Muscles and Muscle Scars in Fossil Malacostracan Crustaceans T ⁎ Adiël A

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Muscles and Muscle Scars in Fossil Malacostracan Crustaceans T ⁎ Adiël A Earth-Science Reviews 194 (2019) 306–326 Contents lists available at ScienceDirect Earth-Science Reviews journal homepage: www.elsevier.com/locate/earscirev Muscles and muscle scars in fossil malacostracan crustaceans T ⁎ Adiël A. Klompmakera,b,c, , Matúš Hyžnýd,e, Roger W. Portellb, Clément Jauvionf,g, Sylvain Charbonnierf, Shane S. Fussellc, Aaron T. Klierh, Raymond Tejerac, Sten L. Jakobseni a Department of Integrative Biology & Museum of Paleontology, University of California, Berkeley, 1005 Valley Life Sciences Building #3140, Berkeley, CA 94720, USA b Florida Museum of Natural History, University of Florida, 1659 Museum Road, Gainesville, FL 32611, USA c Department of Geological Sciences, University of Florida, 241 Williamson Hall, Gainesville, FL 32611, USA d Department of Geology and Paleontology, Faculty of Natural Sciences, Comenius University, Mlynská dolina G1, Ilkovičova 6, SVK-842 15 Bratislava, Slovakia e Geological-Paleontological Department, Natural History Museum Vienna, Burgring 7, 1010 Vienna, Austria f Muséum national d'Histoire naturelle, Centre de Recherche en Paléontologie - Paris (CR2P, UMR 7207), CNRS, Sorbonne Université, 57 rue Cuvier, F-75005 Paris, France g Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie, CNRS UMR 7590, Sorbonne Université, Muséum national d'Histoire naturelle, IRD UMR 206, 61 rue Buffon, F-75005 Paris, France h Department of Biology, University of Florida, 220 Bartram Hall, Gainesville, FL 32611, USA i Geomuseum Faxe, Østervej 2, DK-4640 Faxe, Denmark ARTICLE INFO ABSTRACT Keywords: Exceptionally preserved specimens yield critical information about the soft-part anatomy and the evolution of Crustacea organisms through time. We compiled the first global dataset of exceptionally preserved muscles in malacos- Decapoda tracans consisting of 47 occurrences, including 18 new records, predominantly preserved in Mesozoic Konservat- Exceptional preservation Lagerstätten (> 70% of occurrences). Early diagenetic mineralization through phosphatization is the dominant Lagerstätten process for exceptional preservation of muscles in malacostracans. Over 70% of taxon occurrences with muscles Malacostraca preserved are compressed. Rarer, three-dimensionally preserved specimens allow more detailed study of mus- Muscle cles. One example are specimens of the mid-Holocene ghost shrimp Sergio sp. from Panama, showing exquisitely preserved strings of muscle fibers attached to the shell interior, resembling the muscle arrangement ofmodern ghost shrimps. Other fossil malacostracans, including the oldest known fossil shrimp, also show musculature similar to modern taxa. We hypothesize that this muscle conservatism may be related to the confined space within the malacostracan shell in conjunction with the relatively stable body plan of several clades. We also assembled the first dataset on muscle attachment scars in malacostracans. Unlike muscles, muscle scars aremore common. Approximately 24% of the 357 articles analyzed yielded evidence of muscle scars, but such scars were only recognized for 19% of the 162 taxon occurrences that showed muscle scars. Muscle scars are common from the Late Jurassic onwards, are found primarily in Brachyura and Axiidea, and do not suffer from a Lagerstätten- effect. Rocks with well-preserved specimens should yield an additional wealth of information on thesoftpart anatomy of malacostracans. Similarly, muscle scars represent an almost untapped, complementary source of information on muscle evolution. 1. Introduction 1930; Feldmann and Schweitzer, 2010; Wilby and Briggs, 1997). The most diverse clade among malacostracans are the Decapoda, with a The preservation of soft tissues in fossils provides exceptional in- fossil record of ~3700 species (Schweitzer and Feldmann, 2016) and sight into the biology of ancient metazoans. Muscles have been used to major species- and genus-level diversifications from the Mesozoic on- infer the functioning of organisms, their taxonomic identity, and evo- wards (Klompmaker et al., 2013; Schweitzer and Feldmann, 2015; lutionary relationships among clades (e.g., Bergström et al., 1989; Kaji Sepkoski, 2000). Other, less diverse malacostracan clades with a mac- et al., 2018; Parry et al., 2015; Trinajstic et al., 2007; Young and rofossil record are Isopoda, Phyllocarida, and Hoplocarida. Muscles in Vinther, 2017). Muscles are preserved in a variety of arthropods (e.g., fossil malacostracans are almost exclusively mentioned as part of sys- Briggs et al., 2005; Hu et al., 2017; Siveter et al., 2010; Vannier et al., tematic descriptions thus far, but have the potential to provide insight 2014), including in multiple clades of Malacostraca (e.g., Beurlen, into the evolution of myoanatomy through time. ⁎ Corresponding author. E-mail address: [email protected] (A.A. Klompmaker). https://doi.org/10.1016/j.earscirev.2019.04.012 Received 21 December 2018; Received in revised form 8 April 2019; Accepted 8 April 2019 Available online 10 April 2019 0012-8252/ © 2019 Elsevier B.V. All rights reserved. A.A. Klompmaker, et al. Earth-Science Reviews 194 (2019) 306–326 Fig. 1. Thoracic/carapace muscles (A) and muscle scars (B) in the brachyuran decapod crustacean Dromia personata (Linnaeus, 1758). Modified from McLaughlin (1980: Fig. 53A) and redrawn from Glaessner (1969: Fig. 224). Muscle attachment traces or scars on the hard parts of fossil me- 2.1. Thoracic muscles tazoans can provide complementary information on many aspects of metazoan biology in deep time. Muscle scars have helped gain insight Thoracic muscles (Fig. 1) provide support for the animal body and into the evolution of digestive tracts, the function of skeletal elements, interconnect body parts such as the thorax and pleon. The thorax in the size of soft tissues, life habit, and the relatedness among organisms decapods is rather inflexible and contains mainly thoracopleonal mus- (e.g., Doguzhaeva and Mutvei, 1991; Dzik, 2010; Knight and Morris, cles, in addition to those connecting the internal with the external 2019; Kröger and Mutvei, 2005; Lerosey-Aubril and Peel, 2018; Richter skeleton (Glaessner, 1969). Nevertheless, the thoracic musculature is and Fischer, 2002; Topper and Skovsted, 2017). Such scars have been extraordinarily complex and the number of individual muscles is large found in fossil malacostracans (e.g., Glaessner, 1960; Hof and Schram, in lobsters and most anomurans, whereas the whole arrangement in 1998; Schweigert and Koppka, 2011), but, again, they are primarily brachyurous crabs is less complicated (Pilgrim, 1973). In hoplocar- mentioned as part of taxon descriptions. idans, the thorax is more flexible and contains also bundles of flexors Here we review muscles and muscle scars in fossil malacostracans to and extensors (Pilgrim, 1964). In decapods, various paired bundles of evaluate (1) muscle preservation through geologic time based on dorsal thoracic muscles are situated either between the inner side of the known and new occurrences, (2) how fossil muscles compare to those in carapace and the endophragmal skeleton or between elements of the extant representatives, (3) the taxa with muscle attachment scars and endophragmal skeleton (Keiler et al., 2016). The attachment areas of their location, and (4) the frequency and the degree of recognition of muscles are recognizable on the inner surface of the carapace muscle scars. (Glaessner, 1960, 1969). Institutional abbreviations. GBA: Geologische Bundesanstalt, In decapods, the most important groups of muscles attached to the Vienna, Austria; MAB: Oertijdmuseum, Boxtel, The Netherlands; carapace are the epimeral attractor muscle (muscle inserting along the MGUH: Natural History Museum of Denmark, Geological Museum, branchiocardiac groove that connects the epimeral wall of the ventral University of Copenhagen, Denmark; MNHN: Muséum national thorax to the dorsal carapace), mandibular muscles (operating mand- d'Histoire naturelle, Paris, France; NHMW: Department of Geology and ibles), gastric muscles (responsible for moving the gastric mill), and a Palaeontology, Natural History Museum Vienna, Austria; SMF: small portion of the thoraco-pleonal muscles (interconnecting thorax Forschungsinstitut Senckenberg, Frankfurt am Main, Germany; UF: with pleon). Ventral thoracic muscles are extrinsic muscles (flexors + Florida Museum of Natural History at the University of Florida, extensors) of the bases of appendages and are located directly above the Gainesville, USA; UMJGPA: Geological-palaeontological Department, sternum (Keiler et al., 2016). There is considerable variation in the Universalmuseum Joanneum, Graz, Austria. development of mandibular muscles. In lobsters, the posterior (ad- ductor) muscle is very strong and its area of attachment covers a large 2. Major muscle groups and muscle scars of extant malacostracans part of the lateral internal surface of the carapace. In squat lobsters and with a fossil record crab-like decapods, this muscle is very weak and the lateral adductor muscle occupies more space on its surface (Glaessner, 1960). Skeletal muscles coupled with the nervous system provide the ne- Of the external gastric muscles, only the group of the posterior cessary equipment for organisms to actively move. The neuromuscular muscles is attached to the carapace. It is connected with two small morphology in malacostracans is responsible for distinct ways of mo- calcareous projections of its apodemes close to the median line of the tion, including swimming, tail-flipping (e.g., escape response,
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