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      Freshwater gobies 30 million years ago: New insights into character evolution and phylogenetic relationships of †Pirskeniidae (Gobioidei, Teleostei)

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          Abstract

          The modern Gobioidei (Teleostei) comprise eight families, but the extinct †Pirskeniidae from the lower Oligocene of the Czech Republic indicate that further families may have existed in the past. However, the validity of the †Pirskeniidae has been questioned and its single genus † Pirskenius has been assigned to the extant family Eleotridae in previous works. The objective of this study is to clarify the status of the †Pirskeniidae. Whether or not the †Pirskeniidae should be synonymised with the Eleotridae is also interesting from a biogeographical point of view as Eleotridae is not present in Europe or the Mediterranean Sea today. We present new specimens and re-examine the material on which the two known species of † Pirskenius are based († P. diatomaceus Obrhelová, 1961; † P. radoni Přikryl, 2014). To provide a context for phylogenetically informative characters related to the palatine and the branchiostegal rays, three early-branching gobioids ( Rhyacichthys, Protogobius, Perccottus), an eleotrid ( Eleotris) and a gobiid ( Gobius) were subjected to micro-CT analysis. The new data justify revalidation of the family †Pirskeniidae, and a revised diagnosis is presented for both † Pirskenius and †Pirskeniidae. Moreover, we provide for the first time an attempt to relate a fossil gobioid to extant taxa based on phylogenetic analysis. The results indicate a sister-group relationship of †Pirskeniidae to the Thalasseleotrididae + Gobiidae + Oxudercidae clade. Considering the fossil record, the arrival of gobioids in freshwater habitats in the early Oligocene apparently had generated new lineages that finally were not successful and became extinct shortly after they had diverged. There is currently no evidence that the Eleotridae was present in the European ichthyofauna in the past.

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          Phylogenetic classification of bony fishes

          Background Fish classifications, as those of most other taxonomic groups, are being transformed drastically as new molecular phylogenies provide support for natural groups that were unanticipated by previous studies. A brief review of the main criteria used by ichthyologists to define their classifications during the last 50 years, however, reveals slow progress towards using an explicit phylogenetic framework. Instead, the trend has been to rely, in varying degrees, on deep-rooted anatomical concepts and authority, often mixing taxa with explicit phylogenetic support with arbitrary groupings. Two leading sources in ichthyology frequently used for fish classifications (JS Nelson’s volumes of Fishes of the World and W. Eschmeyer’s Catalog of Fishes) fail to adopt a global phylogenetic framework despite much recent progress made towards the resolution of the fish Tree of Life. The first explicit phylogenetic classification of bony fishes was published in 2013, based on a comprehensive molecular phylogeny (www.deepfin.org). We here update the first version of that classification by incorporating the most recent phylogenetic results. Results The updated classification presented here is based on phylogenies inferred using molecular and genomic data for nearly 2000 fishes. A total of 72 orders (and 79 suborders) are recognized in this version, compared with 66 orders in version 1. The phylogeny resolves placement of 410 families, or ~80% of the total of 514 families of bony fishes currently recognized. The ordinal status of 30 percomorph families included in this study, however, remains uncertain (incertae sedis in the series Carangaria, Ovalentaria, or Eupercaria). Comments to support taxonomic decisions and comparisons with conflicting taxonomic groups proposed by others are presented. We also highlight cases were morphological support exist for the groups being classified. Conclusions This version of the phylogenetic classification of bony fishes is substantially improved, providing resolution for more taxa than previous versions, based on more densely sampled phylogenetic trees. The classification presented in this study represents, unlike any other, the most up-to-date hypothesis of the Tree of Life of fishes. Electronic supplementary material The online version of this article (doi:10.1186/s12862-017-0958-3) contains supplementary material, which is available to authorized users.
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            The Tree of Life and a New Classification of Bony Fishes

            The tree of life of fishes is in a state of flux because we still lack a comprehensive phylogeny that includes all major groups. The situation is most critical for a large clade of spiny-finned fishes, traditionally referred to as percomorphs, whose uncertain relationships have plagued ichthyologists for over a century. Most of what we know about the higher-level relationships among fish lineages has been based on morphology, but rapid influx of molecular studies is changing many established systematic concepts. We report a comprehensive molecular phylogeny for bony fishes that includes representatives of all major lineages. DNA sequence data for 21 molecular markers (one mitochondrial and 20 nuclear genes) were collected for 1410 bony fish taxa, plus four tetrapod species and two chondrichthyan outgroups (total 1416 terminals). Bony fish diversity is represented by 1093 genera, 369 families, and all traditionally recognized orders. The maximum likelihood tree provides unprecedented resolution and high bootstrap support for most backbone nodes, defining for the first time a global phylogeny of fishes. The general structure of the tree is in agreement with expectations from previous morphological and molecular studies, but significant new clades arise. Most interestingly, the high degree of uncertainty among percomorphs is now resolved into nine well-supported supraordinal groups. The order Perciformes, considered by many a polyphyletic taxonomic waste basket, is defined for the first time as a monophyletic group in the global phylogeny. A new classification that reflects our phylogenetic hypothesis is proposed to facilitate communication about the newly found structure of the tree of life of fishes. Finally, the molecular phylogeny is calibrated using 60 fossil constraints to produce a comprehensive time tree. The new time-calibrated phylogeny will provide the basis for and stimulate new comparative studies to better understand the evolution of the amazing diversity of fishes.
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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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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: ResourcesRole: VisualizationRole: Writing – review & editing
                Role: ResourcesRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                24 August 2020
                2020
                : 15
                : 8
                : e0237366
                Affiliations
                [1 ] Department of Earth and Environmental Sciences, Ludwig-Maximilians-Universität München, Munich, Germany
                [2 ] GeoBio-Center LMU, Ludwig-Maximilians-Universität München, Munich, Germany
                [3 ] Institute of Geology of the Czech Academy of Sciences, Praha, Czech Republic
                [4 ] Section Evertebrata varia, SNSB-Bavarian State Collection of Zoology, Munich, Germany
                [5 ] Laboratoire de Biologie des organismes et écosystèmes aquatiques (BOREA), Muséum national d’Histoire naturelle, Centre National de la Recherche Scientifique, Institut de Recherche pour le Développement, Sorbonne Université, Paris, France
                [6 ] SNSB-Bavarian State Collection of Palaeontology and Geology, Munich, Germany
                Università degli Studi di Torino, ITALY
                Author notes

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

                Author information
                http://orcid.org/0000-0001-6678-5080
                http://orcid.org/0000-0002-9393-0885
                Article
                PONE-D-20-14246
                10.1371/journal.pone.0237366
                7446829
                32834000
                e8107946-4225-4fde-928f-391dadd17a6d
                © 2020 Reichenbacher 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
                : 13 May 2020
                : 23 July 2020
                Page count
                Figures: 11, Tables: 5, Pages: 34
                Funding
                Funded by: German Science Foundation (DFG)
                Award ID: RE 1113/20-1
                Award Recipient :
                Funded by: Czech Academy of the Sciences
                Award ID: RVO67985831
                Award Recipient :
                We acknowledge funding for this project from the Deutsche Forschungsgemeinschaft to B.R. (RE- 1113/20-1). T.P.’s research was institutionally supported by the Czech Academy of the Sciences, Institute of Geology (RVO67985831). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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                Custom metadata
                The new CT slice data and 3D files of Rhyacichthys guilberti (2 specimens), Protogobius attiti (1 specimen), Eleotris pisonis (2 specimens) and Gobius incognitus (1 specimen) are available from the MorphoSource repository (Project P1063, www.morphosource.org/Detail/ProjectDetail/Show/project_id/1063).

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