Current IF 1.9
Latest issue (RSS 2.0)
Contact Editorial Office at
bulletin@geology.cz

Bulletin of Geosciences
Published by ©
Czech Geological Survey,
W. Bohemia Museum Pilsen
Individual sponsors
ISSN: 1802-8225 (online),
1214-1119 (print)

The evolutionary history of body organisation in the lineage towards modern scorpions
Published in: Bulletin of Geosciences, volume 94, issue 4; pages: 389 - 408; Received 21 February 2019; Accepted in revised form 21 October 2019; Online 10 December 2019
Keywords: tagmosis, tagmatization, feeding apparatus, character polarisation, pectines, book lungs,
Abstract
The enormous evolutionary success of euarthropods (insects, crustaceans, myriapods, chelicerates, and their relatives) is generally thought to be coupled to their specific mode of body organisation, also called tagmosis. Their body segments are organised into groups of segments, which share specific functions; these functional units are called tagmata. The patterns of tagmosis differ between the different euarthropod groups, and some of these patterns appear to be constant since the earliest appearance of the group. However, often no strict criteria have been applied which characterise a tagma as such. We provide here a new view on the tagmosis of scorpions and the evolutionary history behind it, by applying criteria already successfully used for elucidating the tagmosis of other euarthropods. Our study shows that the tagmosis changed several times from the ground pattern of Euarthropoda to modern scorpions, the latter ones possessing a tagmosis not present in the earliest scorpions. This difference mainly concerns the region of the sternum, the genital operculum and the pectines. We provide additional data which cast doubt on the presence of pectines in early scorpions. Our argumentation provides an explanation for the evolution of tagmosis in modern scorpions with less conflict than hypotheses proposed earlier.References
Arango, C.P. 2002. Morphological phylogenetics of the sea spiders (Arthropoda: Pycnogonida). Organisms Diversity & Evolution 2, 107-125.
Arango, C.P. & Wheeler, W.C. 2007. Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23, 255-293.
Assis, L.C. 2009. Coherence, correspondence, and the renaissance of morphology in phylogenetic systematics. Cladistics 25, 528-544.
Averof, M., Pavlopoulos, A. & Kontarakis, Z. 2010. Evolution of new appendage types by gradual changes in Hox gene expression-the case of crustacean maxillipeds. Palaeodiversity 3 (Suppl.), 141-146.
Ax, P. 1995. Das System der Metazoa I. Ein Lehrbuch der phylogenetischen Systematik. 226 pp. Gustav Fischer Verlag, Stuttgart.
Ballesteros, J.A. & Sharma, P.P. 2019. A critical appraisal of the placement of Xiphosura (Chelicerata) with account of known sources of phylogenetic error. Systematic Biology 68(6), 896-917.
Bergström, J., Stürmer, W. & Winter, G. 1980. Palaeoisopus, Palaeopantopus and Palaeothea, pycnogonid arthropods from the Lower Devonian Hunsrück Slate, West Germany. Paläontologische Zeitschrift 54, 7-54.
Braddy, S.J., Aldridge, R.J., Gabbott, S.E. & Theron, J.N. 1999. Lamellate book-gills in a late Ordovician eurypterid from the Soom Shale, South Africa: support for a eurypterid-scorpion clade. Lethaia 32, 72-74.
Brenneis, G., Ungerer, P. & Scholtz, G. 2008. The chelifores of sea spiders (Arthropoda, Pycnogonida) are the appendages of the deutocerebral segment. Evolution & Development 10, 717-724.
Briggs, D.E.G., Siveter, D.J., Siveter, D.J., Sutton, M.D., Garwood, R.J. & Legg, D. 2012. Silurian horseshoe crab illuminates the evolution of arthropod limbs. Proceedings of the National Academy of Sciences 109, 15702-15705.
Chen, J., Waloszek, D. & Maas, A. 2004. A new ’great-appendage’ arthropod from the Lower Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral appendages. Lethaia 15, 3-20.
Donoghue, P.C. 2005. Saving the stem group-a contradiction in terms? Paleobiology 31, 553-558.
Dunlop, J.A. 1998. The origins of tetrapulmonate book lungs and their significance for chelicerate phylogeny, 9-16. In Proceedings of the 17th European Colloquium of Arachnology, Edinburgh.
Dunlop, J.A. 2002. Arthropods from the Lower Devonian Severnaya Zemlya Formation of October Revolution Island (Russia). Geodiversitas 24, 349-379.
Dunlop, J.A. 2010. Geological history and phylogeny of Chelicerata. Arthropod Structure & Development 39, 124-142.
Dunlop, J.A. & Arango, C.P. 2005. Pycnogonid affinities: a review. Journal of Zoological Systematics and Evolutionary Research 43, 8-21.
Dunlop, J.A. & Lamsdell, J.C. 2017. Segmentation and tagmosis in Chelicerata. Arthropod Structure & Development 46, 395-418.
Dunlop, J.A. & Webster, M. 1999. Fossil evidence, terrestrialization and arachnid phylogeny. Journal of Arachnology 27, 86-93.
Dunlop, J.A., Tetlie, E.O. & Prendini, L. 2008. Reinterpretation of the Silurian scorpion Proscorpius osborni (Whitfield): integrating data from Palaeozoic and Recent scorpions. Palaeontology 51, 303-320.
Edgecombe, G.D. & Legg, D.A. 2014. Origins and early evolution of arthropods. Palaeontology 57, 457-468.
Eldredge, N. 1974. Revision of the suborder Synziphosurina (Chelicerata, Merostomata), with remarks on merostome phylogeny. American Museum Novitates 2543, 1-41.
Farley, R.D. 2005. Developmental changes in the embryo, pronymph, and first molt of the scorpion Centruroides vittatus (Scorpiones: Buthidae). Journal of Morphology 265, 1-27.
Garwood, R.J. & Dunlop, J. 2014. Three-dimensional reconstruction and the phylogeny of extinct chelicerate orders. PeerJ 2, e641.
Giribet, G. 2018. Current views on chelicerate phylogeny-A tribute to Peter Weygoldt. Zoologischer Anzeiger 273, 7-13.
Hammen, L. van der 1963. The addition of segments during the postembryonic ontogenesis of the Actinotrichida (Acarida) and its importance for the recognition of the primary subdivision of the body and the original segmentation. Acarologia 5, 443-457.
Hammen, L. van der 1980. Glossary of acarological terminology, Vol. 1 General terminology. 245 pp. Dr. W. Junk, The Hague.
Haug, C. & Rötzer, M.A.I.N. 2018. The ontogeny of Limulus polyphemus (Xiphosura s. str., Euchelicerata) revised: looking “under the skin”. Development Genes and Evolution 228, 49-61.
Haug, C., Haug, J.T., Waloszek, D., Maas, A., Frattigiani, R. & Liebau, S. 2009. New methods to document fossils from lithographic limestones of southern Germany and Lebanon. Palaeontologia Electronica 12(3), 6T, 12p.
Haug, C., Sallam, W.S., Maas, A., Waloszek, D., Kutschera, V. & Haug, J.T. 2012b. Tagmatization in Stomatopoda - reconsidering functional units of modern-day mantis shrimps (Verunipeltata, Hoplocarida) and implications for the interpretation of fossils. Frontiers in Zoology 9, art. 31.
Haug, C., Van Roy, P., Leipner, A., Funch, P., Rudkin, D.M., Schöllmann, L. & Haug, J.T. 2012a. A holomorph approach to xiphosuran evolution-a case study on the ontogeny of Euproops. Development Genes and Evolution 222, 253-268.
Haug, J.T., Briggs, D.E.G. & Haug, C. 2012b. Morphology and function in the Cambrian Burgess Shale megacheiran arthropod Leanchoilia superlata and the application of a descriptive matrix. BMC Evolutionary Biology 12, art. 162.
Haug, J.T., Haug, C. & Ehrlich, M. 2008. First fossil stomatopod larva (Arthropoda: Crustacea) and a new way of documenting Solnhofen fossils (Upper Jurassic, Southern Germany). Palaeodiversity 1, 103-109.
Haug, J.T., Haug, C., Kutschera, V., Mayer, G., Maas, A., Liebau, S., Castellani, C., Wolfram, U., Clarkson, E.N.K. & Waloszek, D. 2011. Autofluorescence imaging, an excellent tool for comparative morphology. Journal of Microscopy 244, 259-272.
Haug, J.T., Maas, A., Haug, C. & Waloszek, D. 2013. Chapter 2. Evolution of crustacean appendages, 34-73. In Watling, L. & Thiel, M. (eds) Vol. 1. Functional Morphology and Diversity. The Natural History of the Crustacea. Oxford University Press, Oxford.
Haug, J.T., Waloszek, D., Maas, A., Liu, Y. & Haug, C. 2012a. Functional morphology, ontogeny and evolution of mantis shrimp-like predators in the Cambrian. Palaeontology 55, 369-399.
Hedgpeth, J.W. 1947. On the evolutionary significance of the Pycnogonida. Smithsonian Miscellaneous Collection 106, 1-53.
Hennig, W. 1966. Phylogenetic systematics. 263 pp. University of Illinois Press, Urbana, IL.
Jager, M., Murienne, J., Clabaut, C., Deutsch, J., Le Guyader, H. & Manuel, M. 2006. Homology of arthropod anterior appendages revealed by Hox gene expression in a sea spider. Nature 441, 506-508.
Jeram, A.J. 1998. Phylogeny, classification and evolution of Silurian and Devonian scorpions, 17-31. In Proceedings of the 17th European Colloquium of Arachnology, Edinburgh.
Kerp, H. & Bomfleur, B. 2011. Photography of plant fossils - new techniques, old tricks. Review of Palaeobotany and Palynology 166, 117-151.
Kjellesvig-Waering, E.N. 1986. A restudy of the fossil Scorpionida of the world. Palaeontographica Americana 55, 1-287.
Klußmann-Fricke, B.J. & Wirkner, C.S. 2016. Comparative morphology of the hemolymph vascular system in Uropygi and Amblypygi (Arachnida): complex correspondences support Arachnopulmonata. Journal of Morphology 277, 1084-1103.
Kühl, G., Poschmann, M. & Rust, J. 2013. A ten-legged sea spider (Arthropoda: Pycnogonida) from the Lower Devonian Hunsrück Slate (Germany). Geological Magazine 150, 556-564.
Lamsdell, J.C. 2013. Revised systematics of Palaeozoic ’horseshoe crabs’ and the myth of monophyletic Xiphosura. Zoological Journal of the Linnean Society 167, 1-27.
Lamsdell, J.C. 2016. Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation. Palaeontology 59, 181-194.
Legg, D. 2013. Multi-segmented arthropods from the Middle Cambrian of British Columbia (Canada). Journal of Paleontology 87, 493-501.
Lehmann, W.M. 1956. Beobachtungen an Weinbergina opitzi (Merost., Devon). Senckenbergiana lethaia 37, 67-77.
Liu, Y., Hou, X.G. & Bergström, J. 2007. Chengjiang arthropod Leanchoilia illecebrosa (Hou, 1987) reconsidered. GFF 129, 263-272.
Maas, A. & Waloszek, D. 2001. Cambrian derivatives of the early arthropod stem lineage, pentastomids, tardigrades and lobopodians-an ’Orsten’ perspective. Zoologischer Anzeiger - A Journal of Comparative Zoology 240, 451-459.
Maas, A., Waloszek, D., Chen, J., Braun, A., Wang, X. & Huang, D. 2004. Phylogeny and life habits of early arthropods-predation in the Early Cambrian sea. Progress in Natural Science 14, 158-166.
Manuel, M., Jager, M., Murienne, J., Clabaut, C. & Le Guyader, H. 2006. Hox genes in sea spiders (Pycnogonida) and the homology of arthropod head segments. Development Genes and Evolution 216, 481-491.
Marshall, D.J., Lamsdell, J.C., Shpinev, E. & Braddy, S.J. 2014. A diverse chasmataspidid (Arthropoda: Chelicerata) fauna from the Early Devonian (Lochkovian) of Siberia. Palaeontology 57, 631-655.
Minelli, A. 2016. Species diversity vs. morphological disparity in the light of evolutionary developmental biology. Annals of Botany 117, 781-794.
Moczek, A.P. 2010. Phenotypic plasticity and diversity in insects. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 593-603.
Moczek, A.P., Sultan, S., Foster, S., Ledón-Rettig, C., Dworkin, I., Nijhout, H.F., Abouheif, E. & Pfennig, D.W. 2011. The role of developmental plasticity in evolutionary innovation. Proceedings of the Royal Society B: Biological Sciences 278, 2705-2713.
Moore, R.A., Briggs, D.E.G. & Bartels, C. 2005b. A new specimen of Weinbergina opitzi (Chelicerata: Xiphosura) from the Lower Devonian Hunsrück Slate, Germany. Paläontologische Zeitschrift 79, 399-408.
Moore, R.A., McKenzie, S.C. & Lieberman, B.S. 2007. A Carboniferous synziphosurine (Xiphosura) from the Bear Gulch Limestone, Montana, USA. Palaeontology 50, 1013-1019.
Moore, R.A., Briggs, D.E.G., Braddy, S.J., Anderson, L.I., Mikulic, D.G. & Kluessendorf, J. 2005a. A new synziphosurine (Chelicerata: Xiphosura) from the late Llandovery (Silurian) Waukesha lagerstätte, Wisconsin, USA. Journal of Paleontology 79, 242-250.
Moore, R.A., Briggs, D.E.G., Braddy, S.J. & Shultz, J.W. 2011. Synziphosurines (Xiphosura: Chelicerata) from the Silurian of Iowa. Journal of Paleontology 85, 83-91.
Pechmann, M. & Prpic, N.M. 2009. Appendage patterning in the South American bird spider Acanthoscurria geniculata (Araneae: Mygalomorphae). Development Genes and Evolution 219, 189-198.
Poschmann, M. & Dunlop, J.A. 2006. A new sea spider (Arthropoda: Pycnogonida) with a flagelliform telson from the Lower Devonian Hunsrück Slate, Germany. Palaeontology 49, 983-989.
Poschmann, M., Dunlop, J.A., Kamenz, C. & Scholtz, G. 2008. The Lower Devonian scorpion Waeringoscorpio and the respiratory nature of its filamentous structures, with the description of a new species from the Westerwald area, Germany. Paläontologische Zeitschrift 82, 418-436.
Reif, W.E. 2002. Evolution of organ systems: phylogeny, function and reciprocal illumination. Senckenbergiana lethaea 82, 356-366.
Scholl, G. 1977. Beiträge zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86, 99-154.
Scholtz, G. & Edgecombe, G.D. 2006. The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence. Development Genes and Evolution 216, 395-415.
Selden, P.A., Lamsdell, J.C. & Qi, L. 2015. An unusual euchelicerate linking horseshoe crabs and eurypterids, from the Lower Devonian (Lochkovian) of Yunnan, China. Zoologica Scripta 44, 645-652.
Sharma, P.P., Kaluziak, S.T., Perez-Porro, A.R., Gonzalez, V.L., Hormiga, G., Wheeler, W.C. & Giribet, G. 2014a. Phylogenomic interrogation of Arachnida reveals systemic conflicts in phylogenetic signal. Molecular Biology and Evolution 31, 2963-2984.
Sharma, P.P., Schwager, E.E., Extavour, C.G., & Wheeler, W.C. 2014b. Hox gene duplications correlate with posterior heteronomy in scorpions. Proceedings of the Royal Society B: Biological Sciences 281, 20140661.
Shultz, J.W. 2001. Gross muscular anatomy of Limulus polyphemus (Xiphosura, Chelicerata) and its bearing on evolution in the Arachnida. Journal of Arachnology 29, 283-303.
Shultz, J.W. 2007a. A phylogenetic analysis of the arachnid orders based on morphological characters. Zoological Journal of the Linnean Society 150, 221-265.
Shultz, J.W. 2007b. Morphology of the prosomal endoskeleton of Scorpiones (Arachnida) and a new hypothesis for the evolution of cuticular cephalic endoskeletons in arthropods. Arthropod Structure & Development 36, 77-102.
Snodgrass, R.E. 1948. The feeding organs of Arachnida, including mites and ticks. Smithsonian Miscellaneous Collections 110, 1-93.
Soleglad, M.E. & Fet, V. 2003. The scorpion sternum: structure and phylogeny (Scorpiones: Orthosterni). Euscorpius 2003(5), 1-34.
Stürmer, W. & Bergström, J. 1981. Weinbergina, a xiphosuran arthropod from the Devonian Hunsrück Slate. Paläontologische Zeitschrift 55, 237-255.
Sutton, M.D., Briggs, D.E.G., Siveter, D.J., Siveter, D.J. & Orr, P.J. 2002. The arthropod Offacolus kingi (Chelicerata) from the Silurian of Herefordshire, England: computer based morphological reconstructions and phylogenetic affinities. Proceedings of the Royal Society of London B: Biological Sciences 269, 1195-1203.
Tollerton, V.P. 1989. Morphology, taxonomy, and classification of the order Eurypterida Burmeister, 1843. Journal of Paleontology 63, 642-657.
Vilpoux, K. & Waloszek, D. 2003. Larval development and morphogenesis of the sea spider Pycnogonum litorale (Ström, 1762) and the tagmosis of the body of Pantopoda. Arthropod Structure & Development 32, 349-383.
Vogel, B.R. & Durden, C.J. 1966. The occurrence of stigmata in a Carboniferous scorpion. Journal of Paleontology 40, 655-658.
Waddington, J., Rudkin, D.M. & Dunlop, J.A. 2015. A new mid-Silurian aquatic scorpion-one step closer to land? Biology Letters 11, 20140815.
Walossek, D. & Müller, K.J. 1998. Cambrian ’Orsten’-type arthropods and the phylogeny of Crustacea, 139-153. In Fortey, R.A. & Thomas, R.H. (eds) Arthropod relationships, Systematics Association Special Volume Series 55. Chapman & Hall, London.
Waterston, C.D. 1975. Gill structure in the Lower Devonian eurypterid Tarsopterella scotica. Fossils and Strata 4, 241-254.
Weygoldt, P. & Paulus, H.F. 1979. Untersuchungen zur Morphologie, Taxonomie und Phylogenie der Chelicerata 1 II. Cladogramme und die Entfaltung der Chelicerata. Journal of Zoological Systematics and Evolutionary Research 17, 177-200.
Wolff, C. & Scholtz, G. 2008. The clonal composition of biramous and uniramous arthropod limbs. Proceedings of the Royal Society B: Biological Sciences 275, 1023-1028.