Advertisement

Development Genes and Evolution

, Volume 223, Issue 6, pp 363–373 | Cite as

Diversity of developmental patterns in achelate lobsters—today and in the Mesozoic

  • Joachim T. Haug
  • Denis Audo
  • Sylvain Charbonnier
  • Carolin Haug
Original Article

Abstract

Modern achelate lobsters, slipper and spiny lobsters, have a specific post-embryonic developmental pattern with the following phases: phyllosoma, nisto (slipper lobsters) or puerulus (spiny lobsters), juvenile and adult. The phyllosoma is a peculiar larva, which transforms through a metamorphic moult into another larval form, the nisto or puerulus which largely resembles the juvenile. Unlike the nisto and puerulus, the phyllosoma is characterised by numerous morphological differences to the adult, e.g. a thin head shield, elongate appendages, exopods on these appendages and a special claw. Our reinvestigation of the 85 million years old fossil “Eryoneicus sahelalmae” demonstrates that it represents an unusual type of achelatan lobster larva, characterised by a mixture of phyllosoma and post-phyllosoma characters. We ascribe it to its own genus: Polzicaris nov. gen. We study its significance by comparisons with other cases of Mesozoic fossil larvae also characterised by a mixture of characters. Accordingly, all these larvae are interpreted as ontogenetic intermediates between phyllosoma and post-phyllosoma morphology. Remarkably, most of the larvae show a unique mixture of retained larval and already developed post-larval features. Considering the different—and incompatible—mixture of characters of each of these larvae and their wide geographical and temporal distribution, we interpret all these larvae as belonging to distinct species. The particular character combinations in the different larvae make it currently difficult to reconstruct an evolutionary scenario with a stepwise character acquisition. Yet, it can be concluded that a larger diversity of larval forms and developmental patterns occurred in Mesozoic than in modern faunas.

Keywords

Fossil larvae Phyllosoma Sahel Alma Metamorphosis Palaeo-evo-devo Cretaceous 

Notes

Acknowledgments

Gideon T. Haug, Greifswald, is thanked for assisting during photographing the specimens. We thank Roger Frattigiani, Laichingen and Eric A. Lazo-Wasem, Yale Peabody Museum, New Haven, for kindly providing specimens for this study. JTH was kindly supported by the Alexander von Humboldt Foundation with a Feodor Lynen Return Fellowship. Funding for CH was kindly provided by the German Academic Exchange Service (DAAD). The visit of JTH to the MNHN was funded by a grant from the European Commission's (FP 6) Integrated Infrastructure Initiative programme SYNTHESYS (FR-TAF 2590). This work is part of the project “Palaeo-Evo-Devo of Malacostraca” kindly supported by the German Research Foundation (DFG) under HA 6300/3-1. JTH and CH would like to thank Steffen Harzsch, Greifswald, for his support. This paper is a contribution to the UMR CNRS 7207 Centre de Recherche sur la Paléobiodiversité et les Paléoenvironnements and to the Département Histoire de la Terre of the Muséum national d'Histoire naturelle, Paris.

Supplementary material

427_2013_452_Fig4_ESM.jpg (82 kb)
Online Resource 1

Part (a) and counterpart (b) of Polzicaris sahelalmae, MNHN.F.B18905 (JPEG 81 kb)

427_2013_452_MOESM1_ESM.tif (14.5 mb)
High resolution image (TIFF 14856 kb)
427_2013_452_MOESM2_ESM.xls (23 kb)
Online Resource 2 Descriptive matrix of Polzicaris sahelalmae with complete description (see Haug et al. 2012 for technical details) (XLS 23 kb)

References

  1. Aguirre-Urreta MB, Buatois LA, Chernoglasov GCB, Medina FA (1990) First Polychelidae (Crustacea, Palinura) from the Jurassic of Antarctica. Antarct Sci 2:157–162CrossRefGoogle Scholar
  2. Ahyong ST (2009) The polychelidan lobsters: phylogeny and systematics (Polychelida: Polychelidae). In: Martin JW, Crandall KA, Felder DL (eds) Decapod crustacean phylogenetics. Crustacean issues 18. CRC, Boca Raton, pp 369–396CrossRefGoogle Scholar
  3. Audo D, Charbonnier S (2012) New nisto of slipper lobster (Decapoda: Scyllaridea) from the Hadjoula Lagerstätte (Late Cretaceous, Lebanon). J Crustac Biol 32:583–590CrossRefGoogle Scholar
  4. Audo D, Charbonnier S (2013) The crest-bearing shrimps from the Sahel Alma Lagerstätte (Late Cretaceous, Lebanon). Acta Palaeontol Pol 58:335–349Google Scholar
  5. Balss H (1927) Decapoda Latreille 1802 = Zehnfüsser. In: Kükenthal WG, Krumbach T (eds) Handbuch der Zoologie eine Naturgeschichte der Stämme des Tierreiches 3:840–1038Google Scholar
  6. Bouvier EL (1917) Crustacés décapodes Macroures marcheurs provenant des campagnes des yachts Hirondelle et Princesse-Alice (1885–1915). In: Grimaldi AH, Richard J (eds) Résultats des campagnes scientifiques accomplies sur son yacht par Albert 1er prince souverain de Monaco 50:1–149, 11 plsGoogle Scholar
  7. Burkenroad MD (1963) The evolution of the Eucarida, (Crustacea, Eumalacostraca), in relation to the fossil record. Tulane Stud Geol 2:2–17Google Scholar
  8. Dixon CJ, Ahyong ST, Schram FR (2003) A new hypothesis of decopod phylogeny. Crustaceana 76:935–975CrossRefGoogle Scholar
  9. Ferry S, Merran Y, Grosheny D, Mroueh M (2007) The Cretaceous of Lebanon in the Middle East (Levant) context. In: Bulot LG, Ferry S, Grosheny D (eds) Relations between the northern and southern margins of the Tethys ocean during the Cretaceous period. Carnets de Géologie, Memoir 2007/02, Abstract 08:38–42Google Scholar
  10. Förster R (1984) Bärenkrebse aus dem Cenoman des Libanon und dem Eozän Italiens. Mitt Bayer Staatssamml Paläontol hist Geol 24:57–66Google Scholar
  11. Garassino A, Schweigert G (2006) The Upper Jurassic Solnhofen decapod crustacean fauna: review of the types from old descriptions (infraorders Astacidea, Thalassinidea, and Palinura). Mem Soc Ital Sci Nat Mus Civ Storia nat Milano 34:1–64Google Scholar
  12. Gore RH (1985) Molting and growth in decapod larvae. In: Wenner AM (ed) Larval growth. Crustacean issues 2. Balkema, Rotterdam, pp 1–65Google Scholar
  13. Grote AR (1873) Deidamia. Nature 8:485CrossRefGoogle Scholar
  14. Gurney R (1937) Notes on some decapod Crustacea from the Red Sea I. The genus Processa. II. The larvae of Upogebia savignyi Strahl. Proc Zool Soc London 1937:85–101Google Scholar
  15. Hart MW, Grosberg RK (2009) Caterpillars did not evolve from onychophorans by hybridogenesis. Proc Natl Acad Sci U S A 106:19906–19909PubMedCrossRefGoogle Scholar
  16. Haug JT, Ahyong S, Haug C (2013) Fossil malacostracan larvae. In: Martin JW, Olesen J, Høeg JT (eds) Atlas of crustacean larvae. Johns Hopkins University PressGoogle Scholar
  17. Haug JT, Haug C (2011) Fossilien unter langwelligem Licht: Grün-Orange-Fluoreszenz an makroskopischen Objekten. Archaeopteryx 29:20–23Google Scholar
  18. Haug JT, Haug C (2013) An unusual fossil larva, the ontogeny of achelatan lobsters, and the evolution of metamorphosis. Bull Geosci 88:195–206Google Scholar
  19. Haug JT, Haug C, Waloszek D, Maas A, Wulf M, Schweigert G (2009) Development in Mesozoic scyllarids and implications for the evolution of Achelata (Reptantia, Decapoda, Crustacea). Palaeodiv 2:97–110Google Scholar
  20. Haug JT, Maas A, Waloszek D (2010) †Henningsmoenicaris scutula, †Sandtorpia vestrogothiensis gen. et sp. nov. and heterochronic events in early crustacean evolution. Earth Environ Sci Trans R Soc Edinb 100:311–350CrossRefGoogle Scholar
  21. 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 244:259–272PubMedCrossRefGoogle Scholar
  22. Haug JT, Haug C, Waloszek D, Schweigert G (2011b) The importance of lithographic limestones for revealing ontogenies in fossil crustaceans. Swiss J Geosci 104(Suppl 1):S85–S98CrossRefGoogle Scholar
  23. Haug JT, Briggs DEG, Haug C (2012) Morphology and function in the Cambrian Burgess Shale megacheiran arthropod Leanchoilia superlata and the application of a descriptive matrix. BMC Evol Biol 12:162PubMedCrossRefGoogle Scholar
  24. Hughes NC, Minelli A, Fusco G (2006) The ontogeny of trilobite segmentation: a comparative approach. Paleobiology 32:602–627CrossRefGoogle Scholar
  25. ICZN (1964) Opinion 702. Bull Zool Nomencl 21:111–112Google Scholar
  26. ICZN (1999) International Code of Zoological Nomenclature. International Trust for Zoological Nomenclature. The Natural Museum, London, v-xxix + 306 ppGoogle Scholar
  27. Kukalová-Peck J (1978) Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. J Morphol 156:53–126CrossRefGoogle Scholar
  28. Latreille PA (1802) Histoire naturelle, générale et particulière des crustacés et des insectes. Tome 3. F. Dufart, Paris, p 467Google Scholar
  29. Marinovic B, Lemmens JWTJ, Knott B (1994) Larval development of Ibacus peronni Leach (Decapoda: Scyllaridae) under laboratory conditions. J Crustac Biol 14:80–96CrossRefGoogle Scholar
  30. Martin JW (2013) Infraorder Polychelida. In: Martin JW, Olesen J, Høeg, JT (eds) Atlas of crustacean larvae. Johns Hopkins University PressGoogle Scholar
  31. Matsuda H, Yamakawa T (2000) The complete development and morphological changes of larval Panulirus longipes (Decapoda, Palinuridae) under laboratory conditions. Fish Sci 66:278–293CrossRefGoogle Scholar
  32. Mikami S, Greenwood JG (1997) Complete development and comparative morphology of larval Thenus orientalis and Thenus sp. (Decapoda: Scyllaridae) reared in the laboratory. J Crustac Biol 17:289–308CrossRefGoogle Scholar
  33. Münster G (1839) Decapoda Macroura. Abbildung und Beschreibung der fossilen langschwänzigen Krebse in den Kalkschiefern von Bayern mit XXX nach der Natur gezeichneten Tafeln. Beitr Petrefaktenkd 2:1–88Google Scholar
  34. Pasini G, Garassino A (2009) A new phyllosoma form (Decapoda, ?Palinuridae) from the Late Cretaceous (Cenomanian) of Lebanon. Atti Soc Ital Sci nat Mus civ Storia nat Milano 150:21–28Google Scholar
  35. Polz H (1971) Eine weitere Phyllosoma-Larve aus den Solnhofener Plattenkalken. N Jb Geol Paläontol Mh 1971:474–488Google Scholar
  36. Polz H (1972) Entwicklungsstadien bei fossilen Phyllosomen (Form A) aus den Solnhofener Plattenkalken. N Jb Geol Paläontol Mh 1972:678–689Google Scholar
  37. Polz H (1973) Entwicklungsstadien bei fossilen Phyllosomen (Form B) aus den Solnhofener Plattenkalken. N Jb Geol Paläontol Mh 1973:284–296Google Scholar
  38. Polz H (1987) Zur Differenzierung der fossilen Phyllosomen (Crustacea, Decapoda) aus den Solnhofener Plattenkalken. Archaeopteryx 5:23–32Google Scholar
  39. Polz H (1995) Ein außergewöhnliches Jugendstadium eines palinuriden Krebses aus den Solnhofener Plattenkalken. Archaeopteryx 13:67–74Google Scholar
  40. Polz H (1996) Eine Form-C-Krebslarve mit erhaltenem Kopfschild (Crustacea, Decapoda, Palinuroidea) aus den Solnhofener Plattenkalken. Archaeopteryx 14:43–50Google Scholar
  41. Roger J (1944a) Eryoneicus ? Sahel almae n. sp., Crustacé décapode du Sénonien du Liban. Bull Mus nat Hist nat Paris 16:191–194, Sér 2Google Scholar
  42. Roger J (1944b) La faune carcinologique des Couches à Poissons du Crétacé supérieur du Liban. C r séances Acad Sci 218:848–850Google Scholar
  43. Roger J (1946) Les invertébrés des couches à poisons du Crétacé supérieur du Liban. Mém Soc géol France (Nouv Sér) 12(51):1–92Google Scholar
  44. Sánchez M (2012) Embryos in deep time. University of California Press, BerkeleyCrossRefGoogle Scholar
  45. Scholtz G, Richter S (1995) Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca). Zool J Linn Soc 113:289–328Google Scholar
  46. Spence Bate C (1882) Eryoneicus, a new genus allied to Willemoesia. Ann Mag Nat Hist 10:456–458CrossRefGoogle Scholar
  47. Tanaka G, Smith RJ, Siveter DJ, Parker AR (2009) Three dimensionally preserved decapod larval compound eyes from the Cretaceous Santana Formation of Brazil. Zool Sci 26:846–850PubMedCrossRefGoogle Scholar
  48. Truman JW, Riddiford LM (1999) The origins of insect metamorphosis. Nature 401:447–452PubMedCrossRefGoogle Scholar
  49. Urdy S, Wilson LAB, Haug JT, Sánchez-Villagra MR (2013) On the unique perspective of paleontology in the study of developmental evolution and biases. Biol Theory. doi: 10.1007/s13752-013-0115-1
  50. Villamar DF, Brusca GJ (1988) Variation in the larval development of Crangon nigricauda (Decapoda: Caridea), with notes on larval morphology and behavior. J Crustac Biol 8:410–419CrossRefGoogle Scholar
  51. Walossek D (1993) The Upper Cambrian Rehbachiella kinnekullensis and the phylogeny of Branchiopoda and Crustacea. Fossils Strata 32:1–202Google Scholar
  52. Webber WR, Booth JD (2001) Larval stages, developmental ecology, and distribution of Scyllarus sp. Z (probably Scyllarus aoteanus Powell, 1949) (Decapoda: Scyllaridae). New Zeal J Mar Freshw Res 35:1025–1056CrossRefGoogle Scholar
  53. Williamson DI (1969) Names of larvae in the Decapoda and Euphausiacea. Crustaceana 16:210–213CrossRefGoogle Scholar
  54. Williamson DI (1988) Incongruous larvae and the origin of some invertebrate life histories. Prog Oceanogr 19:87–116CrossRefGoogle Scholar
  55. Williamson DI (2006) Hybridization in the evolution of animal form and life-cycle. Zool J Linn Soc 148:585–602CrossRefGoogle Scholar
  56. Williamson DI (2009) Caterpillars evolved from onychophorans by hybridogenesis. Proc Natl Acad Sci U S A 106:19901–19905PubMedCrossRefGoogle Scholar
  57. Williamson DI (2012) The origins of chordate larvae. Cell Dev Biol 1:101Google Scholar
  58. Willis JH, Cox-Foster DL (2010) Insect metamorphosis via hybridogenesis: an evidentiary rebuttal. J Insect Physiol 56:333–335PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Joachim T. Haug
    • 1
  • Denis Audo
    • 2
  • Sylvain Charbonnier
    • 2
  • Carolin Haug
    • 1
  1. 1.Department of Cytology and Evolutionary Biology, Zoological Institute and MuseumUniversity of GreifswaldGreifswaldGermany
  2. 2.Département Histoire de la Terre, CP38, UMR 7207 CNRS, UPMC, MNHNMuséum national d’Histoire naturelleParisFrance

Personalised recommendations