Establishment of the dorsoventral axis in nemertean embryos: Evolutionary considerations of spiralian development

Jonathan Q. Henry, Mark Q. Martindale

Research output: Contribution to journalArticle

Abstract

The Nemertea represent one of a number of invertebrate phyla that display a highly conserved pattern of cell division known as spiral cleavage. The fates of the early blastomeres are known for representatives of some spiralian phyla (i.e., molluscs and annelids) and in these species there appears to be a high degree of conservation in the ultimate fates of particular embryonic cells. The first two cleavage planes bear an invariant relationship to the symmetry properties of the future larval and adult body plan. To investigate whether these properties of spiralian embryo‐genesis are shared (conserved) amongst members of other spiralian phyla, individual blastomeres in two‐ and four‐cell embryos of the nemertean, Nemertopsis bivittata, were microinjected with bi‐otinylated dextran lineage tracers. N. bivittata is a direct‐developing hoplonemertean that forms a nonfeeding larva. When individual blastomeres are injected at the two‐cell stage, two sets of complementary labeling patterns (a total of four different patterns) were observed in the ectoderm of the larvae. When cells were injected at the four‐cell stage, four different patterns were observed that represented subsets of the four patterns observed in the previous experiment. Unlike the case in the annelids and molluscs, in which the first cleavage plane bears a strict 45° angular relationship to the future dorsoventral axis, the first cleavage plane in N. bivittata can bear one of two different relationships relative to the larval/adult dorsoventral axis. In half the cases examined, the first cleavage plane corresponded roughly to the plane of bilateral symmetry, and in the rest, it lay along a frontal plane. A similar result was observed for the embryos of the indirect‐developing heteronemertean, Cerebratutus lacteus. These results indicate that the fates of the four cell quadrants in nemerteans are not directly homologous to those in other spira‐lians, such as the annelids and molluscs. For instance, no single cell quadrant appears to contribute a greater share to the formation of ectoderm, as is the case in the formation of the post‐trochal region by the D‐cell quadrant in annelids and mol‐luscs. Rather, two adjacent cell quadrants contribute nearly equally to the formation of dorsal or ventral ectoderm in the larvae. Possible explanations for the determination of dorsoventrality in nemerte‐ans, as well as implications of these findings regarding the evolution of spiralian development, are discussed. © 1994 Wiley‐Liss, Inc.

Original languageEnglish (US)
Pages (from-to)64-78
Number of pages15
JournalDevelopmental Genetics
Volume15
Issue number1
DOIs
StatePublished - 1994

Keywords

  • Nemertea
  • Spiralians
  • cell lineage
  • development
  • evolution

ASJC Scopus subject areas

  • Genetics
  • Developmental Biology
  • Cell Biology

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