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      Homology of the Fifth Epibranchial and Accessory Elements of the Ceratobranchials among Gnathostomes: Insights from the Development of Ostariophysans

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          Abstract

          Epibranchials are among the main dorsal elements of the gill basket in jawed vertebrates (Gnathostomata). Among extant fishes, chondrichthyans most resemble the putative ancestral condition as all branchial arches possess every serially homologous piece. In osteichthyans, a primitive rod-like epibranchial 5, articulated to ceratobranchial 5, is absent. Instead, epibranchial 5 of many actinopterygians is here identified as an accessory element attached to ceratobranchial 4. Differences in shape and attachment of epibranchial 5 in chondrichthyans and actinopterygians raised suspicions about their homology, prompting us to conduct a detailed study of the morphology and development of the branchial basket of three ostariophysans ( Prochilodus argenteus, Characiformes; Lophiosilurus alexandri and Pseudoplatystoma corruscans, Siluriformes). Results were interpreted within a phylogenetic context of major gnathostome lineages. Developmental series strongly suggest that the so-called epibranchial 5 of actinopterygians does not belong to the epal series because it shares the same chondroblastic layer with ceratobranchial 4 and its ontogenetic emergence is considerably late. This neomorphic structure is called accessory element of ceratobranchial 4. Its distribution among gnathostomes indicates it is a teleost synapomorphy, occurring homoplastically in Polypteriformes, whereas the loss of the true epibranchial 5 is an osteichthyan synapomorphy. The origin of the accessory element of ceratobranchial 4 appears to have occurred twice in osteichthyans, but it may have a single origin; in this case, the accessory element of ceratobranchial 4 would represent a remnant of a series of elements distally attached to ceratobranchials 1–4, a condition totally or partially retained in basal actinopterygians. Situations wherein a structure is lost while a similar neomorphic element is present may lead to erroneous homology assessments; these can be avoided by detailed morphological and ontogenetic investigations interpreted in the light of well-supported phylogenetic hypotheses.

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          A Devonian tetrapod-like fish and the evolution of the tetrapod body plan.

          The relationship of limbed vertebrates (tetrapods) to lobe-finned fish (sarcopterygians) is well established, but the origin of major tetrapod features has remained obscure for lack of fossils that document the sequence of evolutionary changes. Here we report the discovery of a well-preserved species of fossil sarcopterygian fish from the Late Devonian of Arctic Canada that represents an intermediate between fish with fins and tetrapods with limbs, and provides unique insights into how and in what order important tetrapod characters arose. Although the body scales, fin rays, lower jaw and palate are comparable to those in more primitive sarcopterygians, the new species also has a shortened skull roof, a modified ear region, a mobile neck, a functional wrist joint, and other features that presage tetrapod conditions. The morphological features and geological setting of this new animal are suggestive of life in shallow-water, marginal and subaerial habitats.
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            The braincase and jaws of a Devonian 'acanthodian' and modern gnathostome origins.

            Modern gnathostomes (jawed vertebrates) emerged in the early Palaeozoic era, but this event remains unclear owing to a scant early fossil record. The exclusively Palaeozoic 'acanthodians' are possibly the earliest gnathostome group and exhibit a mosaic of shark- and bony fish-like characters that has long given them prominence in discussions of early gnathostome evolution. Their relationships with modern gnathostomes have remained mysterious, partly because their un-mineralized endoskeletons rarely fossilized. Here I present the first-known braincase of an Early Devonian (approximately 418-412 Myr bp) acanthodian, Ptomacanthus anglicus, and re-evaluate the interrelationships of basal gnathostomes. Acanthodian braincases have previously been represented by a single genus, Acanthodes, which occurs more than 100 million years later in the fossil record. The braincase of Ptomacanthus differs radically from the osteichthyan-like braincase of Acanthodes in exhibiting several plesiomorphic features shared with placoderms and some early chondrichthyans. Most striking is its extremely short sphenoid region and its jaw suspension, which displays features intermediate between some Palaeozoic chondrichthyans and osteichthyans. Phylogenetic analysis resolves Ptomacanthus as either the most basal chondrichthyan or as the sister group of all living gnathostomes. These new data alter earlier conceptions of basal gnathostome phylogeny and thus help to provide a more detailed picture of the acquisition of early gnathostome characters.
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              The oldest articulated osteichthyan reveals mosaic gnathostome characters.

              The evolutionary history of osteichthyans (bony fishes plus tetrapods) extends back to the Ludlow epoch of the Silurian period. However, these Silurian forms have been documented exclusively by fragmentary fossils. Here we report the discovery of an exceptionally preserved primitive fish from the Ludlow of Yunnan, China, that represents the oldest near-complete gnathostome (jawed vertebrate). The postcranial skeleton of this fish includes a primitive pectoral girdle and median fin spine as in non-osteichthyan gnathostomes, but a derived macromeric squamation as in crown osteichthyans, and substantiates the unexpected mix of postcranial features in basal sarcopterygians, previously restored from the disarticulated remains of Psarolepis. As the oldest articulated sarcopterygian, the new taxon offers insights into the origin and early divergence of osteichthyans, and indicates that the minimum date for the actinopterygian-sarcopterygian split was no later than 419 million years ago.
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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
                2013
                18 April 2013
                : 8
                : 4
                Affiliations
                [1 ]Laboratório de Ictiologia de Ribeirão Preto (LIRP), Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, PPG Biologia Comparada, Ribeirão Preto, SP, Brazil
                [2 ]Laboratório de Ictiologia, Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil
                Monash University, Australia
                Author notes

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

                Conceived and designed the experiments: MC FAB MRC. Performed the experiments: MC FAB MRC. Analyzed the data: MC FAB MRC. Contributed reagents/materials/analysis tools: MC FAB MRC. Wrote the paper: MC FAB MRC.

                Article
                PONE-D-12-30358
                10.1371/journal.pone.0062389
                3630151
                23638061
                74b93e2a-4413-44f9-9cf9-83b00bd8e06c

                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.

                Page count
                Pages: 21
                Funding
                MC is supported by the Conselho Nacional de Desenvolvimento iientífico e Tecnológico (CNPq, 140415/2006-8) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 2012/05152-0); FAB by CNPq (309752/2010-8) and FAPESP (2004/09219–6, 2009/54931–0, 2012/21159–5); MRC by CNPq (303061/2008-1, 304615/2011-0) and FAPESP (2010/51193-5, 2012/02349-8, 2012/09877-0, 2012/05391-5). Funding agencies had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Evolutionary Biology
                Evolutionary Systematics
                Cladistics
                Phylogenetics
                Paleontology
                Vertebrate Paleontology
                Histology
                Paleontology
                Vertebrate Paleontology
                Zoology
                Animal Phylogenetics
                Comparative Anatomy
                Ichthyology

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                Uncategorized

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