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Conservation and innovation in spiralian development

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Reproductive Strategies and Developmental Patterns in Annelids

Part of the book series: Developments in Hydrobiology ((DIHY,volume 142))

Abstract

It is clear that the spiralian developmental program represents a highly flexible platform for the generation of diverse larval and adult body plans. The widespread occurrence of this pattern of early development attests to its tremendous evolutionary success. Despite the large degree of conservation in the spiral cleavage pattern and other basic aspects of early development, changes in cell fate maps and in the mechanisms of blastomere specification have arisen. While we have learned a great deal about this mode of development, a number of important questions remain to be answered. To what extent do these conditions apply to the lesser studied spiralian phyla? What constraints have led to the preservation of the early spiral cleavage program? How has this developmental program been adapted for the construction of the various spiralian body plans (e.g. the segmental body plans of annelids or to the potential secondary loss of segmentation)? Are most changes associated with the elaboration of these different larval and adult body plans restricted to the late period of development? What molecular/genetic processes underlie this developmental program? Clearly, the spiralian phyla represent an important group of organisms for further studies on development and evolution.

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References

  • Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff J. A. Lake, 1997. Evidence for a c1ade of nematodes, arthropods and other molting animals. Nature 387: 489–493.

    Article  PubMed  CAS  Google Scholar 

  • Anderson, D. T., 1973. Embryology and phylogeny in annelids and arthropods. Pergamon, Oxford.

    Google Scholar 

  • Arnold, J. M., 1965. Normal embryonic stages of the squid Loligo pealii. Biol. Bull. 128: 24–32.

    Article  Google Scholar 

  • Arnold, J. M., 1971. Cephalopods. In G. Reverberi, (ed.), Experimental Embryology of Marine and Freshwater Invertebrates. North Holland Publishing. Co. Chapter 10: 265–311.

    Google Scholar 

  • Arnolds, W. J. A., J. A. M. van den Biggelaar N. H. Verdonk, 1983. Spatial aspects of cell interactions involved in the determination of dorsoventral polarity in equally cleaving gastropods and regulative abilities of their embryos, as studied by micromere deletions in Lymnaea and Patella. W. Roux’s Arch. Dev. Biol. 192: 75–85.

    Article  Google Scholar 

  • Ax, P., 1987. The phylogenetic system. John Wiley and Sons, Chichester, 340 pp.

    Google Scholar 

  • Ax, P., 1995. Das System der Metazoa I. Ein Lehrbuch der phylogenetischen Systematik. Fischer, Stuttgart, 226 pp.

    Google Scholar 

  • Bakke, T., 1990. Pogonophora. In Adiyodi, K. G. R. Adiyodi (eds), Reproductive Biology of Invertebrates, Vol. IV, Part B, John Wiley and Sons, Chichester. 37–48.

    Google Scholar 

  • Balavoine, G., 1997. The early emergence of platyhelminths is contradicted by the agreement between I 8s rRNA and Hox genes data. Evolution 320: 83–94.

    CAS  Google Scholar 

  • Boyer, B. C., 1986. Determinative development in the polyclad turbellarian, Hoploplana inquilina. Int. J. Invert. Reprod. Dev. 9: 243–25 1.

    Google Scholar 

  • Boyer, B. C., 1987. Development of in vitro fertilized embryos of the polyclad flatworm, Hoploplana inquilina, following blastomere separation and deletion. W. Roux’s Arch. Dev. Biol. 196: 158–164.

    Google Scholar 

  • Boyer, B. C., 1989. The role of the first quartet micromeres in the development of the polyclad Hoploplana inquilina. Biol. Bull. 177: 338–343.

    Google Scholar 

  • Boyer, B. C., J. Q. Henry M. Q. Martindale, 1996a. Dual origins of mesoderm in a basal member of the spiralian clade: cell lineage analyses in the polyclad turbellarian Hoploplana inquilina. Dev. Biol. 179: 329–338.

    Google Scholar 

  • Boyer, B. C., J. Q. Henry M. Q. Martindale, I996b. Modified spiral cleavage: The duet cleavage pattern and early blastomere fates in the acoel turbellarian Neochildia fusta. Biol. Bull. 191: 285–286.

    Google Scholar 

  • Boyer, B. C., J. Q. Henry M. Q. Martindale, 1998. The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev. Biol., 204: 111–123.

    Google Scholar 

  • Boyer, B. C. J. Q. Henry, 1998. Evolutionary modifications of the spiralian developmental program. Am. Zool. 38: 621–633.

    Google Scholar 

  • Conklin, E. G., 1897. The embryology of Crepidula. J. Morph. 13: 1–226.

    Article  Google Scholar 

  • Costello, D. P. C. Henley, 1976. Spiralian development: a perspective. Am. Zool. 16: 277–291.

    Google Scholar 

  • Damen, P., 1994. Cell lineage, and specification of developmental fate and dorsoventral organization in the mollusc Patella vulgata. Thesis Universiteit Utrecht. Cip-Data Koninklijke Bibliotheek, Den Haag.

    Google Scholar 

  • Damen, R. W. J. A. G. Dictus, 1994. Cell lineage of the prototroch of Patella vulgata ( Gastropoda, Mollusca). Dev. Biol. 162: 364383.

    Google Scholar 

  • Dorresteijn, A. W. C., 1990. Quantitative analysis of cellular differentiation during early embryogenesis of Platvnereis dumerilii. Roux’s Arch. Dev. Biol. 199: 14–30.

    Google Scholar 

  • Dorresteijn, A. W. C., H. Bornewasser A. Fischer, 1987. A correlative study of experimentally changed first cleavage and Janus development in the trunk of Platynereis dumerilii ( Annelida, Polychaeta). Roux’s Arch. Dev. Biol. 196: 51–58.

    Google Scholar 

  • Eernisse, D. J., J. S. Albert F. E. Anderson, 1992. Annelida and Arthropoda are not sister taxa: A phylogenetic analysis of spiralian metazoan morphology. Syst. Biol. 41: 305–330.

    Google Scholar 

  • Field, K. G., G. J. Olsen, G. J. Lane, S. J. Giovannoni N. R. Pace, 1988. Molecular phylogeny of the animal kingdom. Science 239: 748–753.

    Article  PubMed  CAS  Google Scholar 

  • Fioroni, P., 1979. Zur Struktur der Pollappen und der Dottermakromeren - eine vergleichende Ubersicht. Zool. Jb. Anat. 102: 395–430.

    Google Scholar 

  • Freeman, G. J. W. Lundelius, 1982. The developmental genetics of dextrality and sinistrality in the gastropod Lvmnaea peregra. W. Roux’s Arch. Dev. Biol. 191: 69–83.

    Google Scholar 

  • Freeman, G. J. W. Lundelius, 1992. Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J. evol. Biol. 5: 205–247.

    Google Scholar 

  • Furuya, H., K. Tsuneki Y. Koshida, 1996. The cell lineages of two types of embryos and a hermaphrodite gonad in dycyemid mesozoans. Dev. Growth Diff. 38: 453–463.

    Google Scholar 

  • Guerrier, R, J. A. M. van den Biggelaar, C. A. M. van Dongen N. H. Verdonk, 1978. Significance of the polar lobe for the determination of dorsoventral polarity in Deutalium vulgare (da Costa). Dev. Biol. 63: 233–242.

    Google Scholar 

  • Halanych, K. M., J. D. Bachelier, A. M. A. Aguinaldo, S. M. Liva, D. M. Hillis J. A. Lake, 1995. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science 267: 1641–1643.

    Article  PubMed  CAS  Google Scholar 

  • Henry, J. J., 1986. The role of unequal cleavage and the polar lobe in the segregation of developmental potential during first cleavage in the embryo of Chaetopterus variopedatus. Roux’s Arch. Dev. Biol. 195: 103–116.

    Google Scholar 

  • Henry, J. J., 1989. Removal of the polar lobe leads to the formation of functionally deficient photocytes in the annelid Chaetopterus variopedatus. Roux’s Arch. Dev. Biol. 198: 129–136.

    Google Scholar 

  • Henry, J. J. M. Q. Martindale, 1987. The organizing role of the D quadrant as revealed through the phenomenon of twinning in the polychaete Chaetopterus variopedatus. Roux’s Arch. Dev. Biol. 196: 499–510.

    Google Scholar 

  • Henry, J. Q. M. Q. Martindale, 1994. Establishment of the dorsoventral axis in nemertean embryos: Evolutionary considerations of spiralian development. Developmental Genetics 15: 64–78.

    Google Scholar 

  • Henry, J. Q. M. Q. Martindale, 1995. The experimental alteration of cell lineages in the nemertean Cerebratulus lacteus: Implications for the precocious establishment of embryonic axial properties. Biol. Bull. 189: 192–193

    Google Scholar 

  • Henry, J. Q. M. Q. Martindale, 1996a. The origins of mesoderm in the equal-cleaving nemertean worm Cerebratulus lacteus. Biol. Bull. 191: 286–288.

    Google Scholar 

  • Henry, J. Q. M. Q. Martindale, 1996b. The establishment of embryonic axial properties in the nemertean, Cerebratulus lacteus. Dev. Biol. 180: 713–721.

    Google Scholar 

  • Henry, J. M. Q. Martindale, 1997. The Nemertea. In S. Gilbert (ed.), Embryology, the Construction of Life, Sinauer, MA.

    Google Scholar 

  • Henry. J. Q. M. Q. Martindale, 1998. Conservation of the spiralian developmental program: Cell lineage of the nemertean, Cerebratulus lacteus. Dev. Biol., 201: 253–269.

    Google Scholar 

  • Henry, J. Q., M. Q. Martindale B. C. Boyer, 1995. Axial specification in a basal member of the spiralian clade: Lineage relationships of the first four cells to the larval body plan in the polyclad turbellarian Hoploplana inquilina. Biol. Bull. 189: 194–195.

    Google Scholar 

  • Katayama, T., M. Nishioika M. Yamamoto, 1996. Phylogenetic relationships among the turbellarian orders inferred from I 8s rDNA sequences. Zool. Sci. 13: 747–756.

    Google Scholar 

  • Lillie, F. R., 1895. The embryology of the Unionidae. J. Morph. 10: I - I00.

    Article  Google Scholar 

  • Lillie, F. R., 1899. Adaptation in cleavage. Biol. Lects. MBL, summers of 1897–98. Ginn, Boston.

    Google Scholar 

  • Luetjens, C. M. A. W. C. Dorresteijn, 1995. Multiple. alternative cleavage patterns precede uniform larval morphology during normal development of Dreisaena po/yinorpho (Mollusca, Lamellibranchia). Roux’s Arch. Dev. Biol. 205: 138–149

    Google Scholar 

  • Martindale, M. Q., 1986. The organizing role of the D quadrant in an equal-cleaving spiralian, 4innaea stagnalis, as studied by UV laser deletion of macromeres at intervals between third and fourth quartet formation. Int. J. Invert. Reprod. Dev., 9: 229–242.

    Google Scholar 

  • Martindale, M. Q., C. Q. Doe J. B. Morrill, 1985. The role of animal-vegetal interaction with respect to the determination of dorsoventral polarity in the equal-cleaving spiralian, Luinaea palustris. Roux’s Arch. Dev. Biol., 194: 281–295.

    Google Scholar 

  • Martindale, M. Q. J. Q. Henry, 1995. Novel patterns of spiralian development: Alternate modes of cell fate specification in two species of equal-cleaving nemertean worms. Development 121: 3175–3185.

    Google Scholar 

  • McHugh, D., 1997. Molecular evidence that echiurans and pogonophorans are derived annelids. Proc. natn. Acad. Sci. 94: 8006–8009.

    Google Scholar 

  • Mead, A. D., 1897. The early development of marine annelids. J. Morph. 13: 227–322.

    Article  Google Scholar 

  • Newby, W. W., 1940. The embryology of the echiuroid worm Urechis caupo. Mem. am. Phil. Soc. 16: 1–219.

    Google Scholar 

  • Philippe, H., A. Chenuil A. Adoutte, 1994. Can the Cambrian explosion be inferred through molecular phylogeny? Development (Suppl.): 15–25.

    Google Scholar 

  • Raff, R. A., C. R. Marshall J. M. Turbeville, 1994. Using DNA sequences to unravel the Cambrian radiation of the animal phyla. Ann. Rev. Ecol. Syst. 25: 351–375.

    Google Scholar 

  • Render, J. A., 1989. Development of Ilyanassa obsoleta embryos after equal distribution of polar lobe material at first cleavage. Dev. Biol. 132: 241–250.

    Google Scholar 

  • Render, J. A., 1991. Fate maps of the first quartet micromeres in the gastropod IIs’anassa obsoleta. Development 113: 495–501.

    PubMed  CAS  Google Scholar 

  • Render, J. A., 1997. Cell fate maps in the Ifvanas.sa obso/eta embryobeyond the third division. Dev. Biol. 189: 301–310

    Google Scholar 

  • Rice, M. E., 1975. Sipunculida. In Giese, A. C. J. S. Pearse (eds), Reproduction of Marine Invertebrates, Academic Press, New York: 67–127.

    Chapter  Google Scholar 

  • Smith, C. M. D. A. Weisblat, 1994. Micromere fate maps in leech embryos: lineage-specific differences in rates of cell proliferation. Development 120: 3427–3438.

    PubMed  CAS  Google Scholar 

  • Sterrer, W., 1974. Gnathostomulida. In Giese, A. C. J. S. Pearse (eds), Reproduction of Marine Invertebrates. Academic Press, New York. Vol. 1: 345–357.

    Google Scholar 

  • Torrey, J. C., 1903. The early embryology of Thalassema mellites. Ann. N. Y. Acad. Sci. 14: 165–246.

    Google Scholar 

  • Treadwell, A. L, 1901. Cytogeny of Podarke obscwzo Verrill. J. Morph. 17: 399–486.

    Article  Google Scholar 

  • Turbeville, J. M., K. G. Field R. A. Raff, 1992. Phylogenetic position of phylum Nemertini, inferred from 18s rRNA sequences: Molecular data as a test of morphological character homology. Mol. Biol. Evol. 9: 235–249.

    Google Scholar 

  • Tyler, A., 1930. Experimental production of double embryos in annelids and mollusks. J. exp. Zool. 57: 347–407.

    Google Scholar 

  • Valentine, J. W., 1997. Cleavage patterns and the topology of the metazoan tree of life. Proc. natn. Acad. Sci. 94: 8001–8005.

    Google Scholar 

  • Valentine, J. W., D. H. Erwin D. Jablonski, 1996. Developmental evolution of metazoan body plans: The fossil evidence. Dev. Biol. 173: 373–381.

    Google Scholar 

  • Biggelaar, J. A. M., 1977. Development of dorsoventral polarity and mesentoblast determination in Pate//a ru/gata. J. Morph. 154: 157–186.

    Article  PubMed  Google Scholar 

  • Biggelaar, J. A. M. P. Guerrier, 1979. Dorsoventral polarity and mesentoblast determination as concomitant results of cellular interactions in the mollusk Patella rulgata. Dev. Biol. 68: 462–471.

    Google Scholar 

  • Biggelaar, J. A. M. P. Guerrier, 1983. Origin of spatial information. In Verdonk, N. H., J. A. M. van den Biggelaar A. S. Tompa (eds), The Mollusca, Academic Press, New York. 179–213.

    Google Scholar 

  • Verdonk, N. H. J. N. Cather, 1983. Morphogenetic determination and differentiation. In Verdonk, N. H., J. A. M. van den Biggelaar A. S. Tompa (eds), The Mollusca, Academic Press, New York. 215–252.

    Google Scholar 

  • Verdonk, N. H. J. A. M. van den Biggelaar, 1983. Early development and the formation of the germ layers. In Verdonk, N. H., J. A. M. van den Biggelaar A. S. Tompa (eds), The Mollusca, Academic Press, New York: 91–122.

    Google Scholar 

  • Watase, S., 1888. Observations on the development of cephalopods: homology of the germ layer. Stud. Johns Hopkins Biol. Lab. 4: 165–183.

    Google Scholar 

  • Willmer, P., 1990. Invertebrate relationships, patterns in animal evolution. Cambridge University Press. Cambridge: 199–222. Wilson. E. B., 1892. The cell lineage of Nerds. J. Morph. 6: 361–481

    Google Scholar 

  • Wilson, E. B., 1898. Considerations on cell-lineage and ancestral reminiscence. Ann. N. Y. Acad. Sci. 11: 1–27.

    Google Scholar 

  • Winnepennickx, B., T. Backeljau, Y. van de Peer R. de Wachter, 1992. Structure of the small ribosomal subunit RNA of the pulmonate snail Limiclaria kambeul, and phylogenetic analysis of the Metazoa. FEBS 309: 123–126.

    Article  CAS  Google Scholar 

  • Woltereck, R.. 1904. Beitrilge zur praktischen Analyse der Po/vgordius-Entwicklung nach dem Nordsee und dem Mittelmeer Typus. 1. Der für beide Typen gleichverlaufende Entwicklungsabschnitt vom Ei bis zum jüngsten TrochophoraStadium. Arch. Entw. mech. Org. 18: 377–403.

    Google Scholar 

  • Young, C. M., E. Velaquez, A. Metaxas P.A. Tyler, 1996. Embryology of vestimentiferan tube worms from deep-sea methane/sulphide seeps. Nature 381: 514–516.

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Cell and Structural Biology, University of Illinois, Urbana, IL, 61801, USA

    Jonathan J. Henry

  2. Kewalo Marine Laboratory, PBRC/University of Hawaii, 41 Ahui St., Honolulu, HI, 96813, USA

    Mark Q. Martindale

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  1. Jonathan J. Henry
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Editors and Affiliations

  1. Institut für Zoologie, FB 21, Johannes-Gutenberg-Universität, D-55099, Mainz, Germany

    Adriaan W. C. Dorresteijn

  2. Spezielle Zoologie, FB 5, Universität Osnabrück, D-49069, Osnabrück, Germany

    Wilfried Westheide

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Henry, J.J., Martindale, M.Q. (1999). Conservation and innovation in spiralian development. In: Dorresteijn, A.W.C., Westheide, W. (eds) Reproductive Strategies and Developmental Patterns in Annelids. Developments in Hydrobiology, vol 142. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-2887-4_15

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  • DOI: https://doi.org/10.1007/978-94-017-2887-4_15

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