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      Rhodopsin gene evolution in early teleost fishes

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      PLoS ONE
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          Abstract

          Rhodopsin mediates an essential step in image capture and is tightly associated with visual adaptations of aquatic organisms, especially species that live in dim light environments (e.g., the deep sea). The rh1 gene encoding rhodopsin was formerly considered a single-copy gene in genomes of vertebrates, but increasing exceptional cases have been found in teleost fish species. The main objective of this study was to determine to what extent the visual adaptation of teleosts might have been shaped by the duplication and loss of rh1 genes. For that purpose, homologous rh1/ rh1-like sequences in genomes of ray-finned fishes from a wide taxonomic range were explored using a PCR-based method, data mining of public genetic/genomic databases, and subsequent phylogenomic analyses of the retrieved sequences. We show that a second copy of the fish-specific intron-less rh1 is present in the genomes of most anguillids (Elopomorpha), Hiodon alosoides (Osteoglossomorpha), and several clupeocephalan lineages. The phylogenetic analysis and comparisons of alternative scenarios for putative events of gene duplication and loss suggested that fish rh1 was likely duplicated twice during the early evolutionary history of teleosts, with one event coinciding with the hypothesized fish-specific genome duplication and the other in the common ancestor of the Clupeocephala. After these gene duplication events, duplicated genes were maintained in several teleost lineages, whereas some were secondarily lost in specific lineages. Alternative evolutionary schemes of rh1 and comparison with previous studies of gene evolution are also reviewed.

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          The zebrafish reference genome sequence and its relationship to the human genome.

          Zebrafish have become a popular organism for the study of vertebrate gene function. The virtually transparent embryos of this species, and the ability to accelerate genetic studies by gene knockdown or overexpression, have led to the widespread use of zebrafish in the detailed investigation of vertebrate gene function and increasingly, the study of human genetic disease. However, for effective modelling of human genetic disease it is important to understand the extent to which zebrafish genes and gene structures are related to orthologous human genes. To examine this, we generated a high-quality sequence assembly of the zebrafish genome, made up of an overlapping set of completely sequenced large-insert clones that were ordered and oriented using a high-resolution high-density meiotic map. Detailed automatic and manual annotation provides evidence of more than 26,000 protein-coding genes, the largest gene set of any vertebrate so far sequenced. Comparison to the human reference genome shows that approximately 70% of human genes have at least one obvious zebrafish orthologue. In addition, the high quality of this genome assembly provides a clearer understanding of key genomic features such as a unique repeat content, a scarcity of pseudogenes, an enrichment of zebrafish-specific genes on chromosome 4 and chromosomal regions that influence sex determination.
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            Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates.

            The uneven distribution of species richness is a fundamental and unexplained pattern of vertebrate biodiversity. Although species richness in groups like mammals, birds, or teleost fishes is often attributed to accelerated cladogenesis, we lack a quantitative conceptual framework for identifying and comparing the exceptional changes of tempo in vertebrate evolutionary history. We develop MEDUSA, a stepwise approach based upon the Akaike information criterion for detecting multiple shifts in birth and death rates on an incompletely resolved phylogeny. We apply MEDUSA incompletely to a diversity tree summarizing both evolutionary relationships and species richness of 44 major clades of jawed vertebrates. We identify 9 major changes in the tempo of gnathostome diversification; the most significant of these lies at the base of a clade that includes most of the coral-reef associated fishes as well as cichlids and perches. Rate increases also underlie several well recognized tetrapod radiations, including most modern birds, lizards and snakes, ostariophysan fishes, and most eutherian mammals. In addition, we find that large sections of the vertebrate tree exhibit nearly equal rates of origination and extinction, providing some of the first evidence from molecular data for the importance of faunal turnover in shaping biodiversity. Together, these results reveal living vertebrate biodiversity to be the product of volatile turnover punctuated by 6 accelerations responsible for >85% of all species as well as 3 slowdowns that have produced "living fossils." In addition, by revealing the timing of the exceptional pulses of vertebrate diversification as well as the clades that experience them, our diversity tree provides a framework for evaluating particular causal hypotheses of vertebrate radiations.
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              Whole-genome duplication in teleost fishes and its evolutionary consequences.

              Whole-genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, by far the most species-rich vertebrate clade. After initial controversy, there is now solid evidence that such event took place in the common ancestor of all extant teleosts. It is termed teleost-specific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosage selection (preserving genes to maintain dosage balance between interconnected components). Since the frequency of these mechanisms is influenced by the genes' properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massive radiation of teleosts, have been matter of controversial debate. It is evident that gene duplications are crucial for generating complexity and that WGDs provide large amounts of raw material for evolutionary adaptation and innovation. However, it is less clear whether the TS-WGD is directly linked to the evolutionary success of teleosts and their radiation. Recent studies let us conclude that TS-WGD has been important in generating teleost complexity, but that more recent ecological adaptations only marginally related to TS-WGD might have even contributed more to diversification. It is likely, however, that TS-WGD provided teleosts with diversification potential that can become effective much later, such as during phases of environmental change.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: ValidationRole: Writing – original draft
                Role: Funding acquisitionRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                5 November 2018
                2018
                : 13
                : 11
                : e0206918
                Affiliations
                [1 ] Institute of Oceanography, National Taiwan University, Taipei, Taiwan
                [2 ] Institute de Systématique, Évolution, Biodiversité (ISYEB), Muséum National d’Histoire Naturelle–CNRS, Sorbonne Université, EPHE, Paris, France
                Laboratoire de Biologie du Développement de Villefranche-sur-Mer, FRANCE
                Author notes

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

                Author information
                http://orcid.org/0000-0003-4751-7632
                Article
                PONE-D-18-08558
                10.1371/journal.pone.0206918
                6218077
                30395593
                a3dbe4f1-f426-4fa2-bc5b-b457a6555611
                © 2018 Chen et al

                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
                : 20 March 2018
                : 22 October 2018
                Page count
                Figures: 5, Tables: 1, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: MOST 102-2923-B-002 -001 -MY3
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR 12-ISV7-0005-01
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004663, Ministry of Science and Technology, Taiwan;
                Award ID: MOST 107-2611-M-002-007-
                Award Recipient :
                This work was supported by bilateral cooperation research entitled “Taiwan France marine diversity exploration and evolution of deep-sea fauna, TFDeepEvo” funded by the Ministry of Science and Technology, Taiwan (MOST 102-2923-B-002 -001 -MY3 and MOST 107-2611-M-002-007, both to WJC) and the French National Research Agency (ANR 12-ISV7-0005-01 to SS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Genetics
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Computer and Information Sciences
                Data Management
                Taxonomy
                Evolutionary Systematics
                Phylogenetics
                Phylogenetic Analysis
                Biology and Life Sciences
                Evolutionary Biology
                Molecular Evolution
                Gene Duplication
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Fish
                Osteichthyes
                Eels
                Biology and Life Sciences
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                Vertebrates
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Fish
                Osteichthyes
                Actinopterygii
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Fish
                Marine Fish
                Biology and Life Sciences
                Marine Biology
                Marine Fish
                Earth Sciences
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                Marine Biology
                Marine Fish
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
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                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
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                Custom metadata
                The DNA sequences data obtained and examined in this study were deposited in the NCBI Genbank under the accession nos., MH674300, MH769447~MH769543 and are available for public at https://www.ncbi.nlm.nih.gov/genbank/. All relevant data/info/results are within the paper and its Supporting Information files.

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