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Northern Hemisphere Origin, Transoceanic Dispersal, And Journal of Biogeography (J. Biogeogr.) (2011) 38, 517–530 ORIGINAL Northern Hemisphere origin, transoceanic ARTICLE dispersal, and diversification of Ranunculeae DC. (Ranunculaceae) in the Cenozoic Khatere Emadzade1,2 and Elvira Ho¨randl1* 1Department of Systematic and Evolutionary ABSTRACT Botany, University of Vienna, Rennweg 14, Aim The role of dispersal versus vicariance for plant distribution patterns has 1030 Vienna, Austria, 2Department of Botany, Research Institute of Plant Sciences, Ferdowsi long been disputed. We study the temporal and spatial diversification of University of Mashhad, Mashhad, Iran Ranunculeae, an almost cosmopolitan tribe comprising 19 genera, to understand the processes that have resulted in the present inter-continental disjunctions. Location All continents (except Antarctica). Methods Based on phylogenetic analyses of nuclear and chloroplast DNA sequences for 18 genera and 89 species, we develop a temporal–spatial framework for the reconstruction of the biogeographical history of Ranunculeae. To estimate divergence dates, Bayesian uncorrelated rates analyses and four calibration points derived from geological, fossil and external molecular information were applied. Parsimony-based methods for dispersal–vicariance analysis (diva and Mesquite) and a maximum likelihood-based method (Lagrange) were used for reconstructing ancestral areas. Six areas corresponding to continents were delimited. Results The reconstruction of ancestral areas is congruent in the diva and maximum likelihood-based analyses for most nodes, but Mesquite reveals equivocal results at deep nodes. Our study suggests a Northern Hemisphere origin for the Ranunculeae in the Eocene and a weakly supported vicariance event between North America and Eurasia. The Eurasian clade diversified between the early Oligocene and the late Miocene, with at least three independent migrations to the Southern Hemisphere. The North American clade diversified in the Miocene and dispersed later to Eurasia, South America and Africa. Main conclusions Ranunculeae diversified between the late Eocene and the late Miocene. During this time period, the main oceanic barriers already existed between continents and thus dispersal is the most likely explanation for the current distribution of the tribe. In the Southern Hemisphere, a vicariance model related to the break-up of Gondwana is clearly rejected. Dispersals between continents could have occurred via migration over land bridges, such as the Bering Land Bridge, or via long-distance dispersal. *Correspondence: Elvira Ho¨randl, Department of Systematic and Evolutionary Botany, Keywords University of Vienna, Rennweg 14, 1030 Vienna, Austria. Cenozoic, historical biogeography, long-distance dispersal, molecular dating, E-mail: [email protected] Ranunculeae, transoceanic dispersal, vicariance. (e.g. Wiley, 1998; de Queiroz, 2005; Waters & Craw, 2006). INTRODUCTION Molecular-based phylogenetic studies based on DNA Today it is widely accepted that disjunct distributions can be sequences and estimates of divergence times of lineages explained either by fragmentation of widespread ancestors supported the role of dispersal as a primary process shaping by vicariant (isolating) events or by dispersal across a barrier distribution patterns in both animals and plants (reviewed by ª 2010 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/jbi 517 doi:10.1111/j.1365-2699.2010.02404.x K. Emadzade and E. Ho¨ randl de Queiroz, 2005). These studies provide evidence supporting dating by Paun et al. (2005) just one external calibration, a hypothesis of transoceanic dispersal versus vicariance (Giv- namely the time period between the minimum and maximum nish & Renner, 2004; Sanmartı´n & Ronquist, 2004; de Queiroz, age of the split between Ranunculus and Xanthorhiza, was 2005). available. This calibration was based on a dating approach Widespread and species-rich plant families such as the using the angiosperm family tree, which confers some uncer- Ranunculaceae Juss. provide model systems for studying tainty on terminal nodes (Wikstro¨m et al., 2001). The distant biogeographical processes. This family has a crown age of relationship of Xanthorhiza and Ranunculus within Ranuncul- c. 75 Ma (Anderson et al., 2005). The fossil record documents aceae (Wang et al., 2009) is another source of inaccuracy. the considerable differentiation of Ranunculaceae and their Hoffmann et al. (2010) simply derived two calibration points radiation throughout the world during the Neogene in the from Paun et al. (2005). Moreover, previous age estimates for Northern Hemisphere (Ziman & Keener, 1989). Although the tribe suffered from incomplete sampling of genera and the Ziman & Keener (1989) proposed the origin of some tribes lack of internal calibration points. Therefore, the timing of within the ancient floras of eastern Asia (e.g. Anemoneae, biogeographical events has remained tentative. To get a reliable Clematideae) or in North America (e.g. Hydrastideae), they temporal framework for our biogeographical hypotheses, we emphasized that it is difficult to pinpoint the origin of some aimed to refine the divergence times within Ranunculeae by tribes such as the cosmopolitan Ranunculeae. using a new external and three additional internal calibrations, Ranunculeae DC. comprise 19 genera (Emadzade et al., and a more complete sampling of the tribe. 2010) and about 650 species (Tamura, 1995), most of which We combine here the results from molecular dating and are adapted to temperate and cold climates and occur in biogeographical analyses to provide a comprehensive hypoth- mountain regions of the world. Molecular phylogenetic studies esis of the history of Ranunculeae. The aims of this study are within Ranunculaceae suggest that this tribe is monophyletic to: (1) reconstruct divergence dates within Ranunculeae; (2) (Hoot, 1995; Johansson, 1995, 1998; Ro et al., 1997; Lehnebach determine the geographical origin for the tribe; (3) reconstruct et al., 2007; Hoot et al., 2008; Wang et al., 2009). Former the main factor(s) shaping the modern distribution of the molecular phylogenetic studies on Ranunculeae have concen- tribe, including the relative role of long-distance dispersal trated either on certain geographical areas (e.g. New Zealand, (LDD) and vicariance; and (4) identify the main migration Lockhart et al., 2001; the Mediterranean area, Paun et al., routes. 2005; the Southern Hemisphere, Lehnebach, 2008; Africa, Gehrke & Linder, 2009; the Arctic, Hoffmann et al., 2010) or MATERIALS AND METHODS certain genera of the tribe (e.g. Ranunculus,Ho¨randl et al., 2005; Laccopetalum, Lehnebach et al., 2007; Hamadryas, Hoot Taxon sampling et al., 2008). Phylogenetic relationships and taxonomy of genera have been established based on molecular and mor- We sampled 89 taxa, representing 18 of the 19 genera phological data (Emadzade et al., 2010). However, a complete (Emadzade et al., 2010) included in the Ranunculeae. The biogeographical study of all genera of the tribe is still lacking. number of species sampled and the number of species in total The distribution patterns of this tribe provide a model is given for each genus in Fig. 1. Eight genera were sampled system for studying vicariance versus dispersal. Ranunculus is completely; for the others our sampling of species aimed to the only genus distributed on all continents (Fig. 1h). In cover the distribution range of the genus. For the large genus contrast, most other genera in this tribe have very restricted Ranunculus s. str., at least two species were studied from each distributions, and the monotypic genera are endemic to small of the clades and subclades identified in previous studies areas, e.g. Arcteranthis, Beckwithia, Cyrtorhyncha and Kumlie- (Ho¨randl et al., 2005; Paun et al., 2005; Hoffmann et al., nia (North America; Fig. 1a, c, e), Callianthemoides and 2010; Emadzade et al., submitted). Only the monotypic genus Laccopetalum (South America; Fig. 1b, f), Paroxygraphis (Asia; Paroxygraphis, endemic to the Himalayas, was not included Fig. 1g) and Peltocalathos (South Africa; Fig. 1g). Some small because material was not available. For reconstruction of the genera, such as Ceratocephala and Myosurus, are mainly phylogeny of the tribe we used Anemone and Isopyrum as distributed in the Northern Hemisphere (Fig. 1b, f), but some outgroup taxa and 89 species of Ranunculeae for a maximum species occur in the Southern Hemisphere (Tamura, 1995). parsimony analysis of the combined data set as in Emadzade Trautvetteria has a disjunct distribution in eastern Asia and et al. (2010) (see Appendix S1 in Supporting Information). eastern and western North America (Fig. 1h). The species of To improve the external calibration for age estimates (see this genus have been considered as relicts of the Cenozoic below), we used two outgroup taxa from two different (Tertiary) temperate flora (Thorne, 1973). Interestingly, some subgenera of Clematis (Clematis ganpiniana and Clematis of the closely related genera in Ranunculeae, e.g. Callianthe- patens; Wencai & Gilbert, 2001) from Anemoneae, the sister moides, Hamadryas and Peltocalathos, occur on different tribe to Ranunculeae (Wang et al., 2009), and 86 taxa of continents (Fig. 1b, e). Ranunculeae for Bayesian analysis (see below). We included Previous age estimates based on molecular data suggested 68 species of Ranunculus for age estimates because two that the origin of Ranunculeae dates back to the mid Eocene internal calibration points were available within
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