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      An Expanded Combined Evidence Approach to the Gavialis Problem Using Geometric Morphometric Data from Crocodylian Braincases and Eustachian Systems

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          The phylogenetic position of the Indian gharial ( Gavialis gangeticus) is disputed - morphological characters place Gavialis as the sister to all other extant crocodylians, whereas molecular and combined analyses find Gavialis and the false gharial ( Tomistoma schlegelii) to be sister taxa. Geometric morphometric techniques have only begun to be applied to this issue, but most of these studies have focused on the exterior of the skull. The braincase has provided useful phylogenetic information for basal crurotarsans, but has not been explored for the crown group. The Eustachian system is thought to vary phylogenetically in Crocodylia, but has not been analytically tested. To determine if gross morphology of the crocodylian braincase proves informative to the relationships of Gavialis and Tomistoma, we used two- and three-dimensional geometric morphometric approaches. Internal braincase images were obtained using high-resolution computerized tomography scans. A principal components analysis identified that the first component axis was primarily associated with size and did not show groupings that divide the specimens by phylogenetic affinity. Sliding semi-landmarks and a relative warp analysis indicate that a unique Eustachian morphology separates Gavialis from other extant members of Crocodylia. Ontogenetic expansion of the braincase results in a more dorsoventrally elongate median Eustachian canal. Changes in the shape of the Eustachian system do provide phylogenetic distinctions between major crocodylian clades. Each morphometric dataset, consisting of continuous morphological characters, was added independently to a combined cladistic analysis of discrete morphological and molecular characters. The braincase data alone produced a clade that included crocodylids and Gavialis, whereas the Eustachian data resulted in Gavialis being considered a basally divergent lineage. When each morphometric dataset was used in a combined analysis with discrete morphological and molecular characters, it generated a tree that matched the topology of the molecular phylogeny of Crocodylia.

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          Insights into the Ecology and Evolutionary Success of Crocodilians Revealed through Bite-Force and Tooth-Pressure Experimentation

          Background Crocodilians have dominated predatory niches at the water-land interface for over 85 million years. Like their ancestors, living species show substantial variation in their jaw proportions, dental form and body size. These differences are often assumed to reflect anatomical specialization related to feeding and niche occupation, but quantified data are scant. How these factors relate to biomechanical performance during feeding and their relevance to crocodilian evolutionary success are not known. Methodology/Principal Findings We measured adult bite forces and tooth pressures in all 23 extant crocodilian species and analyzed the results in ecological and phylogenetic contexts. We demonstrate that these reptiles generate the highest bite forces and tooth pressures known for any living animals. Bite forces strongly correlate with body size, and size changes are a major mechanism of feeding evolution in this group. Jaw shape demonstrates surprisingly little correlation to bite force and pressures. Bite forces can now be predicted in fossil crocodilians using the regression equations generated in this research. Conclusions/Significance Critical to crocodilian long-term success was the evolution of a high bite-force generating musculo-skeletal architecture. Once achieved, the relative force capacities of this system went essentially unmodified throughout subsequent diversification. Rampant changes in body size and concurrent changes in bite force served as a mechanism to allow access to differing prey types and sizes. Further access to the diversity of near-shore prey was gained primarily through changes in tooth pressure via the evolution of dental form and distributions of the teeth within the jaws. Rostral proportions changed substantially throughout crocodilian evolution, but not in correspondence with bite forces. The biomechanical and ecological ramifications of such changes need further examination.
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            Combined support for wholesale taxic atavism in gavialine crocodylians.

            Morphological and molecular data sets favor robustly supported, contradictory interpretations of crocodylian phylogeny. A longstanding perception in the field of systematics is that such significantly conflicting data sets should be analyzed separately. Here we utilize a combined approach, simultaneous analyses of all relevant character data, to summarize common support and to reconcile discrepancies among data sets. By conjoining rather than separating incongruent classes of data, secondary phylogenetic signals emerge from both molecular and morphological character sets and provide solid evidence for a unified hypothesis of crocodylian phylogeny. Simultaneous analyses of four gene sequences and paleontological data suggest that putative adaptive convergences in the jaws of gavialines (gavials) and tomistomines (false gavials) offer character support for a grouping of these taxa, making Gavialinae an atavistic taxon. Simple new methods for measuring the influence of extinct taxa on topological support indicate that in this vertebrate order fossils generally stabilize relationships and accentuate hidden phylogenetic signals. Remaining inconsistencies in minimum length trees, including concentrated hierarchical patterns of homoplasy and extensive gaps in the fossil record, indicate where future work in crocodylian systematics should be directed.
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              Extended mitogenomic phylogenetic analyses yield new insight into crocodylian evolution and their survival of the Cretaceous-Tertiary boundary.

              The mitochondrial genomes of the dwarf crocodile, Osteolaemus tetraspis, and two species of dwarf caimans, the smooth-fronted caiman, Paleosuchus trigonatus, and Cuvier's dwarf caiman, Paleosuchus palpebrosus, were sequenced and included in a mitogenomic phylogenetic study. The phylogenetic analyses, which included a total of ten crocodylian species, yielded strong support to a basal split between Crocodylidae and Alligatoridae. Osteolaemus fell within the Crocodylidae as the sister group to Crocodylus. Gavialis and Tomistoma, which joined on a common branch, constituted a sister group to Crocodylus/Osteolaemus. This suggests that extant crocodylians are organized in two families: Alligatoridae and Crocodylidae. Within the Alligatoridae there was a basal split between Alligator and a branch that contained Paleosuchus and Caiman. The analyses also provided molecular estimates of various divergences applying recently established crocodylian and outgroup fossil calibration points. Molecular estimates based on amino acid data placed the divergence between Crocodylidae and Alligatoridae at 97-103 million years ago and that between Alligator and Caiman/Paleosuchus at 65-72 million years ago. Other crocodilian divergences were placed after the Cretaceous-Tertiary boundary. Thus, according to the molecular estimates, three extant crocodylian lineages have their roots in the Cretaceous. Considering the crocodylian diversification in the Cretaceous the molecular datings suggest that the extinction of the dinosaurs was also to some extent paralleled in the crocodylian evolution. However, for whatever reason, some crocodylian lineages survived into the Tertiary.

                Author and article information

                Role: Editor
                PLoS One
                PLoS ONE
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                8 September 2014
                : 9
                : 9
                : e105793
                [1 ]Richard Gilder Graduate School, American Museum of Natural History, New York, New York, United States of America
                [2 ]Division of Paleontology, American Museum of Natural History, New York, New York, United States of America
                [3 ]Department of Earth and Environmental Sciences, University of Iowa, Iowa City, Iowa, United States of America
                BiK-F Biodiversity and Climate Research Center, Germany
                Author notes

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

                Conceived and designed the experiments: MELG CAB MAN. Performed the experiments: MELG. Analyzed the data: MELG. Contributed reagents/materials/analysis tools: MELG CAB MAN. Wrote the paper: MELG CAB MAN.


                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.

                : 14 March 2014
                : 24 July 2014
                Page count
                Pages: 12
                This work was funded by the University of Iowa Department of Earth and Environmental Sciences, the Littlefield Foundation, Tim Rowe (University of Texas at Austin), the Richard Gilder Graduate School, and the American Museum of Natural History. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Research Article
                Biology and Life Sciences
                Biological Tissue
                Connective Tissue
                Evolutionary Biology
                Evolutionary Systematics
                Animal Phylogenetics
                Molecular Systematics
                Organismal Evolution
                Animal Evolution



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