An unusual fossil larva, the ontogeny of achelatan lobsters, and the evolution of metamorphosis


Authors: Haug JT, Haug C

Published in: Bulletin of Geosciences, volume 88, issue 1; pages: 195 - 206; Received 4 July 2012; Accepted in revised form 6 October 2012; Online 5 December 2012

Keywords: metamorphosis, Palaeo-Evo-Devo, larval biology, Decapoda, Eucrustacea,

full text (PDF, 2.01 MB)

Export to RIS



Metamorphosis is a striking feature in the development of an animal. For arthropods, metamorphosis is usually understood as a rapid morphological change, which occurs within one or two moults. We describe here two conspecific fossil larvae of an achelatan lobster from the Solnhofen Lithographic Limestones (Upper Jurassic, southern Germany). These phyllosoma-like larvae represent successive instars. Both have a combination of characters specific for phyllosoma larvae and those typical for post-phyllosoma instars. This find indicates that the developmental pattern of this achelatan species was more gradual or “less metamorphic” than in all other achelatans known, and probably represents the plesiomorphic condition. Obviously, heterochrony played an important role in the evolution of metamorphosis in Achelata. Developmental data from other fossil arthropods, e.g., stomatopod crustaceans or pterygote insects, also point to a more gradual ontogenetic pattern in the ancestors of these lineages, which show a “real” metamorphosis today. The evolution of metamorphosis is linked to selective pressure on early developmental stages, resulting in morphological disparity between pre- and post-metamorphic stages, and a condensation of the ontogenetic pattern, leading to a more rapid morphological change. The influence of both factors can be better evaluated if fossil information is taken into account.


Bainbridge, S.P. & Bownes, M. 1981. Staging the metamorphosis of Drosophila melanogaster. Journal of Embryology and Experimental Morphology 66, 57–80.

Barnes, R.S.K., Calow, P. & Olive, P.J.W. 1993. The Invertebrates – a Synthesis. Third Edition. 505 pp. Blackwell Science Ltd., Malden, Oxford, Melbourne, Berlin.

Beer, G.R. de 1958. Embryos and Ancestors. 197 pp. Clarendon Press, Oxford.

Briggs, D.E.G., Sutton, M.D., Siveter, D.J. & Siveter, D.J. 2005. Metamorphosis in a Silurian barnacle. Proceedings of the Royal Society of London B – Biological Sciences 272, 2365–2369. View article

Damen, W.G.M. 2007. Evolutionary conservation and divergence of the segmentation process in arthropods. Developmental Dynamics 236, 1379–1391. View article

Donoghue, M.J., Doyle, J.A., Gauthier, J., Kluge, A.G. & Rowe, T. 1989. The importance of fossils in phylogeny reconstruction. Annual Review of Ecology and Systematics 20, 431–460. View article

Edgecombe, G.D. 2010. Palaeomorphology: fossils and the inference of cladistic relationships. Acta Zoologica 91, 72–80. View article

Felder, D.L., Martin, J.W. & Goy, J.W. 1985. Patterns in early postlarval development of decapods, 163–225. In Wenner, A.M. (ed.) Larval Growth. Crustacean Issues 2. Balkema, Rotterdam.

Ferrari, F.D., Fornshell, J., Vagelli, A.A., Ivanenko, V.N. & Dahms, H.-U. 2011. Early post-embryonic development of marine chelicerates and crustaceans with a nauplius. Crustaceana 84, 869–893. View article

Hart, M.W. & Grosberg, R.K. 2009. Caterpillars did not evolve from onychophorans by hybridogenesis. Proceedings of the National Academy of Sciences of the United States of America 106, 19906–19909.

Haug, C., Haug, J.T., Waloszek, D., Maas, A., Frattigiani, R. & Liebau, S. 2009a. New methods to document fossils from lithographic limestones of southern Germany and Lebanon. Palaeontologia Electronica 12(3), 6T, 12 pp.

Haug, C., Haug, J.T. & Waloszek, D. 2009b. Morphology and ontogeny of the Upper Jurassic mantis shrimp Spinosculda ehrlichi n. gen. n. sp. from southern Germany. Palaeodiversity 2, 111–118.

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.,Maas, A., Kutschera, V.&Waloszek, D. 2010b. Evolution of mantis shrimps (Stomatopoda, Malacostraca) in the light of new Mesozoic fossils. BMC Evolutionary Biology 10(290), 1–17.View article

Haug, J.T., 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). Palaeodiversity 2, 97–110.

Haug, J.T., Haug, C., Waloszek, D. & Schweigert,G. 2011. The importance of lithographic limestones for revealing ontogenies in fossil crustaceans. Swiss Journal of Geosciences, Supplement 1, S85–S98. View article

Haug, J.T., Maas, A. & Waloszek, D. 2010a. †Henningsmoenicaris scutula, †Sandtorpia vestrogothiensis gen. et sp. nov. and heterochronic events in early crustacean evolution. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 100, 311–350. View article

Hoeg, J.T., Lagersson, N.C. & Glenner, H. 2004. The complete cypris larva and its significance in thecostracan phylogeny, 197–215. In Scholtz, G. (ed.) Evolutionary Developmental Biology of Crustacea. Crustacean Issues 15, Balkema, Lisse.

Hoeg, J.T. & Moller, O.S. 2006. When similar beginnings lead to different ends: Constraints and diversity in cirripede larval development. Invertebrate Reproduction & Development 49, 125–142. View article

Inoue, N., Minami, H. & Sekiguchi, H. 2004. Distribution of phyllosoma larvae (Crustacea: Decapoda: Palinuridae, Scyllaridae, Synaxidae) in the Western North Pacific. Journal of Oceanography 60, 963–976. View article

Jeffs, A. 2007. Revealing the natural diet of the phyllosoma larvae of spiny lobster. Bulletin of Fisheries Research Agency 20, 9–13.

Johnson, M.W. 1951. A giant phyllosoma larva of a loricate crustacean from the tropical Pacific. Transactions of the American Microscopical Society 70, 274–278. View article

Kolbasov, G.A., Grygier, M.J., Hoeg, J.T. & Klepal, W. 2008. External morphology of the two cypridiform ascothoracid-larva instars of Dendrogaster: The evolutionary significance of the two-step metamorphosis and comparison of lattice organs between larvae and adult males (Crustacea, Thecostraca, Ascothoracida). Zoologischer Anzeiger 247, 159–183. View article

Kukalová-Peck, J. 1978. Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. Journal of Morphology 156, 53–126. View article

Kutschera, V., Maas, A., Waloszek, D., Haug, C. & Haug, J.T. 2012. Re-study of larval stages of Amphionides reynaudii (Malacostraca: Eucarida) with modern imaging techniques. Journal of Crustacean Biology 32, 916–930.View article

Marinovic, B., Lemmens, J.W.T.J. & Knott, B. 1994. Larval development of Ibacus peronni Leach (Decapoda: Scyllaridae) under laboratory conditions. Journal of Crustacean Biology 14, 80–96. View article

Meigen, J.W. 1830. Systematische Beschreibung der bekannten europäischen zweiflügeligen Insekten. Volume 6. 401 pp. + 12 pl. Schulzische Buchhandlung, Hamm.

Mikami, S. & Greenwood, J.G. 1997. Complete development and comparative morphology of larval Thenus orientalis and Thenus sp. (Decapoda: Scyllaridae) reared in the laboratory. Journal of Crustacean Biology 17, 289–308. View article

Müller, K.J. 1983. Crustacea with preserved soft parts from the Upper Cambrian of Sweden. Lethaia 16, 93–109. View article

Müller, O.F. 1776. Zoologiae Danicae prodromus, seu Animalium Daniae et Norvegiae indigenarum characteres, nomina, et synonyma imprimis popularium. 322 pp. Havniae, typis Hallageriis.

Münster, G. Graf zu 1839. Decapoda Macroura. Abbildung und Beschreibung der fossilen langschwänzigen Krebse in den Kalkschiefern von Bayern mit XXX nach der Natur gezeichneten Tafeln. Beiträge zur Petrefaktenkunde 2, 1–88.

Olesen, J. 2005. Larval development of Lynceus brachyurus (Crustacea, Branchiopoda, Laevicaudata): redescription of unusual crustacean nauplii, with special attention to the molt between last nauplius and first juvenile. Journal of Morphology 264, 131–148. View article

Pasini, G. & Garassino, A. 2009. A new phyllosoma form (Decapoda, ?Palinuridae) from the Late Cretaceous (Cenomanian) of Lebanon. Atti della Societa Italiana di Scienze naturali e del Museo civico di Storia naturale in Milano 150(1), 21–28.

Pechenik, J.A. 2006. Larval experience and latent effects – metamorphosis is not a new beginning. Integrative & Comparative Biology 46, 323–333. View article

Polz, H. 1972. Entwicklungsstadien bei fossilen Phyllosomen (Form A) aus den Solnhofener Plattenkalken. Neues Jahrbuch für Geologie und Paläontologie, Monatshefte 11, 678–689.

Polz, H. 1973. Entwicklungsstadien bei fossilen Phyllosomen (Form B) aus den Solnhofener Plattenkalken. Neues Jahrbuch für Geologie und Paläontologie, Monatshefte 5, 284–296.

Polz, H. 1984. Krebslarven aus den Solnhofener Plattenkalken. Archaeopteryx 2, 30–40.

Polz, H. 1995. Ein außergewöhnliches Jugendstadium eines palinuriden Krebses aus den Solnhofener Plattenkalken. Archaeopteryx 13, 67–74.

Polz, H. 1996. Eine Form-C-Krebslarve mit erhaltenem Kopfschild (Crustacea, Decapoda, Palinuroidea) aus den Solnhofener Plattenkalken. Archaeopteryx 14, 43–50.

Rowe, L. & Ludwig, D. 1991. Size and timing of metamorphosis in complex life cycles: time constraints and variation. Ecology 72, 413–427. View article

Rust, J. 2006. Die Bedeutung von Fossilien für phylogenetische Rekonstruktionen. Species, Phylogeny and Evolution 1, 73–87.

Saunders, M.I, Thompson, P.A., Jeffs, A.G., Säwström, C., Sachlikidis, N., Beckley, L.E. & Waite, A.M. 2012. Fussy feeders: phyllosoma larvae of the Western Rocklobster (Panulirus cygnus) demonstrate prey preference. PLoS ONE 7, e36580. View article

Scholtz, G. 2005. Homology and ontogeny: Pattern and process in comparative developmental biology. Theory in Biosciences 124, 121–143.View article

Stimpson, W. 1866. Descriptions of new genera and species of macrurous Crustacea from the coasts of North America. Proceedings of the Chicago Academy of Sciences 1, 46-48.

Tanaka, G., Smith, R.J., Siveter, D.J. & Parker, A.R. 2009. Threedimensionally preserved decapod larval compound eyes from the Cretaceous Santana formation of Brazil. Zoological Science 26, 846–850. View article

Truman, J.W. & Riddiford, L.M. 1999. The origins of insect metamorphosis. Nature 401, 447–452.View article

Walossek, D. 1993. The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Fossils & Strata 32, 1–202.

Walossek, D., Hoeg, J.T. & Shirley, T.C. 1996. Larval development of the rhizocephalan cirripede Briarosaccus tenellus (Maxillopoda: Thecostraca) reared in the laboratory: a scanning electron microscopy study. Hydrobiologia 328, 9–47. View article

Waloszek, D. 2003. Cambrian ‘Orsten’-type preserved arthropods and the phylogeny of Crustacea, 69–87. In Legakis, A., Sfenthourakis, S., Polymeni, R. & Thessalou-Legaki, M. (eds) The New Panorama of Animal Evolution. Proceedings of the 18th International Congress on Zoology.

Waloszek, D. & Maas, A. 2005. The evolutionary history of crustacean segmentation: a fossil-based perspective. Evolution & Development 7, 515–527. View article

Webber, W.R. & Booth, J.D. 2001. Larval stages, developmental ecology, and distribution of Scyllarus sp. Z (probably Scyllarus aoteanus Powell, 1949) (Decapoda: Scyllaridae). New Zealand Journal of Marine and Freshwater Research 35, 1025–1056. View article

Williamson, D.I. 1969. Names of larvae in the Decapoda and Euphausiacea. Crustaceana 16, 210–213. View article

Williamson, D.I. 1982. Larval morphology and diversity, 43–110. In Abele, L.G. (ed.) The Biology of Crustacea 2. Embryology, Morphology and Genetics. Academic Press, New York, London.

Williamson, D.I. 1988. Incongruous larvae and the origin of some invertebrate lifehistories. Progress in Oceanography 19, 87–116. View article

Williamson, D.I. 2006. Hybridization in the evolution of animal form and life-cycle. Zoological Journal of the Linnean Society 148, 585–602. View article

Williamson, D.I. 2009. Caterpillars evolved from onychophorans by hybridogenesis. Proceedings of the National Academy of Sciences of the United States of America 106, 19901–19905.View article

Williamson, D.I. 2012. The origins of chordate larvae. Cell & Developmental Biology 1, 101.

Willis, J.H. & Cox-Foster, D.L. 2010. Insect metamorphosis via hybridogenesis: An evidentiary rebuttal. Journal of Insect Physiology 56, 333–335. View article