Journal of Biogeography (J. Biogeogr.) (2011) 38, 517–530

ORIGINAL Northern Hemisphere origin, transoceanic ARTICLE dispersal, and diversification of Ranunculeae DC. () 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 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 , 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, 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 (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 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; , Hoot Taxon sampling et al., 2008). Phylogenetic relationships and 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 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, , 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 and , 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 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 this genus (Paun et al., 2005; Hoffmann et al., 2010). However, for the (Fig. 2a, asterisks). Altogether 150 new sequences of a nuclear

518 Journal of Biogeography 38, 517–530 ª 2010 Blackwell Publishing Ltd Northern Hemisphere origin and transoceanic dispersal of Ranunculeae

(a) (b)

Arcteranthis (1/1) Callianthemoides (1/1)

Beckwithia (1/1) Ceratocephala (2/4)

(c) (d)

Coptidium (2/2) (2/5)

Cyrtorhyncha (1/1) (2/11)

(e) (f)

Hamadryas (1/6)

Krapfia (1/8) Laccopetalum (1/1)

Kumlienia (1/1) Myosurus (1/15)

(g) (h)

Oxygraphis (1/8)

Paroxygraphis (0/1) Ranunculus (69/ca. 630)

Peltocalathos (1/1) Trautvetteria (1/3)

Figure 1 Extant distribution of Ranunculeae. Genera are ordered alphabetically. The number of species used in this study/total numbers of species are given in parentheses.

DNA extraction, amplification and sequencing marker [internal transcribed spacer (ITS) of the nuclear ribosomal DNA] and chloroplast markers (matK/trnK and Total genomic DNA from silica-dried or herbarium material psbJ–petA) were obtained from new samples and combined was extracted using a modified cetyl trimethyl ammonium with data from previous studies (Ho¨randl et al., 2005; Paun bromide (CTAB) technique (Doyle & Doyle, 1987). For et al., 2005; Gehrke & Linder, 2009; Hoffmann et al., 2010). amplification and sequencing of the nuclear ribosomal (nr) Voucher information and GenBank accession numbers are ITS, matK/trnK and psbJ–petA regions we used the protocols of provided in Appendix S2. Ho¨randl et al. (2005), Paun et al. (2005) and Shaw et al.

Journal of Biogeography 38, 517–530 519 ª 2010 Blackwell Publishing Ltd K. Emadzade and E. Ho¨ randl

(b) (a)

Figure 2 Temporal diversification of Ranunculeae. (a) Maximum clade credibility chronogram of Ranunculeae, with nodes represented by their mean ages estimated using the matK data set based on beast analyses. Numbers in circles refer to nodes of the tree in Fig. 3. Nodes labelled with an asterisk refer to the positions of calibration points used, branches labelled with arrows show branches with posterior probability less than 0.9. The geological time scale (Gradstein et al., 2004) is shown at the bottom: Plio., Pliocene; Plei., Pleistocene. (b) Historical biogeography of Ranunculeae. The maps show the position of plates in different geological periods (based on Hay et al., 1999) and ancestral areas inferred from Fig. 3. Solid arrows depict predominant dispersal events. Numbers in circles refer to nodes of the tree in Fig. 3. Dashed arrows indicate hypothetical recent dispersal events within genera.

520 Journal of Biogeography 38, 517–530 ª 2010 Blackwell Publishing Ltd Northern Hemisphere origin and transoceanic dispersal of Ranunculeae

(2007), respectively. Sequence alignment was performed as 4. The age of an oceanic island is expected to be the maximum described in Emadzade et al. (2010). age for the split of island endemics from their closest relatives if it can be assumed that speciation has occurred on that island. This situation can be assumed if the history of the archipelago Molecular age estimation was not complicated by, for example, sunken islands, and if We used the Bayesian relaxed clock methodology as speciation was not accompanied by major radiations on the implemented in beast v.1.4.5 to calibrate a temporal archipelago. This assumption applies to Ranunculus caprarum, framework of the phylogeny (Drummond & Rambaut, the only endemic buttercup of the Juan Ferna´ndez Archipel- 2007). beast uses Bayesian inference and a Markov chain ago, occurring only on Masafuera (one of the three islands, Monte Carlo (MCMC) analysis to reconstruct branch 1–2 Myr old; Stuessy et al., 1984, 2006). The geological history lengths, tree topology and dates. It allows the user to of the archipelago is not complex (Stuessy et al., 1984), and optimize distribution models and prior distribution rather anagenetic speciation of endemics from mainland ancestors is than assigning to point estimates, for example a prior predominant in the Juan Ferna´ndez Islands (Stuessy et al., distribution defined in terms of its mean and standard 2006). Therefore, we use the age of the island as the maximum deviation (Drummond et al., 2006). age for the respective node that splits R. caprarum from its We used matK as a maternally inherited gene rather than mainland relative. We used uniform prior distributions for this ITS or combined sequences for age estimates in general to point in our analysis. Since we use this calibration point for the avoid the problems of recombination and concerted evolu- dating of ectopic events, we avoid circular reasoning for tion in the nuclear marker. A separate analysis of ITS data biogeographical hypotheses. only revealed a tree with low resolution, as in previous A normal distribution was used for the age of the split of studies (Ho¨randl et al., 2005; Emadzade et al., 2010). More- Ranunculus and Clematis and R. carpaticola and R. notabilis, over, matK is more conserved over the level of evolutionary with the mean 46.6 and 0.914 Ma, respectively. The standard divergence studied. Because of a high percentage of missing deviation was set to contain the lower and higher boundaries data in the selected region, we excluded Arcteranthis from of the 95% highest posterior density values. this data set. We calibrated our phylogenetic tree with The partitioned beast.xml input file was created with information obtained from three different principal sources: BEAUti v.1.4.5 (Drummond & Rambaut, 2007). The matK geological events, the fossil record and estimated nodes from data set was tested using MrModeltest 2.2 (Nylander, 2004) other molecular dating studies. This strategy is expected to to determine the sequence evolution model that best described minimize errors from inaccurate calibration (Forest, 2009). the present data. A GTR+I+C substitution model and the Uncertainty in fossil calibration is a source of error in the gamma distribution were modelled with four categories. dating (Gandolfo et al., 2008). Four nodes of the tree were A Yule prior on branching rates was employed and four used for calibration. independent MCMC analyses were each run for 10,000,000 1. The age of the split of Ranunculus (Ranunculeae) and generations, sampling every 1000 generations. Convergence Clematis (Anemoneae) estimated as 46.6 Ma, based on a fossil- and acceptable mixing of the sampled parameters was checked calibrated study of (Anderson et al., 2005). using the program Tracer 1.2 (Rambaut & Drummond, 2. Within genera, one node of the tree was calibrated using 2003). Taxon subsets were specified for each clade of interest, records of fossil achenes of Myosurus from the Oligocene (Mai allowing recording of the mean time to the most recent & Walter, 1978). Achenes of Myosurus have such unique common ancestor (TMRCA), the 95% highest posterior morphological and anatomical features within the tribe density (HPD) intervals and the effective sample size (ESS). (Tamura, 1995; Emadzade et al., 2010) that the fossil deter- After discarding the burn-in steps, the four runs were mination of the genus can be regarded as reliable. In contrast, combined using TreeAnnotator (Rambaut & Drummond, other records of fossil , and of Ranunculeae 2002) to obtain an estimate of the posterior probability (Martin-Closas, 2003; Kalis et al., 2006) cannot be reliably distribution of the divergence dates of the ancestral nodes. assigned to certain nodes because of the great intra- and inter- generic variation of these characters (Anderson et al., 2005; Optimization of ancestral distributions Emadzade et al., 2010). Since a fossil represents a minimum age, it is preferable to use the upper boundary of the geological To infer vicariance and dispersal events three methods were division in a molecular dating study as a minimum constraint used: a parsimony-based method (diva v.1.1; Ronquist, 1997), (Forest, 2009). Thus, we used a minimum age for Myosurus of a maximum likelihood-based method (Lagrange v.2.0.1; Ree 23 Ma with an exponential prior distribution with an offset of & Smith, 2008) and Fitch parsimony optimization imple- 23.0 Myr and a mean of 1.0 Myr. mented in Mesquite v.2.6 (Maddison & Maddison, 2009). 3. Within Ranunculus, we further used the divergence time Dispersal–vicariance analysis optimizes distributions for between Ranunculus carpaticola and Ranunculus notabilis each node of the tree by minimizing the number of assumed (0.914 Ma) according to Nei’s (1975) genetic distance, which dispersals and extinctions and favouring the vicariance events has been calculated from allelic frequencies of allozymes (Ronquist, 1996, 1997). The diva program reconstructs (Ho¨randl, 2004). widespread ancestral distributions, restricting them to single

Journal of Biogeography 38, 517–530 521 ª 2010 Blackwell Publishing Ltd K. Emadzade and E. Ho¨ randl areas. Moreover, because allopatric speciation by vicariance is Maddison, 2009). Fitch parsimony calculates the most parsi- the null model in diva, vicariance and range division would monious ancestral states at the nodes of the tree assuming one always be the preferred explanation if ancestors are widespread step per state change. In general the FPO assumes that (Sanmartı´n, 2006). To avoid inferring a widespread ancestor at geographical distributions are the result of dispersal events the root because of the presence of widespread taxa (e.g. rather than vicariance. Ranunculus and Myosurus) a limit of three areas was set For diva and Mesquite, we performed a parsimony (maxareas = 3) in diva (Ronquist, 1997), which reflects the analysis as described in Emadzade et al. (2010) with paup* maximum number of areas for 15 of the 17 genera used (see v.4.0b8 (Swofford, 2002), on the combined sequence data of 89 Fig. 3). Additionally, an analysis with unconstrained areas was taxa (Appendix S1). For Lagrange an ultrametric tree is performed. needed, which we computed based on a Bayesian analysis by A newly developed method represents a significant advance using the program beast v.1.4.5 (Drummond & Rambaut, in biogeographical methodology by using a maximum likeli- 2007) with the same data set (not shown). Both tree topologies hood (ML) statistical model (Lagrange; Ree & Smith, 2008). showed congruence. Then we reduced the number of species of This method includes information from biological and biotic each genus to one and used this data set in diva,Mesquite factors by calculating the likelihood of biogeographical routes and Lagrange for optimization of ancestral areas. and areas occupied by the most recent common ancestor for a Distribution data were compiled from the literature (e.g. given phylogenetic tree topology and the present distributions Ovczinnikov, 1937; Meusel et al., 1965; Lourteig, 1984; Iran- of taxa. For example, the rate of dispersal and local extinction, shahr et al., 1992; Tamura, 1995; Whittemore, 1997; Wencai & the time of lineage survival and the probabilities of dispersal Gilbert, 2001). Areas were delimited by continental divisions between geographical ranges at different geological times (Ree as: Africa (AF, excluding the Mediterranean coast), Asia (ASI), et al., 2005) can all be incorporated in the reconstruction. Europe (EUR; delimitation against Asia followed Tutin et al., We further reconstructed ancestral states based on Fitch 1993), North America (NA), South America (SA) and Oceania parsimony optimization (FPO) using Mesquite (Maddison & (OCE, including Indonesia and New Guinea). The records of

Ranunculus ASI, EUR, NA, SA, AF, OCE * SA 4 Krapfia 100/1.0 EUR/ SA,EUR/ ASI/ SA,ASI 100/1.0 SA 3 SA Laccopetalum 80/1.0

I

100/1.0 ASI, EUR, OCE e EUR/ ASI 2 Ceratocephala d

a

l EUR/ ASI 5 C Myosurus ASI, EUR, NA, SA, OCE 100/1.0

100/0.9 ASI, EUR, NA Coptidium EUR/ ASI 6 ASI, EU Ficaria

NA EUR, NA/ ASI,NA NA Arcteranthis -/1.0 12 NA ASI, NA 1 11 Trautvetteria EUR,NA/ ASI,NA/ EUR,NA,ASI 10 92/1.0

ASI, NA, SA a Halerpestes - I

I

NA 8 e

d

92/1.0 a

l

Oxygraphis ASI, EUR C -/- 100/1.0 Beckwithia NA NA 7 NA 13 Cyrtorhyncha NA North America (NA) Africa (AF) -/- Callianthemoides SA South America (SA) Asia (ASI) SA -/1.0

b

14 SA -

Hamadryas I

All six areas I

9 -/- 15 e North Hemisphere SA, NA SA,AF d

a -/0.9 l Oceania (OCE) Peltocalathos AF C Europe (EUR) Equivocal NA

Figure 3 Biogeographical optimization of Ranunculeae performed with the software diva,Lagrange and Mesquite. This tree is based on the ITS, matK/trnK and psbJ–petA data set. Relevant nodes are numbered (in circles). Numbers listed close to branches in italics show bootstrap values ‡80% and posterior probabilities ‡0.9. The distribution of genera, as coded for biogeographical analyses, is indicated next to each taxon. Most recent common ancestors reconstructed by diva are indicated on each node. Different lines show the migration routes suggested by Lagrange. Shading shows ancestral area reconstruction under parsimony in Mesquite. Coded as stated in the figure: NA, North America; SA, South America; EUR, Europe; ASI, Asia; AF, South Africa; OCE, New Zealand, Australia. Asterisk, several combinations of areas have been optimized by diva, as presented in Table 1, node 4.

522 Journal of Biogeography 38, 517–530 ª 2010 Blackwell Publishing Ltd Northern Hemisphere origin and transoceanic dispersal of Ranunculeae

) Ceratocephala, Myosurus and Ficaria in the narrow Mediter- birth rate was 0.134 (HPD: 9.13 · 10 2 to 0.178). Values for ranean zone of Africa were coded for EUR to avoid overes- 95% HPD and the ESS of nodes of interest are presented in timates of inter-continental dispersal. The distribution of each Table 1. genus of Ranunculeae included in this analysis is shown in The chronogram based on matK sequences (Fig. 2a) illus- Figs 1 & 3. trates the crown group age of the tribe and a split between two To illustrate possible historical biogeographical scenarios for main clades (clades I and II) in the late Eocene (38.36 Ma; Ranunculeae, maps were designed to show the respective HPD: 28.64–47.07; Fig. 2a, node 1). The genera of clade I position of continental plates at different time periods using a diversified in the Oligocene and the Miocene (nodes 2–6). program provided by the Ocean Drilling Stratigraphic Net- Ranunculus diverged from its South American sisters Krapfia work (ODSN; established by GEOMAR, Research Center for and Laccopetalum in the early Miocene (21.25 Ma; HPD: Marine Geosciences, Kiel, and the Geological Institute of the 14.13–28.43; node 4). Ceratocephala split from Myosurus in the University Bremen; see http://www.odsn.de) that is based on early Miocene (22.84 Ma; HPD: 13.72–32.16, node 5), while data used by Hay et al. (1999). Ficaria separated from Coptidium in the Miocene (11.07 Ma; HPD: 4.51–18.46, node 6). The estimated age for the split of the Myosurus–Ceratocephala clade and Ranunculus (28.46 Ma; RESULTS Fig. 2a, node 3) is in good agreement with records of Anderson et al. (2005; 30 Ma). Clade II diversified in the early Miocene Divergence time estimation (19.14 Ma; HPD: 11.61–26.61, node 8). Kumlienia, from Our dating analysis reveals that the mean evolutionary rate western North America, apparently diverged from its Southern ) was 1.396 · 10 3 substitutions per site per million years Hemisphere relatives also in the early Miocene (18.71 Ma; ) ) (95% HPD: 1.052 · 10 1 to 0.779 · 10 3). The Yule process HPD: 11.10–26.33, node 9). The African genus Peltocalathos

Table 1 Results for age estimates and biogeographical analyses of Ranunculeae globally. The optimal ancestral areas at each node presented under diva and all equally optimal reconstructions are shown (separated by a slash). Under Lagrange, the ancestral areas with the highest likelihood scores and the highest probabilities among the alternatives are presented. In cases where two ranges are separated by a bar, the first area is inherited by the upper branch in Fig. 3; the second area is inherited by the lower branch.

Age estimates diva Lagrange

Unconstrained areas Constrained areas Node ESS 95% HPD (Ma) (maxareas = 6) (maxareas = 3) Split )lnL* Rel. prob.

1 158.746 28.639–47.072 EN/AN EN/AN [N|A] –45.80 0.08068 2 154.805 25.322–44.679 E/A E/A [A|A] –45.28 0.1347 3 120.632 19.654–37.063 E/SE/A/SA E/SE/A/SA [A|SEAONF] –45.58 0.1 4 119.476 14.132–28.431 S/SE/SA/SEA/SEO/SAO/ S/SE/SA/SEA/SEO/ [S|SEAONF] –44.75 0.2298 SEAO/SEN/SAN/SEAN/ SAO/SEN/SAN/SEF/SAF SEON/SAON/SEAON/SEF/ SAF/SEAF/SEOF/SAOF/ SEAOF/SENF/SANF/SEANF/ SEONF/SAONF/SEAONF 5 171.557 13.716–32.164 E/A E/A [A|A] –44.13 0.4281 6 244.512 4.512–18.456 E/A E/A [A|A] –45.06 0.1692 7 116.54 12.609–28.174 N N [N|N] –43.90 0.5363 8 130.716 11.607–26.607 N N [N|N] –43.68 0.673 9 127.849 11.1–26.326 SN SN [S|N] –43.58 0.7401 10 185,243 7.759–21.72 EN/AE/AEN EN/AE/AEN [N|A] –44.23 0.386 11 242.947 4.237–11.885 N N [N|N] –44.20 0.3983 12 N N [N|N] –54.19 0.7061 13 339.147 2.683–11.885 N N [N|N] –53.85 1.0 14 182.683 3.887–14.146 S S [S|SF] –43.91 0.5337 15 267.858 2.021–10.802 SF SF [S|F] –43.28 1.0

Nodes refer to labels in Fig. 3. ESS, effective sample size; HPD, highest posterior density intervals; Rel. prob., relative probability. Areas are coded as: A, Asia; E, Europe; F, South Africa; N, North America; O, Oceania; S, South America. *Likelihood of the two alternative biogeography models calculated with Lagrange. This node shows incongruence between the chronogram and the tree topology of biogeographical analysis due to the lack in Arcteranthis in the chronogram.

Journal of Biogeography 38, 517–530 523 ª 2010 Blackwell Publishing Ltd K. Emadzade and E. Ho¨ randl split from the Southern American Hamadryas in the late unconstrained analysis and 27 dispersals when maxareas was Miocene (6.11 Ma; HPD: 2.02–10.80; node 15). limited to 3. The first Eurasian common ancestor in clade II appeared in the Miocene (14.54 Ma; HPD: 7.76–11.89, node 10). Two DISCUSSION North American genera, Beckwithia and Cyrtorhyncha, diverged from each other in the early Miocene (6.89 Ma; The dating approach HPD: 2.68–11.89, node 13). The lack of pre-Quaternary species-specific in Ranun- culus made age calibration difficult. Records of fossil pollen Biogeographical analyses and leaves of Ranunculeae in different areas cannot be reliably Parsimony analysis of the combined data set (ITS, matK/trnK assigned (Anderson et al., 2005) to certain taxa because of the and psbJ–petA) used for dispersal–vicariance analysis (diva, great intra- and inter-generic variation of these characters; in Mesquite) revealed tree topologies congruent with the extant taxa, only achenes are characteristic for genera (Emad- Bayesian inference tree that was used for the maximum zade et al., 2010). Therefore, previous studies dated Ranuncu- likelihood method (using Lagrange). Despite the greater lus and allied genera only with the age of the split between complexity and flexibility of the maximum likelihood Ranunculus and Xanthorhiza (Paun et al., 2005; Hoffmann approach compared with parsimony-based methods (Ree et al., 2010). This dating could be improved by using et al., 2005; Kodandaramaiah, 2010), all methods overall calibration points obtained from geological events, the external revealed very similar results (Table 1). In clades without fossil record and age estimates from other molecular data, as widespread taxa (clade II), the Fitch parsimony optimization recommended by Forest (2009). The age of the split between implemented in Mesquite reconstructed almost the same Ranunculus and Clematis is based on a tree calibrated with areas as the other methods. In clade I, which includes several reliable fossils of the whole order Ranunculales widespread taxa such as Ranunculus and Myosurus,Mesquite (Anderson et al., 2005), and represents a node of sister tribes revealed equivocal areas for all nodes. in Ranunculaceae (Wang et al., 2009). Although the fossil All analyses suggest that Ranunculeae most probably origi- records of Ranunculeae have been regarded in general as nated in the Northern Hemisphere and then might have split doubtful (Anderson et al., 2005), we regard the records of into two clades by vicariance (Fig. 3, clades I and II). However, fossil achenes of Myosurus as an exception. The morphological since this node has bootstrap support of less than 50, this and anatomical features of the achenes of this genus are so biogeographical conclusion must be taken as tentative. diva peculiar (Tamura, 1995; Emadzade et al., 2010) that confusion showed that the most recent common ancestor (MRCA) of clade with any other taxon can be excluded. The fossils of this genus I occupied Europe or Asia, while the maximum likelihood provide an internal calibration point at the genus level. At the analysis (Lagrange) restricted its occurrence to Eurasia. Fitch species level, the split between R. notabilis and R. carpaticola, parsimony (implemented in Mesquite), however, reveals the two diploid sexual species of the R. auricomus group (Ho¨randl origin of this node to be equivocal (Fig. 3, node 2). All three et al., 2009), has been estimated as 0.914 Ma (Ho¨randl, 2004). analyses reconstructed the MRCA of clade II in North America This relatively young age is in accordance with an overall low (Fig. 3, node 7). Biogeographical analyses and present distribu- divergence of DNA sequence data within the respective tion of genera revealed that dispersal between continents could R. auricomus clade (Ho¨randl et al., 2005, 2009). The geological have occurred independently via different routes in different calibration with the age of the oceanic island Masafuera for the time periods such as: Eurasia to South America (Fig. 3, node split of the endemic R. caprarum from its mainland relative can 2 fi 3), North America to South America (Fig. 3, node 9 fi 14) be regarded a maximum age, since endemics from other genera and South America to Africa (Fig. 3, node 14 fi 15). on Masafuera have been estimated as slightly younger (Ruiz diva reconstructed Asia or Europe as the ancestral area of et al., 2004, based on allozyme data). the Coptidium–Ficaria clade (Eurasian distribution) and the Our age estimates refined the results of previous studies Ceratocephala–Myosurus clade; however, Lagrange revealed (Paun et al., 2005; Hoffmann et al., 2010). The values in our that the MRCA of these clades occurred only in Asia (Fig. 3, analysis mostly fall between the ages of respective nodes of the nodes 5, 6). The node separating Kumlienia from other genera two previous studies. The main difference between these of clade II-b, and the node separating Beckwithia + Cyrtorhyn- studies is the crown group age of the tribe (42 Ma in Paun cha from other genera of clade II-a are all reconstructed with et al., 2005; more than 50 Ma in Hoffmann et al., 2010; and ancestral distributions in North America under all three 28.64–47.07 Ma in the present study), which is probably due to geographical analyses. different calibrations (Anderson et al., 2005) and different Results of unconstrained and constrained diva analyses taxon sampling (Linder et al., 2005). However, all age show congruence except for node 4 (Table 1). Unconstrained estimates suggest that the diversification of the tribe took diva analysis placed the MRCA of node 4 in one of the 25 area place in the Cenozoic when the main oceanic barriers already combinations, but constrained area analysis (maxareas = 3) existed between continents (Fig. 2b). Therefore, the differences reduced the number of combinations to 10 (Table 1, node 4). in age estimates are of minor relevance for understanding Optimal reconstruction required 24 dispersal events for the inter-continental disjunctions within the Ranunculeae.

524 Journal of Biogeography 38, 517–530 ª 2010 Blackwell Publishing Ltd Northern Hemisphere origin and transoceanic dispersal of Ranunculeae

high Arctic (Fig. 1c) could be the result of recent migrations Spatio-temporal diversification of the genera after the Pleistocene glaciations (Fig. 2b-iii, arrows 6) or Our results suggest that Ranunculeae most probably originated survival of the descendants in refugia during the glaciations, in the Northern Hemisphere, which has also been inferred for e.g. in the Bering Land Bridge (BLB; Hulte´n, 1937; Abbott & other clades of Ranunculaceae (Schuettpelz et al., 2002; Brochmann, 2003). The Arctic was colonized multiple times by Schuettpelz & Hoot, 2004). The age of the crown group and species of Ranunculus s. str. (Hoffmann et al., 2010). the split into the main two clades (Fig. 3, node 1) probably Due to the wide distribution of Ranunculus (Fig. 1h), the date back to the late Eocene (38.36 Ma), which almost diva analysis (in constrained and unconstrained analyses) coincides with the break-up of the connection between revealed several possibilities for the place of occurrence of the Greenland and Europe and the opening of the North Atlantic MRCA of the Ranunculus–Krapfia–Laccopetalum clade (Fig. 3, (De Geer Bridge; Tiffney, 2000; Sanmartı´n et al., 2001). Clades node 4). The biogeography and age estimates of this large clade I and II diversified separately on both sides of the Atlantic will be discussed in a separate paper. (Fig. 2b–i). At the end of the Eocene South America and North Patterns of distribution and the history of migration routes America were not connected (Sanmartı´n & Ronquist, 2004), in clade II are less complicated than in clade I. The MRCA of and in the Southern Hemisphere the splitting up of Gondwana this clade occurred in North America in the early Miocene. had already been completed (Lomolino et al., 2006). Based on the extant distribution of Halerpestes, Oxygraphis and All biogeographical analyses suggest multiple dispersal Trautvetteria (Fig. 1d, g, h), dispersal events from North events from the Northern Hemisphere (in clade I from Eurasia America to Eurasia are likely. The similarity between the flora and in clade II from North America) to the Southern of North America and Europe and previous molecular studies Hemisphere in the late Palaeogene and early Neogene. One suggest that some exchange of taxa could have continued until of the migrations from Eurasia to the Southern Hemisphere the Miocene (Wen, 1999; Hably et al., 2000; Manos & (South America) probably happened in clade I (node 2 to 3 Donoghue, 2001). Biological and geological studies indicate and/or 3 to 4, Fig. 3), in the Oligocene and early Miocene. The that the BLB was open from the early Palaeocene and closed in most parsimonious explanation is LDD from Europe to South the late Miocene (Tiffney & Manchester, 2001). According to America (Fig. 2b-ii, arrow 2 fi 3). LDD over the Atlantic the age of the clade (c. 19 Ma, Fig. 2a), migration via the BLB Ocean has also been suggested in other families with similar or LDD across the Atlantic or Pacific is plausible (Fig. 2b-v, distributions (e.g. Wendel & Albert, 1992; Coleman et al., arrows 8 fi 10). According to the area optimization of node 2001, 2003; Tremetsberger et al., 2005). 14 (Fig. 3) as South America in all analyses, migration from Migrations from Eurasia to the Southern Hemisphere North to South America is well supported. During the (South America, New Zealand and Australia) are also inferred Miocene, South America had considerable contact with North for the Myosurus–Ceratocephala clade at two separate times America via the region of the Isthmus of Panama (Briggs, (Fig. 3, node 5). We cannot infer from our data whether the 1987). So the ancestor of clade II-b could have migrated over ancestors of these genera had already arrived in the Southern this land bridge (Fig. 2b-iii, arrow 9 fi 14). Hemisphere or whether this migration happened within A close floristic relationship between Pacific North America genera. Nevertheless, according to the age of node 5 (early and East Asia has been observed in many genera (Xiang et al., Miocene), the occurrence of some species of Myosurus and 1998; Milne & Abbott, 2002). Trautvetteria is one example of Ceratocephala endemic to New Zealand (Garnock-Jones, 1984; this transoceanic connection. Our data suggest migration of Fig. 1b, f) is explained by LDD or by island-hopping via New the MRCA of Trautvetteria from North America to Asia Guinea and Australia (Fig. 2b-iii, arrow 5). This route has been (Fig. 2b-iii, arrow 12), which supports Gray’s (1878) hypoth- suggested not only for Australian (Armstrong, 2003) and New esis. He suggested that a continuous flora existed across the Zealand (Lehnebach, 2008) species of Ranunculus, but also for BLB and the disjunction of taxa between different continents other taxa (Gunnera, Wanntorp & Wanntorp, 2003; Chenopo- could be explained by the break-up of this flora during the diaceae, Kadereit et al., 2005). Myosurus could have migrated Pleistocene glaciations. The same migration route was prob- via LDD from Australia and New Zealand to South Africa and ably also used by Halerpestes (Fig. 2b-iii, arrow 11). South America, or the other way around (Fig. 2b-iv). Alter- The closely related genera Hamadryas and Peltocalathos, natively, Myosurus could have moved from Eurasia to North endemic to South America and South Africa, respectively, are America and then to the Southern Hemisphere. The long time probably c. 6.11 Myr old (Fig. 2a). According to this age period since the early Miocene implies many possibilities for estimate, LDD from South America to South Africa is inferred, different migrations. In these genera, anthropochorous dis- while a vicariance model due to the break-up of Gondwana at persal is also likely. However, further studies including more 130–100 Ma (Lomolino et al., 2006) is not supported. taxa and biogeographical analyses within these two genera are necessary to pinpoint migration routes and biogeographical Long-distance dispersal or vicariance scenarios within this clade. The MRCA of the Coptidium–Ficaria clade occurred in The biogeographical scenarios presented here mainly suggest Eurasia during the Miocene (Fig. 3, node 6). The presence of migrations over land bridges and transoceanic dispersal rather the descendants of this clade, such as Coptidium pallasii, in the than vicariance events in the tribe. On the other hand, it

Journal of Biogeography 38, 517–530 525 ª 2010 Blackwell Publishing Ltd K. Emadzade and E. Ho¨ randl presents another example of a Northern Hemisphere origin of morphological features and LDD may be poor. In general, temperate plants followed by the expansion towards the seeds can germinate in the bodies of birds after 2 weeks Southern Hemisphere (Bell & Donoghue, 2005; Inda et al., (Proctor, 1968). Endozoochorous dispersal, i.e. in the diges- 2008). Northern Hemispheric origin and dispersal to the tive system of a vector, can be also assumed for Ranunculus s. Southern Hemisphere is supported by similar links found str. (Mu¨ller-Schneider, 1986). Moreover, local or transoceanic within other genera of Ranunculaceae (Anemone; Schuettpelz whirlwinds could carry the small and light achenes of et al., 2002; Caltha, Schuettpelz & Hoot, 2004). The break-up Ranunculi. Indeed, transfer of achenes by wind (anemoch- of Gondwana has been assumed to be the main factor ory), birds (ornithochory) and water (hydrochory) has explaining the Southern Hemisphere distribution of these been documented in species of Ranunculus s. str. (Mu¨ller- genera (Schuettpelz et al., 2002; Schuettpelz & Hoot, 2004). Schneider, 1986). However, recent molecular and phylogenetic studies on plants have rejected the break-up of Gondwana as the main factor ACKNOWLEDGEMENTS behind the modern distribution of some taxa and showed that dispersal, including transoceanic dispersal, may be more The authors are grateful to the Commission for Interdisci- effective than previously recognized (reviewed by de Queiroz, plinary Ecological Studies (KIO¨ S) of the Austrian Academy of 2005; Harbaugh et al., 2009; Schaefer et al., 2009; Renner et al., Sciences (O¨ AW) and to National Geographic for grants to E.H. 2010). and the Austrian Exchange Service (O¨ AD) for a PhD student Recent analyses revealed that the historical biogeography of grant to K.E. for financial support. We are grateful to the Northern Hemisphere (Wen, 1999, 2001; Donoghue et al., B. Gehrke, M. Ghahremanii, J.T. Johansson, C. Keener, 2001; Xiang & Soltis, 2001) and Southern Hemisphere F. Lone, G. Schneeweiss, P. Scho¨nswetter, M. Tajeddini and (Sanmartı´n & Ronquist, 2004) cannot be explained by a A. Tribsch for collecting materials, B. Gehrke and N. Tkach for simple vicariance model. Dispersal must have been a major some data from Ranunculus s. str., K. Tremetsberger for help factor generating biogeographical patterns in the Northern with the age estimates, and the curators of the herbaria of the Hemisphere. Bishop Museum in Honolulu, the Obero¨sterreichische Land- LDD of plants via seeds or propagules to oceanic islands, esmuseum in Linz, the Botanische Staatssammlung in Munich, followed by speciation, is a key factor in determining the the University of Wyoming, the University of Vienna, the richness of their flora (Wagner & Funk, 1995; Cowie & Natural History Museum in Vienna and the University of Holland, 2006; Lomolino et al., 2006). The presence of Zurich for the loan of herbarium specimens and permission to endemic species of Ranunculus on some oceanic islands, far use materials for DNA extractions. away from the continents (e.g. the Hawaii Islands, Juan Ferna´ndez Islands and Canary Islands), also indicates that REFERENCES LDD is possible in this tribe. Smith (1986) showed that only one successful LDD and establishment event needs to occur Abbott, R.J. & Brochmann, C. (2003) History and evolution of approximately every 10,000 years to explain the species the arctic flora: in the footsteps of Eric Hulte´n. Molecular richness observed in the Australasian alpine and tropic-alpine Ecology, 12, 299–313. flora. LDD does not need to be frequent or regular to be Alsos, I.G., Eidesen, P.B., Ehrich, D., Skrede, I., Westergaard, effective (Berg, 1983). K., Jacobsen, G.H., Landvik, J.Y., Taberlet, P. & Brochmann, Our data support multiple independent colonizations of the C. 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Journal of Biogeography 38, 517–530 529 ª 2010 Blackwell Publishing Ltd K. Emadzade and E. Ho¨ randl

Whittemore, A. (1997) Ranunculus. Flora of North America, Appendix S1 Maximum parsimony analysis of all taxa. Strict north of Mexico, Vol. 3 (ed. by Flora of North America consensus tree of 33 most parsimonious trees from the Committee), pp. 88–135. Oxford University Press, New combined ITS, matK/trnK and psbJ–petA data set used for York. diva and Mesquite. Wikstro¨m, N., Savolainen, V. & Chase, M.W. (2001) Evolution Appendix S2 Materials used in this study. of the angiosperms: calibrating the family tree. Proceedings of As a service to our authors and readers, this journal provides the Royal Society B: Biological Sciences, 268, 2211–2220. supporting information supplied by the authors. Such mate- Wiley, E.O. (1998) Vicariance biogeography. Annual Review of rials are peer-reviewed and may be reorganized for online Ecology and Systematics, 19, 513–542. delivery, but are not copy-edited or typeset. Technical support Winkworth, R.C., Wagstaff, S.J., Glenny, D. & Lockhart, P.J. issues arising from supporting information (other than (2005) Evolution of the New Zealand mountain flora: ori- missing files) should be addressed to the authors. gins, diversification and dispersal. Organisms Diversity and Evolution, 5, 237–247. Xiang, Q. & Soltis, D.E. (2001) Dispersal–vicariance analyses of intercontinental disjuncts: historical biogeographical impli- cations for angiosperms in the Northern Hemisphere. International Journal of Plant Sciences, 162, S29–S39. Xiang, Q., Soltis, D.E. & Soltis, P.S. (1998) The eastern Asian and eastern and western North American floristic disjunc- BIOSKETCHES tion: congruent phylogenetic patterns in seven diverse gen- era. Molecular Phylogenetics and Evolution, 10, 178–190. Khatere Emadzade’s main interests are phylogenetic anal- Ziman, S.N. & Keener, C.S. (1989) A geographical analysis of yses and biogeographical studies with a special focus on Irano- the family Ranunculaceae. Annals of the Missouri Botanical Turanian taxa. Garden, 76, 1012–1049. Elvira Ho¨ randl is interested in the phylogeny, evolution and taxonomy of Ranunculus and related genera, and in the SUPPORTING INFORMATION evolution and biogeography of apomictic plants.

Additional supporting information may be found in the online version of this article: Editor: Pauline Ladiges

530 Journal of Biogeography 38, 517–530 ª 2010 Blackwell Publishing Ltd