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

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The Roles of Dispersal and Mass Extinction in Shaping Palm Diversity Across the Caribbean DOI: 10.1111/jbi.13225 RESEARCH PAPER The roles of dispersal and mass extinction in shaping palm diversity across the Caribbean Angela Cano1,2 | Christine D. Bacon2,3 | Fred W. Stauffer1 | Alexandre Antonelli2,3,4 | Martha L. Serrano-Serrano5 | Mathieu Perret1 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 | Journal of Biogeography. 2018;1–12. wileyonlinelibrary.com/journal/jbi © 2018 John Wiley & Sons Ltd 1 2 | CANO ET AL. 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)
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