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      A Mitogenomic Perspective on the Phylogenetic Position of the Hapalogenys Genus (Acanthopterygii: Perciformes) and the Evolutionary Origin of Perciformes

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          Abstract

          The Hapalogenys genus was the most controversial and problematic in phylogenetic position of Percoidei. In this study, we rechecked the taxonomic status of Hapalogenys in Percoidei using complete mitochondrial genome data. We purposefully added a new complete mitochondrial sequence from chosen species of Hapalogenys and conducted phylogenetic analyses using a large complete mitochondrial data set. The resultant tree topologies were congruent from partitioned Bayesian and Maximum-likelihood methods. The results indicated that Hapalogenys was distantly related to Haemulidae and could be removed from Haemulidae. The results supported the Hapalogeny was upgraded to a family rank titled Hapalogenyidae, and it should be recognized in a separate family of Hapalogenyidae. A relaxed molecular-clock Bayesian analysis indicated that the divergence times of Perciformes groups had a much older than the available old fossil records. The origin of the common ancestral lineage of Perciformes fish was estimated in the late Jurassic about 149 Myr ago.

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          MRBAYES: Bayesian inference of phylogenetic trees.

          The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
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            Use of mitogenomic information in teleostean molecular phylogenetics: a tree-based exploration under the maximum-parsimony optimality criterion.

            We explored the phylogenetic utility and limits of the individual and concatenated mitochondrial genes for reconstructing the higher-level relationships of teleosts, using the complete (or nearly complete) mitochondrial DNA sequences of eight teleosts (including three newly determined sequences), whose relative phylogenetic positions were noncontroversial. Maximum-parsimony analyses of the nucleotide and amino acid sequences of 13 protein-coding genes from the above eight teleosts, plus two outgroups (bichir and shark), indicated that all of the individual protein-coding genes, with the exception of ND5, failed to recover the expected phylogeny, although unambiguously aligned sequences from 22 concatenated transfer RNA (tRNA) genes (stem regions only) recovered the expected phylogeny successfully with moderate statistical support. The phylogenetic performance of the 13 protein-coding genes in recovering the expected phylogeny was roughly classified into five groups, viz. very good (ND5, ND4, COIII, COI), good (COII, cyt b), medium (ND3, ND2), poor (ND1, ATPase 6), and very poor (ND4L, ND6, ATPase 8). Although the universality of this observation was unclear, analysis of successive concatenation of the 13 protein-coding genes in the same ranking order revealed that the combined data sets comprising nucleotide sequences from the several top-ranked protein-coding genes (no 3rd codon positions) plus the 22 concatenated tRNA genes (stem regions only) best recovered the expected phylogeny, with all internal branches being supported by bootstrap values >90%. We conclude that judicious choice of mitochondrial genes and appropriate data weighting, in conjunction with purposeful taxonomic sampling, are prerequisites for resolving higher-level relationships in teleosts under the maximum-parsimony optimality criterion. Copyright 2000 Academic Press.
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              Evolutionary history of Otophysi (Teleostei), a major clade of the modern freshwater fishes: Pangaean origin and Mesozoic radiation

              Background Freshwater harbors approximately 12,000 fish species accounting for 43% of the diversity of all modern fish. A single ancestral lineage evolved into about two-thirds of this enormous biodiversity (≈ 7900 spp.) and is currently distributed throughout the world's continents except Antarctica. Despite such remarkable species diversity and ubiquity, the evolutionary history of this major freshwater fish clade, Otophysi, remains largely unexplored. To gain insight into the history of otophysan diversification, we constructed a timetree based on whole mitogenome sequences across 110 species representing 55 of the 64 families. Results Partitioned maximum likelihood analysis based on unambiguously aligned sequences (9923 bp) confidently recovered the monophyly of Otophysi and the two constituent subgroups (Cypriniformes and Characiphysi). The latter clade comprised three orders (Gymnotiformes, Characiformes, Siluriformes), and Gymnotiformes was sister to the latter two groups. One of the two suborders in Characiformes (Characoidei) was more closely related to Siluriformes than to its own suborder (Citharinoidei), rendering the characiforms paraphyletic. Although this novel relationship did not receive strong statistical support, it was supported by analyzing independent nuclear markers. A relaxed molecular clock Bayesian analysis of the divergence times and reconstruction of ancestral habitats on the timetree suggest a Pangaean origin and Mesozoic radiation of otophysans. Conclusions The present timetree demonstrates that survival of the ancestral lineages through the two consecutive mass extinctions on Pangaea, and subsequent radiations during the Jurassic through early Cretaceous shaped the modern familial diversity of otophysans. This evolutionary scenario is consistent with recent arguments based on biogeographic inferences and molecular divergence time estimates. No fossil otophysan, however, has been recorded before the Albian, the early Cretaceous 100-112 Ma, creating an over 100 million year time span without fossil evidence. This formidable ghost range partially reflects a genuine difference between the estimated ages of stem group origin (molecular divergence time) and crown group morphological diversification (fossil divergence time); the ghost range, however, would be filled with discoveries of older fossils that can be used as more reasonable time constraints as well as with developments of more realistic models that capture the rates of molecular sequences accurately.
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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
                31 July 2014
                : 9
                : 7
                : e103011
                Affiliations
                [1]Laboratory of Fish Biogenetics & Immune Evolution, College of Marine Science, Zhejiang Ocean University, Zhoushan, China
                Institute of Biochemistry and Biology, Germany
                Author notes

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

                Conceived and designed the experiments: TW TX. Performed the experiments: TW YS BZ. Analyzed the data: TW TX. Contributed reagents/materials/analysis tools: RW YS. Contributed to the writing of the manuscript: TW TX.

                Article
                PONE-D-14-17641
                10.1371/journal.pone.0103011
                4117523
                25077480
                ccc49893-ea1d-46b2-97b3-30eb926bdac4
                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
                : 23 April 2014
                : 26 June 2014
                Page count
                Pages: 5
                Funding
                This study was supported by National Natural Science Foundation of China (31272661), Zhejiang Provincial Natural Science Foundation (LY13C040001), and grant of Young Academic Leaders in Zhejiang Province (PD2013220). 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 Systematics
                Phylogenetics
                Animal Phylogenetics
                Zoology
                Animal Taxonomy
                Chordata
                Vertebrata
                Animal Phylogenetics
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All sequence files are available from the GenBank database accession number NC019646.

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