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      The Covert World of Fish Biofluorescence: A Phylogenetically Widespread and Phenotypically Variable Phenomenon

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          Abstract

          The discovery of fluorescent proteins has revolutionized experimental biology. Whereas the majority of fluorescent proteins have been identified from cnidarians, recently several fluorescent proteins have been isolated across the animal tree of life. Here we show that biofluorescence is not only phylogenetically widespread, but is also phenotypically variable across both cartilaginous and bony fishes, highlighting its evolutionary history and the possibility for discovery of numerous novel fluorescent proteins. Fish biofluorescence is especially common and morphologically variable in cryptically patterned coral-reef lineages. We identified 16 orders, 50 families, 105 genera, and more than 180 species of biofluorescent fishes. We have also reconstructed our current understanding of the phylogenetic distribution of biofluorescence for ray-finned fishes. The presence of yellow long-pass intraocular filters in many biofluorescent fish lineages and the substantive color vision capabilities of coral-reef fishes suggest that they are capable of detecting fluoresced light. We present species-specific emission patterns among closely related species, indicating that biofluorescence potentially functions in intraspecific communication and evidence that fluorescence can be used for camouflage. This research provides insight into the distribution, evolution, and phenotypic variability of biofluorescence in marine lineages and examines the role this variation may play.

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          Most cited references55

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          Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea.

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            Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes.

            Spiny-rayed fishes, or acanthomorphs, comprise nearly one-third of all living vertebrates. Despite their dominant role in aquatic ecosystems, the evolutionary history and tempo of acanthomorph diversification is poorly understood. We investigate the pattern of lineage diversification in acanthomorphs by using a well-resolved time-calibrated phylogeny inferred from a nuclear gene supermatrix that includes 520 acanthomorph species and 37 fossil age constraints. This phylogeny provides resolution for what has been classically referred to as the "bush at the top" of the teleost tree, and indicates acanthomorphs originated in the Early Cretaceous. Paleontological evidence suggests acanthomorphs exhibit a pulse of morphological diversification following the end Cretaceous mass extinction; however, the role of this event on the accumulation of living acanthomorph diversity remains unclear. Lineage diversification rates through time exhibit no shifts associated with the end Cretaceous mass extinction, but there is a global decrease in lineage diversification rates 50 Ma that occurs during a period when morphological disparity among fossil acanthomorphs increases sharply. Analysis of clade-specific shifts in diversification rates reveal that the hyperdiversity of living acanthomorphs is highlighted by several rapidly radiating lineages including tunas, gobies, blennies, snailfishes, and Afro-American cichlids. These lineages with high diversification rates are not associated with a single habitat type, such as coral reefs, indicating there is no single explanation for the success of acanthomorphs, as exceptional bouts of diversification have occurred across a wide array of marine and freshwater habitats.
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              Identifying Canadian Freshwater Fishes through DNA Barcodes

              Background DNA barcoding aims to provide an efficient method for species-level identifications using an array of species specific molecular tags derived from the 5′ region of the mitochondrial cytochrome c oxidase I (COI) gene. The efficiency of the method hinges on the degree of sequence divergence among species and species-level identifications are relatively straightforward when the average genetic distance among individuals within a species does not exceed the average genetic distance between sister species. Fishes constitute a highly diverse group of vertebrates that exhibit deep phenotypic changes during development. In this context, the identification of fish species is challenging and DNA barcoding provide new perspectives in ecology and systematics of fishes. Here we examined the degree to which DNA barcoding discriminate freshwater fish species from the well-known Canadian fauna, which currently encompasses nearly 200 species, some which are of high economic value like salmons and sturgeons. Methodology/Principal Findings We bi-directionally sequenced the standard 652 bp “barcode” region of COI for 1360 individuals belonging to 190 of the 203 Canadian freshwater fish species (95%). Most species were represented by multiple individuals (7.6 on average), the majority of which were retained as voucher specimens. The average genetic distance was 27 fold higher between species than within species, as K2P distance estimates averaged 8.3% among congeners and only 0.3% among concpecifics. However, shared polymorphism between sister-species was detected in 15 species (8% of the cases). The distribution of K2P distance between individuals and species overlapped and identifications were only possible to species group using DNA barcodes in these cases. Conversely, deep hidden genetic divergence was revealed within two species, suggesting the presence of cryptic species. Conclusions/Significance The present study evidenced that freshwater fish species can be efficiently identified through the use of DNA barcoding, especially the species complex of small-sized species, and that the present COI library can be used for subsequent applications in ecology and systematics.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                8 January 2014
                : 9
                : 1
                : e83259
                Affiliations
                [1 ]Department of Ichthyology, American Museum of Natural History, Division of Vertebrate Zoology, New York, New York United States of America
                [2 ]Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, New York, United States of America
                [3 ]Biodiversity Institute, University of Kansas, Lawrence, Kansas, United States of America
                [4 ]Marine Biology Department, The Leon H. Charney School of Marine Sciences, University of Haifa, Mount Carmel, Haifa, Israel
                [5 ]Department of Cellular and Molecular Physiology, The John B. Pierce Laboratory, Inc., Yale University, New Haven, Connecticut, United States of America
                [6 ]Department of Natural Sciences, Baruch College, City University of New York, New York, New York, United States of America
                Consiglio Nazionale delle Ricerche (CNR), Italy
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JSS RCS WLS MPD DT VAP DFG. Performed the experiments: JSS RCS WLS MPD DT VAP DFG. Analyzed the data: JSS RCS WLS MPD VAP DFG. Contributed reagents/materials/analysis tools: JSS RCS WLS MPD VAP DFG. Wrote the paper: JSS RCS WLS MPD VAP DFG.

                Article
                PONE-D-13-39818
                10.1371/journal.pone.0083259
                3885428
                24421880
                0b4a6fae-91db-4aec-b146-e627599c117c
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 28 September 2013
                : 31 October 2013
                Page count
                Pages: 1
                Funding
                This work was supported by the American Museum of Natural History, City University of New York, National Science Foundation grants DEB-0444842, IOS-0749943, and DEB-1258141 to JSS, MCB-0920572 and DRL-1007747 to DFG, DEB-0732642 and DEB-1060869 to WLS, DEB-1257555 and DEB-1258141 to MPD, WLS, and JSS, National Institutes of Health (NIH) grants U24NS057631 and R01NS083875 to VAP and National Geographic Waitt Grants #W101-10 to DFG and #W214-12 to JSS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Biotechnology
                Genetic Engineering
                Ecology
                Physiological Ecology
                Evolutionary Biology
                Evolutionary Ecology
                Marine Biology
                Fisheries Science
                Neuroscience
                Neuroethology
                Zoology
                Animal Phylogenetics
                Animal Physiology
                Ichthyology

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                Uncategorized

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