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. 2013 Mar 10;111(5):873–886. doi: 10.1093/aob/mct053

Post-Boreotropical dispersals explain the pantropical disjunction in Paederia (Rubiaceae)

Ze-Long Nie 1, Tao Deng 1, Ying Meng 1,2, Hang Sun 1,*, Jun Wen 3,*
PMCID: PMC3631337  PMID: 23478944

Abstract

Background and Aims

Pantropical intercontinental disjunction is a common biogeographical pattern in flowering plants exhibiting a discontinuous distribution primarily in tropical Asia, Africa and the Americas. Only a few plant groups with this pattern have been investigated at the generic level with molecular phylogenetic and biogeographical methods. Paederia (Rubiaceae) is a pantropical genus of 31 species of woody lianas, with the greatest species diversity in continental Asia and Madagascar and only two species from tropical America. The aim of this study was to reconstruct the biogeographical history of Paederia based on phylogenetic analyses to explore how the genus attained its pantropical distribution.

Methods

Maximum parsimony and Bayesian inference were used for phylogenetic analyses using sequences of five plastid markers (the rbcL gene, rps16 intron, trnT-F region, atpB-rbcL spacer and psbA-trnH spacer). Biogeographical inferences were based on a Bayesian uncorrelated lognormal relaxed molecular clock together with both Bayesian and likelihood ancestral area reconstructions.

Key Results

The data suggest an early diverged Asian lineage sister to the clade of the remaining species consisting of a predominantly Asian sub-clade and a primarily Malagasy sub-clade. Paederia is inferred to have originated in the Oligocene in tropical continental Asia. It then reached Africa in the early to middle Miocene, most probably via long-distance dispersal across the Indian Ocean. The two Neotropical species are inferred to have derived independently in the late Miocene from ancestors of Asia and East Africa, respectively.

Conclusions

The results demonstrate the importance of post-Boreotropical long-distance dispersals (across three major oceans) in shaping the global pantropical disjunction in some plants, such as Paederia, with small, winged diaspores adapted to long-distance dispersal by various agents including wind, ocean currents or birds. Overland migration is less likely to explain its palaeotropical disjunction between Asia and Africa.

Keywords: Intercontinental disjunction, long-distance dispersal, Paederia, pantropical, post-Boreotropical, Rubiaceae

INTRODUCTION

Tropical forests are the most complex and richest terrestrial ecosystems on the planet (Morley, 2000, 2007). Studies of the origin and diversification of tropical intercontinental disjunctions in plants may provide important insights into the evolutionary assembly of tropical forests. Pantropical disjunctions usually involve tropical regions of the Americas, Africa, south-eastern Asia and Australia (Thorne, 1972). These disjunct patterns have sometimes been attributed to vicariance involving the break up of the Gondwanan supercontinent or continental rafting (Raven and Axelrod, 1974; Conti et al., 2002), but recent studies have shown that many tropical groups are of more recent origin (Givnish and Renner, 2004; Renner, 2004a). Molecular dating suggests that many disjunctions at the family or generic level are the result of degradation of the Boreotropical flora or other deep-time vicariance events with migrations across land bridges during times when the climate was favourable (Davis et al., 2002; Erkens et al., 2009). Many recent biogeographical analyses, especially at the generic level, have shown the importance of long-distance dispersal in the assembly of modern tropical floras (Renner, 2004a, b; Clayton et al., 2009; Christenhusz and Chase, 2013).

The number of studies on tropical plant groups has increased considerably in recent years, with improved phylogenetic reconstruction, molecular dating and ancestral area inferences (Lavin et al., 2000; Davis et al., 2002; Muellner et al., 2006; Clayton et al., 2009). However, most studies have focused on the family level, and only a few groups have been examined at the generic level with molecular phylogenetic and biogeographical methods, such as Anisophyllea (Zhang et al., 2007), Hernandia (Michalak et al., 2010), Peperomia and Piper (Smith et al., 2008), Sideroxylon (Smedmark and Anderberg, 2007) and Badula (Bone et al., 2012). In addition, among many genera of flowering plants showing intercontinental disjunctions, comparatively few of these genera are pantropical with taxa spanning all major tropical regions, and even fewer of these pantropical disjunct genera have well-resolved species-level molecular phylogenetic analyses, which are essential for testing alternative biogeographical hypotheses. The relatively few biogeographical analyses of this pattern may be partially due to the fact that many of the pantropical genera are species rich, making it difficult to obtain adequate taxon sampling, such as Begonia (approx. 1400 spp., Begoniaceae), Ficus (approx. 850 spp., Moraceae), Diospyros (approx. 550 spp., Ebenaceae), Terminalia (approx. 200 spp., Combretaceae) and Homalium (approx. 180 spp., Salicaceae) (Mabberley, 2008).

Paederia (Rubiaceae) is a small genus of only 31 species of woody climbers and shows a predominantly palaeotropical distribution, with most species in Asia and Madagascar–Africa and only two species in the Neotropics. The genus is an adequate group for testing hypotheses on the evolution of pantropical intercontinental disjunctions, although there is no species of the genus occurring in tropical Australia and the Pacific islands (Puff, 1991b; Razafimandimbison and Taylor, 2000). Moreover, Paederia exhibits a Malagasy–Asian disjunct pattern, with only two taxa in East Africa. This pattern is not common in Rubiaceae because relationships of taxa from Madagascar lie primarily with continental African relatives (Koechlin, 1972; Robbrecht, 1988).

Paederia was monographed by Puff (1991a), who recognized three subgenera: subgenus Paederia, subgenus Alatopaederia Puff and subgenus Lecontea (A. Rich.) Puff, based on corolla morphology and size, anther position, style length, presence of petaloid bracts and fruit morphology. Puff et al. (1991) hypothesized that the common ancestor of Paederia first diverged into subgenus Paederia (four Asian species with rounded fruits and unwinged diaspores) and subgenus Alatopaederia (12 Asian, eight Malagasy–African and two Neotropical species with laterally compressed fruits and winged diaspores). Subgenus Lecontea (five species endemic to Madagascar and Africa) was suggested to derive from subgenus Alatopaederia based on its similarly winged but larger diaspores (Puff, 1991a).

Backlund et al. (2007) conducted phylogenetic analyses of tribe Paederieae to which Paederia belongs, based on plastid DNA sequences. The results showed that Paederia consists of an Asian and an African clade, respectively. However, their study focused on tribal phylogeny and was limited in sampling of Paederia from Asia (16 species), one of the two species diversity centres. The recent biogeographical analysis by Wikström et al. (2010) suggested that Paederia originated in Asia with a single dispersal event to Madagascar and tropical East Africa from Asia, but similarly this biogeographical study included few samples from Asia and was not based on a dated inference. At present, a broader sampling from Asia in a temporal framework is needed to understand the biogeographical history of Paederia.

This study tests the systematic and biogeographical hypotheses of Puff (1991a) for Paederia. Phylogenetic relationships in Paederia are reconstructed with a broader sampling scheme from its entire distributional range, with extensive sampling from Asia based on sequences of five plastid DNA regions (the rbcL gene, rps16 intron, trnT-F region, atpB-rbcL spacer and psbA-trnH spacer). We employ a Bayesian uncorrelated lognormal relaxed molecular clock approach to estimate the ages of major diversification events in Paederia. Multiple calibration protocols including normal, uniform and exponential priors were applied to test the robustness of our dating estimation. The ancestral area of Paederia and subsequent range expansion are inferred and discussed in the context of the molecular dating results and palaeoclimatic evidence to explore the evolution of its pantropical distribution.

MATERIALS AND METHODS

Taxon sampling and sequencing

Sixty-six taxa were included in our phylogenetic data set (Appendix). We sampled 23 of the 31 Paederia spp. from continental Africa, Madagascar, Asia and the Neotropics. Although three species from Madagascar and five from Asia are unsampled, our sampling covered the entire extant geographical range of Paederia from the Palaeotropics and the Neotropics, and represented a wide range of morphological diversity of the three subgenera. Of the taxa analysed, sequences for five species were obtained from GenBank (Appendix). Widespread taxa were sampled with multiple accessions. Four representative species from the other three genera in the tribe (Spermadictyon, Leptodermis and Serissa) were selected as outgroups based on previous studies (Puff, 1982; Backlund et al., 2007).

Total DNA was extracted from silica gel-dried or herbarium materials using the DNeasy Plant Mini Kit (QIAGEN, Crawley, UK) or AutoGenPrep 965 (AutoGen, Holliston, USA) following the protocol specified by the manufacturers. Five different plastid regions were selected: the rbcL gene; the rps16 intron; the trnT-F region; and the atpB-rbcL and psbA-trnH intergenic spacers. Primers used for amplification and sequencing were Z1 and 3' for rbcL (Olmstead et al., 1992), and F and R2 for the rps16 intron (Oxelman et al., 1997). The trnT-F region was amplified and sequenced in two segments, with the first segment using the primer pair A (or A1) and D, and the second using the primer pair c and f (Taberlet et al., 1991; Bremer et al., 2002). The atpB-rbcL and psbA-trnH spacers were amplified and sequenced using the primers as described by Manen et al. (1994) and Sang et al. (1997), respectively. All sequences were amplified and sequenced based on the protocol in Nie et al. (2005). DNA sequences were assembled using Sequencher v4.1.4 (Gene Codes Corp., Ann Arbor, MI, USA). Sequence alignment was initially performed using with MUSCLE 3·8·31 (Edgar, 2004) in the multiple alignment routine followed by manual adjustment in Se-Al v2·0a11 (http://tree.bio.ed.ac.uk/software/seal/).

Phylogenetic analyses

Because all DNA sequences come from the plastid genome and preliminary analyses suggest no conflicts among each region (results not shown), we combined all the data (rbcL, rps16, trnT-F, atpB-rbcL and psbA-trnH) in our analysis using maximum parsimony (MP) and Bayesian inference (BI) as implemented in PAUP∗ 4·0b10 (Swofford, 2003) and MrBayes 3·2·1 (Huelsenbeck and Ronquist, 2001), respectively. The most parsimonious trees (MPTs) were estimated using heuristic searches with 1000 random addition-sequence replicates, tree bisection and reconnection (TBR) branch swapping, and no limiting MaxTrees. To assess clade support, non-parametric bootstrapping was conducted using 1000 bootstrap replicates, each with ten random-addition replicates, and only a single MPT was saved per replicate.

For BI analyses, we partitioned our data set by sequence region and determined the evolutionary model and parameters that best fit each partition using the Akaike information criterion implemented in MrModelTest 2·3 (Nylander, 2004). Model parameters (statefreq, revmat and shape) were unlinked between partitions. We ran two independent analyses consisting of four Markov chains sampled every 1000 generations for 10 million generations. We used the online program AWTY (Nylander et al., 2008) to check for stationarity and estimate the burn-in parameter. After discarding the first 2 million generations as burn-in, the remaining trees from both analyses were pooled for a consensus tree. The proportions of bifurcations found in this consensus tree are given as Bayesian posterior probabilities (PPs).

Molecular dating

We analysed the Paederia clade in the broad phylogenetic framework of Rubiaceae to enable multiple fossil calibrations. In the dating data set, we sampled 80 taxa from Rubiaceae plus Gelsemium sempervirens (Gelsemiaceae) as outgroup, of which 60 were obtained from GenBank (Supplementary Data Table S1). For the molecular dating analyses, the strict molecular clock model was rejected (P < 0·01) for our data set based on a likelihood ratio test (Felsenstein, 1981). We thus estimated node ages of Paederia using a Bayesian relaxed clock model as implemented in BEAST v1.7.4 (Drummond and Rambaut, 2007).

The four DNA regions (rbcL, rps16, trnT-F and atpB-rbcL) were partitioned using BEAUti 1·7·4 (within BEAST) with the appropriate substitution model estimated by MrModeltest. The psbA-trnH sequences were not used in our estimation because there were relatively few sequences of Rubiaceae available in GenBank. A Yule speciation tree prior was specified; this prior assumes a constant rate of speciation per lineage and has been recommended for species-level phylogenetic analyses (Drummond and Rambaut, 2007). An uncorrelated lognormal distributed (UCLD) relaxed clock model was used which permits evolutionary rates to vary along branches according to lognormal distribution (Drummond and Rambaut, 2007). After optimal operator adjustment as suggested by the output diagnostics from several preliminary BEAST runs, two independent MCMC (Markov chain Monte Carlo) runs (each of 50 million generations, with sampling every 1000 generations) were performed on a cluster of Mac XServers at the Smithsonian Institution (http://topazweb.si.edu). Tracer version 1.5 was used to check for convergence between the runs (Drummond and Rambaut, 2007). Results were considered reliable once the effective sampling size (ESS) for all parameters exceeded 200 as suggested by the program manual. The sampled posterior trees were summarized to generate a maximum clade credibility tree using the program TreeAnnotator 1.7.4 (Drummond and Rambaut, 2007) with a PP limit of 0·5 and mean node heights.

Fossil calibration

The most reliable Rubiaceae fossils are fruits reported from Cephalanthus from the late Eocene to the Pliocene in almost 20 fossil sites (Dorofeev, 1960, 1963; Friis, 1985; Mai and Walther, 1985; Antonelli et al., 2009), with convincing morphological features that make them taxonomically recognizable by means of overall similarity (see more in Antonelli et al., 2009). The oldest fossil of Cephalanthus was found from Kireevski in western Siberia in the late Eocene (Dorofeev, 1960, 1963) and is used here to place a normal constraint of the stem age of Cephalanthus as 33·9 ± 1·0 million years ago (Mya). Another well-preserved fruit fossil of a head-shaped infructescence was described as a new species, Morinda chinensis Shi, Liu & Jin, from the Changchang Formation in Hainan of China (Shi et al., 2012). Because Morinda is paraphyletic in tribe Morideae (Razafimandimbison et al., 2009) and the phylogenetic position of this fossil species is unclear, we used this fossil to calibrate the crown age of the tribe with the prior set to 44 ± 1 Mya, which falls into the fossil age estimated from the late early Eocene to the early late Eocene (Shi et al., 2012).

Most of the reported Rubiaceae fossils are dispersed pollen grains of a common tricolporate type. However, we used only the two most reliable pollen fossils in our analyses. The oldest pollen fossils of Faramea from the late Eocene (34–40 Mya) in Panama to the Pliocene in Veracruz, Mexico (Graham, 2009), which are characterized by the orientation of the bacula at the apertures (two- to four-porate) and the size and the shape of the pollen (Erdtman, 1966; Bremer and Eriksson, 2009). Thus, the Faramea stem node was fixed at 37 ± 1 Mya. Two pollen fossils of Scyphiphora were reported at 16 Mya from Japan and at 23 Mya from the Marshall Islands in the northern Pacific Ocean (Leopold, 1969; Saenger, 1998). Scyphiphora is the only extant genus of Rubiaceae that inhabits mangrove vegetation, and its pollen character is unique in the family, with distinct pores having a protruding papilla-like rim (Bremer and Eriksson, 2009). We therefore used 23 ± 1 Mya as a normal prior for the Scyphiphora node.

Four fossils from Rubiaceae (two fruit and two pollen) were selected as calibration points in our analyses, which have been used to estimate divergence times in various groups in the family (Nie et al., 2005; Antonelli et al., 2009; Bremer and Eriksson, 2009; Smedmark et al., 2010; Huang et al., 2013). For rooting the tree, we followed Antonelli et al. (2009) to set the stem Rubiaceae age as 78 ± 1 Mya based on the crown age estimate of Gentianales (Bremer et al., 2004). To test the robustness of our dating results based on normal priors, we also performed the dating analyses using more conservative uniform priors, i.e. each calibrating point is extending from the age of the oldest reliable fossil to the age of the root. An exponential prior is a viable alternative to allow for some probability of an earlier divergence than the appearance of the fossils (Ho and Phillips, 2009). Here we also used exponential prior distributions with a mean of 1 for all the fossil calibrations.

Ancestral area reconstruction

We used Bayesian and likelihood methods for biogeographical inference that have been recently proposed that take into account genetic branch lengths and/or phylogenetic uncertainty (Ree and Smith, 2008; Lemey et al., 2009). A smaller data set including only Paederia and its relatives (derived from the dating data set) was used for the biogeographical analyses. Five areas of endemism were delimited based on the distributions of Paederia spp.: A, continental Asia; B, south-eastern Asia; C, Madagascar and Africa; D, Central America; and E, South America. For comparison, we repeated the biogeographical analyses using a six-area scheme with Madagascar (C) and Africa (F) split as independent range units.

The Bayesian method is a discrete phylogeographic analysis using a standard continuous-time Markov chain (CTMC) (Lemey et al., 2009) and integrates over phylogenetic uncertainty and Markov model parameter uncertainty (Sanmartín et al., 2008). Each taxon can be allocated to a geographical location, corresponding to the distribution of each species. For each node, CTMC reconstructs the probability distribution for the different states. The relative PP of each location state at any position along the phylogenetic tree is also estimated. The Bayesian CTMC method was implemented in BEAST using a 10 million MCMC chain length, saving trees every 10 000 steps.

The ancestral area of the Paederia was also reconstructed with the likelihood analysis using the program Lagrange version 20120508 (Ree et al., 2005; Ree and Smith, 2008). The likelihood approach incorporates an explicit dispersal–extinction–cladogenesis (DEC) model of dispersal routes available at historical intervals correlating stochastic events with lineage persistence (Ree and Smith, 2008).

In contrast to the CTMC method, DEC is prone to estimate unrealistically widespread ancestral ranges for early-branching lineages (Lamm and Redelings, 2009; Ree and Sanmartin, 2009). In our case, the maximum ancestral area size was constrained to 2 because there is no species in our studied taxa distributed in more than two areas.

RESULTS

Phylogenetic analyses

The combined five-marker data matrix consisted of 6078 nucleotides. In the combined MP analyses, 497 characters were variable, 246 of which were potentially parsimony-informative. The MP analyses resulted in >10 000 equally MPTs with a length of 635 steps, a consistency index of 0·83, a retention index of 0·92 and a rescaled consistency index of 0·76. For the Bayesian analysis, all partitions had a best-fit model of GTR + G + I, with the exception of rbcL, for which it was GTR + I.

A strict consensus of the MPTs found in PAUP* indicates a backbone phylogenetic pattern for Paederia identical to the Bayesian result (Fig. 1), but low resolution for each major clade (results not shown). Paederia was strongly supported as monophyletic (MP bootstrap = 100 %; PP = 1·00). Three clades were recognizable in Paederia with robust support (clades I–III in Fig. 1). The first diverging group included two species (P. verticillata and P. spectatissima) endemic to tropical Asia (clade I, MP bootstrap = 94 %; PP = 0·91); this group was sister to clades II and III collectively. Clade II (MP bootstrap = 97 %; PP = 1·00) comprised all Malagasy and African species in subgenus Alatopaederia and all species of subgenus Lecontea plus the single species from Central America, P. ciliata (Fig. 1). Clade III (MP bootstrap = 100 %; PP = 1·00) consisted of almost all Asian members of subgenus Alatopaederia and all taxa of subgenus Paederia plus the single South American species, P. brasiliensis (Fig. 1).

Fig. 1.

Fig. 1.

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The Bayesian consensus tree of Paederia and closely related taxa based on five plastid sequences (rbcL, rps16, trnT-F, atpB-rbcL and psbA-trnH). The Bayesian posterior probabilities are shown above the branches and the bootstrap values below.

Biogeographical analyses

The BEAST analysis generated a well-resolved tree for Paederia, which was consistent with the topologies from the MP and Bayesian analyses (Fig. 1). Estimation from different calibration protocols (i.e. normal, uniform or exponential priors) produced similar results (Supplementary Data Table S2). Here we only report and discuss the mean ages and 95 % highest posterior density (HPD) intervals based on normal constraints as presented in Fig. 2 and Table 1. The uncorrelated-rates relaxed molecular clock suggested an origin of the Paederia stem lineage in the early Oligocene (30·73 Mya; 95 % HPD: 22·84–39·67 Mya; node 1 in Fig. 2) and the initial diversification of the Paederia crown group in the late Oligocene (24·21 Mya; 95 % HPD: 16·41–32·5 Mya; node 2 in Fig. 2). The Afro-Asian disjunction was dated to 15·99 (10·28–22·68) Mya (node 4 in Fig. 2). The two disjunctions between the Palaeotropics and the Neotropics were estimated at 6·08 (1·87–11·33) Mya for node 6 and 10·01 (5·57–15·47) Mya for node 8, respectively (Fig. 2, Table 1).

Fig. 2.

Fig. 2.

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Chronogram of Paederia and relatives based on four plastid sequences (rbcL, rps16, trnT-F and atpB-rbcL) as inferred from BEAST. Grey bars represent the 95 % highest posterior density intervals for node ages. Global temperature means are shown by the curve adapted from Zachos et al. (2001). C1–C5 are calibration points; 1–8 indicate nodes with interests (see Table 1 for details).

Table Table 1.

Posterior age distributions of major nodes of Paederia in Rubiaceae, with results of ancestral reconstruction using the Bayesian CTMC and Lagrange

Age estimates
 Bayesian CTMC
 Lagrange
Node Mean (Mya) 95 % HPD (Mya) Five-area Six-area Five-area Six-area
C1: Rubiaceae stem 78·57 76·64–80·54
C2: Cephalanthus stem 33·48 31·59–35·47
C3: Scyphiphora stem 22·88 20·98–24·82
C4: Faramea stem 36·84 34·94–38·8
C5: Morinda crown 43·36 41·46–45·27
1: Paederia stem 30·73 22·84–39·67 A (0·83) A (0·86) A | A (0·43) A | A (0·44)
2: Paederia crown 24·21 16·41–32·5 A (0·83) A (0·86) A | A (0·40) A | A (0·41)
3: Paederia clade I crown 15·92 5·11–26·21 A (0·77) A (0·81) B | A (0·65) B | A (0·49)
4: Asian – African disjunction 15·99 10·28–22·68 A (0·80) A (0·83) C | A (0·68) C | A (0·43)
5: Paederia clade II crown 8·68 4·59–14·43 C (0·74) C (0·23) C | C (0·49) D | C (0·39)
D (0·22)
F (0·23) CD | C (0·49) F | C (0·39)
6: African–Central American disjunction 6·08 1·87–11·33 C (0·74) C (0·30) C | D (0·86) F | D (0·60)
D (0·30)
7: Paederia clade III crown 12·13 7·9–17·93 A (0·95) A (0·96) A | A (0·78) A | A (0·81)
8: Asian–South American disjunction 10·01 5·57–15·47 A (0·95) A (0·96) E | A (0·65) E | A (0·65)
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Node numbers correlate with those in Figs 2 and 3 (C1–C5, calibration nodes). Letters represent results of ancestral reconstruction (as defined in Fig. 3).

Bayesian CTMC analyses based on both the five-area and the six-area definitions produced similar results of ancestral areas with the probabilities of ancestral distributions (see Table 1). For example, both analyses suggested continental Asia as the ancestral area for Paederia (node 1 in Fig. 3). The clade dominant in Madagascar and Africa was inferred to have dispersed or migrated from continental Asia in the middle to late Miocene (node 4 in Figs 2 and 3). For node 6, dispersals were inferred from Africa–Madagascar to Mexico based on the five-area analysis, or each (Africa, Madagascar or Mexico) is equally possible as the ancestral area based on the six-area analysis. For the Asian–South American disjunction (node 8 in Fig. 3), all analyses suggested continental Asia as the ancestral area. As shown in Table 1, results estimated from Lagrange are similar to those from CTMC. Only CTMC results based on five-area analysis are shown in Fig. 3.

Fig. 3.

Fig. 3.

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Bayesian CTMC ancestral area reconstruction from the BEAST tree (right) with branches coloured according to the most probable location state of their descendent nodes. The letter and colour coding for areas are indicated on the map (left upper). Left below are state posterior probability distributions for selected nodes as shown on the right-hand tree (see Fig. 2 and Table 1 for details).

DISCUSSION

Phylogenetics and morphology of Paederia

With a broader sampling from Asia, our analyses confirm the monophyly of Paederia as suggested by previous studies (Backlund et al., 2007; Rydin et al., 2009; Wikström et al., 2010). Paederia is a well-defined group of woody lianas, a growth form not particularly common in Rubiaceae. Paederia spp. all emit an unpleasant foetid odour with sulfur-containing iridoid glucosides when the tissue is bruised (Takeda et al., 1991; Zou et al., 2006). This chemical character is also known from a few other rubiaceous taxa, including Saprosma, Danais and Coprosma.

The first diverged lineage in Paederia includes only two Asian species: P. verticillata and P. spectatissima. Paederia verticillata is distributed in the Malay Peninsula, Sumatra, western Java, Borneo, Celebes and the Philippines, and P. spectatissima is confined to south-west China and adjacent parts of Vietnam (Puff, 1991c). The species share the synapomorphies of evergreen leaves, with a hypodermis and diaspores with by far the largest wings in the genus (Puff et al., 1991). The species pair was considered to be the most derived among the Asian taxa of subgenus Alatopaederia by Puff et al. (1991) based on these characters. Nevertheless, Puff et al. (1991) also pointed out that the two species remained ‘conservative’ with regard to chromosome number (diploid for P. verticillata, but unknown for P. spectatissima) and leaf arrangement (decussate for P. spectatissima and in whorls of three in P. verticillata; all other taxa have only opposite leaves), which is supported by our phylogenetic results (i.e. the first-branching position in the genus, Fig. 1).

Subgenus Alatopaederia is the largest subgenus recognized by Puff (1991b). Its monophyly is not supported by our results, with species from this subgenus placed into all three major clades of the genus (Fig.1); it was also considered to be paraphyletic by Puff et al. (1991) in their analyses based on morphological data. Our analyses also show that subgenus Lecontea is not monophyletic and is nested with the taxa of subgenus Alatopaederia from Madagascar (Fig. 1). Members of subgenus Lecontea have seeds resembling those of subgenus Alatopaederia, except that the former bears larger seeds, but subgenus Lecontea is distinguished from the others by its showy bracts, elongated and fused styles, and long and narrow corollas (Puff, 1991a). Subgenus Paederia is restricted to Asia with only four species (Puff, 1991c; Chen and Taylor, 2011), and is the only monophyletic subgenus recognized by Puff (1991b). However, phylogenetic resolution in this subgenus is extremely low when multiple collections were sampled, as shown by a large polytomy in Fig. 1.

Post-Boreotropical origin in continental Asia

Accurate calibration with multiple fossils has been suggested as a key factor in age estimation of lineages (Renner, 2005; Sauquet et al., 2009). Our age estimates employed four reliable fossils, and the results are largely close to those of Bremer and Eriksson (2009). The origin and early diversification of Paederia in the Oligocene (nodes 1 and 2; Fig. 2) are in a time frame well after the existence of the Boreotropical floras from the Palaeocene to the Eocene. Asia harbours the largest number of the Boreotropical genera, perhaps due to the continuous land connection between the northern latitudes and the equatorial zone in Asia (Tiffney, 1985a, b; Morley, 2003). The earliest diverging lineage of Paederia shows a disjunct distribution between the Malesian region (P. verticillata) and continental Asia (P. spectatissima) in the early to middle Miocene, which is consistent with this connection (node 3; Fig. 2).

Puff et al. (1991) generally hypothesized an Asian origin of Paederia according to its high species diversity in this region. Wikström et al. (2010) also suggested Asia as the ancestral area of Paederia based on molecular biogeographical analyses. Our results are largely congruent with the hypothesis of Asian origin of the genus (Fig. 3). However, our analyses further revealed that continental Asia (especially Indochina, the centre of highest diversity for the genus with 15 species) is the most likely ancestral range of Paederia, whereas there is only one endemic species (P. verticillata) found in the Malesian region of south-eastern Asia.

Palaeotropical intercontinental disjunction

The observed pattern of the African and Malagasy taxa (clade II in Figs 1 and 2) being nested in the continental Asian taxa is compatible with dispersal and/or migration from continental Asia to Africa and Madagascar. Both CTMC and Lagrange analyses further indicated a continental Asian origin of the Malagasy–African group in the middle to late Miocene (node 4 in Fig. 3 and Table 1). Since the estimated stem age for the Malagasy–African Paederia lineage at 15·99 Mya (95 % HPD: 10·28–22·68 Mya) in the early to mid Miocene is too recent (Fig. 2), several hypotheses seem to be unlikely to explain how such intercontinental disjunctions might have originated, such as ‘rafting’ on the Indian tectonic plate (Le Thomas and Doyle, 1996; Conti et al., 2002), migration through the Eocene Boreotropical flora (Wolfe, 1975) or Eocene–Oligocene dispersal from India to Madagascar through the ‘Lemurian stepping stones’ across the western Indian Ocean (Schatz, 1996). Long-distance dispersal across the Indian Ocean seems to be the most likely explanation for the disjunction of Paederia from continental Asia to Madagascar/Africa.

Many Afro-Asian plant disjunctions, especially those of very recent origin, have been explained by long-distance dispersal in both directions. It is of interest to note that fewer dispersal events have been reported from Asia to Africa. Nevertheless examples of the latter can be found in Bridelia (Phyllanthaceae) at approx. 10·00–1·85 Mya (Li et al., 2009) and Macaranga and Mallotus (Euphorbiaceae) at <27 Mya (Kulju et al., 2007). Dispersal from Africa and/or Madagascar to Asia has been suggested in Osbeckia (Melastomataceae) at approx. 16–7 Mya (Renner and Meyer, 2001; Renner, 2004b), Gaertnera (Rubiaceae) at approx. 6–5 Mya (Malcomber, 2002), Exacum (Gentianaceae) at less than approx. 35 Mya (Yuan et al., 2005), Cucumis (Cucurbitaceae) <10 Mya (Renner et al., 2007), Uvaria (Annonaceae) at 16·1–21·4 Mya (Zhou et al., 2012) and Eurycoma–Brucea–Soulamea (Simaroubaceae) during the Oligocene (Clayton et al., 2009).

As suggested by the biogeographical inferences based on our six-area analysis, either Madagascar or Africa is possible as the ancestral area of crown II (node 5 in Table 1). Wikström et al. (2010) also proposed that it is unclear whether the dispersal route is from Asia to Eastern Tropical Africa and finally to Madagascar (with further dispersal to the Comores because the Comorian species was nested in the Malagasy clade) or an opposite scenario (i.e. Asia → Madagascar → Africa). However, we prefer to adopt the former route, which seems to be consistent with the phylogenetic results (i.e. the single north-eastern African species of P. pospischilii plus the Mexican P. ciliata sister to a clade including all species from Madagascar, Fig. 2).

A recent comprehensive review on Malagasy biota suggested that dispersal of taxa from Africa was by far the most important contributing source to the Malagasy flora (Yoder and Nowak, 2006). For example, multiple dispersals from Africa to Madagascar have taken place in the Sapotaceae tribe Chrysophylloideae during the Tertiary (Bartish et al., 2011). Long-distance dispersals from Africa to Madagascar have also been reported from frogs (Vences et al., 2003, 2004), chameleons (Raxworthy et al., 2002), snakes (Nagy et al., 2003), lemurs (Yoder and Yang, 2004) and lorises (Masters et al., 2005). This hypothesis may be corroborated by our study on the Asian origin of Paederia with a recent dispersal from Africa to Madagascar in the late Miocene (node 5 in Figs 2 and 3, Table 1). Similarly, Wikström et al. (2010) found that the two other Rubiaceae tribes Knoxieae and Vanguerieae have their origins in eastern tropical and southern Africa and dispersed to Madagascar numerous times. Another taxon (P. bojeriana var. foetens, not sampled in this study) also occurs in Africa with its sister pair (P. bojeriana var. bojeriana) in Madagascar, which might indicate another dispersal event between Madagascar and Africa.

Another possibility is an overland migration from eastern Asia through south-west Asia to north-east Africa (Kappelman et al., 2003). This route of migration became available after the collision between the Arabian peninsula and the Anatolian Plate, the closing of the Tethys Sea with the formation of the ‘Gomphotherium land bridge’ (Rögl, 1998, 1999), and the global warming period between late Oligocene and middle Miocene (Zachos et al., 2001). The possibility of dispersal of tropical plants across northern Africa and Arabia is supported by fossil evidence in Meliaceae in Europe, Africa and Asia (Muellner et al., 2006) and the ‘out-of-Africa’ dispersal pattern in Uvaria of Annonaceae (Zhou et al., 2012). However, it seems less likely for the Paederia Asian–African disjunction, with a relatively young split age of 15·99 Mya at the boundary between the early and mid Miocene (Table 1). The rising of mountains (such as the Himalayas and the Tibetan Plateau) and increasingly cooler climates from the mid Miocene onwards (An et al., 2001; Zachos et al., 2001; Spicer et al., 2003; Sun et al., 2005) may have further constrained tropical and sub-tropical forests to lowlands and prevented floristic exchanges of tropical elements including Paederia between Asia and Africa.

Long-distance dispersals to the Neotropics

Paederia also shows a trans-Atlantic tropical disjunction between Central America and Africa at 6·08 (95 % HPD: 1·87–11·33) Mya in the late Miocene (node 6; Fig. 2). This divergence time is well after the last possible connection of Africa and South America at around 96–105 Mya and the last opening of the North Atlantic land bridge at 20–25 Mya (Tiffney, 1985a; McLoughlin, 2001; Morley, 2003). We thus argue that long-distance dispersal is also the most plausible mechanism for this trans-Atlantic disjunction in Paederia. Dispersal from the Caribbean or South America to São Tomé has been inferred for the primarily Neotropical genus Cayaponia (Cucurbitaceae), which has a single west African species estimated to have diverged at 2–5 Mya (Duchen and Renner, 2010). Trans-Atlantic tropical disjunctions are common in plants, and Renner (2004) enumerated a total of 109 plant lineages at the genus level showing this pattern, many apparently due to long-distance dispersal. However, most of them are disjunct between South America and west Africa, such as Vochysiaceae (Sytsma et al., 2004), Maschalocephalus in Rapateaceae (Givnish et al., 2004) and Pitcairnia in Bromeliaceae (Givnish et al., 2004). Paederia seems to be an unusual case exhibiting a disjunction between north-eastern Africa and Central America.

The divergence time of 10·01 (95 % HPD: 5·57–15·47) Mya in the late Miocene was estimated for the Paederia disjunction between continental Asia and South America (node 8 in Fig. 2 and Table 1). Disjunctions between the tropical Pacific and the Neotropics are less common, with about 89 genera of flowering plants known with the amphi-Pacific tropical distribution (Thorne, 1972). The continental Asian–tropical American disjunction may invoke land bridge vicariance, such as the amphi-Pacific disjunction in Persea that may have resulted from the disruption of the Boreotropical flora by climatic cooling during the mid to late Eocene (Li et al., 2011). In the case of the tropical Asian–South American disjunction in Paederia, direct transoceanic dispersal across the Pacific seems to be the most plausible explanation due to its recent split in the late Miocene (node 8 in Figs 2 and 3). There are many examples of long-distance dispersal between the tropical Pacific islands and the Neotropics, such as in Hernandia (Hernandiaceae) exhibiting a trans-Pacific disjunction with transoceanic dispersal from tropical Australia to the Neotropics in the Miocene (Michalak et al., 2010). Paederia provides one of the few examples of disjunctions between continental Asia and tropical South America which are tentatively explained by transoceanic dispersal.

Dispersal mechanism in Paederia

A number of recent studies have attempted to explain the pantropical disjunctions in plants with relatively young divergence times (Li et al., 2009; Michalak et al., 2010; Zhou et al., 2012). The stepping-stone mechanism, birds capable of long-distance flight and monsoon trade winds coupled with oceanic currents may be important factors related to dispersal (Ali et al., 2012). The small subgenus Paederia has sub-globose fruits without obviously winged diaspores and without distinct carpophores, but they are restricted to Asia. Most taxa of the genus (subgenus Alatopaederia and subgenus Lecontea) possess small, winged diaspores, showing a remarkable adaptation to wind dispersal (Puff, 1991a; Puff et al., 1991). It is not only the conspicuous diaspore wings but also the presentation and orientation of the diaspores which have been interpreted as a functional adaptation (Igersheim and Puff, 1991). The winged diaspores are held in a vertical position by the stout carpophores in order to be exposed effectively to the wind (Igersheim and Puff, 1991).

For many tropical tree diaspores, on the other hand, transport via ocean currents or in rafting mats of vegetation is a much more feasible scenario than dispersal by wind. Houle's study demonstrated that during the Miocene, intercontinental rafting could have occurred in <2 weeks on the North and South Equatorial counter currents between Africa and the Neotropics and on the North and South Equatorial counter current between East Africa and South India/south-east Asia (Houle, 1998). With small and winged seeds, it is also likely that seeds of Paederia spp. could travel by attaching to birds (while wet) or that propagules could have rafted across water barriers in large mats of vegetation. Therefore, the winged diaspores in Paederia may have facilitated long-distance dispersal by various agents including wind, ocean currents or even birds. The noni plant (Morinda citrifolia) is another example in Rubiaceae with a pantropical disjunction, and buoyant fruits and seeds that are transported by oceanic current drifting (Razafimandimbison et al., 2010).

Conclusions

Long-distance dispersal may be much more common than previously thought and may represent an important mechanism in the assembly of modern tropical floras (Givnish and Renner, 2004; Renner, 2004a; de Queiroz, 2005; Michalak et al., 2010). Our results from Paederia with robust molecular dating provide strong evidence for the divergence of Paederia from its sister group in tropical continental Asia in the Oligocene, with three dispersal events inferred into the other tropical areas. The trans-Indian Ocean dispersal into Madagascar–Africa is inferred to have occurred between the early and mid Miocene. The two Neotropical species are suggested to have dispersed from south-eastern Asia (trans-Pacific) and east Africa (trans-Atlantic) in the late Miocene via long-distance dispersal, respectively. The data presented here suggest the potential of post-Boreotropical divergence and long-distance dispersals across the three major oceans in shaping the global pantropical disjunction in Paederia.

SUPPLEMENTARY DATA

Supplementary data are available online at www.aob.oxfordjournals.org and consist of the following. Table S1: taxa with accession numbers obtained from GenBank. Table S2: posterior age distributions of major nodes of Paederia based on different calibration protocols. Node numbers correlate with those in Fig. 2.

Supplementary Data
supp_111_5_873__index.html (928B, html)

ACKNOWLEDGEMENTS

This study was supported by grants from Natural Sciences Foundation of China (NSFC 30970193 to Z.-L.N.), the One Hundred Talents Program of the Chinese Academy of Sciences (2011312D11022 to H.S.), United Fund of the NSFC and Yunnan Natural Science Foundation (U1136601 to H.S.), NSFC–International (Region) Cooperation Project (31061160184 to H.S.), the “Strategic Priority Research Program (B)” of the Chinese Academy of Sciences, XDB03030112 to H.S.) and the John D. and Catherine T. MacArthur Foundation to J. Wen, R. Ree and G. Mueller. Laboratory work was done at and partially supported by the Laboratory of Analytical Biology of the National Museum of Natural History, Smithsonian Institution. Fieldwork in North America was supported by the Small Grants Program of the National Museum of Natural History, the Smithsonian Institution. We thank Michael Nee, Fernando Chang, Ruth Kiew, Tze Leong Yao, Richard Chung, Leng Guan Saw, Elizabeth Widjaja, Zhiduan Chen, Tieyao Tu, Yumin Shui and Wenhong Chen for field assistance and sample collection.

APPENDIX

Taxa sequenced with voucher information and GenBank accessions

Taxa Voucher* Location rbcL trnT-F rps16 atpB-rbcL psbA-trnH
Paederia brasiliensis (Hook.f.) Puff Nee & Wen 53771 (US) Bolivia: Santa Cruz KC305897 KC306110 KC306055 KC306006 KC305951
Nee & Wen 53808 (US) Bolivia: Santa Cruz KC305898 KC306111 KC306056 – KC305952
Paederia cavaleriei H.Lév. Nie 1267 (KUN) China: Sichuan KC305899 KC306112 KC306057 KC306007 KC305953
Nie 2193 (KUN) China: Guizhou KC305900 KC306113 KC306058 KC306008 KC305954
Paederia ciliata (Bartl. ex DC.) Standl. Susana Valencia 2971 (FCME) Mexico: Guerrero KC305901 KC306114 – – KC305955
Paederia cruddasiana Prain Nie 1990 (KUN) China: Yunnan KC305902 KC306115 KC306059 KC306009 KC305956
Paederia farinosa var. farinosa (Baker) Puff Wen 9474 (US) Madagascar: Fianarantsoa KC305903 KC306116 KC306060 KC306010 KC305957
Wen 9622 (US) Madagascar: Antsiranana KC305904 KC306117 KC306061 KC306011 KC305958
Wen 9625 (US) Madagascar: Antsiranana KC305905 KC306118 KC306062 KC306012 KC305959
Paederia farinosa var. rosea Puff Wen 9545 (US) Madagascar: Antsiranana KC305906 KC306119 KC306063 KC306013 KC305960
Paederia foetida L. Nie 413 (KUN) China: Yunnan KC305907 KC306120 KC306064 KC306014 KC305961
Wen 9319 (US) China: Hunan KC305908 KC306121 KC306065 KC306015 KC305962
Wen 9371 (US) China: Hunan KC305909 KC306122 KC306066 KC306016 KC305963
Wen 9417 (US) China: Taiwan KC305910 KC306123 KC306067 KC306017 KC305964
Wen 9453 (US) China: Taiwan KC305911 KC306124 KC306068 KC306018 KC305965
Wen 9457 (US) China: Taiwan KC305912 KC306125 KC306069 KC306019 KC305966
Tibet-MacArthur 1931 (US, KUN) China: Sichuan KC305913 KC306126 KC306070 KC306020 KC305967
Shui et al. 81972 (KUN) China: Yunnan KC305914 KC306127 KC306071 KC306021 KC305968
Tibet-MacArthur 2227 (US, KUN) China: Yunnan KC305915 KC306128 KC306072 KC306022 KC305969
Wen 10658 (US) China: Beijing KC305916 KC306129 KC306073 KC306023 KC305970
Nie 1238 (KUN) China: Sichuan KC305917 KC306130 KC306074 KC306024 KC305971
Nie 1535 (KUN) China: Yunnan KC305918 KC306131 KC306075 KC306025 KC305972
Wen 10888 (US) Vietnam: Lao Cai KC305919 KC306132 KC306076 – KC305973
Huang 09918 (IBSC, KUN) China: Guangxi KC305920 KC306133 KC306077 KC306026 KC305974
Nie 0221 (KUN) China: Chongqin KC305921 KC306134 KC306078 KC306027 KC305975
Nie 1952 (KUN) China: Yunnan KC305922 KC306135 KC306079 KC306028 KC305976
Nie 2066 (KUN) China: Sichuan KC305923 KC306136 KC306080 KC306029 KC305977
Nie 2186 (KUN) China: Guizhou KC305924 KC306137 KC306081 KC306030 KC305978
Nie 2323 (KUN) China: Guangxi KC305925 KC306138 KC306082 KC306031 KC305979
Nie 2392 (KUN) China: Guangxi KC305926 KC306139 KC306083 KC306032 KC305980
Nie 3142 (KUN) China: Sichuan KC305927 KC306140 KC306084 KC306033 KC305981
Huang WP 021 (KUN) China: Jiangxi KC305928 KC306141 KC306085 KC306034 KC305982
Xie YP 008 (KUN) China: Shanxi KC305929 KC306142 KC306086 KC306035 KC305983
Deng T 180 (KUN) China: Anhui KC305930 KC306143 KC306087 KC306036 KC305984
Nie 3280 (KUN) China: Yunnan KC305931 KC306144 KC306088 KC306037 KC305985
Nie 3478 (KUN) China: Yunnan KC305932 KC306145 KC306089 KC306038 KC305986
Paederia grandidieri Drake Wen 9486 (US) Madagascar: Fianarantsoa KC305933 KC306146 KC306090 KC306039 KC305987
Paederia lanuginosa Wall. Tibet-MacArthur 2096 (US, KUN) China: Yunnan KC305934 KC306147 KC306091 KC306040 KC305988
Tibet-MacArthur 2238 (US, KUN) China: Yunnan KC305935 KC306148 KC306092 KC306041 KC305989
Tibet-MacArthur 2237 (US, KUN) China: Yunnan KC305936 – KC306093 KC306042 KC305990
Paederia pertomentosa Merr. ex H.L.Li Nie 2239 (KUN) China: Guizhou KC305937 KC306149 KC306094 KC306043 KC305991
Paederia praetermissa Puff Nie 3474 (KUN) China: Yunnan KC305938 KC306150 KC306095 KC306044 KC305992
Nie 3485 (KUN) China: Yunnan – KC306164 KC306109 – KC306005
Paederia sambiranensis Homolle ex Puff Wen 9535 (US) Madagascar: Antsiranana KC305939 KC306151 KC306096 KC306045 KC305993
Paederia sp. Tibet-MacArthur 2236 (US, KUN) China: Yunnan KC305940 KC306152 KC306097 KC306046 KC305994
Paederia spectatissima H.Li Nie 4375 (KUN) China: Yunnan KC305941 KC306153 KC306098 – KC305995
Paederia stenobotrya Merr. Nie 3952 (KUN) China: Hainan KC305942 KC306154 KC306099 – KC305996
Paederia taolagnarensis Razafim. & C.M.Taylor Wen 9678 (US) Madagascar: Toliara KC305943 KC306155 KC306100 KC306047 KC305997
Wen 9671 (US) Madagascar: Toliara KC305944 KC306156 KC306101 KC306048 KC305998
Paederia verticillata Blume Wen 11690 (US) Malaysia: Malay KC305945 KC306157 KC306102 KC306049 KC305999
Wen 11834 (US) Malaysia: Borneo KC305946 KC306158 KC306103 KC306050 KC306000
Paederia yunnanensis (H.Lév.) Rehder Shui et al. 81880 (KUN) China: Yunnan KC305947 KC306159 KC306104 KC306051 KC306001
Nie 546 (KUN) China: Yunnan KC305948 KC306160 KC306105 KC306052 –
Nie 1265 (KUN) China: Sichuan KC305949 KC306161 KC306106 KC306053 KC306002
Nie 1997 (KUN) China: Yunnan KC305950 KC306162 KC306107 KC306054 KC306003
Serissa serissoides (DC.) Druce Chen et al. 20110431 (PE) China: Taiwan – KC306163 KC306108 – KC306004
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* Herbarium acronyms are as follows: IBSC, South China Botanical Garden, Chinese Academy of Sciences; KUN, Kunming Institute of Botany, Chinese Academy of Sciences; FCME, Universidad Nacional Autónoma de México, Ciudad Universitaria; PE, Institute of Botany, Chinese Academy of Sciences; US, US National Herbarium of the Smithsonian Institution.

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