Journal of Biogeography (J. Biogeogr.) (2012) 39, 98–113

ORIGINAL West to east dispersal and subsequent ARTICLE rapid diversification of the mega-diverse genus () in the Malesian archipelago D. C. Thomas1,2*, M. Hughes2, T. Phutthai3, W. H. Ardi4, S. Rajbhandary5, R. Rubite6, A. D. Twyford2,7 and J. E. Richardson2,8

1School of Biological Sciences, University of ABSTRACT Hong Kong, Pok Fu Lam Road, Pokfulam, Aim The complex palaeogeography of the Malesian archipelago, characterized by Hong Kong, China, 2Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh the evolution of an ever-changing mosaic of terrestrial and marine areas EH3 5LR, UK, 3Herbarium, Princess Maha throughout the Cenozoic, provides the geographic backdrop for the remarkable Chakri Sirindhorn Natural History Museum & diversification of Malesian Begonia (> 450 ). This study aimed to Centre for Biodiversity of Peninsular Thailand investigate the origin of Malesian Begonia, the directionality of dispersal events (CBiPT), Department of Biology, Prince of within the Malesian archipelago and the impact of ancient water gaps on Songkla University, Hat Yai, Songkhla, colonization patterns, and to identify drivers of diversification. 4 Thailand 90112, Bogor Botanic Gardens, Jl. Location Asia, Southeast Asia, Malesia. Ir. H. Juanda No. 13, Bogor 16003, Indonesia, 5Central Department of Botany, Tribhuvan Methods Plastid DNA sequence data of representatives of all families of the University, Kirtipur, Kathmandu, Nepal, and Fagales (matK, rbcL, trnL intron, trnL–F spacer, 4076 aligned 6Department of Biology, College of Arts and positions, 92 taxa) and a sample of all major Asian Begonia sections (ndhA intron, Sciences, University of the Philippines Manila, ndhF–rpl32 spacer, rpl32–trnL spacer, 4059 aligned positions, 112 taxa) were Padre Faura, Manila, Philippines, 7School of analysed under an uncorrelated-rates relaxed molecular clock model to estimate Biological Sciences, University of Edinburgh, the age of the Begonia crown group divergence and divergence ages within Asian Mayfield Road, Edinburgh EH9 3JH, UK, Begonia. Ancestral areas were reconstructed using a likelihood approach 8 Universidad de los Andes, Apartado Ae´reo implementing a dispersal–extinction–cladogenesis model, and with a Bayesian 4976, Bogota´, D.C., Colombia approach to dispersal–vicariance analysis. Results The results indicated an initial diversification of Asian Begonia in continental Asia in the Miocene, and subsequent colonization of Malesia by multiple lineages. There was support for at least six independent dispersal events from continental Asia and western Malesia to Wallacea dating from the late Miocene to the Pleistocene. Begonia section Petermannia (> 270 species) originated in Western Malesia, and subsequently dispersed to Wallacea, New Guinea and the Philippines. Lineages within this section diversified rapidly since the Pliocene, coinciding with rapid orogenesis on Sulawesi and New Guinea. Main conclusions The predominant trend of Begonia dispersals between continental Asia and Malesia, and also within Malesia, has been from west to east. The water bodies separating the Sunda Shelf region from Wallacea have been porous barriers to dispersal in Begonia following the emergence of substantial land in eastern Malesia from the late Miocene onwards. We hypothesize two major drivers of the diversification of Malesian Begonia: (1) the formation of topographical heterogeneity and the promotion of microallopatry by orogenesis in the Pliocene and Pleistocene; and (2) cyclic vicariance by frequent habitat fragmentations and amalgamations due to climate and sea-level fluctuations during the Pleistocene. *Correspondence: Daniel C. Thomas, School of Keywords Biological Sciences, University of Hong Kong, Ancestral area reconstruction, Begonia section Petermannia, dispersal, diversi- Pok Fu Lam Road, Pokfulam, Hong Kong, China. fication, historical biogeography, Malesia, Southeast Asia, Sulawesi, vicariance, E-mail: [email protected] Wallacea.

98 http://wileyonlinelibrary.com/journal/jbi ª 2011 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2011.02596.x Historical biogeography of Southeast Asian Begonia

the fragments that formed parts of central Malesia were INTRODUCTION submerged during most of their migration, and substantial The phytogeographic region of Malesia extends from southern land emerged in this area only from the late Miocene onwards Thailand through Malaysia, Singapore, Indonesia, East Timor (Hall, 2001, 2009); (3) major land bridges did not emerge in and the Philippines, to Papua New Guinea and the Solomon central Malesia, even during Pleistocene glacial maxima that Islands (Raes & van Welzen, 2009). It is one of the three substantially lowered sea levels (Voris, 2000; Woodruff, 2010). regions in the world with extensive areas of tropical rain Wallace’s Line, the demarcation of the perceived sharp biotic forests, and comprises biodiversity hotspots such as the Sunda transition in central Malesia (Figs 1 & 2), coincides with the Shelf area, Wallacea, the Philippines and New Guinea, eastern border of the Eurasian plate, the Sunda Shelf, harbouring an estimated 42,000 species of vascular substantial parts of which were exposed and supported (Roos, 1993; Brooks et al., 2006). The biogeography of the extensive areas of rain forest for long periods during the Malesian archipelago has intrigued biologists since Alfred Cenozoic (Morley, 2007; Cannon et al., 2009; Hall, 2009). Russel Wallace’s seminal biogeographic studies in the 19th Wallace’s Line also coincides with the ancient deep-water century. Wallace (1860) identified a multi-taxon faunistic channels of the Lombok Strait and the Makassar Straits, which break between the neighbouring central Malesian islands of remained physical barriers to dispersal even at times of low sea Bali and Lombok, and emphasized the impact of past levels caused by glacioeustatic sea-level fluctuations during the geological connections and past biotic migrations on current Pleistocene (Voris, 2000). distribution patterns (Lomolino et al., 2006). Research in the While the profound impact of the palaeogeography of 20th and 21st centuries has supported many of Wallace’s ideas, Malesia on current broad-scale floristic patterns in the region and the multitude of islands in Malesia indeed differ greatly in has been recognized (van Welzen et al., 2005; van Welzen & their origin, age and their past land connections, as well as in Slik, 2009), the temporal and geographic origins of Malesian the composition of their floras (Hall, 2002, 2009; van Welzen island biota, especially on central Malesian islands such as et al., 2005; van Welzen & Slik, 2009). Van Welzen et al. Sulawesi, remain enigmatic. Malesia has been the interface of a (2005) summarized geological correlates of the sharp biotic complex biotic exchange, and four main geographic origins of transition in central Malesia: (1) the continental fragments that Malesian lineages can be hypothesized: (1) Eurasia, with constitute parts of central Malesia migrated to their current colonization of Malesia via continental Southeast Asia, e.g. position only during the Cenozoic, while some terrestrial areas numerous taxa of boreotropical origin (Mai, 1995; Kubitzki & in western Malesia were in place already (Hall, 2001, 2009); (2) Krutzsch, 1996; Morley, 2003); (2) Eurasia, with colonization

Huxley’s Line 20°N

N

Wallace’s Line

Lydekker’s Line

0°

1000 km

100°E

Figure 1 The distribution of Begonia in Malesia. Black circles represent georeferenced collections in the Southeast Asian Begonia Database (Hughes & Pullan, 2007).

Journal of Biogeography 39, 98–113 99 ª 2011 Blackwell Publishing Ltd D. C. Thomas et al.

B. oxyloba b 2 B. goudotii b 3 B. polygonoides b 4 B. poculifera b B. dregei b 7 B. sutherlandii b 6 B. radicans a 8 B. nelumbiifolia a 9 B. boliviensis a B. dipetala c 1 B. socotrana b A12 13 B. samhaensis b 11 B15 B. malabarica c B. floccifera c 18 B. hymenophylla c B. smithiae c 14 17 19* B. tenuifolia de B. elisabethae cd 20 B. spec. Vietnam 1 c 21 B. spec. Thailand 1 c 5 C16 B. grandis c B. alicida c 22 B. puttii c 25 B. spec. China 1 c 23 B. rabilii c 27 B. brandisiana c 24 28 B. aceroides c 29 B. demissa c B. flagellaris c 26 B. versicolor c B. venusta d 30 32 33 B. decora d 34 B. pavonina d 10 B. sikkimensis c 31 36 B. sizemoreae c 37 B. palmata c B. roxburghii c B. obovoidea c 35 40 39 B. acetosella c B. silletensis c 41 42* 38 B. longifolia cde 43* B. aptera eg B. hatacoa c B. spec. China 2 c 44 B. spec. Sulawesi 1 e 45* 47* B. areolata d 46* B. robusta de 48* B. multangula de B. masoniana c 50 B. morsei c B. kingiana d 54 B. spec. Sumbawa 1 e B. goegoensis d D49 53* 55 B. muricata de 56 B. sudjanae d B. cleopatrae f 51 B. nigritarum f 57 B. fenicis cf 58 59 B. hernandioides f 60 B. chloroneura f AreaAreas 62 B. lepida d B. verecunda d 52 a: Americas 63 B. spec. Sumatra 1 d 64 B. spec. Sumatra 2 d b: Africa 67 B. wrayi d B. multijugata d c: Continental Asia 66 68 B. chlorosticta d 69 B. spec. Borneo 1 d d: Sunda Shelf B. spec. Sumatra 3 d 61 71 B. laruei d e: Wallacea 70 72 B. corrugata d B. aff. congesta d f: Philippines 73 B. spec. Borneo 2 d B. spec. Sumbawa 2 e g: New Guinea 77 B. symsanguinea g B. strigosa g ab: America + Africa 65 75 78 B. argenteomarginata g abc: America + Africa + Continental Asia B. spec. New Guinea 1 g 76 80 B. spec. New Guinea 2 g 81 B. weigallii g cd: Continental Asia + Sunda Shelf 79 B. brevirimosa g 83 B. serratipetala g ce: Continental Asia + Wallacea B. spec. Philippines 1 f 82 de: Sunda Shelf + Wallacea 84 B. negrosensis f 74 85 B. polilloensis f B. hekensis e 88 B. stevei e 89 B. varipeltata e 87 B. chiasmogyna e 90 91 B. macintyreana e N B. mendumiae e 92 B. masarangensis e 1000 km 93 B. capituliformis e 86 94 B. hispidissima e B. bonthainensis e 96 B. siccacaudata e 98 B. ozotothrix e B. nobmanniae 95 e 99 B. prionota e 100 B. aff. didyma e 97 B. watuwilensis e Wallace’s Line 102 B. flacca e B. lasioura e 101 B. koordersii e Equator 103 B. pseudolateralis f 105 B. comestibilis e 104 106 108 B. vermeulenii e B. torajana e 107 B. sanguineopilosa e 109 B. aff. mekonggensis e 110 B. guttapila e 111 B. rantemarioensis e 20 15 10 5 0 Ma

Figure 2 Likelihood ancestral area reconstructions under the dispersal–extinction–cladogenesis model. Branches are coloured according to the optimal reconstructions (Table 1). Arrows represent dispersal events between the defined regions. Numbers at nodes indicate clade names in Table 1. Asterisks indicate nodes for which multiple equally probable ancestral areas were reconstructed in Bayes-DIVA and/or likelihood reconstructions (Table 1). Lower-case letters after taxon names indicate taxon distributions. Broken branches indicate posterior clade probabilities < 0.95. Geological epochs are indicated with three shades of grey in the background: light grey, Holocene and Pleistocene (0–2.6 Ma); mid-grey, Pliocene (2.6–5.3 Ma); dark grey, Miocene (5.3–23.0 Ma). The inset map indicates the distribution of Asian Begonia and the delimitation of Asian area units used in the reconstructions.

100 Journal of Biogeography 39, 98–113 ª 2011 Blackwell Publishing Ltd Historical biogeography of Southeast Asian Begonia via the mountain ranges of Taiwan and the Philippines (van set), sequence data of four plastid DNA regions (matK gene, Steenis, 1964); (3) , with colonization by taxa of rbcL gene, trnL intron, trnL–F spacer) of 92 taxa representing a Gondwanan origin via the rafting Indian fragment or via the sample of all families of the orders Fagales and Cucurbitales Indian raft and continental Southeast Asia, e.g. Crypteronia- (sensu Angiosperm Phylogeny Group, 2009) was analysed. This ceae (Rutschmann et al., 2004), Dipterocarpaceae (Morley, allowed the integration of multiple fossil-based calibration 2003); (4) Australia, with colonization of Malesia from the points in order to estimate the divergence ages of the Begonia Australian continent, e.g. Proteaceae (Barker et al., 2007), crown group. In stage 2 (Begonia dataset), the divergence age Nothofagus (Morley, 2003), Eucalyptus (Ladiges et al., 2003). estimate of the Begonia crown inferred in stage 1 were applied However, few studies have combined a phylogenetic frame- as a secondary calibration point. Secondary calibration, the use work and molecular divergence age estimates to elucidate the of molecular age estimates from previous analyses to calibrate a temporal and geographic origins of taxa whose distri- molecular clock, is potentially problematic as errors of the butions cover the wider Malesian archipelago (Muellner et al., primary analysis are propagated in the secondary analysis 2008, 2009; Su & Saunders, 2009; Webb & Ree, in press). (Graur & Martin, 2004; Renner, 2005). However, in the This study focuses on the historical biogeography of the absence of suitable fossils for primary calibrations, secondary mega-diverse genus Begonia (c. 1500 species), which has a calibration is a reasonable alternative (Hedges & Kumar, centre of diversity in Southeast Asia (> 550 species; Hughes, 2004). A 112-taxon Begonia data matrix, including data from 2008). The great potential of this genus with regard to the three non-coding plastid DNA regions (ndhA intron, ndhF– detection of biogeographic patterns in Southeast Asia lies in its rpl32 spacer, rpl32–trnL spacer), which were shown to be of wide distribution, which spans Malesia, continental Southeast considerable phylogenetic utility at the inter- and infrasec- Asia and large parts of continental Asia (Fig. 1); in its good tional level in Asian Begonia (Thomas et al., 2011a), was representation with regard to species numbers on all major utilized. The Begonia dataset included 103 taxa from the islands and island groups in Malesia (c. 450 species in species-rich Asian Begonia sections Coelocentrum, Diploclini- Malesia); and in the preponderance of narrow-range endemics um, Parvibegonia, Petermannia, Platycentrum, Reichenheimia, limited to primary rain forest habitats (Hughes & Hollings- Sphenanthera and Symbegonia, as well as the small sections worth, 2008). The majority of Asian Begonia species are Alicida, Bracteibegonia, Haagea and Ridleyella, and the two anemochorous and produce winged capsules, which produce species endemic to Socotra (section Peltaugustia). A particular hundreds to thousands of minute seeds. At 300–600 lmin focus was put on Malesian lineages, and data of 29 species, length, Begonia seeds could potentially be distributed by wind c. 65% of the known Begonia species from Sulawesi (Thomas (de Lange & Bouman, 1992, 1999). However, numerous et al., 2011b), were included because of its biogeographically anemochorous species are narrow endemics, and anemochory significant location in central Malesia. Six African and three is unlikely to result in long dispersal distances in the sheltered American species were used as the outgroup, based on conditions of the moist ground layer habitats preferred by the molecular phylogenetic studies by Goodall-Copestake et al. majority of Asian Begonia species (Hughes & Hollingsworth, (2010) and Plana et al. (2004). DNA sequences were down- 2008). Rain-ballist fruit syndromes and fleshy, putatively loaded from the nucleotide database of the National Centre for zoochorously dispersed fruits have evolved in several Asian Biotechnology Information (http://www.ncbi.nlm.nih.gov), Begonia lineages (Tebbitt et al., 2006; Thomas et al., 2011a). and 133 sequences were newly generated for this study. tend to have poor dispersal capabilities and often Voucher information and GenBank accession numbers are exhibit low rates of gene flow between populations in listed in Appendix S1 in Supporting Information. fragmented habitats (Matolweni et al., 2000; Hughes et al., 2003; Hughes & Hollingsworth, 2008), making them ideal DNA extraction, amplification and sequencing trackers of biogeographic events at both more recent and deeper time scales. Total genomic DNA was extracted from living or silica gel- By producing a well sampled, dated phylogeny of Southeast dried material using the DNeasy Plant Mini Kit (Qiagen, Asian Begonia, this study addresses the following questions. (1) Germantown, MD, USA) according to the manufacturer’s When and how was the Malesian archipelago colonized by protocols. For amplification of the cpDNA regions, each 25 lL

Begonia? (2) Have purported barriers to dispersal, such as the polymerase chain reaction (PCR) contained 15.25 lL ddH2O, long-standing deep-water channels of the Lombok Strait and the 2.5 lL10· reaction buffer, 1.25 lL25mm MgCl2, 2.5 lL Makassar Straits, had an effect on colonization? (3) When and dNTPs (2 mm), 0.75 lL of each forward and reverse primer where has most cladogenesis occurred, and what has driven it? (10 lm), 0.8 lL bovine serum albumin (BSA, 0.4%), 0.2 lL Biotaq DNA polymerase (Bioline, London, UK) and 1 lL DNA template. Primers and amplification protocols were the MATERIALS AND METHODS same as in Thomas (2010) and Thomas et al. (2011a). Poly A/T homonucleotide strands composed of eight or more Methodological approach and taxon sampling nucleotides, which were present in the sequences of most For the molecular divergence age estimates, this study adopted accessions, can cause PCR artefacts by slipped-strand mispair- a two-stage approach. In stage 1 (Cucurbitales–Fagales data- ing (Shinde et al., 2003). An alternative amplification protocol

Journal of Biogeography 39, 98–113 101 ª 2011 Blackwell Publishing Ltd D. C. Thomas et al. was applied for problematic samples using Phusion polymerase (ndhA intron, ndhF–rpl32 spacer, rpl32–trnL spacer) based on (Finnzymes, Espoo, Finland), which has been shown to reduce coding region, spacer and intron identity. Models of sequence slipped-strand mispairing (Fazekas et al., 2010). Amplification evolution for each partition were determined using products were visualized under UV light after electrophoretic MrModeltest v. 2 (Nylander, 2004) under the Akaike separation on a 1% agarose gel stained with SYBR Safe gel stain information criterion. The general time-reversible nucleotide- (Invitrogen, Carlsbad, CA, USA). PCR products were subse- substitution model with among-site rate variation modelled quently purified using ExoSAP-IT (Affymetrix, Santa Clara, with a gamma distribution (GTR+C) was selected for all CA, USA) according to the manufacturer’s protocols. Sequenc- partitions, and the proportion of invariable sites parameter ing PCRs used the same primers as for amplification, and were was additionally selected for the ndhA intron, ndhF–rpl32 and quarter reactions using the BigDye Terminator v. 3.1 Cycle rbcL partitions (GTR+C+I). The Yule process was selected as Sequencing Kit (Applied Biosystems, Foster City, CA, USA). tree prior and a single overall UCLD model was applied for Sequencing PCR products were purified and sequenced at the all partitions. For analyses of the Cucurbitales–Fagales GenePool facilities at the University of Edinburgh using an AB dataset, a starting tree satisfying all calibration priors was 3730 DNA Analyser (Applied Biosystems). generated by taking a maximum likelihood (ML) tree from a RAxML v. 7.2.6 (Stamatakis, 2006) analysis and transforming it into an ultrametric tree in TreeEdit v. 1.0a10 (Rambaut & Alignment Charleston, 2002). For each analysis of both datasets, two Sequences were assembled, edited and aligned using geneious separate Markov chain Monte Carlo (MCMC) analyses were v. 5.1.7 (Drummond et al., 2010). Alignment of the Cucurbi- run, each with 4 · 107 generations and sampling every tales–Fagales dataset posed few difficulties, but a highly 1000th generation. Time-series plots of all parameters were variable region of the trnL intron (14–65 bp) was removed analysed in Tracer v. 1.5 (Rambaut & Drummond, 2009) to due to uncertain homology. An inversion (24–44 bp) charac- check for adequate effective sample sizes (ESS > 200) and terizing all taxa except Austrobryonia argillicola convergence of the model likelihood and parameters between and Neoalsomitra sarcophylla (see Kocyan et al., 2007) was each run. Trees were combined in LogCombiner v. 1.5.4 reverse complemented in the trnL–F spacer alignment to retain (Drummond & Rambaut, 2007), setting the burn-in to 25% substitution information. Several inversions were identified in of the initial samples of each MCMC run. Trees were then the Begonia dataset. An autapomorphic inversion of 48 bp is summarized using the maximum clade credibility (MCC) present in the ndhA intron sequence of the Neotropical option in TreeAnnotator v. 1.5.4 (Drummond & Rambaut, Begonia radicans Vell., and inversions of 355, or (due to 2007). deletion) of 309 bp, flanked on both sides by A/T homonu- cleotide strands, were identified in the ndhF–rpl32 spacer Fossil constraints and secondary calibration region of all Philippine samples of Begonia section Diploclin- ium. A third inversion, flanked by homonucleotide repeats of Four fossil constraints were used in the analysis of the four G/Cs on each side, was identified in the rpl32–trnL spacer. Cucurbitales–Fagales dataset: C1–C4. This 11 bp inversion was present in Begonia masoniana Irmscher ex Ziesenh. (section Coelocentrum), and Begonia Constraint C1 roxburghii A.DC. (section Sphenanthera). These species are only distantly related in phylogenetic trees resulting from the The first occurrence of tricolpate pollen indicative of analysis of the cpDNA sequence data, indicating a homoplas- (Hughes & McDougall, 1990; Doyle & Hotton, 1991) was used ious origin of this inversion in the two sections. All inversions as a provisonary maximum constraint on the root node. This were reverse-complemented. Nineteen mutational hotspots, constraint was applied by assigning a uniform prior with a most of which were length differences of homonucleotide lower boundary of 96.55 (see constraint C2) and an upper strands, together c. 5.1% of the aligned positions, were boundary of 125 Ma to the Cucurbitales stem node. excluded from the final matrix because of uncertain homology (Kelchner, 2000; Borsch & Quandt, 2009). Constraint C2 The first occurrences of fagalean Normapolles type pollen Bayesian divergence age estimation grains and associated fossil floral structures in the middle Bayesian divergence time estimation was performed using Cenomanian (Friis et al., 2006) was used as a fossil constraint beast v. 1.5.4 (Drummond & Rambaut, 2007). The datasets by assigning an exponential prior to the stem node of core were run using an uncorrelated-rates relaxed molecular clock Fagales (offset: 96.55 Ma, mean: 1.02), i.e. the divergence of model assuming a lognormal distribution of rates (UCLD). Fagaceae and core Fagales. A mean of 1.02 was chosen so that Data partitions were defined a priori. The Cucurbitales– 95% of the probability is contained in an interval between the Fagales dataset was partitioned into four partitions (matK midpoint and the upper boundary of the Cenomanian (96.55– gene, rbcL gene, trnL intron, trnL–F spacer) and the 99.6 Ma). An exponential prior distribution was chosen, Begoniaceae dataset was partitioned into three partitions reflecting the assumption that, based on the good fossil record

102 Journal of Biogeography 39, 98–113 ª 2011 Blackwell Publishing Ltd Historical biogeography of Southeast Asian Begonia from numerous localities and well dated strata, and the lack of islands (islands east of Lydekker’s Line, the Bismarck Archi- similar fossils from older strata, the age of the oldest relevant pelago, Solomon Islands). Distributions were assigned to taxa fossils is relatively close to the actual divergence date. based on distribution data in Doorenbos et al. (1998), Hughes (2008), or in more recent new species descriptions. Constraint C3 Ancestral area reconstructions Tetrameles-like fossil bark described as Tetrameleoxylon prenu- diflora has been described from the Deccan intertrappean beds Ancestral areas at internal nodes within the phylogenetic tree at Mohgaonkalan in India (Lakhanpal & Verma, 1965). This were inferred using two methods: (1) a Bayesian approach to fossil constraint was assigned to constrain the Tetramelaceae dispersal–vicariance analysis (Bayes-DIVA) (Ronquist, 1997; stem node using the upper boundary of the Maastrichtian Nylander et al., 2008) implemented in s-diva v. 1.9beta (Yu (70.6 Ma) as the lower hard bound of a uniform prior et al., 2010); (2) a likelihood approach using the dispersal– distribution. The upper boundary was set to 125 Ma (see extinction–cladogenesis model implemented in Lagrange constraint C1). build20101113 (Ree & Smith, 2008). In both analyses, the maximum number of areas in ancestral ranges was con- strained to three. The most widespread Asian species is Constraint C4 Begonia longifolia Blume, the distribution of which includes Seed fossils from the Uppermost Palaeocene and Lower Eocene three of the defined area units (continental Asia, Sunda Shelf, London Clay have been assigned to Cucurbitaceae (Chandler, Wallacea). The constraint on ancestral ranges reflects the 1964; Collinson, 1986; Collinson et al., 1993). This study assumption that the ranges of ancestral begonias were similar follows Schaefer et al. (2009) by assigning a prior with uniform to those of their extant descendants. For the Bayes-DIVA, distribution to the Cucurbitaceae crown node with a lower ancestral areas were reconstructed independently on 1000 hard bound of 65.5 Ma, which is at the Palaeocene–Eocene randomly chosen post burn-in trees of the beast analysis. boundary, and the upper boundary set to 125 Ma (see Relative frequencies of ancestral areas reconstructed for each constraint C1). node were recorded and plotted onto the maximum clade credibility tree of the beast analysis. For the likelihood ancestral area analysis, Python scripts were generated using Secondary constraint in the analysis of the Begonia dataset the online Lagrange configurator (http://www.reelab.net/ Divergence age estimates of the most recent common ancestor lagrange/configurator). The MCC tree of the beast analysis (MRCA) of Begonia derived from the analysis of the Fagales– was used as the input tree. The probability of dispersal Cucurbitales dataset were used as secondary calibration. To between areas was modelled as equal, and all values in the account for the uncertainty of the age estimates of the primary dispersal constraint matrix were set to 1. analysis, the calibration prior of the MRCA of the Begonia crown group was modelled with a normal distribution, with its RESULTS mean set to the mean estimates of the primary analysis (24 Ma), and the standard deviation set to 3.57 (95% Phylogenetics of Socotran–Asian Begonia probability interval: 17–31 Ma), to include the 95% highest posterior density (HPD) interval of the estimate of the Begonia The maximum clade credibility chronogram resulting from crown group divergence of the primary analysis (18.2–31 Ma). the analyses of the Begonia dataset is shown in Fig. 3. Posterior probabilities (PP) are given in Table 1 and in Appendix S2. Clade names (A–D) and numbers (clades Ancestral area reconstruction 1–111) are the same as in Fig. 2. The relationships of two clades, A and B, which diverge at two of the deepest nodes Area delimitation within the Asian–Socotran crown group, are only poorly Seven areas based on the extant distribution of Asian Begonia, supported. Clade A (clade 12, PP: 0.95) includes the Indian the geological history of Asia, and areas of Begonia endemism Begonia dipetala Graham (section Haagea) as sister to a (Hughes, 2008), were considered in the analyses (Fig. 2): (1) strongly supported clade including two Socotran species of America; (2) Africa including the Yemenite Socotra Archipel- section Peltaugustia. Clade B (clade 15, PP: 1) is composed ago; (3) continental Asia (including adjacent major islands of two South Indian–Sri Lankan species, Begonia floccifera such as Sri Lanka, Taiwan, Hainan); (4) the Sunda Shelf Bedd. (section Reichenheimia) and Begonia malabarica Lam. region, which extends from just north of the Thai–Malay (unplaced to section). The rest of the Asian species fall into border, through the Malay Peninsula, Sumatra, Borneo, and two major clades: Clade C (clade 16), which is dominated Java to Bali; (5) Wallacea, which comprises Sulawesi and by species with distribution in continental Asia, and clade D adjacent islands, the Lesser Sunda Islands (except Bali), and the (clade 49), which is dominated by taxa with Malesian Maluku Islands between Wallace’s and Lydekker’s lines; (6) the distributions. Within the strongly supported clade C (PP: 1), Philippines, including Palawan; (7) New Guinea and adjacent a clade consisting of continental Asian species Begonia

Journal of Biogeography 39, 98–113 103 ª 2011 Blackwell Publishing Ltd D. C. Thomas et al.

B. oxyloba b 2 B. goudotii b 3 B. polygonoides b 4 B. poculifera b B. dregei b 7 B. sutherlandii b 6 B. radicans a 8 B. nelumbiifolia a 9 B. boliviensis a B. dipetala c 1 B. socotrana b A12 13 B. samhaensis b 11 B15 B. malabarica c B. floccifera c 18 B. hymenophylla c B. smithiae c 14 17 19 B. tenuifolia de B. elisabethae cd 20 B. spec. Vietnam 1 c 21 B. spec. Thailand 1 c 5 C16 B. grandis c B. alicida c 22 B. puttii c 25 B. spec. China 1 c 23 B. rabilii c 27 B. brandisiana c 24 28 B. aceroides c 29 B. demissa c B. flagellaris c 26 32 B. versicolor c B. venusta d 30 33 B. decora d 34 B. pavonina d 10 B. sikkimensis c 31 36 B. sizemoreae c 37 B. palmata c B. roxburghii c B. obovoidea c 35 40 39 B. acetosella c B. silletensis c 41 42 38 B. longifolia cde 43 B. aptera eg B. hatacoa c B. spec. China 2 c 44 B. spec. Sulawesi 1 e 45 47 B. areolata d 46 B. robusta de 48 B. multangula de B. masoniana c 50 B. morsei c B. kingiana d 54 B. spec. Sumbawa 1 e B. goegoensis d D49 53 55 B. muricata de 56 B. sudjanae d B. cleopatrae f 51 B. nigritarum f 57 B. fenicis cf 58 59 B. hernandioides f 60 B. chloroneura f 62 B. lepida d B. verecunda d 52 63 B. spec. Sumatra 1 d 64 B. spec. Sumatra 2 d 67 B. wrayi d B. multijugata d 66 68 B. chlorosticta d 69 B. spec. Borneo 1 d B. spec. Sumatra 3 d 61 71 B. laruei d 70 72 B. corrugata d B. aff. congesta d 73 B. spec. Borneo 2 d B. spec. Sumbawa 2 e 75 77 B. symsanguinea g B. strigosa g 65 78 B. argenteomarginata g B. spec. New Guinea 1 g 76 80 B. spec. New Guinea 2 g 81 B. weigallii g 79 B. brevirimosa g 83 B. serratipetala g 82 B. spec. Philippines 1 f 84 B. negrosensis f 74 85 B. polilloensis f B. hekensis e 88 B. stevei e 89 B. varipeltata e 87 B. chiasmogyna e 91 B. macintyreana e 90 B. mendumiae e 92 B. masarangensis e 93 B. capituliformis e 86 94 B. hispidissima e B. bonthainensis e 96 B. siccacaudata e 98 B. ozotothrix e 95 B. nobmanniae e 99 B. prionota e 100 B. aff. didyma e 97 B. watuwilensis e 102 B. flacca e B. lasioura e 101 B. koordersii e 103 105 B. pseudolateralis f Geological epoch [Ma] B. comestibilis e 104 106 108 B. vermeulenii e Holocene + Pleistocene (0-2.6) B. torajana e Pliocene (2.6-5.3) 107 B. sanguineopilosa e 109 B. aff. mekonggensis e Miocene (5.3-23.0) 110 B. guttapila e 111 B. rantemarioensis e 20 15 10 5 0 Ma

Figure 3 Maximum clade credibility chronogram: Begoniaceae dataset. Node heights indicate mean ages. Node bars indicate 95% highest posterior density date ranges. Numbers and letters at nodes represent clade names in Table 1. Broken branches indicate posterior clade probabilities < 0.95. Geological epochs are indicated in three shades of grey: light grey, Holocene and Pleistocene (0–2.6 Ma); mid-grey, Pliocene (2.6–5.3 Ma); dark grey, Miocene (5.3–23.0 Ma).

104 Journal of Biogeography 39, 98–113 ª 2011 Blackwell Publishing Ltd Historical biogeography of Southeast Asian Begonia

Table 1 Clade support, divergence age estimates and ancestral area reconstructions for Asian Begonia.

Divergence ages mean Clade Clade support [PP] (95% HPD) [Ma] Likelihood-DEC [RP]* Bayes-DIVA [MP]

1 1 22.3 (15.2–29.5) [b|abc] 0.42 abc 100 [b|bc] 0.17 [b|bcd] 0.1 5 0.85 18.2 (11.3–25.8) [ab|c] 0.47 ac 65 [b|cd] 0.11 abc 35 [b|bc] 0.1 6 1 12.5 (6.9–18.8) [b|a] 1 ab 100 7 1 6.5 (2.6–10.9) [b|b] 1 b 100 8 0.73 10.8 (5.1–15.7) [a|a] 1 a 100 9 0.36 – [a|a] 1 a 100 10 1 16.1 (9.1–22.5) [c|c] 0.47 c 100 [bc|c] 0.21 [c|cd] 0.19 A12 0.95 13.6 (7.3–19.5) [c|b] 1 bc 100 B15 1 6.3 (2.6–10.7) [c|c] 1 c 100 C16 1 14.3 (8.2–20.2) [c|c] 1 c 100 17 1 12 (6.7–17.4) [c|c] 0.94 c 100 19 1 4.6 (2.1–7.5) [d|cd] 0.68 cd 33 [de|c] 0.14 ce 33 cde 33 22 1 13 (7.6–18.5) [c|c] 1 c 100 31 1 5.6 (3.1–8.3) [c|c] 0.66 c 100 [cd|c] 0.34 32 0.91 4.8 (2.4–7.2) [c|d] 1 cd 100 33 1 2.2 (0.9–3.7) [d|d] 1 d 100 42 0.34 – [c|c] 0.81 c 50 [c|ce] 0.13 ce 50 43 1 1 (0.1–1.2) [ce|e] 0.71 e 17 [cde|e] 0.26 ce 17 cde 17 cg 17 cdg 17 ceg 17 44 0.95 4.1 (2.3–6.2) [c|c] 0.9 c 100 45 1 3.2 (1.6–4.9) [c|e] 0.69 cd 33 [c|d] 0.2 ce 33 [c|de] 0.11 cde 33 46 1 1.3 (0.5–2.3) [e|de] 0.5 e 50 [e|e] 0.48 de 50 D49 1 13 (7.7–18.9) [c|d] 0.58 cd 100 [c|df] 0.14 50 1 4.3 (1.5–7.5) [c|c] 1 c 100 51 1 11.5 (6.6–16.5) [d|d] 0.53 d 100 [d|df] 0.2 53 0.31 – [d|f] 0.60 df 50 [de|f] 0.22 def 50 54 1 6 (3.1–9.2) [e|de] 0.55 de 100 [e|d] 0.42 55 1 4.5 (2.1–7.1) [d|de] 0.58 d 100 [d|d] 0.42 57 1 6.7 (3.1–10.1) [f|f] 0.87 f 100 [f|cf] 0.13 62 1 3.6 (1.5–5.9) [d|d] 1 d 100 64 1 1.7 (0.5–3.1) [d|d] 1 d 100 65 1 5.8 (3.3–8.4) [d|e] 0.88 de 100

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Table 1 Continued

Divergence ages mean Clade Clade support [PP] (95% HPD) [Ma] Likelihood-DEC [RP]* Bayes-DIVA [MP]

[d|eg] 0.33 66 1 4.2 (2.3–6.2) [d|d] 1 d 100 68 1 2.4 (1–4.1) [d|d] 1 d 100 70 0.97 2.9 (1.2–4.7) [d|d] 1 d 100 74 0.95 5.2 (3–7.5) [e|e] 0.49 e 100 [eg|e] 0.47 75 0.26 – [e|g] 0.93 eg 100 79 0.35 – [g|g] 0.84 g 100 [g|fg] 0.16 82 0.97 3.4 (1.8–5.2) [g|f] 1 fg 100 86 0.67 4.6 (2.7–6.6) [e|e] 1 e 100 87 1 3 (1.5–4.6) [e|e] 1 e 100 95 0.99 4.1 (2.3–6) [e|e] 1 e 100 104 0.28 – [e|e] 0.96 e 100 105 1 2.1 (0.9–3.6) [e|f] 1 ef 100

*Following Fig. 1, the vertical bar separates the inferred ancestral range for the upper branch (left letter) from the one reconstructed for the lower branch (right letter) descending from the node. Values represent the relative probability of that inference. Alternative ancestral area reconstructions that fall within two log-likelihood units of the optimal scenario and have a relative probability ‡ 0.1 are given. Differences in optimal reconstructions of the Bayes-DIVA and the likelihood analysis are indicated in bold. DEC, dispersal–extinction–cladogenesis model; DIVA, dispersal–vicariance analysis; HPD, highest posterior density date range; Ma, million years ago; PP, posterior probability; MP, marginal probability; RP, relative probability. A table with data on all nodes is given in Appendix S2. hymenophylla Gagnep. (section Reichenheimia) and Begonia species of section Petermannia s.l. (including section Symbe- smithiae Geddes (section Platycentrum), as well as three gonia). Within the Begonia section Petermannia clade (clade continental Asian and one Malesian species placed in section 65), well supported subclades of species with a Sunda Shelf Parvibegonia (clade 17, PP: 1), is sister to the rest of the distribution (clade 66, PP: 1), predominantly Sulawesian clade (clade 22, PP: 1). Within clade 22, continental Asian distribution (clade 87, PP: 1; clade 95, PP: 0.99), and New species assigned to section Diploclinium, but also the Guinean–Philippine distribution (clade 82, 0.97) can be continental Asian Begonia alicida C.B. Clarke (section differentiated. Alicida), Begonia brandisiana Kurz (section Reichenheimia) and Begonia demissa Craib (section Parvibegonia), form a Phylogenetics of Sulawesi Begonia grade. Species placed in sections Platycentrum and Sphenan- thera form a strongly supported clade (clade 31, PP: 1) of Sulawesi Begonia species fall into three clades including two predominantly continental Asian taxa, but also include the subclades of clade C (B. longifolia and B. aptera in clade 43, PP: most widespread Asian species B. longifolia (continental Asia, 1; Begonia aff. multangula in clade 46, PP: 1) and one poorly Sunda Shelf, Wallacea) and the more widespread Malesian supported subclade of clade D (26 species in clade 86; PP: 0.67) Begonia robusta Blume and Begonia multangula Blume (Fig. 2). Two strongly supported subclades of Begonia section (Sunda Shelf and Wallacea), as well as Begonia aptera Petermannia from Sulawesi can be differentiated: clades 87 and Blume (Sulawesi, New Guinea). 95 (Fig. 4). The following clade names (A–H) and numbers Within the strongly supported clade D (clade 49, PP: 1), two (86–111) refer to Fig. 4. Clade 87 (PP: 1) comprises two well species of the predominantly Chinese section Coelocentrum are supported subclades which are formed by species from the ) sister (clade 50, PP: 1) to the strongly supported rest of the northern arm (B1 6, PP: 1) and by species from the central ) clade (clade 51, PP: 1), which comprises four strongly eastern arm of the island (A1 3, PP: 1). Clade 95 (PP: 0.99) supported predominantly Malesian subclades: clade 54 con- comprises species which are mainly distributed in south-east, tains Malesian species of section Reichenheimia; clade 57 south-west and central Sulawesi, although some more wide- comprises Philippine Begonia species of section Diploclinium, spread species also show distributions on the central eastern and Begonia fenicis Merr., which has a distribution including arm and northern arm. A single Philippine species, Begonia both the Philippines (islands of the Taiwan–Luzon arc) and pseudolateralis Warb., which is the sister of Begonia koordersii ) Taiwan; clade 62 comprises species with a distribution in the Warb. ex L.B.Sm. & Wassh. (G1 2, PP: 1), is nested within this Sunda Shelf region assigned to section Bracteibegonia. This clade of 17 Sulawesi endemics. Subclades of two species ) clade is the sister clade to clade 64, which contains Malesian endemic to the south-western arm (C1 2, PP: 1) and of two

106 Journal of Biogeography 39, 98–113 ª 2011 Blackwell Publishing Ltd Historical biogeography of Southeast Asian Begonia

(a) (b)

Figure 4 Phylogeny of Begonia section Petermannia from Sulawesi. (a) Map of Sulawesi. Capital letters and associated superscript numbers stand for single accessions included in the analyses. Colours correspond to the colours of the clades in the chronogram (b). White bars indicate the borders of multi-taxon areas of endemism identified by Evans et al. (2003b). (b) Maximum clade credibility chronogram. Node heights indicate mean ages, node bars indicate 95% highest posterior density date ranges. Numbers at nodes represent clade names in Table 1. Broken branches indicate posterior clade probabilities < 0.95. Lower-case letters after taxon names indicate geographic distribution in Sulawesi (a–e) and the Philippines (f): a, northern arm; b, central; c, central eastern arm; d, south-western arm; e, south-eastern arm. Capital letters stand for strongly supported clades (A–H).

) species endemic to the south-eastern arm (E1 2, PP: 1) can be most wider ancestral ranges inferred at internal nodes include differentiated. only two adjacent area units and decay rapidly to single areas. Optimal ancestral area reconstructions under the DEC models are shown in Fig. 2. Molecular age estimates Continental Asia is reconstructed as the most probable ancestral area at the crown node of the Asian–Socotran clade Cucurbitales–Fagales dataset (clade 10), as well as for the stem nodes of both major clades C The maximum clade credibility chronogram resulting from the (node 14) and D (node 10). Within clade C, the reconstruc- analyses using four fossil calibrations is shown in Appendix S3. tions indicate continental Asia as most probable ancestral area The mean divergence age estimate for the Begonia crown node for most clades. Four independent dispersals to Malesia was 24 Ma, the 95% HPD date range extended from 18.2 to (between nodes 17 and 19, 31 and 32, 42 and 43, and 44 31 Ma. and 45) are supported, although reconstructions within two of these Malesian clades (the B. robusta complex clade, clade 43; and the B. longifolia clade, clade 46) are ambiguous (Table 1). Begoniaceae dataset Within clade D, only species in section Coelocentrum, which The maximum clade credibility chronogram is shown in Fig. 3. form the sister clade to the rest of the clade, show a continental Divergence age estimates are given in Table 1 and Appendix S2. Asian distribution. A range in continental Asia and the Sunda Shelf is reconstructed for the crown node of clade D (node 49), the descendant lineages of which inherit a continental Asian Ancestral area reconstructions range (Coelocentrum clade, node 50) and a Sunda Shelf range Optimal likelihood reconstructions under the dispersal– (the rest of the clade, clade 51), respectively. Within clade D, extinction–cladogenesis (DEC) model and reconstructions by several dispersal events to the Philippines and to Wallacea are Bayes-DIVA were highly congruent (Table 1; Appendix S2). inferred, although posterior clade probabilities of the respec- Differences between the results of the reconstructions are tive clades are sometimes poor (Fig. 2). Three dispersals from highlighted in Table 1 and Appendix S2. In both analyses, the Sunda Shelf region to Wallacea are supported. Two of these

Journal of Biogeography 39, 98–113 107 ª 2011 Blackwell Publishing Ltd D. C. Thomas et al. involve a clade of species assigned to section Reichenheimia in mangroves (Wikramanayake et al., 2002). These forests are (clade 54), and a third event occurred within the large section devoid of Begonia, and only relatively few Begonia species can Petermannia (clade 65). A dispersal event from the Sunda Shelf be found in other types of lowland forests in Sumatra and to the Philippines is inferred between nodes 53 and 57. Within Kalimantan (Hughes & Pullan, 2007; Fig. 1). Moreover, the clade containing all samples of eastern Malesian species palynological and geomorphological data indicate the presence assigned to section Petermannia (clade 74), dispersals from of a seasonal climate corridor across the Sunda Shelf in the Wallacea to New Guinea (between nodes 74 and 75), from Quaternary (Bird et al., 2005; Cannon et al., 2009). These Wallacea to the Philippines (between nodes 104 and 105), and edaphic and climatic conditions would certainly have provided from New Guinea to the Philippines (between nodes 79 and significant barriers to the migration of Begonia species. Hence, 82), are supported. although forest cover was more widespread, suitable habitat for colonization by Begonia species would probably have been archipelago-like in nature, and the spread of the genus across DISCUSSION the Sunda Shelf would have occurred through both overland Begonia colonized the Malesian archipelago from the Asian migration and dispersal over longer distances. The Bornean mainland multiple times during the Miocene and into the species of Begonia section Petermannia in this analysis do not Pleistocene. This colonization was characterized by west-to- form a monophyletic clade, but fall into mixed clades with east dispersal and massive island-endemic radiations. Phylo- species from Sumatra (clades 68 and 70, Fig. 2), indicating genetic data and molecular divergence age estimates indicate potential dispersal or vicariance events. A wider sample of that Begonia initially diversified in Africa, and subsequently Begonia section Petermannia is required to better understand dispersed independently to the New World and Asia in the the colonization of the Sunda Shelf by this group. Miocene (Plana et al., 2004; Goodall-Copestake, 2005; Goo- dall-Copestake et al., 2010). Either long-distance dispersal or Colonization of central and eastern Malesia overland dispersal via an Arabian corridor to Western Asia during a more mesic period than at present has been The inferred west-to-east trend of dispersal between continen- hypothesized to explain the migration of Begonia from Africa tal Asia and Malesia as well as within Malesia is consistent with to Asia (Plana et al., 2004; Goodall-Copestake, 2005; Goodall- reconstructions of the geological history of the region. While Copestake et al., 2010). Congruent with these scenarios, the substantial parts of western Malesia were emergent throughout results presented here show that Socotran–Asian Begonia the Cenozoic, substantial land east of Wallace’s Line, in initially diversified in continental Asia in the Miocene and Wallacea and New Guinea, emerged only during the late subsequently dispersed into Malesia. However, ancestral area Miocene and Pliocene (Hall, 2001, 2009). The divergence ages reconstruction at the deepest nodes of the presented tree suggest that once substantial land became available in Wall- remain largely ambiguous (Fig. 2). acea, at least six Begonia lineages (in sections Parvibegonia, Petermannia, Platycentrum s.l. and Reichenheimia) indepen- dently dispersed to the region east of Wallace’s Line from the Early colonization of the Sunda Shelf late Miocene onwards. The monophyly of a large eastern Dispersal from continental Asia to the Sunda Shelf region can Malesian clade, which comprises all samples of Begonia section potentially be explained by overland dispersal. The region has Petermannia from Sulawesi, New Guinea and the Philippines, been colonized by five lineages, with three leading to consid- shows that, despite massive autochtonous diversifications on erable localized radiations (clade 33, Begonia section Platycen- the major islands and island groups in eastern Malesia, there is trum, 23 species in Peninsular Malaysia; clade 55, Begonia no indication of dispersal from Wallacea back to the Sunda section Reichenheimia, c. 20 species in Sumatra; clade 66, Shelf region. One explanation for this pattern may be niche Begonia section Petermannia, c. 100 species in Sumatra and pre-emption (Silvertown, 2004; Silvertown et al., 2005), the Borneo). Direct land connections across continental Asia and filling of niche space by the island endemic radiations, which the Sunda Shelf existed throughout most of the Miocene and may have inhibited the establishment of later, closely related onwards, and these were probably forest-covered for long arrivals (species in section Petermannia). Similarly, simple phases (Hall, 2001, 2009; Morley, 2007). Large parts of the colonizations of Eastern Malesia from Western Malesia with Sunda Shelf between present-day Sumatra and Borneo would substantial subsequent species diversification but without or have been covered by lowland forest during eustatic sea-level very infrequent subsequent back-dispersal have been inferred lows in the Quaternary (Cannon et al., 2009). However, the for the species-rich and widespread Malesian fanged frogs edaphic evolution of the soils after exposure and the types of (Limnonectes, Evans et al., 2003a) and Pseuduvaria (Annona- forests they would have supported are very poorly understood. ceae; Su & Saunders, 2009). Reconstructions of the historical It is unlikely that these lowland forests would have provided biogeography of (; Muellner et al., 2008, hospitable habitats for Begonia. The Sundaland heath- and 2009) show a similar sequence, with an origin in western peat-swamp forests, which cover extensive parts of south Malesia and multiple dispersal events from the Sunda Shelf Borneo, grow on peat layers and white-sand soils that resulted region to Sulawesi and New Guinea in the late Miocene and partly from the accumulation of sediments and organic matter Pliocene. The ancestral area reconstructions of clades contain-

108 Journal of Biogeography 39, 98–113 ª 2011 Blackwell Publishing Ltd Historical biogeography of Southeast Asian Begonia ing fleshy-fruited, putatively zoochorous, widespread Begonia both the West Sulawesi fragment and the Australian conti- species (in the B. longifolia and B. robusta complexes) nental microfragments (Banggai-Sula, Buton-Tukang Besi), presented here are largely ambiguous, and phylogeographic which amalgamated to form parts of Sulawesi, were submerged approaches based on data of multiple populations are needed during long phases of the migration to their current position to clarify the frequency and directionality of dispersal between (Hall, 2001, 2009). Thus it is highly unlikely that tectonic western and eastern Malesia in these groups. migration was a factor in the dispersal of Begonia in Malesia. The period from the late Miocene onwards seems to have Within the clade of Sulawesi species assigned to Begonia offered the best opportunities for dispersal to and across section Petermannia (Fig. 3), two patterns are notable. Firstly, Wallacea to New Guinea, as substantial land masses that there is no indication of exchange between neighbouring emerged in Sulawesi and New Guinea and the emergence of islands, except for the presence of the Philippine B. pseudolat- volcanic islands along the Sunda Arc, the Banda Arc and the eralis nested within this clade. This species belongs to a Halmahera Arc offered potential avenues for dispersal by taxonomically difficult species complex, which also includes island-hopping (Hall, 2001, 2009). New Guinea is recon- B. koordersii and Begonia strictipetiolaris Irmsch. (Sulawesi), structed as the ancestral area for a clade comprising three B. rieckei (Sulawesi, Moluccas, New Guinea), Begonia brachy- Philippine Begonia species assigned to section Petermannia, botrys Merr. & L.M.Perry (New Guinea and surrounding indicating dispersal, against the general trend, across Wallace’s islands), and Begonia peekelii Irmsch. (Bismarck Archipelago) Line from east to west in the Pliocene. Biotic exchange between (Hughes, 2008). These taxa may be best considered as one the Philippines and New Guinea in the Pliocene may have been widespread species, as they show only minor morphological facilitated by the emergence of volcanic islands of the differences (Hughes, 2008). The presence of B. pseudolateralis Halmahera Arc. Dispersal of Pseuduvaria between the Philip- nested within a clade of Sulawesi endemics shows that this pines and New Guinea in the Pliocene was supported in the species complex probably originated from Sulawesi ancestors in analyses by Su & Saunders (2009), and putative genealogical the Pliocene or Pleistocene, and subsequently became wide- connections of other taxa from northern New Guinea, spread east of Huxley’s Line (Sulawesi, Philippines, Moluccas, Halmahera and the southern Philippines have been described New Guinea). Interestingly, this is one of the few taxa in Begonia as the Melanesian arc track (Michaux, 2001; Ladiges et al., section Petermannia possessing fleshy fruit, but nothing is 2003). Other indicated geographic origins of Philippine known about its dispersal ecology. Secondly, the clade of Begonia include the Sunda Shelf (for the clade of Philippine Sulawesi species assigned to Begonia section Petermannia species assigned to section Diploclinium; clade 57, Fig. 1), and exhibits considerable geographic structure, and every major Sulawesi (for the Begonia rieckei Warb. complex; clade 105, peninsula (north, east, south-west and south-east) shows clades Fig. 1). These relationships evoke long-distance dispersal or of endemics. In general, geographic proximity seems to be island-hopping routes via Palawan or the Sulu Archipelago highly correlated with the observed phylogenetic patterns. between Borneo and the Philippines and the Sangihe Arc Several studies indicate a geographic partitioning of the between Sulawesi and the Philippines (Jones & Kennedy, distribution of Sulawesi endemics, and the distributions of taxa 2008). in several of the recovered Begonia clades are largely congruent with areas of endemism identified for toads (Evans et al., 2003b), fanged frogs (Evans et al., 2003a), tarsiers (Shekelle The diversification of Sulawesi Begonia et al., 2010) and macaques (Evans et al., 2003b) (Fig. 3). The The Indonesian island of Sulawesi is of particular biogeo- archipelago-like character of the different Sulawesi fragments graphic interest because of its central position in Malesia and prior to their amalgamation, and eustatic sea-level changes its geologically composite character, resulting from the amal- during the Pleistocene, have been hypothesized to have played gamation of Eurasian and Australian continental fragments, key roles in shaping these modern patterns of diversity (Evans ophiolites and elements of volcanic origin (Moss & Wilson, et al., 2003b; Shekelle & Leksono, 2004; Merker et al., 2009). 1998; Hall, 2002, 2009). The phylogeny of Sulawesi Begonia However, Bridle et al. (2004) cautioned that apparent patterns presented here provides evidence for three independent of geographic partitioning on Sulawesi can reflect simple colonizations of the island in the late Miocene (in Begonia isolation by distance or adaptation to local ecological condi- section Petermannia) and the Pliocene to Pleistocene (in the tions. These explanations may be particularly applicable to B. longifolia and B. robusta complexes), only the first of which Begonia, a genus including many microendemics with limited resulted in a large radiation (Hughes, 2008; Thomas et al., dispersal capabilities (Hughes & Hollingsworth, 2008). How- 2011b). Tectonic migration (rafting on continental microfrag- ever, palaeogeographic reconstructions indicate that substan- ments) has been proposed as mechanism aiding dispersal into tial parts of the northern peninsula of Sulawesi were an and within Malesia (Morley, 2000; Ladiges et al., 2003; archipelago of volcanic islands separated from each other and Michaux, 2010). However, the molecular divergence age the rest of Sulawesi by large marine gaps in the Pliocene (Moss estimates indicate that the rifting of a West Sulawesi fragment & Wilson, 1998; Hall, 2009). Moreover, oceanic inundations from the eastern margin of Borneo in the Eocene long split the northern peninsula during phases of sea level high preceded the diversification of Begonia within Malesia (Hall, stands in the Pleistocene (Whitten et al., 2002). This isolation 2001, 2009). Palaeogeographic reconstructions suggest that and frequent habitat fragmentation and amalgamation may

Journal of Biogeography 39, 98–113 109 ª 2011 Blackwell Publishing Ltd D. C. Thomas et al. explain the distinctness of the north-eastern Sulawesi Begonia vermeulenii D.C. Thomas from Tanah Toraja in south-west clade and the strong faunal boundaries observed at the Isthmus central Sulawesi; and Begonia watuwilensis Girm. & Wiriad. of Gorontalo (Evans et al., 2003b; Shekelle et al., 2010). The and Begonia flacca Irmsch. from the south-eastern arm Togian Islands, located between the eastern central arm and (Fig. 4). Based on these patterns, and the evidence for weakly the northern peninsula of Sulawesi, were more extensive, and developed mechanisms to maintain species cohesion in possibly connected to the eastern central Peninsula during fragmented habitats in Begonia from population genetic Pliocene and Pleistocene oceanic regressions (Froehlich & studies (Matolweni et al., 2000; Hughes et al., 2003; Hughes Supriatna, 1996), but a full land bridge never formed (Voris, & Hollingsworth, 2008), it can be hypothesized that the 2000). A route via this potential shortcut for dispersal from formation of topographical heterogeneity and suitable micro- north to central eastern Sulawesi may explain the close habitats by orogenesis and associated microallopatry were phylogenetic relationships between Begonia clades from the crucial factors in the autochthonous Begonia radiations on the northern and the central eastern arm. However, the lack of major eastern Malesian islands. Cyclic vicariance by frequent samples from the western parts of the north arm and north- habitat and range fragmentations and amalgamations by western central Sulawesi does not allow us to identify the climate and sea-level fluctuations during the Pleistocene may precise borders of the distribution of this clade, which seems to have accelerated these radiations, resulting in the remarkable have no overlap with the second major Sulawesi clade except Begonia species diversity found in Malesia today. for the distribution of the widespread B. koordersii. Long isolation until the Pliocene or Pleistocene has also been ACKNOWLEDGEMENTS reconstructed for the south-western peninsula of Sulawesi, and frequent oceanic intrusion into the Tempe Depression peri- We are grateful to E.B. Walujo (LIPI, Cibinong Science Centre, odically isolated the south-west arm from central Sulawesi BO), and M. Siregar and Hartutiningsih (LIPI, Bogor Botanic during the Pleistocene and Holocene (Moss & Wilson, 1998; Gardens), for their support of our expeditions in Indonesia; to Whitten et al., 2002; Hall, 2009), which may have resulted in K. Armstrong, D. Girmansyah, M. Newman, A. Poulsen and the formation of endemic clades of Begonia and other biota in H. Wiriadinata for providing plant material; to the horticul- the south-west (Evans et al., 2003b; Shekelle et al., 2010). The ture staff at Bali Botanic Garden, Bogor Botanic Gardens, the palaeogeography of Sulawesi clearly imposed constraints on Royal Botanic Garden Edinburgh and the Royal Botanic the geographic diversification of its biota, and processes such Gardens Glasgow for their expert care of the Begonia collec- as dispersal to, and isolation on, islands of the proto-Sulawesi tions; to the curators of A, B, BM, BO, CEB, E, L, K, SING and archipelago may explain some of the observed geographic WAG for allowing us access to herbarium material and living structure at the deeper nodes of the clade containing species of collections; and to A.N. Muellner, S.S. Renner, R.M.K. Begonia section Petermannia from Sulawesi. Saunders and an anonymous referee for their constructive comments on the manuscript. This research would not have been possible without the support of the Indonesian Ministry Drivers of Begonia diversification in Malesia of Research and Technology (RISTEK) and Direktorat Jenderal The inferred timing of the major diversification of section Perlindungan Hutan dan Konservasi (DITJET PHKA). The Petermannia (> 270 species) in the Pliocene and Pleistocene funding of the first author’s studies by the M.L. MacIntyre coincides with rapid orogenesis on Sulawesi and New Guinea Trust, and support of two expeditions to Sulawesi in 2008 and (Moss & Wilson, 1998; Hall, 2009), as well as pronounced sea- 2009 by the Royal Horticultural Society, the Stanley Smith level and climate fluctuations and associated shifts in forest (UK) Horticultural Trust and the Systematics Association is distributions (Cannon et al., 2009; Woodruff, 2010). 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Appendix S2 Clade support, divergence age estimates and & Swensen, S.M. (2006) Phylogenetic relationships of Asian ancestral area reconstructions for Asian Begonia. Begonia, with an emphasis on the evolution of rain-ballist Appendix S3 Maximum clade credibility chronogram: Cuc- and animal dispersal mechanisms in sections Platycentrum, urbitales–Fagales dataset. Sphenanthera and Leprosae. Systematic Botany, 31, 327–336. Thomas, D.C. (2010) Phylogenetics and historical biogeography As a service to our authors and readers, this journal provides of Southeast Asian Begonia (Begoniaceae). PhD Thesis, supporting information supplied by the authors. Such mate- University of Glasgow, UK. Available at: http://theses.gla. rials are peer-reviewed and may be reorganized for online ac.uk/1997. delivery, but are not copy-edited or typeset. Technical support Thomas,D.C., Hughes,M.,Phutthai,T.,Rajbhandary,S.,Rubite, issues arising from supporting information (other than R., Ardi, W.H. & Richardson, J.E. (2011a) A non-coding missing files) should be addressed to the authors. plastid DNA phylogeny of Asian Begonia (Begoniaceae): evi- dence for morphological homoplasy and sectional polyphyly. Molecular Phylogenetics and Evolution, 60, 428–444. BIOSKETCH Thomas, D.C., Ardi, W.H. & Hughes, M. (2011b) Nine new species of Begonia (Begoniaceae) from South and West Daniel C. Thomas completed his doctorate under the Sulawesi, Indonesia. Edinburgh Journal of Botany, 68, 225– auspices of the Royal Botanic Garden Edinburgh and the 255. University of Glasgow in 2010, working on the systematics, Voris, H.K. (2000) Maps of Pleistocene sea levels in Southeast character evolution and historical biogeography of Asian Asia: shorelines, river systems and time durations. Journal of Begonia. He is currently a postdoctoral fellow at the University Biogeography, 27, 1153–1167. of Hong Kong. His main research interests focus on the Wallace, A.R. (1860) On the zoological geography of the Malay historical biogeography, evolution and systematics of Annon- Archipelago. Journal of the Proceedings of the Linnean Society: aceae, Begoniaceae and Boraginaceae. Zoology, 4, 172–184. Webb, C.O. & Ree, R.H. (in press) Historical biogeography The main research interest of the team of authors is centred on inference in Malesia. Biotic evolution and environmental the systematics, evolution and biogeography of flowering change in Southeast Asia (ed. by D. Gower and L. Ruber). plants, especially pantropically distributed families such as Cambridge University Press, Cambridge. Annonaceae, Begoniaceae and Sapotaceae. van Welzen, P.C. & Slik, J.W.F. (2009) Patterns in species Author contributions: D.C.T., M.H. and J.E.R. conceived the richness and composition of plant families in the Malay ideas; D.C.T., M.H., R.R., S.R., T.P. and W.H.A. collected Archipelago. Blumea, 54, 166–171. material and contributed data; D.C.T. collected and analysed van Welzen, P.C., Slik, J.W.F. & Alahuhta, J. (2005) Plant the data; D.C.T., M.H. and J.E.R. led the writing; all authors distribution patterns and plate tectonics in Malesia. Kon- made significant comments on and improvements to the gelige Danske Videnskabernes Selskab Biologiske Skrifter, 55, manuscript. 199–217. Whitten, T., Mustafa, M. & Henderson, G.S. (2002) The ecol- ogy of Sulawesi. Periplus, Jakarta. Editor: Mark Carine

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