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A holomorph approach to xiphosuran evolution—a case study on the ontogeny of Euproops

Abstract

Specimens of Euproops sp. (Xiphosura, Chelicerata) from the Carboniferous Piesberg quarry near Osnabrück, Germany, represent a relatively complete growth series of 10 stages. Based on this growth sequence, morphological changes throughout the ontogeny can be identified. The major change affects the shape of the epimera of the opisthosoma. In earlier stages, they appear very spine-like, whereas in later stages the bases of these spine-like structures become broader; the broadened bases are then successively drawn out distally. In the most mature stage known, the epimera are of trapezoidal shape and approach each other closely to form a complete flange around the thoracetron (=fused tergites of the opisthosoma). These ontogenetic changes question the taxonomic status of different species of Euproops, as the latter appear to correspond to different stages of the ontogenetic series reconstructed from the Piesberg specimens. This means that supposed separate species could, in fact, represent different growth stages of a single species. It could alternatively indicate that heterochrony (=evolutionary change of developmental timing) plays an important role in the evolution of Xiphosura. We propose a holomorph approach, i.e., reconstructing ontogenetic sequences for fossil and extant species as a sound basis for a taxonomic, phylogenetic, and evolutionary discussion of Xiphosura.

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References

  1. Ambrose T, Romano M (1972) New Upper Carboniferous Chelicerata (Arthropoda) from Somerset England. Palaeontology 15:569–578

    Google Scholar 

  2. Anderson LI (1994) Xiphosurans from the Westphalian D of the Radstock Basin, Somerset Coalfield, the South Wales Coalfield and Mazon Creek, Illinois. Proc Geol Assoc 105:265–275

    Article  Google Scholar 

  3. Anderson LI, Selden PA (1997) Opisthosomal fusion and phylogeny of Palaeozoic Xiphosura. Lethaia 30:19–31

    Article  Google Scholar 

  4. Ax P (2000) Multicellular animals: the phylogenetic system of the Metazoa. Springer, Berlin

    Google Scholar 

  5. Bengtson S (2000) Teasing fossils out of shales with cameras and computers. Palaeontol Electron 3(1):14, art. 4

    Google Scholar 

  6. Brauckmann C (1982) Der Schwertschwanz Euproops (Xiphosurida, Limulina, Euproopaceae) aus dem Oberkarbon des Piesbergs bei Osnabrück. Osnabr Naturwiss Mitt 9:17–26

    Google Scholar 

  7. Bruton DL, Nakrem HA (2005) Enrolment in a Middle Ordovician agnostoid trilobite. Acta Palaeontol Pol 50:441–448

    Google Scholar 

  8. Casanova B, De Jong L, Moreau X (2002) Carapace and mandibles ontogeny in the Dendrobranchiata (Decapoda), Euphausiacea, and Mysidacea (Crustacea): a phylogenetic interest. Can J Zool 80:296–306

    Article  Google Scholar 

  9. Chatterton BDE, Speyer SE (1997) Ontogeny. In: Moore RC (ed) Treatise on invertebrate paleontology. Part O, revised. Arthropoda 1, Trilobita. Geological Society of America and University of Kansas Press, Boulder, CO, pp 173–247

    Google Scholar 

  10. Dunlop JA, Webster M (1999) Fossil evidence, terrestrialization and arachnid phylogeny. J Arachnol 27:86–93

    Google Scholar 

  11. Dunlop JA, Brauckmann C, Steur H (2008) A Late Carboniferous fossil scorpion from the Piesberg, near Osnabrück, Germany. Fossil Rec 11:25–32

    Article  Google Scholar 

  12. Dunlop JA, Penney D, Jekel D (2010) A summary list of fossil spiders and their relatives. In: Platnick NI (ed) The world spider catalog, version 11.0 American Museum of Natural History. Available online at http://research.amnh.org/entomology/spiders/catalog/index.html. Accessed 01 March 2012.

  13. Eldredge N (1974) Revision of the suborder Synziphosurina (Chelicerata, Merostomata), with remarks on merostome phylogeny. Am Mus Novit 2543:1–41

    Google Scholar 

  14. Evenhuis NL (2008) A compendium of zoological type nomenclature: a reference source. Bish Mus Tech Rep 41:1–23

    Google Scholar 

  15. Filipiak P, Krawczynski W (1996) Westphalian xiphosurans (Chelicerata) from the Upper Silesia Coal Basin of Sosnowiec, Poland. Acta Palaeontol Pol 41:413–425

    Google Scholar 

  16. Fisher DC (1977) Functional significance of spines in the Pennsylvanian horseshoe crab Euproops danae. Paleobiology 3:175–195

    Google Scholar 

  17. Fisher DC (1979) Evidence for subaerial activity of Euproops danae (Merostomata, Xiphosurida). In: Nitecki MH (ed) Mazon creek fossils. Academic, New York, pp 379–447

    Google Scholar 

  18. Haug JT, Maas A, Haug C, Waloszek D (in press) Chapter 2. Evolution of crustacean appendages. In: Watling L, Thiel M (eds) Vol. 1. Functional morphology and diversity of the Crustacea. The natural history of the Crustacea. Oxford University Press

  19. Haug C, Haug JT, Waloszek D, Maas A, Frattigiani R, Liebau S (2009) New methods to document fossils from lithographic limestones of southern Germany and Lebanon. Palaeontol Electron 12(3):12, 6T

    Google Scholar 

  20. Haug JT, Haug C, Maas A, Kutschera V, Waloszek D (2010a) Evolution of mantis shrimps (Stomatopoda, Malacostraca) in the light of new Mesozoic fossils. BMC Evol Biol 10:17, art. 290

    Article  Google Scholar 

  21. Haug JT, Maas A, Waloszek D (2010b) †Henningsmoenicaris scutula, †Sandtorpia vestrogothiensis gen. et sp. nov. and heterochronic events in early crustacean evolution. Earth Environ Sci Trans R Soc Edinb 100:311–350

    Article  Google Scholar 

  22. Haug JT, Waloszek D, Haug C, Maas A (2010c) High-level phylogenetic analysis using developmental sequences: the Cambrian †Martinssonia elongata, †Musacaris gerdgeyeri gen. et sp. nov. and their position in early crustacean evolution. Arthropod Struct Dev 39:154–173

    PubMed  Article  CAS  Google Scholar 

  23. Haug JT, Haug C, Kutschera V, Mayer G, Maas A, Liebau S, Castellani C, Wolfram U, Clarkson ENK, Waloszek D (2011a) Autofluorescence imaging, an excellent tool for comparative morphology. J Microsc 244:259–272

    PubMed  Article  Google Scholar 

  24. Haug JT, Olesen J, Maas A, Waloszek D (2011b) External morphology and post-embryonic development of Derocheilocaris remanei (Mystacocarida) revisited, with a comparison to the Cambrian taxon Skara. J Crustac Biol 31:668–692

    Article  Google Scholar 

  25. Haug JT, Waloszek D, Maas A, Liu Y, Haug C (2012b) Functional morphology, ontogeny and evolution of mantis shrimp-like predators in the Cambrian. Palaeontology 55:369–399

    Article  Google Scholar 

  26. Hawksworth DL (2010) Terms used in Bionomenclature. The naming of organisms (and plant communities). Global Biodiversity Information Facility, Copenhagen. Available online at http://links.gbif.org/gbif_terms_nomenclature_guide_en_v1.pdf. Accessed 01 March 2012

  27. Hennig W (1966) Phylogenetic systematics. University of Illinois Press, Urbana

    Google Scholar 

  28. Hesselbo SP (1992) Aglaspidida (Arthropoda) from the Upper Cambrian of Wisconsin. J Paleontol 66:885–923

    Google Scholar 

  29. Horner JR, Goodwin MB (2009) Extreme cranial ontogeny in the Upper Cretaceous dinosaur Pachycephalosaurus. PLoS One 4(10):11, art. e7626

    Article  Google Scholar 

  30. Kerp H, Bomfleur B (2011) Photography of plant fossils—new techniques, old tricks. Rev Palaeobot Palynol 166:117–151

    Article  Google Scholar 

  31. Moritz M (1957) Zur Embryonalentwicklung der Phalangiiden (Opiliones, Palpatores) unter besonderer Berücksichtigung der äußeren Morphologie, der Bildung des Mitteldarmes und der Genitalanlage. Zool Jahrb Abt Anat Ontog Tiere 76:331–370

    Google Scholar 

  32. Müller KJ, Walossek D (1987) Morphology, ontogeny, and life habit of Agnostus pisiformis from the Upper Cambrian of Sweden. Fossils Strata 19:1–124

    Google Scholar 

  33. Olesen J, Haug JT, Maas A, Waloszek D (2011) External morphology of Lightiella monniotae (Crustacea, Cephalocarida) in the light of Cambrian ‘Orsten’ crustaceans. Arthropod Struct Dev 40:449–478

    PubMed  Article  Google Scholar 

  34. Raasch GO (1939) Cambrian Merostomata. Spec Pap Geol Soc Am 19:1–146

    Google Scholar 

  35. Racheboeuf PR, Vannier J, Anderson LI (2002) A new three-dimensionally preserved xiphosuran chelicerate from the Montceau-les-Mines lagerstätte (Carboniferous, France). Palaeontology 45:125–147

    Article  Google Scholar 

  36. Raw F (1957) Origin of chelicerates. J Paleontol 31:139–192

    Google Scholar 

  37. Scannella JB, Horner JR (2010) Torosaurus Marsh 1891 is Triceratops Marsh 1889 (Ceratopsidae: Chasmosaurinae): synonymy through ontogeny. J Vertebr Paleontol 30:1157–1168

    Article  Google Scholar 

  38. Schaarschmidt F (1973) Pflanzenfossilien in ungewöhnlichem Licht. Nat Mus 103:247–253

    Google Scholar 

  39. Scholl G (1977) Beiträge zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86:99–154

    Article  Google Scholar 

  40. Scholtz G, Edgecombe GD (2005) Heads, Hox and the phylogenetic position of trilobites. In: Koenemann S, Jenner RA (eds) Crustacea and arthropod relationships. Crustacean issues 16. CRC Press, Boca Raton, pp 139–165

    Chapter  Google Scholar 

  41. Schultka S (1994) Bellinurus cf. truemanii (Merostomata) aus dem tiefen Oberkarbon (Namur B/C) von Fröndenberg (Nordrhein-Westfalen, Deutschland). Paläontol Z 68:339–349

    Google Scholar 

  42. Schultka S (2000) Zur Palökologie der Euproopiden im Nordwestdeutschen Oberkarbon. Mitt Mus Naturwiss Berl Geowiss R 3:87–98

    Google Scholar 

  43. Selden PA, Siveter DJ (1987) The origin of limuloids. Lethaia 20:383–392

    Article  Google Scholar 

  44. Siegfried P (1972) Ein Schwertschwanz (Merostomata, Xiphosurida) aus dem Oberkarbon von Ibbenbüren/Westf. Paläontol Z 46:180–185

    Google Scholar 

  45. Størmer L (1944) On the relationships and phylogeny of fossil and recent Arachnomorpha. A comparative study on Arachnida, Xiphosura, Eurypterida, Trilobita and other fossil Arthropoda. Skr utg Nor Vidensk-Akad Oslo, I. Mat-Naturvidensk Kl 5:1–158

  46. Størmer L (1955) Merostomata. In: Moore RC (ed) Treatise on invertebrate paleontology. Part P. Arthropoda 2. Geological Society of America and University of Kansas Press, Boulder, CO, pp 4–41

    Google Scholar 

  47. Van Roy P (2006) An aglaspidid arthropod from the Upper Ordovician of Morocco with remarks on the affinities and limitations of Aglaspidida. Trans R Soc Edinb Earth Sci 96:327–350

    Google Scholar 

  48. Walcott CD (1881) The trilobite: new and old evidence relating to its organization. Bull Mus Comp Zool Harv 8:191–224

    Google Scholar 

  49. Walossek D (1993) The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils Strata 32:1–202

    Google Scholar 

  50. Waloszek D (2003) Cambrian ‘Orsten’-type preserved arthropods and the phylogeny of Crustacea. In: Legakis A, Sfenthourakis S, Polymeni R, Thessalou-Legaki M (eds) The New panorama of animal evolution. Proceedings of the 18th International Congress of Zoology. Pensoft, Sofia, pp 69–87

    Google Scholar 

  51. Waterston CD (1985) Chelicerata from the Dinantian of Foulden, Berwickshire, Scotland. Trans R Soc Edinb Earth Sci 76:25–33

    Article  Google Scholar 

  52. Weygoldt P, Paulus HF (1979a) Untersuchungen zur Morphologie, Taxonomie und Phylogenie der Chelicerata. I. Morphologische Untersuchungen. Z Zool Syst Evolutionsforsch 17:85–116

    Article  Google Scholar 

  53. Weygoldt P, Paulus HF (1979b) Untersuchungen zur Morphologie. Taxonomie und Phylogenie der Chelicerata. II. Cladogramme und die Entfaltung der Chelicerata. Z Zool Syst Evolutionsforsch 17:177–200

    Article  Google Scholar 

  54. Whittington HB (1993) Anatomy of the Ordovician trilobite Placoparia. Philos Trans R Soc Lond B 339:109–118

    Article  Google Scholar 

  55. Williams RB (1980) Comment on report of the committee of typification of species of Protozoa. Bull Zool Nomencl 37:137–140

    Google Scholar 

  56. Williams RB (1986) Hapantotypes: a possible solution to some problems of parasite nomenclature. Parasitol Today 2:314–316

    PubMed  Article  CAS  Google Scholar 

  57. Wirkner CS, Richter S (2010) Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea). Cladistics 26:143–167

    Article  Google Scholar 

  58. Zawischa D (1989) Euproops aus dem Oberkarbon vom Piesberg bei Osnabrück. Arbeitskr Paläontol Hann 17(3):53–56

    Google Scholar 

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Acknowledgments

Our acknowledgement for the permission to search for fossils in the Piesberg quarry goes to CEMEX Kies and Splitt GmbH, Steinbruch Piesberg, Osnabrück, Germany. Many thanks to the private collectors that are active at the Piesberg quarry, providing new specimens to the collection of the Museum am Schölerberg (MAS), Osnabrück. Special thanks to Michael Sowiak (Glandorf, Germany) who drastically increased the number of Euproops specimens from the Piesberg quarry by looking systematically for the layers yielding most specimens. He donated many specimens to the MAS. Jean-Bernard Caron, Janet Waddington, Peter Fenton, all Royal Ontario Museum, Toronto, as well as Susan Butts and Jessica Utrup, Yale Peabody Museum, New Haven, kindly provided us access to comparative material. Furthermore, we would like to thank Dieter Waloszek, Ulm, for valuable discussions, especially about image enhancement methods. Two anonymous reviewers made helpful comments to an earlier draft of the manuscript. We also thank all people involved in programming free software that was used during the course of this study, such as GIMP, Inkscape, OpenOffice, and Microsoft Image Composite Editor. JTH is currently kindly funded by the Alexander von Humboldt-Foundation with a Feodor Lynen research fellowship for postdoctoral researchers. PVR was funded by a Special Research Fund (BOF) scholarship from Ghent University. PF was funded by the Forskningsrådet for Natur og Univers (FNU; grant no. 272-06-0534), the EAC Foundation, and Knud Højgaard. CH, PVR and JTH also express their thanks to their host at the Yale University and the Yale Peabody Museum, Derek E. G. Briggs, for his support.

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Correspondence to Carolin Haug.

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Haug, C., Van Roy, P., Leipner, A. et al. A holomorph approach to xiphosuran evolution—a case study on the ontogeny of Euproops . Dev Genes Evol 222, 253–268 (2012). https://doi.org/10.1007/s00427-012-0407-7

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Keywords

  • Euproops danae
  • Euproops rotundatus
  • Fossilized ontogeny
  • Tagmatisation
  • Hapantotype