthes_kamotiana Nepenthes_gracilis2 5,7 Nepenthes_tentaculata Nepenthes_mirabilis 38,68,48 Nepenthes_northiana Nepenthes_kamotiana 36,47 Nepenthes_villosa Nepenthes_tentaculata 75,68 38,68 Nepenthes_villosa3 Nepenthes_northiana 48,4 36,47 5,47 27,6,36 3 Nepenthes_villosa2 75,68 3,7 Nepenthes_edwardsiana3 Nepenthes_villosa3 48,4 5,47 27,6,34,36 Nepenthes_edwardsiana2 Nepenthes_villosa2 68,99 4,95 4,6 3,7 Nepenthes_x_kinabaluensis Nepenthes_edwardsiana3 24,97,34 5,58 Nepenthes_rajah2 Nepenthes_edwardsiana2 68,99 4,9539,4 4,6,55 Nepenthes_rajah Nepenthes_x_kinabaluensis 24,97 3 5,58,84 Nepenthes_lowii Nepenthes_rajah2 39,4,55 4,23 Nepenthes_glandulifera Nepenthes_rajah 34,27,84,84 Nepenthes_chaniana Nepenthes_lowii 7,56 4,23 Nepenthes_maxima Nepenthes_glandulifera 34,27,84 22,6 5,5 Nepenthes_boschiana Nepenthes_chaniana 53,33 7,56 3,79 Nepenthes_hurrelliana Nepenthes_maxima 22,6 5,5 2,7 Nepenthes_fusca Nepenthes_boschiana 53,33 3,79,24 Nepenthes_vogelii Nepenthes_hurrelliana 2,7 Nepenthes_fusca,24 Nepenthes_campanulata 3,52 Nepenthes_vogelii Nepenthes_truncata 4,23 Nepenthes_campanulata Nepenthes_peltata 3,52 Nepenthes_truncata Nepenthes_ventricosa 9,97 4,23 9,5 Nepenthes_peltata Nepenthes_alata 35,28 Nepenthes_ventricosa 9,97 9,5 Nepenthes_specatabilis 8,29 5,93 Nepenthes_alata 35,28 Nepenthes_gymnamphora 3,34 Nepenthes_specatabilis 47,79 3 Nepenthes_insignis 8,29 5,93,63 Nepenthes_gymnamphora 5,89 Nepenthes_bongso 3,34 47,79 Nepenthes_insignis,63Nepenthes_reinwardtiana Nepenthes_bongso 4,8 5,89 Nepenthes_benstonei,5 Nepenthes_reinwardtiana Nepenthes_macfarlanei 4,8 Nepenthes_benstonei,5 3,22 Nepenthes_singalana 8,4 Nepenthes_macfarlanei 3,22 Nepenthes_kongkandana 3,22 2,73 Nepenthes_singalana 8,4 Nepenthes_vieillardii 35,84 3,22 2,52 Nepenthes_kongkandana 6,36 2,73 Nepenthes_andamana Nepenthes_vieillardii 35,84 2,52 Nepenthes_gracillima 6,36 2,4 Nepenthes_andamana Nepenthes_sanguinea Nepenthes_gracillima 3,292,4 Nepenthes_alba,29Nepenthes_sanguinea Nepenthes_ramispina 3,29 2,28 Nepenthes_alba,29 Nepenthes_albomarginata,27Nepenthes_ramispina 2,28 Nepenthes_bokorensis Nepenthes_albomarginata,27 34,47 Nepenthes_bokorensis 34,47 Drosophyllum_lusitanicum 38, Ancistrocladus_abbreviatus 24,32 Habropetalum_dawei,37 Triphyophyllum_peltatum 5,27 Dioncophyllum_thollonii Nepenthes_macrovulgaris 5,6 Nepenthes_bicalcarata Nepenthes_bellii,8 53,3 Nepenthes_merrilliana 7,87 Nepenthes_insignis 4,8 Nepenthes_sibuyanensis 3,64 Nepenthes_ventricosa,63 Nepenthes_burkei 5,85 Nepenthes_murudensis 3,2 Nepenthes_muluensis 7,38 3,88 Nepenthes_glabrata 4,44 Nepenthes_hamata Nepenthes_faizaliana 3,87 6,46 Nepenthes_lowii 4,3 Nepenthes_clipeata 2,69 Nepenthes_ephippiata 8,55 Nepenthes_mira 3,59 Nepenthes_alata Nepenthes_stenophylla 6,66 2,5 Nepenthes_fusca 2,42,95 Nepenthes_burbidgeae 5,6 Nepenthes_pilosa,5 Nepenthes_eymae 3,53 Nepenthes_maxima 2,88 Nepenthes_veitchii Nepenthes_reinwardtiana Nepenthes_mikei,2 Nepenthes_gracillima 7, Nepenthes_sanguinea 4,52 Nepenthes_ramispina,66 Nepenthes_macfarlanei 4,34 Nepenthes_petiolata 2,65 Nepenthes_truncata 6,24 Nepenthes_edwardsiana2 4,46 Nepenthes_edwardsiana3,2 Nepenthes_rajah 3,5 Nepenthes_villosa3 2,36 2,45 8,57 Nepenthes_villosa2,75 Nepenthes_rajah2,5 Nepenthes_villosa_2 Nepenthes_boschiana Nepenthes_thorelii 7,36 2,4 Nepenthes_rafflesiana,72 Nepenthes_albomarginata 6,7 Nepenthes_gracilis2 2,3 Nepenthes_mapuluensis 4,3 9,9 Nepenthes_hirsuta,59 Nepenthes_ampullaria,47 Nepenthes_mirabilis Nepenthes_tobaica 3,62 Nepenthes_lavicola 6, Nepenthes_spathulata 2,96 Nepenthes_talangensis,68 5, Nepenthes_aristolochioides Nepenthes_densiflora 3, 7,58 Nepenthes_singalana,96 Nepenthes_diatas Nepenthes_bongso,7 Nepenthes_gymnamphora 5,9 Nepenthes_dubia,45 Nepenthes_inermis 4,37 Nepenthes_adnata 2,43 Nepenthes_longifolia 3,89 Nepenthes_spectabilis,7 Nepenthes_ovata 2,79 Nepenthes_eustachya 2,5 Nepenthes_sumatrana,62 Nepenthes_rhombicaulis FIGURE. Chronograms Orchidaceae for Nepenthes. Paphiopedilum 44,34 44,34 Node colors represent probabilities. Endemic species Anigozanthos_flavidus 6,75 Musella_lasiocarpa Anigozanthos_flavidus printed in red. 83,97 6,75 Elaeis_oleifera Musella_lasiocarpa 83,97 66,83 6,78 66,83 6,78 59,36 59,36 32,2 32,2 Rhodohypoxis Apostasia 2,4 38,57 Apostasia 2,4 38,57 Neuwiedia Neuwiedia Vanilla upward shift of vegetation zones on 57,72 inabalu compared Vanilla 57,72 Cleistes with other ornean 34,7 Cleistes 34,7 Pogonia Pogonia 77,9 Cypripedium 77,9 34,38 Cypripedium 34,38 Selenipedium 37, Selenipedium 37, Phragmipedium mountains (Grubb, 97; Gawin et al., 24). Niche 26,52 Phragmipedium 26,52 conservatism Paphiopedilum_delenatii 4, Paphiopedilum_delenatii indeed occurs 4, Paphiopedilum_haynaldianum 7,34 Paphiopedilum_haynaldianum 7,34 Codonorchis Codonorchis 49,39 Disperis 49,39 Disperis 39,36 Disa 39,36 9,4 Disa in Nepenthes. The high altitude species N. villosa, occurs 9,4 in Monadenia the alpine zone and 32,6 Monadenia 32,6 Habenaria 23,38 Habenaria 23,38 Orchis 6, Orchis 53,9 53,9 6, 68,88 Platanthera 68,88 34,93 Diuris 34,93 moss forest zone, and seems to be derived from clades of 39,82 Chiloglottis species occurring in 39,82 33,6 Eriochilus 33,6 48,92 48,92 Microtis Chloraea 44,3 44,3 Pterostylis the moss forest and submontane zones. Those ancestral Megastylis 42,76 clades in turn seem 42,76 Exalaria 7,68 4,79 Ponthieva 4,79 28,7 Altenstenia 6,82 6,82 25,59 Sarcoglottis 38,74 6,47 derived from species occurring in lowland forest in the separate Spiranthes nrits and mat Pachyplectron 32,58 Dossinia 3,75 Ludisia 23,48 Goodyera 8,96 Platythelys and combined analyses (Figs., ).Our multi-taxon study Palmorchis shows that inabalu s 4,8 Epipactis 24,5 Listera Sobralia 5, 43,3 Nervilia biodiversity hot spot is of recent origin. This means the mountain Dendrobium_kingianum is an evolutionary 45,63 25,45 Dendrobium_officinale 8,57 Dendrobium_crystallinum Calanthe 38,32 33,24 Pleione cradle, accumulating neo-endemics, as has been suggested for Agrostophyllum_majus other young, high ,22 37,24 33,8 3,92 27,67 35,98 35,98 24,3 24,3 22,56 22,56 6,72,76,76 32,9 32,9 29,23 29,23 3,7 22,84 22,84 4,7 4,7 2, 2, 8,43 8,43 6,55 6,55 3,82 3,82 8,73 8,73 Nypa_fruticans Elaeis_oleifera Astelia Nypa_fruticans Lanaria Astelia Empodium Lanaria Hypoxis Empodium Rhodohypoxis Hypoxis Earina_autumnalis Earina_valida Eria ullschlaegelia Cattleya Masdevallia Phalaenopsis Cymbidium Galeandra Mormodes ifrenaria Lycaste Maxillaria Zygopetalum Vitekorchis Gongora Gongora Stanhopea Stanhopea Trichosanthes 56,82 56,82 39,46 39,46 53,3 53,3 34,5 34,5 5,28 5,28 3,8 3,8 39,86 39,86 37,7 37, ,7 35,7 29,34 2

11 elevation biodiversity hot spots at low latitudes (Favre et al., 24), such as the Tibetan plateau (Schwery et al., 25), the Andean highlands (Hoorn et al., 23), and Afrotropical volcanoes (Price et al., 24). However, probably as a consequence of the rapid emergence of the mountain (Cottam et al., 23) and its unique alpine summit conditions (itayama, 992), many of these neo-endemics have not evolved by drastic niche shifts from local ancestors, but rather by immigration of pre-adapted propagules from elsewhere. This explains the multiple independent colonization events in some taxa (for example, Glomus, Rhododendron and Coeliccia). In addition, local lowland taxa have also generated montane species, but although some of these have reached vegetation zones above 2, m, most do not show substantial niche shifts away from their ancestral niche. The niches of Nepenthes species endemic to Mount inabalu and neighborying Mount Tambyukon appear to be conserved, coincide with the timing of mountain formation and are show a pattern of centric endemism. The fact that the endemic biota of inabalu appears to be composed largely of pre-adapted (eccentric) species and locally derived (centric), ecologically conserved endemics is in line with niche conservatism (Crisp et al., 29). e suggest that our novel approach of molecular dating of multiple clades be applied to larger communities in this and other tropical montane biodiversity hot spots (Culmsee & Leuschner, 23). In combination, such information should allow a detailed dissection of the relative roles of ecological speciation, colonization and habitat filtering in the formation of endemic biotas in this and other tropical mountains. Moreover, such understanding could improve predictions of the likelihood of extinction and evolutionary rescue of endemic species experiencing changing climate conditions (Schiffers et al., 23). 36