Proceedings of the Royal Society B: Biological Sciences
Published:https://doi.org/10.1098/rspb.2007.1327

    We present the first comparative cell lineage analysis of uniramous and biramous limbs of an arthropod, the crustacean Orchestia cavimana. Via single cell labelling of the cells that are involved in limb development, we are able to present the first complete clonal composition of an arthropod limb. We show that the two main branches of crustacean limbs, exopod and endopod, are formed by a secondary subdivision of the growth zone of the main limb axis. Additional limb outgrowths such as exites result from the establishment of new axes. In contrast to general belief, uniramous limbs in Orchestia are not formed by the loss of the exopod but by suppression of the split into exopod and endopod. Our results offer a developmental approach to discriminate between the different kinds of branches of arthropod appendages. This leads to the conclusion that a ‘true’ biramous limb comprising an endopod and an exopod might have occurred much later in euarthropod evolution than has previously been thought, probably either in the lineage of the Mandibulata or that of the Tetraconata.

    References

    • Abzhanov A& Kaufman T.C. 2000Homologs of Drosophila appendage genes in the patterning of arthropod limbs. Dev. Biol. 227, 673–689.doi:10.1006/dbio.2000.9904. . Crossref, PubMed, ISIGoogle Scholar
    • Angelini D.R& Kaufman T.C. 2005Insect appendages and comparative ontogenetics. Dev. Biol. 286, 57–77.doi:10.1016/j.ydbio.2005.07.006. . Crossref, PubMed, ISIGoogle Scholar
    • Averof M& Cohen S.M. 1997Evolutionary origin of insect wings from ancestral gills. Nature. 385, 627–630.doi:10.1038/385627a0. . Crossref, PubMed, ISIGoogle Scholar
    • Bitsch J. 2001The hexapod appendage: basic structure, development and origin. Ann. Soc. Entomol. Fr. (N.S.). 37, 175–193. Google Scholar
    • Borradaile L.A. 1926Notes upon crustacean limbs. Ann. Mag. Nat. Hist. Ser. 9. 17, 193–213. CrossrefGoogle Scholar
    • Boxshall G.A. 2004The evolution of arthropod limbs. Biol. Rev. 79, 253–300.doi:10.1017/S1464793103006274. . Crossref, PubMed, ISIGoogle Scholar
    • Brusca R.C& Brusca G.JInvertebrates. 2002Sunderland, MA:Sinauer Associates. Google Scholar
    • Budd G.E. 1996The morphology of Opabinia regalis and the reconstruction of the arthropod stem-group. Lethaia. 29, 1–14.doi:10.1111/j.1502-3931.1996.tb01831.x. . Crossref, ISIGoogle Scholar
    • Budd G.E. 2002A palaeontological solution to the arthropod head problem. Nature. 417, 271–275.doi:10.1038/417271a. . Crossref, PubMed, ISIGoogle Scholar
    • Campbell G& Tomlinson A. 1995Initiation of the proximodistal axis in insect legs. Development. 121, 619–628. Crossref, PubMed, ISIGoogle Scholar
    • Dohle W& Scholtz G. 1988Clonal analysis of the crustacean segment: the discordance between genealogical and segmental borders. Development. 104, Suppl., 147–160. Crossref, PubMed, ISIGoogle Scholar
    • Giorgianni M.W& Patel N.H. 2004Patterning of the branched head appendages in Schistocerca americana and Tribolium castaneum. Evol. Dev. 6, 402–410.doi:10.1111/j.1525-142X.2004.04049.x. . Crossref, PubMed, ISIGoogle Scholar
    • Gruner, H. E. 1993 Klasse Crustacea. In Lehrbuch der Speziellen Zoologie (ed. H. E. Gruner), pp. 448–1030. Jena, Germany: Gustav Fischer Verlag. Google Scholar
    • Hansen H.JStudies on Arthropoda II. On the comparative morphology of the appendages in the Arthropoda. A. Crustacea. 1925Copenhagen, Denmark:Gyldendalske Boghandel. Google Scholar
    • Hejnol A& Scholtz G. 2004Clonal analysis of Distal-less and engrailed expression patterns during early morphogenesis of uniramous and biramous crustacean limbs. Dev. Genes Evol. 214, 473–485. PubMed, ISIGoogle Scholar
    • Kojima T. 2004The mechanism of Drosophila leg development along the proximodistal axis. Dev. Growth Diff. 46, 115–129.doi:10.1111/j.1440-169X.2004.00735.x. . Crossref, PubMed, ISIGoogle Scholar
    • Lawrence P.AThe making of a fly. 1992Oxford, UK:Blackwell Scientific Publications. Google Scholar
    • Mittmann B& Scholtz G. 2001Distal-less expression in embryos of Limulus polyphemus (Chelicerata, Xiphosura) and Lepisma saccharina (Insecta, Zygentoma) suggests a role in the development of mechanoreceptors, chemoreceptors, and the CNS. Dev. Genes Evol. 211, 232–243.doi:10.1007/s004270100150. . Crossref, PubMed, ISIGoogle Scholar
    • Olesen J, Richter S& Scholtz G. 2001The evolutionary transformation from phyllopodous to stenopodous limbs in the Branchiopoda (Crustacea)—is there a common mechanism for early limb development in arthropods?. Int. J. Dev. Biol. 45, 869–876. PubMed, ISIGoogle Scholar
    • Panganiban G, Serbing A, Nagy L& Carroll S. 1995The development of crustacean limbs and the evolution of arthropods. Science. 270, 1363–1366.doi:10.1126/science.270.5240.1363. . Crossref, PubMed, ISIGoogle Scholar
    • Prpic N.-M, Janssen R, Wigand B, Klingler M& Damen W.G.M. 2003Gene expression in spider appendages reveals reversal of exd/hth spatial specificity, altered leg gap gene dynamics, and suggests divergent distal morphogen signalling. Dev. Biol. 264, 119–140.doi:10.1016/j.ydbio.2003.08.002. . Crossref, PubMed, ISIGoogle Scholar
    • Sato K, Koizumi Y, Takahashi M, Kuroiwa A& Tamura K. 2007Specification of cell fate along the proximo-distal axis in the developing chick limb bud. Development. 134, 1397–1406.doi:10.1242/dev.02822. . Crossref, PubMed, ISIGoogle Scholar
    • Scholtz G. 1990The formation, differentiation and segmentation of the post-naupliar germ band of the amphipod Gammarus pulex (L.) (Crustacea, Malacostraca, Peracarida). Proc. R. Soc. B. 239, 163–211.doi:10.1098/rspb.1990.0013. . Link, ISIGoogle Scholar
    • Snodgrass R.E. 1958Evolution of arthropod mechanisms. Smithsonian Misc. Collec. 138, 1–77. Google Scholar
    • Tanaka K& Truman J.W. 2005Development of the adult leg epidermis in Manduca sexta: contribution of different larval cell populations. Dev. Genes Evol. 215, 78–89.doi:10.1007/s00427-004-0458-5. . Crossref, PubMed, ISIGoogle Scholar
    • Thiele J. 1905Betrachtungen über die Phylogenie der Crustaceenbeine. Z. Wiss. Zool. 82, 445–471. Google Scholar
    • Walossek D. 1993The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Foss. Strat. 32, 1–202. Google Scholar
    • Walossek D& Müller K.JCambrian ‘Orsten’-type arthropods and the phylogeny of Crustacea. Arthropod relationships, Fortey R.A& Thomas R.H. 1997pp. 139–143. Eds. London, UK:Chapman and Hall. Google Scholar
    • Weigmann K& Cohen S.M. 1999Lineage-tracing cells born in different domains along the PD axis of the developing Drosophila leg. Development. 126, 3823–3830. Crossref, PubMed, ISIGoogle Scholar
    • Williams T.AThe evolution and development of crustacean limbs: an analysis of limb homologies. Evolutionary developmental biology of Crustacea& Scholtz G. 2004pp. 169–193. Eds. Lisse, The Netherlands:B.B. Balkema. Google Scholar
    • Wolff C& Scholtz G. 2002Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev. Biol. 250, 44–58.doi:10.1006/dbio.2002.0789. . Crossref, PubMed, ISIGoogle Scholar
    • Wolff C& Scholtz G. 2006Cell lineage analysis of the mandibular segment of the amphipod Orchestia cavimana reveals that the crustacean paragnaths are sternal outgrowths and not limbs. Front. Zool. 3, 19doi:10.1186/1742-9994-3-19. . Crossref, PubMedGoogle Scholar
    • Wolpert L, Jessell T, Lawrence P, Meyerowitz E, Robertson E& Smith JPrinciples of development. 2006Oxford, UK:Oxford University Press. Google Scholar