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Cyperaceae) Through the Southern Hemisphere 1 American Journal of Botany 100(12): 2494–2508. 2013. R ADIATION AND REPEATED TRANSOCEANIC DISPERSAL OF SCHOENEAE (CYPERACEAE) THROUGH THE SOUTHERN 1 HEMISPHERE J AN-ADRIAAN V ILJOEN 2,9 , A. MUTHAMA M UASYA 2 , R USSELL L. BARRETT 3–5 , J EREMY J. BRUHL 6 , A DELE K. GIBBS 6 , J ASPER A . S LINGSBY 7,2 , K AREN L . W ILSON 8,6 , AND G. ANTHONY V ERBOOM 2 2 Department of Biological Sciences, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa; 3 Botanic Gardens and Parks Authority, Kings Park and Botanic Garden, Fraser Avenue, West Perth, Western Australia 6005, Australia; 4 School of Plant Biology, Faculty of Natural and Agricultural Sciences, The University of Western Australia, Crawley, Western Australia 6009, Australia; 5 Western Australian Herbarium, Department of Environment and Conservation, Locked Bag 104, Bentley Delivery Centre, Western Australia 6983, Australia; 6 Botany, School of Environmental and Rural Science, University of New England, Armidale, New South Wales 2351, Australia; 7 South African Environmental Observatory Network, Fynbos Node, Private Bag X7, Rhodes Drive, Newlands 7735, South Africa; and 8 National Herbarium of New South Wales, Royal Botanic Gardens and Domain Trust, Sydney, Australia • Premise of the study: The broad austral distribution of Schoeneae is almost certainly a product of long-distance dispersal. Owing to the inadequacies of existing phylogenetic data and a lack of rigorous biogeographic analysis, relationships within the tribe remain poorly resolved and its pattern of radiation and dispersal uncertain. We employed an expanded sampling of taxa and markers and a rigorous analytic approach to address these limitations. We evaluated the roles of geography and ecology in stimulating the initial radiation of the group and its subsequent dispersal across the southern hemisphere. • Methods: A dated tree was reconstructed using reversible-jump Markov chain Monte Carlo (MCMC) with a polytomy prior and molecular dating, applied to data from two nuclear and three cpDNA regions. Ancestral areas and habitats were inferred using dispersal–extinction–cladogenesis models. • Key results: Schoeneae originated in Australia in the Paleocene. The existence of a “hard” polytomy at the base of the clade refl ects the rapid divergence of six principal lineages ca. 50 Ma, within Australia. From this ancestral area, Schoeneae have traversed the austral oceans with remarkable frequency, a total of 29 distinct dispersal events being reported here. Dispersal rates between landmasses are not explicable in terms of the geographical distances separating them. Transoceanic dispersal generally involved habitat stasis. • Conclusions: Although the role of dispersal in explaining global distribution patterns is now widely accepted, the apparent ease with which such dispersal may occur has perhaps been under-appreciated. In Schoeneae, transoceanic dispersal has been remarkably frequent, with ecological opportunity, rather than geography, being most important in dictating dispersal patterns. Key words: biogeography; Cyperaceae; dispersal–extinction–cladogenesis; habitat shift; niche conservatism; polytomy prior; Schoeneae; transoceanic dispersal. Biologists since the time of Hooker have been intrigued by the more recent evidence from fossils and molecular dating ( Sanmartín phytogeographic affi nities of Australia, southern Africa, and South and Ronquist, 2004 ; Linder et al., 2003 ; Cook and Crisp, 2005 ; America ( Hooker, 1853 ; Levyns, 1964 ; Crisci et al., 1991 ; Crisp Pirie et al., 2008 ; Sauquet et al., 2009 ) has made it clear that many et al., 1999 ; Galley and Linder, 2006 ; Moreira-Muñoz, 2007 ). Vi- plant lineages showing this disjunct distribution originated after cariance associated with the break up of Gondwana by ca. 120 Ma the break up, implicating long-distance dispersal ( Raven and ( Ali and Krause, 2011 ) was previously considered to be the leading Axelrod, 1974 ; de Queiroz, 2005 ; but see Heads, 2011 ). The cause of this pattern ( Levyns, 1964 ; Raven and Axelrod, 1974 ), but schoe noid sedges (Cyperaceae: Schoeneae) are one such group: the sedge family as a whole has a crown age of ca. 75 Ma ( Janssen and Bremer, 2004 ; Besnard et al., 2009 ), and tribe Schoeneae (over 1 Manuscript received 17 March 2013; revision accepted 25 September 450 species) is distributed throughout the southern continents, with 2013. particularly high endemism in Australia and South Africa (data The authors thank M. Britton, J. Henning, P. Musili, and R. Skelton for the from Govaerts et al., 2011 ). Verboom (2006) concluded that at sequences they generated, I. Larridon and C. Ah-Peng for plant material least fi ve transoceanic dispersal events must have taken place in from Madagascar and Mauritius, M. Donoghue and S. Smith for advice on Schoeneae over the last 40 Ma. The precise number and direction biogeographic models in Lagrange, A. Lewis and the ICTS High-Performance of these dispersal events remains unclear, however, due to incon- Cluster at UCT, as well as the CIPRES Science Gateway, for assuming some gruence between published phylogenies, incomplete resolution, of the computational burden, and B. Gehrke, an anonymous reviewer, and the associate editor, whose comments substantially improved the manuscript. and the lack of rigorous biogeographic analysis. We address these This work was funded by the National Research Foundation (RSA). issues by presenting robust phylogenetic and biogeographic recon- 9 Author for correspondence ([email protected]) structions for the tribe. Morphological classifi cation has been problematic in many doi:10.3732/ajb.1300105 clades of Cyperaceae owing to the severe reduction of fl oral American Journal of Botany 100(12): 2494–2508, 2013 ; http://www.amjbot.org/ © 2013 Botanical Society of America 2494 December 2013] VILJOEN ET AL.—SCHOENOID SEDGES: RADIATION AND TRANSOCEANIC DISPERSAL 2495 parts and the rampant convergence of traits in the family, em- limited by dispersal ability. On the other hand, they are almost phasizing the utility of molecular phylogenies in sedge system- entirely confi ned to the southern hemisphere and are most prev- atics ( Muasya et al., 1998 , 2009b ). The cpDNA phylogenies of alent on oligotrophic soils in temperate rather than tropical Verboom (2006) and Muasya et al. (2009a) and the cpDNA + zones, leading us to postulate a signifi cant role for habitat fi lter- ITS tree of Jung and Choi (2013) demonstrate that Schoeneae, ing (i.e., ecological constraints on where populations can be as defi ned by both Bruhl (1995) and Goetghebeur (1998) , is established; Endler, 1982 ; Cavender-Bares et al., 2006 ) in their not monophyletic, on account of their inclusion of Cladium , biogeographic history. Carpha , and Trianoptiles . Schoeneae sensu Goetghebeur The specifi c aims of the present study were to re-evaluate the (1998) contains fi ve further genera shown by Muasya et al. monophyly of the Schoeneae, particularly with regard to the (2009a) to fall outside the core Schoeneae clade. These are placement of the Carpha and Scleria clades, by adding nuclear Arthrostylis , Actinoschoenus , Trachystylis , Pleurostachys , and sequence data to existing chloroplast data sets and by increas- the large genus Rhynchospora , which, on the basis of cpDNA ing taxon sampling; to resolve the relationships of the principal data, belongs in a separate clade containing Cypereae and Ca- schoenoid lineages or else to evaluate whether their polytomous riceae. The Cyperaceae tree of Hinchliff and Roalson (2013) relationship is “hard”, refl ecting rapid divergence; to estimate agrees with the exclusion of these fi ve genera from Schoeneae, (taking phylogenetic uncertainty into account) the times of di- but supports the inclusion of Cladium , Carpha , and Cryptangi- vergence of the principal lineages and the timing and direc- eae in Schoeneae. Support for the monophyly of Schoeneae tionality of transoceanic dispersal events in Schoeneae; to test s.s. is also equivocal. The maximum-parsimony tree of Muasya whether differentiation of the principal schoenoid lineages co- et al. (2009a) , based on rbcL and trnL–F data, found no sup- incided with intercontinental dispersal and/or specialization to port for Schoeneae as a clade, or even for their stricter “Schoe- different habitats (i.e., whether the radiation was adaptive); and neae 1” group, which includes Carpha + Trianoptiles and to explore the roles of geography vs. habitat conservatism on Scleria. In contrast, Verboom’s (2006) Bayesian tree, based on dispersal in Schoeneae. rbcL , rps16 , and trnL–F , weakly supported the monophyly of Schoeneae excluding Carpha + Trianoptiles and Scleria (pos- terior probability [PP] = 0.96), a circumscription of Schoeneae MATERIALS AND METHODS not recovered by Muasya et al. (2009a) . This clade was recov- ered by Jung and Choi (2013) and Hinchliff and Roalson Species and marker sampling — Species were selected in such a way as to (2013) , with PP = 1.00 in the former but with very weak sup- ensure that the concatenated sequence matrix was as complete as possible and port in the latter (bootstrap proportion [BP] = 0.58). These con- that genera (or monophyletic portions of genera) were represented proportion- ally to their size while capturing their biogeographic distribution ( Table 1 ). We fl icting interpretations of the tribal limits of Schoeneae based sampled at least one taxon from each major nonschoenoid lineage of Cyper- on cpDNA data indicate the need for data from independently aceae
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