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West to East Dispersal and Subsequent Rapid Diversification of The Journal of Biogeography (J. Biogeogr.) (2012) 39, 98–113 ORIGINAL West to east dispersal and subsequent ARTICLE rapid diversification of the mega-diverse genus Begonia (Begoniaceae) 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 species). 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, Cucurbitales 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 plants 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 AreasArea 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.
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