Advertisement

Development Genes and Evolution

, Volume 228, Issue 1, pp 49–61 | Cite as

The ontogeny of Limulus polyphemus (Xiphosura s. str., Euchelicerata) revised: looking “under the skin”

  • Carolin Haug
  • Marie A. I. N. Rötzer
Original Article

Abstract

In recent years, methods for investigating the exo-morphology of zoological specimens have seen large improvements. Among new approaches, auto-fluorescence imaging offers possibilities to document specimens under high resolution without introducing additional artifacts as, for example, seen in scanning electron microscopy (SEM) imaging. Additionally, while SEM imaging is restricted to the outer morphology of the current instar, auto-fluorescence imaging can be used to document changes of the outer morphology of the next instar underneath the cuticle of the current instar. Thus, reinvestigating seemingly well known species with these methods may lead to interesting new insights. Here we reinvestigate the late embryonic development of the xiphosuran (“sword tail”) Limulus polyphemus, which is often treated as a proxy for early eucheliceratan evolution. In addition to entire specimens, the appendages of the embryos were dissected off and documented separately with composite-autofluorescence microscopy. Based on these data, we can distinguish six developmental stages. These stages do not match exactly the formerly described stages, as these were largely based on SEM investigation. Our stages appear to represent earlier or later phases within what has in other studies been identified as one stage. This finer subdivision is visible as we can see the developing cuticle under the outer cuticle. In comparison to data from fossil xiphosurans, our results and those of other studies on the ontogeny of L. polyphemus point to a derived mode of development in this species, which argues against the idea of L. polyphemus as a “living fossil.”

Keywords

Xiphosura sensu stricto Embryonic development Autofluorescence microscopy Variability 

Notes

Acknowledgements

We are very grateful to Eric Lazo-Wasem and Daniel Drew, Yale Peabody Museum, New Haven, for collecting, rearing and fixing the specimens. Jakob Krieger, University of Greifswald, is thanked for help with handling the specimens. We would like to thank Joachim T. Haug, LMU Munich, for his technical assistance and valuable discussions about xiphosuran development and tagmatization. Steffen Harzsch, University of Greifswald, and J. Matthias Starck, LMU Munich, are thanked for providing lab space and general support. CH was kindly funded by the Equal Opportunities Sponsorship of the LMU. This study is part of a project kindly funded by the German Research Foundation (DFG) under HA 7066/3-1.

References

  1. Anderson LI (1994) Xiphosurans from the Westphalian D of the Radstock Basin. Proc Geol Assoc 105(4):265–275.  https://doi.org/10.1016/S0016-7878(08)80179-4 CrossRefGoogle Scholar
  2. Botton ML, Tankersley RA, Loveland RE (2010) Developmental ecology of the American horseshoe crab Limulus polyphemus. Curr Zool 56(5):550–562Google Scholar
  3. Brauckmann C (1982) Der Schwertschwanz Euproops (Xiphosurida, Limulina, Euproopacea) aus dem Ober-Karbon des Piesbergs bei Osnabrück. Osnabrücker naturwissenschaftliche Mitteilungen 9:17–26Google Scholar
  4. Brown GG, Clapper DL (1981) Procedures for maintaining adults, collecting gametes, and culturing embryos and juveniles of the horseshoe crab Limulus polyphemus L. In: Hinegardner R, Atz J, Fayet R (eds) Marine invertebrates—laboratory animal management. National Academy Press, Washington DC, pp 268–290Google Scholar
  5. Darwin CR (1859) On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, LondonCrossRefGoogle Scholar
  6. Dunlop JA (2010) Geological history and phylogeny of Chelicerata. Arthropod Struct Dev 39(2):124–142CrossRefPubMedGoogle Scholar
  7. Dunlop JA, Penney D, Tetlie OE, Anderson LI (2008) How many species of fossil arachnids are there? J Arachnol 36(2):267–272CrossRefGoogle Scholar
  8. Farley RD (2010) Book gill development in embryos and first and second instars of the horseshoe crab Limulus polyphemus L. (Chelicerata, Xiphosura). Arthropod Struct Dev 39:369–381CrossRefPubMedGoogle Scholar
  9. Garwood RJ, Dunlop J (2014) Three-dimensional reconstruction and the phylogeny of extinct chelicerate orders. Peer J 2:e641CrossRefPubMedPubMedCentralGoogle Scholar
  10. Haug JT, Haug C, Ehrlich M (2008) First fossil stomatopod larva (Arthropoda: Crustacea) and a new way of documenting Solnhofen fossils (Upper Jurassic, Southern Germany). Palaeodiversity 1:103–109Google Scholar
  11. 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:art.12.3.6TGoogle Scholar
  12. Haug JT, Haug C, Waloszek D, Schweigert G (2011a) The importance of lithographic limestones for revealing ontogenies in fossil crustaceans. Swiss J Geosci 104(Supplement 1):S85–S98CrossRefGoogle Scholar
  13. Haug JT, Haug C, Kutschera V, Mayer G, Maas A, Liebau S, Castellani C, Wolfram U, Clarkson ENK, Waloszek D (2011b) Autofluorescence imaging, an excellent tool for comparative morphology. J Microsc 244:259–272CrossRefPubMedGoogle Scholar
  14. Haug C, Mayer G, Kutschera V, Waloszek D, Maas A, Haug JT (2011c) Imaging and documenting gammarideans. Intern J Zool:art.380829Google Scholar
  15. Haug C, Van Roy P, Leipner A, Funch P, Rudkin DM, Schöllmann L, Haug JT (2012a) A holomorph approach to xiphosuran evolution—a case study on the ontogeny of Euproops. Dev Genes Evol 222:253–268CrossRefPubMedGoogle Scholar
  16. Haug C, Sallam WS, Maas A, Waloszek D, Kutschera V, Haug JT (2012b) Tagmatization in Stomatopoda—reconsidering functional units of modern-day mantis shrimps (Verunipeltata, Hoplocarida) and implications for the interpretation of fossils. Front Zool 9:art.31CrossRefGoogle Scholar
  17. Haug JT, Briggs DEG, Haug C (2012c) Morphology and function in the Cambrian Burgess Shale megacheiran arthropod Leanchoilia superlata and the application of a descriptive matrix. BMC Evol Biol 12:art. 162CrossRefGoogle Scholar
  18. Haug C, Shannon KR, Nyborg T, Vega FJ (2013) Isolated mantis shrimp dactyli from the Pliocene of North Carolina and their bearing on the history of Stomatopoda. Bol Soc Geol Mex 65:273–284Google Scholar
  19. Haug C, Rötzer M (2018) The ontogeny of the 300 million year old xiphosuran Euproops danae (Euchelicerata) and implications for resolving the Euproops species complex. Dev Genes Evol.  https://doi.org/10.1007/s00427-018-0604-0 this issue
  20. Hennig W (1965) Phylogenetic systematics. Ann Rev Entomol 10:97–116CrossRefGoogle Scholar
  21. Hopkins MJ, Lidgard S (2012) Evolutionary mode routinely varies among morphological traits within fossil species lineages. PNAS 109(50):20520–20525CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hunt G, Hopkins MJ, Lidgard S (2015) Simple versus complex models of trait evolution and stasis as a response to environmental change. PNAS 112(16):4885–4890CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jegla TC, Costlow JD (1982) Temperature and salinity effects on developmental and early posthatch stages of Limulus. In: Bonaventura J, Bonaventura C, Tesh S (eds) Physiology and biology of horseshoe crabs. Alan R. Liss, New York, pp 103–113Google Scholar
  24. Kingsley JS (1892) The embryology of Limulus. J Morphol 7:35–68CrossRefGoogle Scholar
  25. Lamsdell JC (2013) Revised systematics of Palaeozoic ‘horseshoe crabs’ and the myth of monophyletic Xiphosura. Zool J Linn Soc 167:1–27CrossRefGoogle Scholar
  26. Lamsdell JC (2016) Horseshoe crab phylogeny and independent colonizations of fresh water: ecological invasion as a driver for morphological innovation. Palaeontology 59(2):181–194CrossRefGoogle Scholar
  27. Lamsdell JC, Briggs DEG, Liu HP, Witzke BJ, McKay RM (2015) A new Ordovician arthropod from the Winneshiek Lagerstätte of Iowa (USA) reveals the ground plan of eurypterids and chasmataspidids. Sci Nature 102(9–10):art. 63CrossRefGoogle Scholar
  28. Liu Y, Haug JT, Haug C, Briggs DEG, Hou X (2014) A 520 million-year-old chelicerate larva. Nature Comm 5:art. 4440Google Scholar
  29. Liu Y, Melzer RR, Haug JT, Haug C, Briggs DEG, Hörnig MK, He Y-y, Hou X (2016) Three-dimensionally preserved minute larva of a great-appendage arthropod from the early Cambrian Chengjiang biota. Proc Nat Acad Sci USA (PNAS) 113:5542–5546CrossRefGoogle Scholar
  30. Mittmann B (2004) Die Embryologie des Pfeilschwanzkrebses Limulus polyphemus (Xiphosura, Chelicerata) und anderer Arthropoden unter besonderer Berücksichtigung der Neurogenese. Dissertation, Humboldt-University of BerlinGoogle Scholar
  31. Racheboeuf PR, Vannier J, Anderson LI (2002) A new three-dimensionally preserved xiphosuran chelicerate from the Montceau-Les-Mines Lagerstätte (Carboniferous, France). Palaeontology 45:125–147CrossRefGoogle Scholar
  32. Rötzer MMA, Haug JT (2015) Larval development of the European lobster and how small heterochronic shifts lead to a more pronounced metamorphosis. Intern J Zool:art. 345172Google Scholar
  33. Rudkin DM, Young GA, Nowlan GS (2008) The oldest horseshoe crab: a new xiphosurid from Late Ordovician Konservat-Lagerstatten deposits, Manitoba, Canada. Palaeontology 51:1–9CrossRefGoogle Scholar
  34. Saltin BD, Haug C, Haug JT (2016) How metamorphic is holometabolous development? Using microscopical methods to look inside the scorpionfly (Panorpa) pupa (Mecoptera, Panorpidae). Spixiana 39:105–118Google Scholar
  35. Scholl G (1977) Beiträge zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86:99–154CrossRefGoogle Scholar
  36. Sekiguchi K, Sugita H (1980) Systematics and hybridization in the four living species of horseshoe crabs. Evolution 34:712–718CrossRefPubMedGoogle Scholar
  37. Sekiguchi K, Yamamichi Y, Costlow JD (1982) Horseshoe crab developmental studies I. Normal embryonic development of Limulus polyphemus compared with Tachypleus tridentatus. In: Bonaventura J, Bonaventura C, Tesh S (eds) Physiology and biology of horseshoe crabs: studies on normal and environmentally stressed animals. Alan R. Liss, New York, pp 53–73Google Scholar
  38. Selden PA, Lamsdell JC, Qi L (2015) An unusual euchelicerate linking horseshoe crabs and eurypterids, from the Lower Devonian (Lochkovian) of Yunnan, China. Zool Scr 44(6):645–652CrossRefGoogle Scholar
  39. Servais T, Harper DA, Munnecke A, Owen AW, Sheehan PM (2009) Understanding the Great Ordovician Biodiversification Event (GOBE): Influences of paleogeography, paleoclimate, or paleoecology. GSA Today 19(4):4–10CrossRefGoogle Scholar
  40. Shultz JW (2007) A phylogenetic analysis of the arachnid orders based on morphological characters. Zool J Linn Soc 150(2):221–265CrossRefGoogle Scholar
  41. Shuster CN Jr, Sekiguchi K (2003) Growing up takes about ten years and eighteen stages. In: Shuster CN Jr, Barlow RB, Brockmann HJ (eds) The American horseshoe crab. Harvard University Press, Cambridge, pp 103–132Google Scholar
  42. Thenius E (2000) Lebende Fossilien: Oldtimer der Pflanzen- und Tierwelt - Zeugen der Vorzeit. Dr. Friedrich Pfeil, MünchenGoogle Scholar
  43. Van Roy P, Orr PJ, Botting JP, Muir LA, Vinther J, Lefebvre B, el Hariri K, Briggs DEG (2010) Ordovician faunas of Burgess Shale type. Nature 465:215–218CrossRefPubMedGoogle Scholar
  44. Waloszek D, Dunlop JA (2002) A larval sea spider (Arthropoda: Pycnogonida) from the Upper Cambrian ‘Orsten’ of Sweden, and the phylogenetic position of pycnogonids. Palaeontology 45:421–446CrossRefGoogle Scholar
  45. Webby BD, Droser ML, Paris F, Percival I (2004) The Great Ordovician Biodiversification Event. Columbia University Press, New YorkCrossRefGoogle Scholar
  46. Wolff C, Scholtz G (2008) The clonal composition of biramous and uniramous arthropod limbs. Proc R Soc London B 275:1023–1028CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology IILMU MunichPlanegg-MartinsriedGermany
  2. 2.GeoBio-Center of the LMU MunichMunichGermany

Personalised recommendations