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      Causes of endemic radiation in the Caribbean: evidence from the historical biogeography and diversification of the butterfly genus Calisto (Nymphalidae: Satyrinae: Satyrini)

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          Abstract

          Background

          Calisto is the largest butterfly genus in the West Indies but its systematics, historical biogeography and the causes of its diversification have not been previously rigorously evaluated. Several studies attempting to explain the wide-ranging diversity of Calisto gave different weights to vicariance, dispersal and adaptive radiation. We utilized molecular phylogenetic approaches and secondary calibrations points to estimate lineage ages. In addition, we used the dispersal-extinction-cladogenesis model and Caribbean paleogeographical information to reconstruct ancestral geographical distributions. We also evaluated different models of diversification to estimate the dynamics of lineage radiation within Calisto. By understanding the evolution of Calisto butterflies, we attempt to identify the main processes acting on insular insect diversity and the causes of its origin and its maintenance.

          Results

          The crown age of Calisto was estimated to the early Oligocene (31 ± 5 Ma), and a single shift in diversification rate following a diversity-dependent speciation process was the best explanation for the present-day diversity found within the genus. A major increase in diversification rate was recovered at 14 Ma, following geological arrangements that favoured the availability of empty niches. Inferred ancestral distributional ranges suggested that the origin of extant Calisto is in agreement with a vicariant model and the origin of the Cuban lineage was likely the result of vicariance caused by the Cuba-Hispaniola split. A long-distance dispersal was the best explanation for the colonization of Jamaica and the Bahamas.

          Conclusions

          The ancestral geographical distribution of Calisto is in line with the paleogeographical model of Caribbean colonization, which favours island-to-island vicariance. Because the sister lineage of Calisto remains ambiguous, its arrival to the West Indies remains to be explained, although, given its age and historical biogeography, the hypothesized GAARlandia land bridge might have been a plausible introduction route from continental America. Intra-island radiation caused by ecological innovation and the abiotic creation of niche spaces was found to be the main force shaping Calisto diversity and island endemism in Hispaniola and Cuba.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12862-014-0199-7) contains supplementary material, which is available to authorized users.

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          Most cited references82

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          Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing

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            Analysis of an evolutionary species-area relationship.

            Large islands typically have more species than comparable smaller islands. Ecological theories, the most influential being the equilibrium theory of island biogeography, explain the species-area relationship as the outcome of the effect of area on immigration and extinction rates. However, these theories do not apply to taxa on land masses, including continents and large islands, that generate most of their species in situ. In this case, species-area relationships should be driven by higher speciation rates in larger areas, a theory that has never been quantitatively tested. Here we show that Anolis lizards on Caribbean islands meet several expectations of the evolutionary theory. Within-island speciation exceeds immigration as a source of new species on all islands larger than 3,000 km2, whereas speciation is rare on smaller islands. Above this threshold island size, the rate of species proliferation increases with island area, a process that results principally from the positive effects of area on speciation rate. Also as expected, the slope of the species-area relationship jumps sharply above the threshold. Although Anolis lizards have been present on large Caribbean islands for over 30 million years, there are indications that the current number of species still falls below the speciation-extinction equilibrium.
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              Genomic outposts serve the phylogenomic pioneers: designing novel nuclear markers for genomic DNA extractions of lepidoptera.

              Increasing the number of characters used in phylogenetic studies is the next crucial step towards generating robust and stable phylogenetic hypotheses - i.e., strongly supported and consistent across reconstruction method. Here we describe a genomic approach to finding new protein-coding genes for systematics in nonmodel taxa, which can be PCR amplified from standard, slightly degraded genomic DNA extracts. We test this approach on Lepidoptera, searching the draft genomic sequence of the silk moth Bombyx mori, for exons > 500 bp in length, removing annotated gene families, and compared remaining exons with butterfly EST databases to identify conserved regions for primer design. These primers were tested on a set of 65 taxa primarily in the butterfly family Nymphalidae. We were able to identify and amplify six previously unused gene regions (Arginine Kinase, GAPDH, IDH, MDH, RpS2, and RpS5) and two rarely used gene regions (CAD and DDC) that when added to the three traditional gene regions (COI, EF-1alpha and wingless) gave a data set of 8114 bp. Phylogenetic robustness and stability increased with increasing numbers of genes. Smaller taxanomic subsets were also robust when using the full gene data set. The full 11-gene data set was robust and stable across reconstruction methods, recovering the major lineages and strongly supporting relationships within them. Our methods and insights should be applicable to taxonomic groups having a single genomic reference species and several EST databases from taxa that diverged less than 100 million years ago.
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                Author and article information

                Contributors
                pavelm14@gmail.com
                rayner_na@yahoo.com
                mycalesis@gmail.com
                jmiller@flmnh.ufl.edu
                asourakov@flmnh.ufl.edu
                niklas.wahlberg@utu.fi
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                16 September 2014
                16 September 2014
                2014
                : 14
                : 1
                : 199
                Affiliations
                [ ]Laboratory of Genetics, Department of Biology, University of Turku, FI-20014 Turku, Finland
                [ ]School of Biological Sciences, University of South Bohemia and Institute of Entomology, Biology Centre AS CR, CZ-37005 Ceske Budejovice, Czech Republic
                [ ]División de Colecciones Zoológicas y Sistemática, Instituto de Ecología y Sistemática, Carretera de Varona km 3.5, Capdevila, Boyeros Ciudad de La Habana, Cuba
                [ ]McGuire Center for Lepidoptera and Biodiversity, Florida Museum of Natural History, University of Florida, Gainesville, FL 32611 USA
                Article
                199
                10.1186/s12862-014-0199-7
                4172866
                25220489
                2f362188-8d75-4e57-9925-7ebc0753f040
                © Matos-Maraví et al.; licensee BioMed Central Ltd. 2014

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 8 May 2014
                : 2 September 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Evolutionary Biology
                caribbean,ecological limits,historical biogeography,intra-island diversification,island-island vicariance,lepidoptera,molecular phylogeny

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