Desktop version

Home arrow Environment

  • Increase font
  • Decrease font


<<   CONTENTS   >>

Perspectives

Malacostracan crustaceans show a number of specific apomorphic features regarding germ band differentiation and segment formation. These include the formation of teloblasts as a special expression of a growth zone in the strict sense and the stereotyped cell lineage of the teloblasts’ progeny. This cell lineage allows a very detailed resolution of cell fate during germ band growth and segment formation. Furthermore, a combination of comparative and experimental studies indicates the role of cell lineages for cell determination and the interaction of germ layers. On the other hand, the reasons how and why the stereotyped cell division patterns evolved in the malacostracan stem lineage and why the teloblasts underwent some evolutionary changes concerning their number and arrangement up to a total loss of ectoteloblasts in amphipods circumstances are still obscure. In any case, the observed changes imply interesting problems related to the interface of ontogeny and homology. To address these developmental and evolutionary questions in even greater detail, studies combining new imaging techniques, molecular approaches, and comparative approaches are desirable.

Acknowledgments

The research summarized in this review has been supported over the years by grants from the Deutsche Forschungsgemeinschaft and from the Einstein Stiftung. This contribution is a largely modified part of a more comprehensive treatment of crustacean embryology that will be published in the series “The Natural History of the Crustacea.”

References

Abzhanov, A., and T. C. Kaufman. 2004. Hox genes and tagmatization of higher Crustacea (Malacostraca). In Evolutionary Developmental Biology of Crustacea, Ed. G. Scholtz, 43-74. Lisse: A.A. Balkema.

Anderson, D. T. 1967. Larval development and segment formation in the branchiopod crustaceans Limnadia stanleyana King (Conchostraca) and Artemia salina (L.) (Anostraca). Austr. J. Zool. 15: 47—91.

Anderson, D. T. 1969. On the embryology of the cirripede crustacean Tetraclita rosea (Krauss), Tetraclita purpurascens (Wood), Chthamalus antennatus (Darwin) and Chamaesipho columna (Spengler) and some considerations of crustacean phylogenetic relationships. Phil. Trans. R. Soc. London В 256: 183-235.

Anderson, D. T. 1973. Embryology and Phytogeny in Annelids and Arthropods. Oxford: Pergamon Press.

Benesch, R. 1969. Zur Ontogenie und Morphologie von Artemia salina L. Zool. Jalirb. Anat. 86: 307-458.

Bergh. R. S. 1893. Beitrage zur Embryologie der Crustaceen. I. Zur Bildungsgeschichte des Keimstreifens von Mysis. Zool. Jahrh. Anat. 6:491-528.

Bergh. R. S. 1894. Beitrage zur Embryologie der Crustaceen. II. Die Drehung des Keimstreifens und die Stellung des Dorsalorgans bei Gammarus pulex. Zool. Jalirb. Anat. 7: 235-248.

Bock, E. 1942. Wechselbeziehungen zwischen den Keimblattern bei der Organbildung von Chrysopa perla (L.) I. Die Entwicklung des Ektoderms in mesodermdefekten Keimteilen. Wilhelm Roux's Arch. Entwickl.-Mech. 141: 159-279.

Bohmer, С., E. Amson. P. Arnold, A. H. van Heteren, and J. A. Nyakatura. 2018. Homeotic transformations reflect departure from the mammalian ‘rule of seven’ cervical vertebrae in sloths: Inferences on the Hox code and morphological modularity of the mammalian neck. BMC Evol. Biol. 18: 84.

Brenneis, G., A. Stollewerk, and G. Scholtz. 2013. Embryonic neurogenesis in Pseudopallene sp. (Arthropoda, Pycnogonida) includes two subsequent phases with similarities to different arthropod groups. EvoDevo 4: 32.

Browne. W. E., A. L. Price, M. Gerberding, and N. H. Patel. 2005. Stages of embryonic development in the amphipod crustacean, Parhyale hawaiensis. Genesis 42: 124-149.

Damen, W. G. M. 2002. Parasegmental organization of spider embryos implies that the para- segment is an evolutionary conserved entity in arthropod embryogenesis. Development 129: 1239-1250.

Deutsch, J. S., E. Mouchel-Viel, H. E. Qucinnec. and J.-M. Gibert. 2004. Genes, segments, and tagmata in cirripedes. In Evolutionary Developmental Biology of Crustacea, Ed. G. Scholtz. 19-42. Lisse: A.A. Balkema.

Dohle. W. 1970. Die Bildung und Differenzierung des postnauplialen Keimstreifs von Diastylis ratlikei (Crustacea, Cumacea) I. Die Bildung der Teloblasten und ihrer Derivate. Zeitschr. Morph. Okol. 67: 307-392.

Dohle. W. 1972. Uber die Bildung und Differenzierung des postnauplialen Keimstreifs von Leptochelia spec. (Crustacea, Tanaidacea). Zool. Jalirb. Anat. 89: 503-566.

Dohle, W. 1976. Die Bildung und Differenzierung des postnauplialen Keimstreifs von Diastylis rathkei (Crustacea, Cumacea) II. Die Differenzierung und Musterbildung des Ektoderrns. Zoomorphologie 84: 235-277.

Dohle, W. 1999. The ancestral cleavage pattern of the clitellates and its phylogenetic deviations. Hydrobiologia 402: 267-283.

Dohle, W. 2001. Are the insects terrestrial crustaceans? A discussion of some new facts and arguments and the proposal of the proper name “Tetraconata” for the monophyletic unit Crustacea + Hexapoda. Ann. Soc. Ent. France 37: 85-103.

Dohle, W„ M. Gerberding, A. Hejnol, and G. Scholtz. 2004. Cell lineage, segment differentiation, and gene expression in crustaceans. In Evolutionary Developmental Biology of Crustacea. Ed. G. Scholtz, 95-133. Lisse: A.A. Balkema.

Dohle, W., and G. Scholtz. 1988. Clonal analysis of the crustacean segment - the discordance between genealogical and segmental borders. Development 104: 147-160.

Fioroni, P. 1970. Die organogenetische und transitorische Rolle der Vitellophagen in der Darmentwicklung von Galathea (Crustacea, Anomura). Zeitschr. Morph. Okol. 67: 263-306.

Fischer, A., T. Pabst, and G. Scholtz. 2010. Germ band differentiation in the stomatopod Gonodactylaceus falcatus and the origin of the stereotyped cell division pattern in Malacostraca (Crustacea). Arthropod Struct. Dev. 39: 411-422.

Fuchs, K. 1914. Die Keimbahnentwicklung von Cyclops viridis Jurine. Zool. Jahrb. Anat. 38: 103-156.

Gerberding, M. 1997. Germ band formation and early neurogenesis of Leptodora kindtii (Cladocera): First evidence for neuroblasts in the entomostracan crustaceans. Invert. Repr. Dev. 32: 63-73.

Gillies, T. E., and C. Cabernard. 2011. Cell division orientation in animals. Curr. Biol. 21: R599-R609.

Goodrich, E. S. 1913. Metameric segmentation and homology. Quart. J. Microsc. Sci. 59: 227.

Haget, A. 1953. Analyse experimental des facteurs de la morphogenese embryonnaire chez le colecptere Leptinotarsa. Bull. Biol. Fr. Belg. 87: 123-217.

Hannibal, R. L., A. L. Price, and N. H. Patel. 2012. The functional relationship between ectodermal and mesodermal segmentation in the crustacean, Parhyale hawaiensis. Dev. Biol. 361: 427-438.

Hartenstein, V., and A. Stollewerk. 2015. The evolution of early neurogenesis. Dev. Cell 32: 390-407.

Hein, H., and G. Scholtz. 2018. Larval neurogenesis in the copepod Tigriopus californicus (Tetraconata, Multicrustacea). Dev. Genes Evol. 228: 119-129.

Hein, H., S. Smyth, X. Altamirano, and G. Scholtz. 2019. Segmentation and limb formation during naupliar development of Tigriopus californicus (Copepoda, Harpacticoida). Arthropod Struct. Dev. 50: 43-52.

Hejnol, A., R. Schnabel, and G. Scholtz. 2006. A 4D-microscopic analysis of the germ band in the isopod crustacean Porcellio scaber (Malacostraca, Peracarida) - developmental and phylogenetic implications. Dev. Genes Evol. 216: 755-767.

Hidalgo, A. 1998. Growth and patterning from the engrailed interface. Int. J. Dev. Biol. 42: 317-324.

Hughes, C. L., and T. C. Kaufman. 2002. Exploring myriapod segmentation: The expression patterns of even-skipped, engrailed, and wingless in a centipede. Dev. Biol. 247:47-61.

Hunnekuhl, V., and C. Wolff. 2012. Reconstruction of cell lineage and spatiotemporal pattern formation of the mesoderm in the amphipod crustacean Orchestia cavimana. Dev. Dyn. 241: 697-717.

Ikuta, K. 2018. Expression of two engrailed genes in the embryo of Vargula hilgendorfii (Muller, 1890) (Ostracoda: Myodocopida) J. Crust. Biol. 38: 23-26.

Irvine, K. D., and E. Wieschaus. 1994. Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 120: 827-841.

Ito, A., M. N. Aoki, K. Yahata, and H. Wada. 2011. Embryonic development and expression analysis of Distal-less in Caprella scaura (Crustacea, Amphipoda, Caprellida). Biol. Bull 221: 206-214.

Jirikowski, G. J., S. Richter, and C. Wolff. 2013. Myogenesis of Malacostraca - the “egg- nauplius” concept revisited. Front. Zool. 10: 76.

Knoblich, J. A. 2010. Asymmetric cell division: Recent developments and their implications for tumour biology. Nature Rev. Mol. Cell Biol. 11: 849-860.

Krause. G. 1939. Die Eitypen der Insekten. Biol. Zentr. 59: 495-536.

Kuhn, A. 1913. Die Sonderung der Keimesbezirke in der Entwicklung der Sommereier von Polyphemus pediculus De Geer. Zool. Jahrb. Anat. 35: 243-340.

Kiihnemund, E. 1929. Die Entwicklung der Scheitelplatte von Polyphemus pediculus De Geer von der Gastrula bis zur Differenzierung der aus ihr hervorgehenden Organe. Zool. Jahrb. Anat. 50: 385-432.

Lawrence, P. A. 1992. The Making of a Fly. Oxford: Blackwell Scientific Publications.

Lesniewska, M., L. Bonato, A. Minelli, and G. Fusco. 2009. Trunk anomalies in the centipede Stigmatogaster subterranea provide insight into late-embryonic segmentation. Arthropod Struct. Dev. 38: 417-426.

Manton, S. M. 1928. On the embryology of a mysid crustacean Hemimysis lamornae. Phil. Trans. R. Soc. London В 216: 363-463.

Manton, S. M. 1934. On the embryology of the crustacean Nebalia bipes. Phil. Trans. R. Soc. London В 498: 163-238.

Manzanares, M., T. A. Williams, R. Marco, and R. Garesse. 1996. Segmentation in the crustacean Artemia: Engrailed expression studied with an antibody raised against the Artemia protein. Roux's Arch. Dev. Biol. 205: 424-431.

McClendon. J. F. 1907. On the development of parasitic copepods. II. Biol. Bull. 12: 57-88.

McMurrich, J. P. 1895. Embryology of the isopod Crustacea. J. Morphol. 11: 63-154.

Mittmann, В., P. Ungerer, M. Klann, A. Stollewerk, and C. Wolff. 2014. Development and staging of the water flea Daphnia magna (Straus, 1820; Cladocera, Daphniidae) based on morphological landmarks. EvoDevo 5: 12.

Morgan. T. H. 1895. A study of metamerism. Quart. J. Microsc. Sci. 37: 395-476.

Muller, G. B., and G. P. Wagner. 1996. Homology, Hox genes, and developmental integration. Am. Zool. 36: 4-13.

Olesen, J., T. Boesgaard, T. M. Iliffe, and L. Watling. 2014. Thermosbaenacea, Spelaeogriphacea, and Mictacea. In Atlas of Crustacean Larvae, Eds. J. W. Martin, J. Olesen, and J. T. Hpeg, 195-198. Baltimore: Johns Hopkins University Press.

Ooishi, S. 1959. Studies on the teloblasts in the decapod embryo: I. Origin of teloblasts in Heptacarpus rectirostris Stimpson. Embryologia 4: 283-309.

Ooishi, S. 1960. Studies on the teloblasts in the decapod embryo: II. Origin of teloblasts in Pagurus samuelis Stimpson and Hemigrapsus sanguineus De Haan. Embryologia 5: 270-282.

Patel, N. H., T. B. Kornberg, and C. S. Goodman. 1988. Expression of engrailed during segmentation of grasshopper and crayfish. Development 107: 201-212.

Patel, N. H., B. G. Condron, and K. Zinn. 1994. Pair-rule expression patterns of even-skipped are found in both short and long-germ beetles. Nature 367: 429-434.

Patten, W. 1890. On the origin of vertebrates from arachnids. Quart. J. Micr. Sci. 31: 317-378.

Ponomarenko, E. A. 2014. The Embryonic Development o/Elminius modestus Darwin, 1854 (Thecostraca: Cirripedia). Doctoral Dissertation, Humboldt-Universitat zu Berlin. Berlin, Germany.

Price, A. L., and N. H. Patel. 2008. Investigating divergent mechanisms of mesoderm development in arthropods: The expression of Ph-twist and Ph-mef2 in Parhyale hawaien- sis. J. Exp. Zool. B: Mol. Dev. Evol. 310: 24-40.

Regier, J. C., J. W. Shultz, A. Zwick, A. Hussey, B. Ball, R. Wetzer, J. W. Martin, and C. W. Cunningham. 2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature 463: 1079-1083.

Reichenbach, H. 1886. Studien zur Entwicklungsgeschichte des Flusskrebses. Ablt. Senckenb. Naturf Ces. 14: 1-137.

Richter, S., and G. Scholtz. 2001. Phylogenetic analysis of the Malacostraca (Crustacea). J. Zool. Syst. Evol. Res. 39: 113-136.

Samter, M. 1900. Studien zur Entwicklungsgeschichte der Leptodora hyalina Lillj. Z. Wiss. Zool. 68: 169-260.

Schnabel, R. 1997. Why does a nematode have an invariant lineage? Sent. Cell Dev. Biol. 8: 341-349.

Scholl, G. 1963. Embryologische Untersuchungen an Tanaidaceen (Heterotanais oerstedi Kroyer). Zool. Jahrb. Anat. 80: 500-554.

Scholtz, G. 1984. Untersuchungen zur Bildung und Differenzierung des postnauplialen Keimstreifs von Neomysis integer Leach (Crustacea, Malacostraca, Peracarida). Zool. Jahrb. Anat. 112:295-349.

Scholtz, G. 1990. The formation, differentiation and segmentation of the post-naupliar germ band of the amphipod Gammarus pulex L. (Crustacea, Malacostraca, Peracarida). Proc. R. Soc. London В 239: 163-211.

Scholtz, G. 1992. Cell lineage studies in the crayfish Cherax destructor (Crustacea, Decapoda): Germ band formation, segmentation, and early neurogenesis. Roux’s Arch. Dev. Biol. 202: 36-48.

Scholtz, G. 1993. Teloblasts in decapod embryos: An embryonic character reveals the mono- phyletic origin of freshwater crayfishes (Crustacea, Decapoda). Zool. Anz. 230: 45-54. Scholtz, G. 2000. Evolution of the nauplius stage in malacostracan crustaceans. J. Zool. Syst. Evol. Res. 38: 175-187.

Scholtz, G. 2002. The Articulata hypothesis - or what is a segment? Org. Divers. Evol. 2: 197-215.

Scholtz, G. 2005. Homology and ontogeny: Pattern and process in comparative developmental biology. Theory Biosci. 124: 121-143.

Scholtz, G. 2008. On comparisons and causes in evolutionary developmental biology. In Evolving Pathways: Key Themes in Evolutionary Developmental Biology, Eds. A. Minelli, and G. Fusco, 144-159. Cambridge: Cambridge University Press.

Scholtz, G. 2017. Segmentierung. Ein zoologisches Konzept von Serialitat. In Serie und Serialitdt. Konzepte und Analysen in Gestaltung und Wissenschaft, Ed. G. Scholtz, 139-166. Berlin: Reimer.

Scholtz, G„ and W. Dohle. 1996. Cell lineage and cell fate in crustacean embryos - a comparative approach. Int. J. Dev. Biol. 40: 211-220.

Scholtz, G., and C. Wolff. 2002. Cleavage pattern, gastrulation, and germ disc formation of the amphipod crustacean Orchestia cavimana. Contr. Zool. 71: 9-28.

Scholtz, G„ and C. Wolff. 2013. Arthropod embryology: Cleavage and germ band development. In Arthropod Biology and Evolution, Eds. A. Minelli, G. Boxshall, and G. Fusco, 63-90. Heidelberg: Springer.

Scholtz, G., A. Abzhanov, F. Alwes, C. Biffis, and J. Pint. 2009. Development, genes, and decapod evolution. In Decapod Crustacean Phylogenetics, Eds. J. W. Martin, K. A. Crandall, and D. L. Felder, 31-46. Boca Raton: CRC Press.

Schwartz, V. 1973. Vergleichende Entwicklungsgeschichte der Tiere. Stuttgart: Thieme. Schwentner, M., D. J. Combosch, J. Pakes Nelson, and G. Giribet. 2017. A phylogenomic solution to the origin of insects by resolving crustacean-hexapod relationships. Curr. Biol. 27: 1818-1824.

Shankland, M. 1991. Leech segmentation: Cell lineage and the formation of complex body patterns. Dev. Biol. 144: 221-231.

Shankland, M., and R. M. Savage. 1997. Annelids, the segmented worms. In Embryology: Constructing the Organism, Ed. S. F. Gilbert, and A. M. Raunio, 219-235. Sunderland: Sinauer Associates.

Shiino, S. M. 1942. Studies on the embryology of Squilla oratorio de Haan. Mem. Coll. Sci., Kyoto Imp. Univ. 17: 77-174.

Stegner, M. E. J., and S. Richter. 2015. Development of the nervous system in Cephalocarida (Crustacea): Early neuronal differentiation and successive patterning. Zoomorphology 134: 183-209.

Stent, G. S. 1985. The role of cell lineage in development. Phil. Trans. R. Soc. London В 312: 3-19.

Stollewerk, A., M. Weller, and D. Tautz. 2001. Neurogenesis in the spider Cupiennius salei. Development 128: 2673-2688.

Storey, K. G. 1989. Cell lineage and pattern formation in the earth-worm embryo. Development 107: 519-532.

Strome, S. 1993. Determination of cleavage planes. Cell 72: 3-6.

Ungerer, R, and G. Scholtz. 2008. Filling the gap between neuroblasts and identified neurons in crustaceans adds new support for Tetraconata. Proc. R. Soc. В 275: 369-376.

Vargas-Vila, M. A., R. L. Hannibal, R. J. Parchem, P. Z. Liu, and N. H. Patel. 2010. A prominent requirement for single-minded and the ventral midline in patterning the dorsoven- tral axis of the crustacean Parhyale hawaiensis. Development 137: 3469-3476.

von Reumont, В. M., R. A. Jenner, M. A. Wills, E. Dell’Ampio, G. Pass, I. Ebersberger, B. Meyer, S. Koenemann, T. M. Iliffe, A. Stamatakis, O. Niehuis, K. Meusemann, and B. Misof. 2012. Pancrustacean phylogeny in the light of new phylogenomic data: Support for Remipedia as the possible sister group of Hexapoda. Mol. Biol. Evol. 29: 1031-1045.

Weisblat, D. A., and M. Shankland. 1985. Cell lineage and segmentation in the leech. Phil. Trans. R. Soc. London В 312: 39-56.

Weygoldt, P. 1958. Die Embryonalentwicklung des Amphipoden Gammarus pulex pulex L. Zool. Jahrb. Anat. 77: 51-110.

Williams, T. A., B. Blachuta, T. A. Hegna, and L. M. Nagy. 2012. Decoupling elongation and segmentation: Notch involvement in anostracan crustacean segmentation. Evol. Dev. 14: 372-382.

Wolff, C. 2009. The embryonic development of the malacostracan crustacean Porcellio scaber (Isopoda, Oniscidea). Dev. Genes Evol. 219: 545-564.

Wolff, C., and G. Scholtz. 2002. Cell lineage, axis formation, and the origin of germ layers in the amphipod crustacean Orchestia cavimana. Dev. Biol, 250: 44-58.

Wolff, C., and G. Scholtz. 2006. Cell 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: 19.

Zilch, R. 1974. Die Embryonalentwicklung von Thermosbaena mirabilis Monod (Crustacea, Malacostraca, Pancarida). Zool, Jahrb. Anat. 93: 462-576.

Zrzavy, J., and P. Stys. 1997. The basic body plan of arthropods: Insights from evolutionary morphology and developmental biology. J. Evol. Biol, 10: 353-367.

 
<<   CONTENTS   >>

Related topics