The Roles of Dispersal and Mass Extinction in Shaping Palm Diversity Across the Caribbean

Home , Chelyocarpus, Coccothrinax, Coryphoideae, Sabal, Sabinaria, Trachycarpeae

DOI: 10.1111/jbi.13225

RESEARCH PAPER

The roles of dispersal and mass extinction in shaping palm diversity across the Caribbean

1Conservatoire et Jardin botaniques de la Ville de Geneve and Department of Botany Abstract and Plant Biology, University of Geneva, Aim: The rich flora of the Caribbean islands and surrounding mainland evolved in a Chambesy, Geneva, Switzerland context of isolation alternated with phases of terrestrial connectivity between land- 2Gothenburg Global Biodiversity Centre, Goteborg,€ Sweden masses, climatic fluctuations and episodes of mass extinctions during the Cenozoic. 3Department of Biological and We explored how these events affected the evolution of the sister palm tribes Environmental Sciences, University of Gothenburg, Goteborg,€ Sweden Cryosophileae and Sabaleae, and how continent-island exchanges, endemic radia- 4Gothenburg Botanical Garden, Goteborg,€ tions and mass extinction shaped their extant diversity. Sweden Location: The American continent including the Caribbean region. 5Department of Ecology and Evolution, University of Lausanne, Lausanne, Methods: We reconstructed a time-calibrated phylogeny of the palm tribes Cryoso- Switzerland phileae and Sabaleae using 84% of the known species. We inferred ancestral distri-

Correspondence bution and tested the effect of island colonization and mass extinction on extant Angela Cano, Conservatoire et Jardin diversity. botaniques de la Ville de Geneve, Chambesy, Geneva, Switzerland. Results: Our results indicate that Cryosophileae and Sabaleae originated c. 77 Ma Email: [email protected] most probably in Laurasia, and their extant species started to diversify between 56– – Funding information 35 Ma and 19 10 Ma respectively. Biogeographical state reconstruction estimated European Research Council, Grant/Award that Cryosophileae dispersed to South America between 56–35 Ma, then dispersed to Number: 331024; Vetenskapsradet, Grant/ – – Award Number: B0569601; Swiss National North-Central America between 39 25 Ma and the Caribbean islands between 34 Science Foundation, Grant/Award Number: 21 Ma. We detected a possible signature of a mass extinction event at the end of the 31003A_175655/1 Eocene, affecting the diversification of Cryosophileae and Sabaleae and we did not Editor: Lyn Cook detect a diversification rate shift related to the colonization of the Caribbean islands. Main conclusions: Species of Cryosophileae in the Caribbean islands are probably derived from a single Oligocene dispersal event that likely occurred overwater from North-Central America rather than through the hypothesized GAARlandia land bridge. Contrastingly, three independent Miocene dispersal events from North-Cen- tral America explain the occurrence of Sabaleae in the Caribbean islands. Contrary to our expectations, island colonization did not trigger increased diversification. Instead, we find that diversification patterns in this clade, and its disappearance from northernmost latitudes, could be the signature of a mass extinction triggered by the global temperature decline at the end of the Eocene.

KEYWORDS Arecaceae, Boreotropical migrations, Caribbean, Coryphoideae, diversification, mass extinction, overwater dispersal, palms, Sabal, West Indies

1 | INTRODUCTION endangered sensu the International Union for Conservation of Nat- ure (Acevedo-Rodrıguez & Strong, 2008; Oleas et al., 2013). Com- The Americas have experienced dramatic geological changes over parative studies have shown a floristic affinity between the the past 100 Myr: North America was temporarily connected to Eur- Caribbean islands and the surrounding mainland (Acevedo-Rodrıguez asia through the North Atlantic and Beringian land bridges (Brikiatis, & Strong, 2008), but our understanding of the underlying evolution- 2014 and references therein), Central America was hit by a massive ary processes that shaped this diversity is still limited (Francisco- meteorite (Schulte et al., 2010), the Caribbean islands emerged and Ortega et al., 2007; Graham, 2003; Nieto-Blazquez, Antonelli, & drifted eastwards in the Caribbean Sea (Iturralde-Vinent & MacPhee, Roncal, 2017; Santiago-Valentin & Olmstead, 2004). Available bio- 1999), and South America ended its isolation with the formation of geographical studies focused on Caribbean plants point to multiple the Panama Isthmus (Montes et al., 2015). How these events influ- biotic exchanges among the islands, between North-Central America enced the outstanding biodiversity of the Neotropics has been a and South America, and local diversifications (Cervantes, Fuentes, subject of long-standing discussion (Antonelli & Sanmartın, 2011a), Gutierrez, Magallon, & Borsch, 2016; van Ee, Berry, Riina, & renewed in recent years with the advent of new molecular dating Gutierrez Amaro, 2008; Santiago-Valentin & Olmstead, 2004). For and biogeographical methods, and cross-taxonomic comparative example, the Caribbean Acalyphoideae (Euphorbiaceae) are esti- analyses (e.g., Bacon et al., 2015; Hoorn et al., 2010; O’Dea et al., mated to have repeatedly colonized the Caribbean islands during the 2016; Rull, 2011). In this context, the Andean and Amazonian Miocene mainly from Central America (Cervantes et al., 2016), regions have drawn the most attention, while much less effort has whereas Brunfelsia (Solanaceae) probably entered the Antilles 8– been devoted to understanding the evolution of the Caribbean, in 6 Ma from South America (Filipowicz & Renner, 2012). Phylogenetic particular its flora. studies in different palm lineages also indicate independent coloniza- The sister palm tribes Cryosophileae and Sabaleae (subfamily tions of the Caribbean islands from the mainland and multiple migra- Coryphoideae), known as the New World Thatch Palms (NWTP; tions between North and South America (Bacon, Baker, & Simmons, Dransfield et al., 2008), have evolved in the dynamic context of the 2012; Bacon, Mora, Wagner, & Jaramillo, 2013; Cuenca, Asmussen- Caribbean. They are currently restricted to the Caribbean islands (34 Lange, & Borchsenius, 2008; Roncal, Zona, & Lewis, 2008). For the species, most of them in the Greater Antilles) and nearby landmasses NWTP, previous phylogenetic hypotheses have suggested an origin of North-Central America (25 species) and South America (10 spe- of the Caribbean taxa from a mainland ancestor (Roncal et al., 2008). cies) (Henderson, Galeano, & Bernal, 1995). However, they had a lar- However, a better resolved phylogeny is needed to trace whether ger past distribution in the Northern hemisphere, as evidenced by their diversity in the Caribbean is the result of multiple mainland- their extensive fossil record (Figure 1) that dates to the Late Creta- island dispersal events or a colonization event followed by local ceous (Manchester, Lehman, & Wheeler, 2010). Combining these diversification. fossil data with a phylogeny of extant NWTP species would help Several geological models have been hypothesized to facilitate retrace their evolution in time and space, and illuminate the origin interchanges between land areas around the Caribbean region. These and diversification of the Caribbean flora. include the Proto-Antilles, connecting North to South America during The Caribbean region, including the Greater and Lesser Antilles, the Late Cretaceous to the Palaeocene (94–63 Ma; Graham, 2003), contains about 13,000 seed plant species. Of these, 72% are ende- the Greater Antilles-Aves Ridge (GAARlandia) connecting the West mic to the region and at least 10% are either endangered or critically Indies to South America during the Oligocene (35–33 Ma; Iturralde-

FIGURE 1 Distribution of extant Cryosophileae and Sabaleae (pink area) and fossils related to them from different epochs: Late Cretaceous (black; 100–66 Ma), Paleogene (grey; 66–23 Ma), Neogene (white; 23–2.6 Ma). Shapes represent different taxonomic groups: triangle Cryosophileae, square Sabal, circle Sabalites. See Appendix S1 for data sources. Map projection: sphere Mollweide (53,009) CANO ET AL. | 3

Vinent & MacPhee, 1999), and the Panama Isthmus formation start- the genera Cryosophila (7 species of 10, sensu Evans, 1995) and Coc- ing in the Miocene (Montes et al., 2015). To what extent these puta- cothrinax (10 species of 14, sensu Henderson et al., 1995). Sampling tive corridors facilitated species dispersal across the Caribbean in the monotypic tribe Sabaleae includes 14 of the 16 accepted spe- region is still debated (e.g. Ali, 2012; Nieto-Blazquez et al., 2017) cies of Sabal (Dransfield et al., 2008). To evaluate the phylogenetic and several studies postulate that overwater dispersal events have position of the NWTP within Coryphoideae, we also sampled repre- played a major role in the biogeographical history of Caribbean plant sentatives of other tribes in this subfamily. Two outgroups were lineages (Cervantes et al., 2016; Gugger & Cavender-Bares, 2013). selected in subfamilies Ceroxyloideae and Arecoideae. Silica-gel dried In addition to dispersal, the dynamics of speciation and extinc- leaf fragments were collected in the field (collection and export per- tion during the history of lineages may also have influenced the cur- mits 111,296 and 113,458 respectively, from the Paraguayan Secre- rent patterns of species richness across the Caribbean and tarıa del Ambiente) or in the living collections of the Conservatoire et surrounding areas (Ricklefs & Bermingham, 2008). The colonization Jardin botaniques de la Ville de Geneve (Switzerland), Montgomery of archipelagos has been frequently associated with an increase of Botanical Center, Fairchild Tropical Botanical Garden (both in the morphological and taxonomic diversity (Bacon et al., 2012; Baldwin USA) and the Jardın Botanico del Quindıo (Colombia). Voucher infor- & Sanderson, 1998; Condamine, Leslie, & Antonelli, 2016; Losos & mation is provided in Table S1.1 (see Appendix S1 in Supporting Ricklefs, 2009). The diversification rate shift estimated for the Carib- Information). bean Coccothrinax (Baker & Couvreur, 2013b), the most diverse genus of the NWTP, is congruent with the hypothesis of a species 2.2 | Phylogenetic analyses radiation triggered by island colonization. Alternatively, mass extinction events could also have influenced how diversity accumulated Four nuclear (CISP4, CISP5, PRK and RPB2) and one plastid (matK) through time (Antonelli & Sanmartın, 2011b; Brocklehurst, Ruta, loci were sequenced following the protocol described in Muller,€ & Frobisch,€ 2015; Crisp & Cook, 2009). In particular, three Appendix S1 and using the primers listed in Table S1.2. The DNA episodes of relatively rapid climatic cooling could have affected the sequences are deposited in GenBank under the accession numbers diversity of frost-intolerant plants in the Caribbean region: (1) the listed in Table S1.1. Sequences were aligned using MAFFT 7.130 Cretaceous–Palaeogene Event (66 Ma), when a large meteorite (Katoh, Misawa, Kuma, & Miyata, 2002). Sites were scored with impacted the Yucatan Peninsula generating immediate global dark- GUIDANCE 1.4.1 (Penn et al., 2010) and excluded from further analy- ness and cooling (Schulte et al., 2010), (2) the Terminal Eocene ses if their score was <0.8 to avoid adding noise to the branch Event (35 Ma), when global temperatures drastically dropped, nega- length and substitution rate estimates (Jordan & Goldman, 2012). tively affecting the Boreotropical flora that covered large parts of The final database contained 4,872 bp. Phylogenetic analyses were Laurasia (Morley, 2003), and (3) the period following the mid-Mio- performed on the CIPRES portal (Miller, Pfeiffer, & Schwartz, 2010). cene climatic optimum (12 Ma), when globally warm, equable cli- Single-gene and combined partitioned phylogenetic analyses were mates shifted to present-day cooler and more seasonal climates carried out with MRBAYES 3.2.2 (Ronquist et al., 2012). In the parti- (Zachos, Dickens, & Zeebe, 2008). It remains unclear if the NWTP, tioned analyses the dataset was divided into five partitions corre- which are considered typical elements of the Boreotropical flora sponding to each marker. The best fitting substitution model for

(Bjorholm, Svenning, Baker, Skov, & Balslev, 2006), were more each partition was selected from 24 models with MRAIC.PL 1.4.6 affected by Cenozoic cooling that caused their extirpation from Eur- (Nylander, 2004) using the Akaike information criterion (AIC). The asia and northern North America (Figure 1), or by the meteorite test selected the models HKY for CISP4, CISP5 and PRK, GTR for impact in the vicinity of their distribution range. matK, and GTR+Γ for RPB2. Four Markov chains were run for We generated a time-calibrated species phylogeny of the NWTP 5 9 106 generations with a heating temperature of 0.15. Samples and used it to infer the biogeographical scenario that best explains were logged every 100th generation. Using TRACER 1.6. (Rambaut, their current distribution and diversity. We addressed the following Suchard, Xie, & Drummond, 2014), we determined burnin (24%) and specific questions: (1) When and where did the NWTP originate? (2) confirmed trace stationarity and sufficient sampling (effective sample Is their diversity in the Caribbean the result of one or multiple dis- size [ESS] >200). persal events, and which colonization routes did they follow? (3) How did island colonization and global episodes of mass extinction 2.3 | Fossil calibration and divergence time analyses influence extant NWTP diversity across the Caribbean and surrounding areas? Three fossils were used to estimate divergence times (Table S1.3). Following Couvreur, Forest, and Baker (2011), fossils of Sabalites carolinensis Berry and Hyphaene kappelmanii Pan et al. were used to 2 | MATERIALS AND METHODS constrain the stem nodes of subfamily Coryphoideae and subtribe Hyphaeninae (Coryphoideae) respectively. In addition, fossilized 2.1 | Taxon sampling seeds of Sabal bigbendense (Manchester et al., 2010) were used to Our sampling includes 89 accessions from 67 species. Sampling in calibrate the stem node of Sabaleae. These seeds from the Late Cre- Cryosophileae (11 genera, 35 species of 42) is complete except in taceous (c. 77 Ma), represent the oldest record attributed to the 4 | CANO ET AL. tribe. Since the use of this fossil for calibrating the NWTP’s phy- accessed 17 July 2014). Conflicting occurrences from GBIF (e.g. logeny has a strong effect on the divergence time estimates (Fig- palms cultivated in botanic gardens) were excluded. ure S1.1), a close evaluation of its relationship with the extant genus We inferred the biogeographical history of the NWTP using the Sabal was conducted, and its classification within Sabaleae was sup- Maximum Likelihood-based Dispersal–Extinction–Cladogenesis (DEC) ported (Appendix S1). model (Ree & Smith, 2008), with and without the parameter “j”

Divergence time analyses were conducted in BEAST 1.8.0 (Drum- accounting for the probability of founder-event speciation, as imple- mond, Suchard, Xie, & Rambaut, 2012), applying the same partitions mented in the R package “BioGeoBEARS” (Matzke, 2014). The and substitution models as for MRBAYES. Substitution and clock mod- DEC+j model is appropriate in this study since the NWTP occur in els were set as unlinked, whereas tree models were linked among areas that have been isolated (South America, the Caribbean islands) partitions. Clock model tests, using stepping-stone sampling (SSS) and therefore instantaneous speciation in conjunction with long-dis- and Bayes factors (BF, Kass & Raftery, 1995), very strongly favoured tance dispersal may be expected. Analyses were applied to the MCC a relaxed clock with an uncorrelated lognormal distribution (UCLN; tree and tree uncertainty was considered for the interpretation of marginal log-likelihood = À23,641.94, BF = 1,111.67) against a strict results. The tree was pruned to include a single terminal per species. clock (marginal log-likelihood = À24,197.77). We used uniform distri- The maximum number of areas at nodes was restricted to three to butions for UCLN mean priors for each data partition, with default simplify the computational effort and because three is the maximum initial and lower values, and upper values set to 100. To assess the number of areas currently inhabited by any NWTP species. Analyses impact of tree-model selection on our divergence time estimations, were conducted with and without dispersal constraints. Dispersal we compared the median node ages obtained with a Yule versus a constraints (Table S1.4) were applied by assigning different dispersal Birth–Death process model. The differences ranged from 0.10 to probabilities as follows: p = 1 for dispersal between adjacent areas, 2.25 Ma and were markedly smaller than the 95% HPD age bars for p = .5 for dispersal over the Caribbean Sea or through non-adjacent each model (Figure S1.2), indicating that both tree models yield simi- land areas (e.g. between N and S), and p = .01 for dispersal over the lar divergence time estimations. Because tree-model tests strongly Atlantic Ocean (e.g. between S and O) or across the fully formed favoured a Yule Process (marginal log-likelihood = À23,641.94, Northern Andes barrier. As a sensitivity test to parameter choice, BF = 71.65) over a Birth–Death process (marginal log- when the lowest dispersal probability was set to 0.1 instead of 0.01, likelihood = À23,677.76), the Yule tree model was implemented in no significant differences were found in the biogeographical recon- further analyses. struction in terms of likelihood (lnL0.1 = À93.35, lnL0.01 = À91.41; To account for uncertainty in fossil dating and identification, lnL difference <2 log-likelihood units) and relative probabilities (Fig- soft-bound lognormal priors were used for all calibration points, with ure S1.3). standard deviations set such that 95% of the age distribution fell Four time periods were defined: (1) 90–33 Ma: probability of dis- within the geological time period of the fossil stratigraphic source persal from areas O to N through the Beringian and North Atlantic (Table S1.3, Yang & Rannala, 2006). Seven independent chains were land bridges (Brikiatis, 2014); (2) 33–15 Ma: land bridges in the run for 50 9 106 generations, sampling every 10,000th generation. Northern Hemisphere were no longer available (Brikiatis, 2014); (3) All the chains converged and their ESS values were above 200. 15–7 Ma Panama Isthmus closure (Montes et al., 2015); and (4)

Trees files were combined using LOGCOMBINER 1.8.0 and TREEANNOTA- 7 Ma-present final uplift of the Northern Andes acting as a barrier

TOR 1.8.0 (Drummond et al., 2012) was used to exclude the adequate for dispersal between Amazonia and Choco (Luebert & Weiged, proportion of burnin samples and obtain a maximum clade credibility 2014; Table S1.5). (MCC) tree displaying median heights. 2.5 | Diversification analyses 2.4 | Biogeographical analyses We used the R package “TreePar” (Stadler, 2011a) to detect the Five biogeographical areas were defined: (O) Old World, (N) North- existence (if any) and number of diversification rate shifts in the Central America, (S) South America, (I) Panama Isthmus, delimited NWTP phylogeny. A set of 120 trees were randomly chosen from between the El Valle area (Panama) and the Uramita suture the BEAST sampling to calculate maximum likelihood estimates of spe- (Colombia; Montes et al., 2015) and (C) Caribbean islands. The lat- ciation and extinction rates and rate shift times. The function ter were treated as a single area to facilitate understanding of bio- bd.shifts.optimum was set to optimize the model parameters in 100 tic exchanges amongst insular-continental regions. A distinction iterations (maxitk), every 1 Myr (grid), from 90 Ma (end) to 5 Ma between the Greater and the Lesser Antilles was not appropriate (start, and not to 0 Ma to avoid the “pull of the present” effect since most of the NWTP species occur in the Greater Antilles (34 [Nee, Holmes, May, & Harvey, 1994]). To determine how many rate species) and only two widespread species are present in the Lesser shifts are most probable given the phylogenies, models with n and Antilles. Species distributions were compiled from the literature n + 1 shifts were compared with likelihood ratio tests following the (Bernal & Galeano, 2013; Cano, Perret, & Stauffer, 2013; Evans, greedy approach by Stadler (2011a). Mean and standard deviation of 1995; Henderson et al., 1995; Zona, 1990) and from the Global diversification rates and shift ages were calculated across the 120 Biodiversity Information Facility (GBIF, http://www.gbif.org/, trees. CANO ET AL. | 5

To evaluate whether shifts in diversification rate could be attrib- 4.2 log-likelihood units by DEC with dispersal constraints uted to a specific clade we used BAMM 2.0 (Rabosky, 2014; (lnL = À95.6), and by DEC+j without dispersal constraints Appendix S2). Controversy exists regarding the adequacy of BAMM (lnL = À102.4). Biogeographical analyses indicate that the NWTP for diversification rate inference (Moore, Hohna, May, Rannala, & most probably originated in North America (pC = 0.45) sometime Huelsenbeck, 2016). However, recent evaluations of the method during the Late Cretaceous. By the Eocene, Cryosophileae dispersed suggested that diversification rate inference with BAMM is accurate to South America (pS = 0.67) giving rise to the genera Chelyocarpus, and consistent (Rabosky, Mitchell, & Chang, 2017). We used the Itaya, Sabinaria and Trithrinax. Later, during the early Oligocene, extension GeoSSE (Goldberg, Lancaster, & Ree, 2011) of the R pack- members of Cryosophileae dispersed back to North-Central America age “Diversitree” (FitzJohn, Maddison, & Otto, 2009) to test whether and colonized the Caribbean islands (around 28 Ma; 34.1–21.3 Ma). the colonization of the Caribbean islands was associated with shifts Sabaleae most probably started diversifying in an area encompassing in diversification rates (Appendix S2). both North America and the Caribbean islands (pNC = 0.50) or only

Finally, to explore whether the temporal gap between stem and in North America (pN = 0.46). Two unambiguous dispersal events crown ages observed in the NWTP phylogeny could be the signature from the continent to the Caribbean islands were inferred between of mass extinction, instead of low diversification followed by recent 15–4 Ma (9.7 Ma) and between 6–2 Ma (3.7 Ma). radiation, trees were simulated with the R package “TreeSim” (Sta- dler, 2011b). Following the approach by Antonelli and Sanmartın 3.3 | Diversification analyses (2011b), the shapes and the ages of Lineage Through Time (LTT) curves of simulated trees were compared to the LTT curve observed A likelihood ratio test indicated that a model accounting for one rate for the crown NWTP MCC tree. Three sets of simulations were run shift was strongly supported against a model without rate shifts with the function sim.rateshift.taxa, where only 5% of the lineages (mean p = .99, Table S2.1). Models with two or more rate shifts did survived (1) the Cretaceous–Palaeogene Event (66 Ma), (2) the Ter- not improve model fit. Figure 3b shows the mean diversification rate minal Eocene Event (35 Ma) or (3) the mid-Miocene cooling (12 Ma). as a function of time with 80% confidence interval across the 120 In all sets, the speciation (0.223) and extinction (0.180) rates were trees sampled. A diversification rate shift was estimated around kept constant (values extracted from “TreePar” for 0 shifts), and 200 10.8 Ma (SD = 8.0). Mean diversification rates were trees were simulated to reflect stochastic variance, with a final num- 0.012 Æ 0.014 MaÀ1 before the rate shift and 0.15 Æ 0.05 MaÀ1 ber of 54 terminals (the number of terminals in the crown NWTP after it. No significant rate shifts were detected in specific branches MCC tree) and accounting for the missing taxa with frac = 0.93. of the MCC tree (Figure S2.6) and diversification rate in Caribbean lineages was not significantly different from that of continental clades (Appendix S2). 3 | RESULTS Most of the trees simulated with a mass extinction occurring 66 Ma did not display the broom-and-handle shape of the empirical 3.1 | Phylogenetic analyses tree and the crown ages of these trees were younger than the The analyses of four independent loci support the sister relationship crown NWTP age (Figure 4a; median crown age: 47 Ma, range of between the tribes Cryosophileae and Sabaleae (posterior probability crown ages: 166.7–19.1 Ma). The majority of the trees simulated [PP] >0.90, see Figures S2.2–5 in Appendix S2). They are not sister under a mass extinction 35 Ma displayed the same broom-and-han- in the CISP4 gene tree (Figure S2.1) but the alternative relationships dle shape as our empirical crown NWTP tree (Figure 4b); the crown are not supported (PP < 0.90). The comparison of individual gene age of our empirical NWTP tree (77 Ma; 78.7–76.1 Ma) fell within trees did not reveal other topological incongruences with PP >0.95. the lower quartile of crown ages of simulated trees, which ranged

MRBAYES and BEAST analyses of the combined partitioned dataset from 203.9 to 21.8 Ma (median crown age: 103 Ma). Most of the recovered congruent results and the MCC tree from BEAST is shown trees simulated with a mass extinction occurring 12 Ma did not dis- in Figure 2. play the broom-and-handle shape of the empirical tree and their crown ages were older than the crown NWTP age (Figure 4c; median crown age = 115 Ma, range of crown ages: 187.2–74.1 Ma). 3.2 | Divergence time and ancestral range estimation 4 | DISCUSSION Calibration analyses (Figure 2) inferred crown ages for the NWTP in the Late Cretaceous (77 Ma [age values correspond to median 4.1 | Divergence times and historical biogeography heights estimated with BEAST]; 78.7–76.1 Ma [age ranges correspond to 95% HPD ranges estimated with BEAST]), for Cryosophileae in the 4.1.1 | Origin of the NWTP in time and space Eocene (45 Ma; 56.2–34.6 Ma), and for Sabaleae in the Miocene (14 Ma; 18.7–9.6 Ma). With all genera and 84% of species sampled, our MCC tree (Fig- The most likely biogeographical model was DEC+j with dispersal ure 2) constitutes the most complete phylogenetic hypothesis constraints (lnL = À91.4; Figure 3a), followed with a difference of assembled to date for the NWTP. Our results are congruent with 6 | CANO ET AL.

FIGURE 2 Maximum clade credibility (MCC) tree of Cryosophileae and Sabaleae estimated using BEAST. All posterior probabilities were above 0.90, unless otherwise indicated. Bars indicate 95% highest posterior densities of ages. The three fossils used for calibration are: (1) Sabalites carolinensis, (2) Hyphaene kappelmanii and (3) Sabal bigbendense (inset, fossil seed modified from Manchester et al. [2010], bar scale 5 mm) are indicated with their placement on the tree. Trithrinax campestris from Cordoba (Argentina) is shown (bottom left; credit Angela Cano) CANO ET AL. | 7

FIGURE 3 Biogeographical and diversification patterns of Cryosophileae and Sabaleae. (a) Ancestral ranges estimated using the Dispersal– Extinction–Cladogenesis +j model. Pie charts represent the relative probabilities of ancestral areas, where white represents 4th to last probable states combined. Inset: biogeographical regions. (b) overall net diversification rate from 90 to 5 Ma (the period from 5 to 0 Ma was excluded to avoid the “pull of the present” effect [Nee et al., 1994]), where the black curve is the mean diversification rate estimated from 120 trees, the grey area is the 80% confidence interval and a rate shift at 10.8 Ma, detected with the “TreePar” analysis, is marked by a dashed line 8 | CANO ET AL.

FIGURE 4 Lineages Through Time (LTT) curve of the New World Thatch Palms (black) plotted together with LTT curves of 200 trees (grey) simulated under mass extinction conditions (5% lineage survival) (a) Cretaceous–Palaeogene Event (66 Ma), (b) Terminal Eocene Event (35 Ma), (c) Mid-Miocene Event, with speciation (0.223) and extinction (0.180) rates extracted from the “TreePar” analysis of 0 shifts. Boxplots summarize the simulated trees’ crown ages: the median is indicated by a vertical line that divides the 25th and 75th percentiles of the data, and the whiskers show the maximum and minimum values excluding outliers previous molecular phylogenetic studies and morphological studies Our most probable scenario hypothesizes that, from North (see Appendix S3 for further discussion). However, divergence time America Cryosophileae colonized South America where they began analyses (Figure 2) inferred much older node ages for the stem and to diversify around 45 Ma (56.2–34.6 Ma). This dispersal likely crown of the NWTP (median ages 82 and 77 Ma respectively), and occurred overwater or via stepping stones along the Proto-Antilles for the crown of Cryosophileae (45 Ma), than previously estimated that may have facilitated the Eocene colonization of South America, (e.g. Couvreur et al., 2011; Faurby, Eiserhardt, Baker, & Svenning, as inferred for the arecoid palm tribe Chamaedoreeae (45 Ma; 2016; Figure S2.7). The use of different taxonomic sampling, dating Cuenca et al., 2008) and other plant groups including Chrysobal- methods or calibration points could explain those differences. Here, anaceae (47 Ma, Bardon et al., 2013), Cinchonoideae (Rubiaceae, however, the most likely explanation is our use of the fossil Sabal 49.2 Ma; Antonelli, Nylander, Persson, & Sanmartın, 2009) and Helio- bigbendense (Manchester et al., 2010), which strongly influenced esti- tropium (Heliotropiaceae; 45.7 Ma, Luebert, Hilger, & Weigend, mates of divergence times (Figure S1.1) and which has not previ- 2011), among others. Diversification of Cryosophileae gave rise to ously been considered in divergence-time analyses of palms. We do lineages that today occur in subtropical South America (Trithrinax) not think we placed the fossil calibration incorrectly because our and in Western Amazonia (Chelyocarpus and Itaya). Such distribu- reassessment of its affinities (Appendix S1) confirmed Manchester tions, deep inland in the tropical rain forest, are quite distinct from et al.’s (2010) placement of it in Sabal. We predict that the calibrated those of other Cryosophileae which occur closer to the coast. How- molecular dating palm genera by Couvreur et al. (2011) would have ever, during the Miocene a marine incursion prolonged by the estimated older node ages for the NWTP if they had used the fossil Palaeo-Orinoco fluvial system periodically connected the Western S. bigbendense as a node constraint. The downstream consequences Amazonian drainage to the Caribbean coast (Hoorn et al., 2010; Jar- of this are minor for the NWTP diversification studies, since its bio- amillo et al., 2017; Salamanca Villegas et al., 2016). We postulate geographical history is here explored for the first time in detail. that this marine incursion and its wetland extensions could have However, further evaluation of S. bigbendense as a calibration point provided corridors facilitating the propagation of these palms deep is necessary to assess the biogeography of palms at the global scale. inside South America. Our biogeographical estimation indicates that the most recent common ancestor of the NWTP was most probably distributed in 4.1.2 | Multiple dispersal events to the Caribbean Laurasia (Figure 3a; P = 0.45) but other geographical origins for N islands the NWTP were also recovered although with lower relative probabilities (Figure 3a; PS = 0.23, PNS = 0.14). A Laurasian origin agrees Our biogeographical reconstruction inferred four dispersal events with the scenario posed by Baker and Couvreur (2013a) in which from the mainland to the Caribbean islands. The most probable sce- the origin of the NWTP was inferred to be North America. It is nario had Cryosophileae first dispersing from South America, into also consistent with fossils of Sabal and Cryosophileae occurring in North-Central America around 31 Ma (38.9–24.9 Ma), then into the a wide range of localities in the Northern Hemisphere, including Caribbean islands around 28 Ma (34.1–21.3 Ma; Figure 3a). Such Europe, since the Early Eocene for Sabal and Early Oligocene for dispersal could have happened overwater, as has been inferred for Cryosophileae (Figure 1; Manchester et al., 2010; Thomas & De various groups of animals (e.g. Fabre et al., 2014) and plants (Cer- Franceschi, 2012). Taken together, these elements indicate that vantes et al., 2016). Although less likely, our reconstruction also ancestors of the NWTP were probably a component of the attributed a probability (pNC = 0.17, pC = 0.16) to the hypothesis Boreotropical plant assemblage that covered most of the southern that the Cryosophileae first colonized the Caribbean islands from part of North America and Eurasia during the Palaeocene and early South America during the early Oligocene (Figure 3a). This alterna- Eocene (Bjorholm et al., 2006). tive dispersal route coincides with the hypothesized GAARlandia CANO ET AL. | 9 corridor (Iturralde-Vinent & MacPhee, 1999) that might have existed Cook, 2009), and our simulations indicate that this hypothesis can- around the same time, although evidence supporting the existence not be rejected for the NWTP. The shapes and ages of LTT plots of of this corridor is not conclusive (Ali, 2012; Nieto-Blazquez et al., trees simulated under a mass extinction at the Terminal Eocene 2017). Event (35 Ma) match most closely those of the NWTP (Figure 4b). Our results also identify more recent island-mainland exchanges Contrastingly, simulations of a mass extinction at the Cretaceous– (Figure 3). Dispersal from North-Central America into the Caribbean Palaeogene transition (66 Ma) and at the mid-Miocene (12 Ma), did islands during the Pliocene probably gave rise to the Caribbean not show the same pattern: crown ages from these simulated mass endemic clade of Sabal causiarum, S. domingensis and S. maritima. extinctions are either too young or too old and show a less evident During the same period, dispersal events in the opposite direction broom-and-handle shape (Figure 4a,c). These results suggest that the were also inferred in Cryosophileae explaining the extant distribution diversification pattern reconstructed for the NWTP could be related of Coccothrinax argentata and Thrinax radiata in North-Central Amer- to a mass extinction event at the Terminal Eocene and a later re- ica. These frequent overwater dispersal events reconstructed for the diversification of the surviving lineages at lower latitudes since the NWTP corroborate Baker and Couvreur’s (2013a) observation that mid-Miocene. The colder conditions at the end of the Eocene could long-distance dispersal is a key mechanism underpinning the distri- explain why these elements of the Boreotropical flora were extir- bution of palm lineages. pated from the northern latitudes (Figure 1; Bjorholm et al., 2006) and may reflect events in other evergreen frost-intolerant taxa that were once part of the Boreotropical flora but became extinct or 4.2 | Diversification of the NWTP: radiation in the migrated southwards (Jaramillo, Rueda, & Mora, 2006; Morley, Caribbean or mass extinction? 2003). Nevertheless, we have not excluded the possibility that a Ter- We did not find evidence that the diversification rate of the NWTP minal Eocene extinction event overwrote the signature of an earlier in the Caribbean was higher than in continental areas (Appendix S2) extinction (e.g. Cretaceous–Palaeogene) from the diversification pat- but there was a rate shift across the group as a whole between 13.7 terns recovered for the NWTP. and 6.2 Ma (10.8 Ma; Figure 3). Although diversification in Coc- cothrinax, Cryosophila and Sabal increased around that time, rate shifts were not significant in any of these specific lineages (Fig- 5 | CONCLUSIONS ure S2.6), contradicting a previous diversification analysis that reported a significant rate shift at the stem node of Coccothrinax We identified two main biogeographical explanations for the distri- (Baker & Couvreur, 2013b). The difference might be explained by bution of the NWTP in the Caribbean region and surrounding land- sampling: the latter included only one representative of each genus masses. First, a pre-Panama Isthmus colonization of South America with diversification rate derived from species counts, whereas we from Laurasia during the Eocene, following a dispersal route shared used a species-level phylogeny but with four of the 14 species by other Boreotropical plants (e.g. Antonelli et al., 2009; Bardon excluded because of missing data. Also, the rate shift detected by et al., 2013; Cuenca et al., 2008; Luebert et al., 2011). Second, a our “TreePar” analyses occurred about 17 Myr after the recon- recolonization of North-Central America around 31 Ma (38.9– structed dispersal of Cryosophileae into the islands rather than con- 24.9 Ma) and a subsequent dispersal to the Caribbean islands around temporaneous with colonization. Therefore, a causal link between 28 Ma (34.1–21.3), which most probably occurred overwater rather island colonization and increased diversification is rejected for the than through GAARlandia. Later overwater dispersal events appear NWTP. Instead, the diversification rate increase coincides temporally to have contributed little to the Caribbean species richness of the with the mid-Miocene cooling that enhanced the expansion of arid NWTP, which mainly underwent local diversification. We did not and semi-arid environments in tropical America (Graham, 2010). find that island lineages diversified at a higher rate than those on Since the greatest diversity of the NTWP is found in dry environ- continents. Instead, we suggest that the diversification history of ments outside the tropical rain forest (e.g. Coccothrinax and Sabal), these palms, with a long temporal gap from their origin to the begin- we hypothesize that the shift to increased seasonality during the ning of their diversification, could reflect the signature of mass mid-Miocene could have triggered an increase in diversification rate extinction. The global climatic cooling at the end of the Eocene for the NWTP, as in other plant groups such as Cactaceae and might have had a more significant impact on the diversity and distri- cycads (Arakaki et al., 2011; Condamine, Nagalingum, Marshall, & bution of Caribbean plants. Morlon, 2015). The wider geographical distribution of the NWTP in the past ACKNOWLEDGEMENTS than today (Figure 1) and the two particularly long branches (at least 20 and 57 Myr) leading to the crown nodes of Cryosophileae and A.C. was supported by the International Palm Society Endowment Sabaleae (Figure 2), suggest that extinctions could also have Fund, the Augustin Lombard grant, the Commission of the travel impacted the diversification of these tribes. Indeed, tree simulations grant and the Foundation Dr. Joachim de Giacomi of the Academie have demonstrated that broom-and-handle patterns can result from des sciences naturelles Suisse, the International Association for Plant ancient mass extinction (Antonelli & Sanmartın, 2011b; Crisp & Taxonomy and the Fondation Schmidheiny. M.P. was funded by the 10 | CANO ET AL.

Swiss National Science Foundation (31003A_175655/1). C.D.B. and Journal of Biogeography, 40, 286–298. https://doi.org/10.1111/j. A.A. were funded by the Swedish (B0569601) and European 1365-2699.2012.02794.x Baldwin, B. G., & Sanderson, M. J. (1998). Age and rate of diversification (331024; FP/2007-2013) Research Councils, a Wallenberg Academy of the Hawaiian silversword alliance (Compositae). Proceedings of the Fellowship and the Swedish Foundation for Strategic Research. We National Academy of Sciences, 95, 9402–9406. https://doi.org/10. † thank R. Bernal, G. Galeano , H.F. Manrique (JBQ), M. Gonzalez, S. 1073/pnas.95.16.9402 Da-Giau, P. Griffith and L. Noblick (MBC), C.E. Lewis, C. Husby and Bardon, L., Chamagne, J., Dexter, K. G., Sothers, C. A., Prance, G. T., & Chave, J. (2013). Origin and evolution of Chrysobalanaceae: Insights M. Griffiths (FTBG), and R. Niba for facilitating samples and data col- into the evolution of plants in the Neotropics. Botanical Journal of the ı lection and I. Sanmart n for her guidance in the simulation analyses. Linnean Society, 171,19–37. https://doi.org/10.1111/j.1095-8339. We thank M.N. Dawson, L. Cook and J. Roncal for their valuable 2012.01289.x insights into the manuscript. Bernal, R., & Galeano, G. (2013). Sabinaria, a new genus of palms (Cryo- sophileae, Coryphoideae, Arecaceae) from the Colombia-Panama bor- der. Phytotaxa, 144,27–44. https://doi.org/10.11646/phytotaxa.144. ORCID 2.1 Bjorholm, S., Svenning, J.-C., Baker, W. J., Skov, F., & Balslev, H. (2006). Angela Cano http://orcid.org/0000-0002-5090-7730 Historical legacies in the geographical diversity patterns of New Christine D. Bacon http://orcid.org/0000-0003-2341-2705 World palm (Arecaceae) subfamilies. Botanical Journal of the Linnean Society, 151, 113–125. https://doi.org/10.1111/j.1095-8339.2006. 00527.x Brikiatis, L. (2014). The De Geer, Thulean and Beringia routes: Key con- REFERENCES cepts for understanding early Cenozoic biogeography. Journal of Bio- geography, 41, 1036–1054. https://doi.org/10.1111/jbi.12310 Acevedo-Rodrıguez, P., & Strong, M. T. (2008). Floristic richness and Brocklehurst, N., Ruta, M., Muller,€ J., & Frobisch,€ J. (2015). Elevated affinities in the West Indies. The Botanical Review, 74,5–36. https://d extinction rates as a trigger for diversification rate shifts: Early oi.org/10.1007/s12229-008-9000-1 amniotes as a case study. Scientific Reports, 5, 17104. https://doi.org/ Ali, J. R. (2012). Colonizing the Caribbean: Is the GAARlandia land-bridge 10.1038/srep17104 hypothesis gaining a foothold?: Commentary. Journal of Biogeography, Cano, A., Perret, M., & Stauffer, F. W. (2013). A revision of the genus 39, 431–433. https://doi.org/10.1111/j.1365-2699.2011.02674.x Trithrinax (Cryosophileae, Coryphoideae, Arecaceae). Phytotaxa, 136, Antonelli, A., Nylander, J. A., Persson, C., & Sanmartın, I. (2009). Tracing 1–53. the impact of the Andean uplift on Neotropical plant evolution. Pro- Cervantes, A., Fuentes, S., Gutierrez, J., Magallon, S., & Borsch, T. (2016). ceedings of the National Academy of Sciences, 106, 9749–9754. Successive arrivals since the Miocene shaped the diversity of the https://doi.org/10.1073/pnas.0811421106 Caribbean Acalyphoideae (Euphorbiaceae). Journal of Biogeography, Antonelli, A., & Sanmartın, I. (2011a). Why are there so many plant spe- 43, 1773–1785. https://doi.org/10.1111/jbi.12790 cies in the Neotropics? Taxon, 60, 403–414. Condamine, F. L., Leslie, A. B., & Antonelli, A. (2016). Ancient islands Antonelli, A., & Sanmartın, I. (2011b). Mass extinction, gradual cooling, or acted as refugia and pumps for conifer diversity. Cladistics, 33,69– rapid radiation? Reconstructing the spatiotemporal evolution of the 92. ancient Angiosperm genus Hedyosmum (Chloranthaceae) using empiri- Condamine, F. L., Nagalingum, N. S., Marshall, C. R., & Morlon, H. (2015). cal and simulated approaches. Systematic Biology, 60, 596–615. Origin and diversification of living cycads: A cautionary tale on the https://doi.org/10.1093/sysbio/syr062 impact of the branching process prior in Bayesian molecular dating. Arakaki, M., Christin, P.-A., Nyffeler, R., Lendel, A., Eggli, U., Ogburn, R. BMC Evolutionary Biology, 15, 65. https://doi.org/10.1186/s12862- M., ... Edwards, E. J. (2011). Contemporaneous and recent radiations 015-0347-8 of the world’s major succulent plant lineages. Proceedings of the Couvreur, T. L., Forest, F., & Baker, W. J. (2011). Origin and global diver- National Academy of Sciences, 108, 8379–8384. https://doi.org/10. sification patterns of tropical rain forests: Inferences from a complete 1073/pnas.1100628108 genus-level phylogeny of palms. BMC Biology, 9, 44. https://doi.org/ Bacon, C. D., Baker, W. J., & Simmons, M. P. (2012). Miocene dispersal 10.1186/1741-7007-9-44 drives island radiations in the palm tribe Trachycarpeae (Arecaceae). Crisp, M. D., & Cook, L. G. (2009). Explosive radiation or cryptic mass Systematic Biology, 61, 426–442. https://doi.org/10.1093/sysbio/ extinction? Interpreting signatures in molecular phylogenies. Evolution, syr123 63, 2257–2265. https://doi.org/10.1111/j.1558-5646.2009.00728.x Bacon, C. D., Mora, A., Wagner, W. L., & Jaramillo, C. A. (2013). Testing Cuenca, A., Asmussen-Lange, C. B., & Borchsenius, F. (2008). A dated geological models of evolution of the Isthmus of Panama in a phylo- phylogeny of the palm tribe Chamaedoreeae supports Eocene disper- genetic framework. Botanical Journal of the Linnean Society, 171, sal between Africa, North and South America. Molecular Phylogenetics 287–300. https://doi.org/10.1111/j.1095-8339.2012.01281.x and Evolution, 46, 760–775. https://doi.org/10.1016/j.ympev.2007. Bacon, C. D., Silvestro, D., Jaramillo, C., Smith, B. T., Chakrabarty, P., & 10.010 Antonelli, A. (2015). Biological evidence supports an early and com- Dransfield, J. B., Uhl, N. W., Asmussen, C. B., Baker, W. J., Harley, M. M., plex emergence of the Isthmus of Panama. Proceedings of the National & Lewis, C. E. (2008). Genera Palmarum - The evolution and classifica- Academy of Sciences, 112, 6110–6115. https://doi.org/10.1073/pnas. tion of palms. Richmond, UK: Kew Publishing. 1423853112 Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian Baker, W. J., & Couvreur, T. L. P. (2013a). Global biogeography and phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and diversification of palms sheds light on the evolution of tropical lin- Evolution, 29, 1969–1973. https://doi.org/10.1093/molbev/mss075 eages. I. Historical biogeography. Journal of Biogeography, 40, 274– Evans, R. J. (1995). Systematics of Cryosophila (Palmae). Systematic Bot- 285. any Monographs, 46,1–70. https://doi.org/10.2307/25027854 Baker, W. J., & Couvreur, T. L. P. (2013b). Global biogeography and Fabre, P.-H., Vilstrup, J. T., Raghavan, M., Sarkissian, C. D., Willerslev, E., diversification of palms sheds light on the evolution of tropical lin- Douzery, E. J. P., & Orlando, L. (2014). Rodents of the Caribbean: eages. II. Diversification history and origin of regional assemblages. Origin and diversification of hutias unravelled by next-generation CANO ET AL. | 11

museomics. Biology Letters, 10, 20140266. https://doi.org/10.1098/ (Heliotropiaceae, Boraginales). Molecular Phylogenetics and Evolution, rsbl.2014.0266 61,90–102. https://doi.org/10.1016/j.ympev.2011.06.001 Faurby, S., Eiserhardt, W. L., Baker, W. J., & Svenning, J.-C. (2016). An Luebert, F., & Weiged, M. (2014). Phylogenetic insights into Andean plant all-evidence species-level supertree for the palms (Arecaceae). Molec- diversification. Frontiers in Ecology and Evolution, 2,1–17. ular Phylogenetics and Evolution, 100,57–69. https://doi.org/10. Manchester, S. R., Lehman, T. M., & Wheeler, E. A. (2010). Fossil palms 1016/j.ympev.2016.03.002 (Arecaceae, Coryphoideae) associated with juvenile herbivorous dino- Filipowicz, N., & Renner, S. S. (2012). Brunfelsia (Solanaceae): A genus saurs in the Upper Cretaceous Aguja Formation, Big Bend National evenly divided between South America and radiations on Cuba and Park, Texas. International Journal of Plant Sciences, 171, 679–689. other Antillean islands. Molecular Phylogenetics and Evolution, 64,1– https://doi.org/10.1086/653688 11. https://doi.org/10.1016/j.ympev.2012.02.026 Matzke, N. J. (2014). Model selection in historical biogeography reveals FitzJohn, R. G., Maddison, W. P., & Otto, S. P. (2009). Estimating trait- that founder-event speciation is a crucial process in island clades. dependent speciation and extinction rates from incompletely resolved Systematic Biology, 63, 951–970. https://doi.org/10.1093/sysbio/ phylogenies. Systematic Biology, 58, 595–611. https://doi.org/10. syu056 1093/sysbio/syp067 Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Francisco-Ortega, J., Santiago-Valentın, E., Acevedo-Rodrıguez, P., Lewis, Science Gateway for inference of large phylogenetic trees. In Pro- C., Pipoly, J., Meerow, A. W., & Maunder, M. (2007). Seed plant gen- ceedings of the gateway computing environments workshop (GCE), New era endemic to the Caribbean Island biodiversity hotspot: A review Orleans, USA, pp. 1-8. and a molecular phylogenetic perspective. The Botanical Review, 73, Montes, C., Cardona, A., Jaramillo, C., Pardo, A., Silva, J. C., Valencia, V., 183–234. https://doi.org/10.1663/0006-8101(2007)73[183:SPGETT] ... Nino,~ H. (2015). Middle Miocene closure of the Central American 2.0.CO;2 Seaway. Science, 348, 226–229. https://doi.org/10.1126/science.aaa Goldberg, E. E., Lancaster, L. T., & Ree, R. H. (2011). Phylogenetic infer- 2815 ence of reciprocal effects between geographic range evolution and Moore, B. R., Hohna, S., May, M. R., Rannala, B., & Huelsenbeck, J. P. diversification. Systematic Biology, 60, 451–465. https://doi.org/10. (2016). Critically evaluating the theory and performance of Bayesian 1093/sysbio/syr046 analysis of macroevolutionary mixtures. Proceedings of the National Graham, A. (2003). Historical phytogeography of the Greater Antilles. Academy of Sciences of the United States of America, 113, 9569–9574. Brittonia, 55, 357–383. https://doi.org/10.1663/0007-196X(2003) https://doi.org/10.1073/pnas.1518659113 055[0357:HPOTGA]2.0.CO;2 Morley, R. J. (2003). Interplate dispersal paths for megathermal angios- Graham, A. (2010). Late Cretaceous and Cenozoic History of Latin American perms. Perspectives in Plant Ecology, Evolution and Systematics, 6,5– Vegetation and Terrestrial Environments. St. Louis, MO: Missouri 20. https://doi.org/10.1078/1433-8319-00039 Botanical Garden Press. Nee, S., Holmes, E. C., May, R. M., & Harvey, P. H. (1994). Extinction Gugger, P. F., & Cavender-Bares, J. (2013). Molecular and morphologi- rates can be estimated from molecular phylogenies. Phylosophical cal support for a Florida origin of the Cuban oak. Journal of Bio- Transactions of the Royal Society B, 344,77–82. https://doi.org/10. geography, 40, 632–645. https://doi.org/10.1111/j.1365-2699.2011. 1098/rstb.1994.0054 02610.x Nieto-Blazquez, M. E., Antonelli, A., & Roncal, J. (2017). Historical bio- Henderson, A., Galeano, G., & Bernal, R. (1995). Field guide to the palms geography of endemic seed plant genera in the Caribbean: Did of the Americas. Princeton, NJ, USA: Princeton University Press. GAARlandia play a role? Ecology and Evolution, 7, 10158–10174. Hoorn, C., Wesselingh, F. P., ter Steege, H., Bermudez, M. A., Mora, A., & https://doi.org/10.1002/ece3.3521 Sevink, J., ... Antonelli, A. (2010). Amazonia through time: Andean Nylander, J. A. (2004). MrAIC.pl. Program distributed by the author. Upp- uplift, climate change, landscape evolution, and biodiversity. Science, sala, Sweden: Evolutionary Biology Centre, Uppsala University. 330, 927–931. https://doi.org/10.1126/science.1194585 O’Dea, A., Lessios, H. A., Coates, A. G., Eytan, R. I., Restrepo-Moreno, S. Iturralde-Vinent, M., & MacPhee, R. D. (1999). Paleogeography of the A., & Cione, A. L., ... Jackson, J. B. (2016). Formation of the Isthmus Caribbean region: Implications for Cenozoic biogeography. Bulletin of of Panama. Science Advances, 2, e1600883. https://doi.org/10.1126/ the American Museum of Natural History, 238,1–95. sciadv.1600883 Jaramillo, C., Romero, I., D’Apolito, C., Bayona, G., Duarte, E., Louwye, S., Oleas, N., Jestrow, B., Calonje, M., Peguero, B., Jimenez, F., Rodrıguez- ... Wesselingh, F. P. (2017). Miocene flooding events of western Pena,~ R., ... Francisco-Ortega, J. (2013). Molecular systematics of Amazonia. Science Advances, 3, e1601693. https://doi.org/10.1126/ threatened seed plant species endemic in the Caribbean Islands. The sciadv.1601693 Botanical Review, 79, 528–541. https://doi.org/10.1007/s12229-013- Jaramillo, C., Rueda, M. J., & Mora, G. (2006). Cenozoic plant diversity in 9130-y the Neotropics. Science, 311, 1893–1896. https://doi.org/10.1126/sc Penn, O., Privman, E., Ashkenazy, H., Landan, G., Graur, D., & Pupko, T. ience.1121380 (2010). GUIDANCE: A web server for assessing alignment confidence Jordan, G., & Goldman, N. (2012). The effects of alignment error and scores. Nucleic Acids Research, 38, W23–W28. https://doi.org/10. alignment filtering on the sitewise detection of positive selection. 1093/nar/gkq443 Molecular Biology and Evolution, 29, 1125–1139. https://doi.org/10. Rabosky, D. L. (2014). Automatic detection of key innovations, rate 1093/molbev/msr272 shifts, and diversity-dependence on phylogenetic trees. PLoS ONE, 9, Kass, R. E., & Raftery, A. E. (1995). Bayes factors. Journal of the American e89543. https://doi.org/10.1371/journal.pone.0089543 Statistical Association, 90, 773–795. https://doi.org/10.1080/ Rabosky, D. L., Mitchell, J. S., & Chang, J. (2017). Is BAMM flawed? The- 01621459.1995.10476572 oretical and practical concerns in the analysis of multi-rate diversifi- Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: A novel cation models. Systematic Biology, 66, 477–498. https://doi.org/10. method for rapid multiple sequence alignment based on fast Fourier 1093/sysbio/syx037 transform. Nucleic Acids Research, 30, 3059–3066. https://doi.org/10. Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2014). Tracer 1093/nar/gkf436 v1.6. Retrieved from http://beast.bio.ed.ac.uk/Tracer. Losos, J. B., & Ricklefs, R. E. (2009). Adaptation and diversification on Ree, R. H., & Smith, S. A. (2008). Maximum likelihood inference of geo- islands. Nature, 457, 830–836. https://doi.org/10.1038/nature07893 graphic range evolution by dispersal, local extinction, and cladogene- Luebert, F., Hilger, H. H., & Weigend, M. (2011). Diversification in the sis. Systematic Biology, 57,4–14. https://doi.org/10.1080/ Andes: Age and origins of South American Heliotropium lineages 10635150701883881 12 | CANO ET AL.

Ricklefs, R., & Bermingham, E. (2008). The West Indies as a laboratory of soft bounds. Molecular Biology and Evolution, 23, 212–226. https://d biogeography and evolution. Philosophical Transactions of the Royal oi.org/10.1093/molbev/msj024 Society B: Biological Sciences, 363, 2393–2413. https://doi.org/10. Zachos, J. C., Dickens, G. R., & Zeebe, R. E. (2008). An early Cenozoic 1098/rstb.2007.2068 perspective on greenhouse warming and carbon-cycle dynamics. Nat- Roncal, J., Zona, S., & Lewis, C. E. (2008). Molecular phylogenetic studies ure, 451, 279–283. https://doi.org/10.1038/nature06588 of Caribbean Palms (Arecaceae) and their relationships to biogeogra- Zona, S. (1990). A monograph of Sabal (Arecaceae: Coryphoideae). Aliso, phy and conservation. The Botanical Review, 74,78–102. https://doi. 12, 583–666. https://doi.org/10.5642/aliso org/10.1007/s12229-008-9005-9 Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Hohna,€ S., ...Huelsenbeck, J. P. (2012). MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. System- BIOSKETCH atic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029 Rull, V. (2011). Neotropical biodiversity: Timing and potential drivers. Angela Cano is interested in understanding how ecological and Trends in Ecology & Evolution, 26, 508–513. https://doi.org/10.1016/j. evolutionary processes shape tropical forest biodiversity. She is tree.2011.05.011 mainly focused on the Neotropical region and uses palms as a Salamanca Villegas, S., van Soelen, E. E., Tunissen, M. L., Flantua, S. G. A., model to unravel the historical assembly of its flora. She con- Ventura, R., Roddaz, M., ... Hoorn, C. (2016). Amazon forest dynamics under changing abiotic conditions in the early Miocene (Colom- ducted her PhD at the University of Geneva and the Botanical bian Amazonia). Journal of Biogeography, 43, 2424–2437. https://doi. Garden of Geneva, in collaboration with the Antonelli Lab at the org/10.1111/jbi.12769 University of Gothenburg. Santiago-Valentin, E., & Olmstead, R. G. (2004). Historical biogeography of Caribbean plants: Introduction to current knowledge and possibili- Author contributions: M.P., F.W.S., A.C., A.A. and C.D.B. con- ties from a phylogenetic perspective. Taxon, 53, 299–319. https://d ceived the ideas; A.C. and F.W.S. collected the data; A.C., M.L.S- oi.org/10.2307/4135610 Schulte, P., Alegret, L., Arenillas, I., Arz, J. A., Barton, P. J., & Bown, P. R., S. and C.D.B. analysed the data; and A.C., M.P., C.D.B., A.A. and ... Willumsen, P. S. (2010). The Chicxulub asteroid impact and mass F.W.S. participated in the writing of the manuscript. extinction at the Cretaceous-Paleogene boundary. Science, 327, 1214–1218. https://doi.org/10.1126/science.1177265 Stadler, T. (2011a). Mammalian phylogeny reveals recent diversification rate shifts. Proceedings of the National Academy of Sciences, 108, SUPPORTING INFORMATION 6187–6192. https://doi.org/10.1073/pnas.1016876108 Stadler, T. (2011b). Simulating trees with a fixed number of extant spe- Additional Supporting Information may be found online in the cies. Systematic Biology, 60, 676–684. https://doi.org/10.1093/sysb supporting information tab for this article. io/syr029 Thomas, R., & De Franceschi, D. (2012). First evidence of fossil Cryoso- phileae (Arecaceae) outside the Americas (early Oligocene and late Miocene of France): Anatomy, palaeobiogeography and evolutionary How to cite this article: Cano A, Bacon CD, Stauffer FW, implications. Review of Palaeobotany and Palynology, 171,27–39. https://doi.org/10.1016/j.revpalbo.2011.11.010 Antonelli A, Serrano-Serrano ML, Perret M. The roles of van Ee, B. W., Berry, P. E., Riina, R., & Gutierrez Amaro, J. E. (2008). dispersal and mass extinction in shaping palm diversity across Molecular phylogenetics and biogeography of the Caribbean-centered the Caribbean. J Biogeogr. 2018;00:1–12. https://doi.org/ Croton subgenus Macoroton (Euphorbiaceae s.s.). The Botanical 10.1111/jbi.13225 Review, 74, 132–165. Yang, Z., & Rannala, B. (2006). Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with

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