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      Three-dimensional kinematics of euchelicerate limbs uncover functional specialization in eurypterid appendages

      1 , 2 , 3 , 4 , 2 , 3
      Biological Journal of the Linnean Society
      Oxford University Press (OUP)

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          Abstract

          Sea scorpions (Euchelicerata: Eurypterida) explored extreme limits of the aquatic euchelicerate body plan, such that the group contains the largest known marine euarthropods. Inferences on eurypterid life modes, in particular walking and eating, are commonly made by comparing the group with horseshoe crabs (Euchelicerata: Xiphosura). However, no models have been presented to test these hypotheses. Here, we reconstruct prosomal appendages of two exceptionally well-preserved eurypterids, Eurypterus tetragonophthalmus and Pentecopterus decorahensis, and model the flexure and extension of these appendages kinematically in three dimensions (3D). We compare these models with 3D kinematic models of Limulus polyphemus prosomal appendages. This comparison highlights that the examined eurypterid prosomal appendages could not have moved prey items effectively to the gnathal edges and would therefore not have emulated the motion of an L. polyphemus walking leg. It seems that these eurypterid appendages were used primarily to walk or grab prey, and other appendages would have moved prey for mastication. Such 3D kinematic modelling highlights how eurypterid appendage morphologies placed substantial limits on their function, suggesting a high degree of specialization, especially when compared with horseshoe crabs. Such three-dimensional kinematic modelling of these extinct groups therefore presents an innovative approach to understanding the position of these animals within their respective palaeoecosystems.

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          X-ray reconstruction of moving morphology (XROMM): precision, accuracy and applications in comparative biomechanics research.

          X-Ray Reconstruction of Moving Morphology (XROMM) comprises a set of 3D X-ray motion analysis techniques that merge motion data from in vivo X-ray videos with skeletal morphology data from bone scans into precise and accurate animations of 3D bones moving in 3D space. XROMM methods include: (1) manual alignment (registration) of bone models to video sequences, i.e., Scientific Rotoscoping; (2) computer vision-based autoregistration of bone models to biplanar X-ray videos; and (3) marker-based registration of bone models to biplanar X-ray videos. Here, we describe a novel set of X-ray hardware, software, and workflows for marker-based XROMM. Refurbished C-arm fluoroscopes retrofitted with high-speed video cameras offer a relatively inexpensive X-ray hardware solution for comparative biomechanics research. Precision for our biplanar C-arm hardware and analysis software, measured as the standard deviation of pairwise distances between 1 mm tantalum markers embedded in rigid objects, was found to be +/-0.046 mm under optimal conditions and +/-0.084 mm under actual in vivo recording conditions. Mean error in measurement of a known distance between two beads was within the 0.01 mm fabrication tolerance of the test object, and mean absolute error was 0.037 mm. Animating 3D bone models from sets of marker positions (XROMM animation) makes it possible to study skeletal kinematics in the context of detailed bone morphology. The biplanar fluoroscopy hardware and computational methods described here should make XROMM an accessible and useful addition to the available technologies for studying the form, function, and evolution of vertebrate animals.
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            Arthropod fossil data increase congruence of morphological and molecular phylogenies.

            The relationships of major arthropod clades have long been contentious, but refinements in molecular phylogenetics underpin an emerging consensus. Nevertheless, molecular phylogenies have recovered topologies that morphological phylogenies have not, including the placement of hexapods within a paraphyletic Crustacea, and an alliance between myriapods and chelicerates. Here we show enhanced congruence between molecular and morphological phylogenies based on 753 morphological characters for 309 fossil and Recent panarthropods. We resolve hexapods within Crustacea, with remipedes as their closest extant relatives, and show that the traditionally close relationship between myriapods and hexapods is an artefact of convergent character acquisition during terrestrialisation. The inclusion of fossil morphology mitigates long-branch artefacts as exemplified by pycnogonids: when fossils are included, they resolve with euchelicerates rather than as a sister taxon to all other euarthropods.
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              The evolution of arthropod limbs.

              Limb morphology across the arthropods is reviewed using external morphological and internal anatomical data from both recent and fossil arthropods. Evolutionary trends in limb structure are identified primarily by reference to the more rigorous of the many existing phylogenetic schemes, but no major new phylogenetic inferences are presented. Tagmosis patterns are not considered, although the origins and patterns of heteronomy within the postantennulary limb series are analysed. The phenomenon of annulation is examined and two basic types of annuli are recognised: terminal and intercalary. The annulation of the apical segment of a limb results in the formation of terminal flagella, and is typical of primarily sensory appendages such as insect and malacostracan antennules and maxillary palps of some hexapods. Intercalary annulation, arising by subdivision of existing subterminal segments, is common, particularly in the tarsal region of arthropodan walking limbs. Differentiating between segments and annuli is discussed and is recognised as a limiting factor in the interpretation of fossils, which usually lack information on intrinsic musculature, and in the construction of groundplans. Rare examples of secondary segmentation, where the criteria for distinguishing between segments and annuli fail, are also highlighted. The basic crown-group arthropodan limb is identified as tripartite, comprising protopodite, telopodite and exopodite, and the basic segmentation patterns of each of these parts are hypothesised. Possible criteria are discussed that can be used for establishing the boundary between protopodite and telopodite in limbs that are uniramous through loss of the exopodite. The subdivision of the protopodite, which is typical of the postantennulary limbs of mandibulates, is examined. The difficulties resulting from the partial or complete failure of expression of articulations within the mandibulate protopodite and subsequent incorporation of partial protopodal segments into the body wall, are also discussed. The development and homology between the various exites, including gills, on the postantennulary limbs of arthropods are considered in some detail, and the question of the possible homology between crustacean gills and insect wings is critically addressed. The hypothesis that there are only two basic limb types in arthropods, antennules and postantennulary limbs, is proposed and its apparent contradiction by the transformation of antennules into walking limbs by homeotic mutation is discussed with respect to the appropriate level of serial homology between these limbs.
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                Author and article information

                Contributors
                (View ORCID Profile)
                Journal
                Biological Journal of the Linnean Society
                Oxford University Press (OUP)
                0024-4066
                1095-8312
                January 01 2022
                January 01 2022
                November 12 2021
                January 01 2022
                January 01 2022
                November 12 2021
                : 135
                : 1
                : 174-183
                Affiliations
                [1 ]Palaeoscience Research Centre, School of Environmental and Rural Science, University of New England, Armidale,NSW 2351,Australia
                [2 ]Bavarian State Collection of Zoology, Bavarian Natural History Collections, Munich,Germany
                [3 ]Department Biology II, Ludwig-Maximilians-Universität München, Munich,Germany
                [4 ]GeoBio-Center, Ludwig-Maximilians-Universität München, Munich,Germany
                Article
                10.1093/biolinnean/blab108
                9ad5f54f-1b5d-46df-b7e6-d381505d9511
                © 2021

                https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model

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