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Colonizing the Caribbean: Biogeography and Evolution Of Journal of Biogeography (J. Biogeogr.) (2016) ORIGINAL Colonizing the Caribbean: biogeography ARTICLE and evolution of livebearing fishes of the genus Limia (Poeciliidae) Pablo F. Weaver1,2*, Alexander Cruz2, Steven Johnson1, Julia Dupin2 and Kathleen F. Weaver1 1Department of Biology, University of La ABSTRACT Verne, 1950 3rd St., La Verne, CA 91750, Aim We investigate the origin and colonization of the West Indian endemic USA, 2Department of Ecology and freshwater fish group Limia. We evaluate the leading hypotheses for the origins Evolutionary Biology, University of Colorado, Boulder, CO 80309-0334, USA of West Indian life, including trans-oceanic dispersal, late Cretaceous vicari- ance, and the GAARlandia land bridge at the Eocene/Oligocene boundary. Location Greater Antilles, with extensive sampling in the Dominican Republic. Methods We obtained DNA from wild sampling and the aquarium trade. We sequenced three mitochondrial (12S, ND2 and Cytb) and two nuclear genes (Rh, MYH6) for a combined molecular phylogenetic analysis to evaluate spe- cies relationships and the timing of divergence events between islands and the mainland. We used Bayesian and likelihood approaches to build phylogenies, a BEAST analysis to establish the timing of colonization, and R package BioGeo- BEARS to perform a historical biogeographical reconstruction. Results Relaxed molecular clock results show that the ancestor to the West Indian clade, which includes the Limia and Hispaniolan Poecilia, diverged from a South American ancestor at the Eocene/Oligocene boundary. The basal Jamaican species, L. melanogaster, split from the rest of Limia at the Oligocene/ Miocene boundary. Cuban and Cayman taxa are sister to a diverse species group from Hispaniola. Historical biogeographical reconstruction supported the GAARlandia DEC+j model as the best fitting model for colonization. Main conclusions Our results support a colonization model for Limia that is concordant with the timing of GAARlandia and climate change during the Eocene/Oligocene boundary. Limia colonization was most likely a result of facilitated dispersal during a period of lower sea levels and shorter passage along the Aves Ridge. These results are also consistent with other recent molec- ular clock studies of dispersal limited cichlids, toads and frogs, indicating a growing body of support for the significance of Eocene/Oligocene climate change for the historical biogeography of West Indian life. *Correspondence: Pablo Weaver, Biology Department, 1950 3rd St., La Verne, CA 91750, Keywords USA. colonization, GAARlandia, Hispaniola, historical biogeographical reconstruc- E-mails: [email protected]; [email protected] tion, Limia, relaxed molecular clocks, vicariance, West Indian biogeography reaching over 90% in some groups (Hedges, 1996; Myers et al., INTRODUCTION 2000). However, the island ecosystems are relatively depauper- After nearly two centuries of debate, biogeographical recon- ate and some major mainland groups, including marsupials, struction in the West Indies continues to be a contentious carnivores, lagomorphs, salamanders and most families of issue, with wide disagreement over the relative importance of frogs, turtles, and snakes are missing (Hedges, 1996, 2001). dispersal–vicariance. The islands of the West Indies exhibit These patterns are typical of isolated oceanic islands, in which exceptional biodiversity and are ranked in the top five of the a few successful dispersers radiate in situ. Molecular clock world’s most important biodiversity hotspots, with endemism analyses across taxa, including some reptiles, amphibians, and ª 2016 John Wiley & Sons Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12798 P. F. Weaver et al. mammals, show a pattern of random and recent divergences One of the groups for which colonization routes is still from mainland sources (mostly from South America), concor- unknown is Limia (family Poeciliidae), a genus of livebearing dant with a dispersal model of colonization (see Hedges, 1996, freshwater fishes endemic to the islands of the West Indies 2001 for figure showcasing random colonization patterns). (Rauchenberger, 1988; Burgess & Franz, 1989; Rodriguez, The primary mechanism of dispersal for these groups is 1997; Hamilton, 2001). With 17 described endemic species thought to be a combination of large flooding events in South on Hispaniola and one endemic species on each of the America, floating mats of debris, and the prevailing north-wes- islands of Cuba, Jamaica and Grand Cayman, Limia is the terly oceanic currents (King, 1962; Vonhof et al., 1998; dominant freshwater fish group in the Greater Antilles (Bur- Hedges, 2001; Glor et al., 2005). Dispersal continues in the gess & Franz, 1989). However, the historical biogeography of present day, as evidenced by a colony of iguanas (Iguana Limia has not been critically assessed using molecular tech- iguana) arriving to the island of Anguilla from nearby Guada- niques and the timing and mechanism of colonization for lupe in the wake of Hurricane Luis in 1995 (Lawrence, 1998). Limia remains unresolved. Our hope is that by reconstruct- Alternatively, the vicariance argument highlights the pres- ing the colonization of Limia, we will gain a vital piece in ence of organisms with poor dispersal abilities and relies on the ever-evolving debate on the origins of West Indian life the correlation between evolutionary patterns and geological and gain insight into other organisms with limited long-dis- reconstructions. Advocates of West Indian vicariance bio- tance dispersal abilities. geography envision entire ecosystems, trapped on drifting Freshwater fish in the Limia genus provide an ideal oppor- island fragments, splitting from a proto-Central America in tunity to evaluate colonization hypotheses because of their the late Cretaceous (65 Ma) through plate tectonics (Rosen, diversity and presence on multiple islands. Using Limia spe- 1975, 1985; Nelson & Platnick, 1981; Guyer & Savage, 1986; cies from Hispaniola (Dominican Republic and Haiti), Page & Lydeard, 1994). The presence of freshwater fish on Jamaica, Cuba, as well as poeciliid species from the main- the islands of the West Indies has sparked much interest over land, evaluation of multiple divergence events is possible: the years because of their diversity and endemism, as well as West Indies from the mainland (all Limia), Jamaica from their presumed limited dispersal abilities (Rosen & Bailey, Cuba/Hispaniola (L. melanogaster split) and Cuba from His- 1963; Rosen, 1975; Rivas, 1986; Poeser, 2003), and they were paniola (L. vittata split). We test the above colonization sce- instrumental in the development of vicariance biogeography narios using a combined gene molecular phylogenetic as a discipline (Rosen, 1975). Previous taxonomic studies of approach with a robust sampling of poeciliids from the West Indian freshwater fish show that species on Hispaniola islands and the mainland, together with a relaxed molecular and Cuba are polyphyletic; northern Hispaniolan species are clock analysis and historical biogeographical reconstruction. more closely related to eastern Cuban and Cayman island The goal for this study was to test biogeographical hypothe- species than they are to southern Hispaniolan species ses of the West Indies through an updated multigene phy- (Rauchenberger, 1988; Burgess & Franz, 1989; Rodriguez, logeny of Limia. We examine three alternative scenarios, with 1997; Hamilton, 2001). These patterns seemed concordant regard to Limia colonization. First, long-distance transoceanic with proposed geological models of island formation and a dispersal models, which predict colonization across the Carib- late Cretaceous connection with the mainland (Pitman et al., bean sea by salt tolerant taxa from diverse mainland sources, 1993; Pindell, 1994). However, the late Cretaceous vicariance with subsequent evolution of the fresh-water clades (Myers, model has received much criticism, mainly because of a lack 1966; Briggs, 1984, 1987; Hedges, 1996, 2001, 2006). Second, of molecular clock support and the unlikely survival of life late Cretaceous vicariance models, which predict colonization in this region during and shortly after the late Cretaceous during the late Cretaceous (65–85 Ma) and persistence of bolide impact near the Yucatan peninsula (Hildebrand & biota on incipient island fragments (Rosen, 1975, 1985; Nelson Boynton, 1990). & Platnick, 1981; Guyer & Savage, 1986; Rauchenberger, 1988; An alternative geological reconstruction that shows a more Page & Lydeard, 1994). Finally, the GAARlandia model, which recent land connection between the mainland and the West postulates inundation of the incipient island fragments after Indies, is the GAARlandia model (Greater Antilles Aves the late Cretaceous and until the Middle Eocene (< 40 Ma), Ridge) (Iturralde-Vinent & MacPhee, 1999; Iturralde-Vinent, with range expansion of South American groups along a short- 2006). In this reconstruction, any late Cretaceous land for- lived, exposed Aves Ridge, which was created by sea level mations in the Caribbean would have been inundated by decline and Caribbean plate uplift during the Eocene/Oligo- subsequent sea level change, and permanent land was only cene boundary (33–35 Ma) (Iturralde-Vinent & MacPhee, present after the Middle Eocene (< 40 Ma). During the 1999; Iturralde-Vinent, 2006). Eocene/Oligocene transition (30–35 Ma), a rapidly cooling planet caused global declines in sea level upwards of 60 m METHODS (Haq et al., 1987; Miller et al.,
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