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      Age estimates for an adaptive lake fish radiation, its mitochondrial introgression, and an unexpected sister group: Sailfin silversides of the Malili Lakes system in Sulawesi

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          Abstract

          Background

          The Malili Lakes system in central Sulawesi (Indonesia) is a hotspot of freshwater biodiversity in the Wallacea, characterized by endemic species flocks like the sailfin silversides (Teleostei: Atherinomorpha: Telmatherinidae) radiation. Phylogenetic reconstructions of these freshwater fishes have previously revealed two Lake Matano Telmatherina lineages (sharpfins and roundfins) forming an ancient monophyletic group, which is however masked by introgressive hybridization of sharpfins with riverine populations. The present study uses mitochondrial data, newly included taxa, and different external calibration points, to estimate the age of speciation and hybridization processes, and to test for phylogeographic relationships between Kalyptatherina from ancient islands off New Guinea, Marosatherina from SW Sulawesi, and the Malili Lakes flock.

          Results

          Contrary to previous expectations, Kalyptatherina is the closest relative to the Malili Lakes Telmatherinidae, and Marosatherina is the sister to this clade. Palaeogeographic reconstructions of Sulawesi suggest that the closer relationship of the Malili Lakes radiation to Kalyptatherina might be explained by a 'terrane-rafting’ scenario, while proto- Marosatherina might have colonized Sulawesi by marine dispersal. The most plausible analysis conducted here implies an age of c. 1.9 My for the onset of divergence between the two major clades endemic to Lake Matano. Diversification within both lineages is apparently considerably more recent (c. 1.0 My); stream haplotypes present in the sharpfins are of even more recent origin (c. 0.4 My).

          Conclusions

          Sulawesi’s Telmatherinidae have most likely originated in the Sahul Shelf area, have possibly reached the island by both, marine dispersal and island/terrane-rafting, and have colonized the Malili Lakes system from rivers. Estimates for the split between the epibenthic sharpfins and the predominantly pelagic to benthopelagic roundfins in Lake Matano widely coincide with geological age estimates of this rift lake. Diversification within both clades clearly predates hybridization events with stream populations. For Lake Matano, these results support a scenario of initial benthic-pelagic divergence after colonization of the lake by riverine populations, followed by rapid radiation within both clades within the last 1 My. Secondary hybridization of stream populations with the sharpfins occurred more recently, and has thus most likely not contributed to the initial divergence of this benthic species flock.

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          Most cited references31

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          SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information

          We present SequenceMatrix, software that is designed to facilitate the assembly and analysis of multi-gene datasets. Genes are concatenated by dragging and dropping FASTA, NEXUS, or TNT files with aligned sequences into the program window. A multi-gene dataset is concatenated and displayed in a spreadsheet; each sequence is represented by a cell that provides information on sequence length, number of indels, the number of ambiguous bases ("Ns"), and the availability of codon information. Alternatively, GenBank numbers for the sequences can be displayed and exported. Matrices with hundreds of genes and taxa can be concatenated within minutes and exported in TNT, NEXUS, or PHYLIP formats, preserving both character set and codon information for TNT and NEXUS files. SequenceMatrix also creates taxon sets listing taxa with a minimum number of characters or gene fragments, which helps assess preliminary datasets. Entire taxa, whole gene fragments, or individual sequences for a particular gene and species can be excluded from export. Data matrices can be re-split into their component genes and the gene fragments can be exported as individual gene files. SequenceMatrix also includes two tools that help to identify sequences that may have been compromised through laboratory contamination or data management error. One tool lists identical or near-identical sequences within genes, while the other compares the pairwise distance pattern of one gene against the pattern for all remaining genes combined. SequenceMatrix is Java-based and compatible with the Microsoft Windows, Apple MacOS X and Linux operating systems. The software is freely available from http://code.google.com/p/sequencematrix/. © The Willi Hennig Society 2010.
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            Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers.

            Evolutionary theory has gained tremendous insight from studies of adaptive radiations. High rates of speciation, morphological divergence, and hybridization, combined with low sequence variability, however, have prevented phylogenetic reconstruction for many radiations. The Hawaiian honeycreepers are an exceptional adaptive radiation, with high phenotypic diversity and speciation that occurred within the geologically constrained setting of the Hawaiian Islands. Here we analyze a new data set of 13 nuclear loci and pyrosequencing of mitochondrial genomes that resolves the Hawaiian honeycreeper phylogeny. We show that they are a sister taxon to Eurasian rosefinches (Carpodacus) and probably came to Hawaii from Asia. We use island ages to calibrate DNA substitution rates, which vary substantially among gene regions, and calculate divergence times, showing that the radiation began roughly when the oldest of the current large Hawaiian Islands (Kauai and Niihau) formed, ~5.7 million years ago (mya). We show that most of the lineages that gave rise to distinctive morphologies diverged after Oahu emerged (4.0-3.7 mya) but before the formation of Maui and adjacent islands (2.4-1.9 mya). Thus, the formation of Oahu, and subsequent cycles of colonization and speciation between Kauai and Oahu, played key roles in generating the morphological diversity of the extant honeycreepers. Copyright © 2011 Elsevier Ltd. All rights reserved.
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              Biogeography of the Indo-Australian Archipelago

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                Author and article information

                Contributors
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central
                1471-2148
                2014
                3 May 2014
                : 14
                : 94
                Affiliations
                [1 ]Museum für Naturkunde Leibniz-Institute für Evolutions- und Biodiversitätsforschung an der Humboldt, Universität zu Berlin, Invalidenstr. 43, D-10115 Berlin, Germany
                [2 ]Department of Ichthyology, Bavarian State Collection of Zoology (ZSM), Münchhausenstr. 21, D-81247 München, Germany
                [3 ]Museum Zoologicum Bogoriense, Ichthyology Laboratory, Division of Zoology, Research Center for Biology, Indonesian Institute of Sciences (LIPI), Jl, Raya Bogor Km 46, 16911 Cibinong, Indonesia
                [4 ]Zoologisches Forschungsmuseum Alexander Koenig, Sektion Ichthyologie, Adenauerallee 160, D-53113 Bonn, Germany
                Article
                1471-2148-14-94
                10.1186/1471-2148-14-94
                4029975
                24886257
                ff5e7aaa-b6f6-4b0c-b39e-b643e642351a
                Copyright © 2014 Stelbrink et al.; licensee BioMed Central Ltd.

                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
                : 17 April 2014
                : 22 April 2014
                Categories
                Research Article

                Evolutionary Biology
                molecular clock,mitochondrial dna,southeast asia,sulawesi,biogeography,adaptive radiation,introgressive hybridization

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