Annelids shed light on the evolution of spiralian development

Abstract

Spiralian development is characterized by stereotypic cell geometry and spindle orientation in early cleavage stage embryos, as well as conservation of ultimate fates of descendent clones. Diverse taxa such as molluscs, annelids, flatworms, and nemerteans exhibit spiralian development, but it is a mystery how such a conserved developmental program gives rise to such diverse body plans. This review highlights examples of variation during early development among spiralians, emphasizing recent experimental studies in the annelid Capitella teleta Blake, Grassle and Eckelbarger, 2009. Intracellular fate mapping studies in C. teleta reveal that many of its cells’ fates are shared among spiralians, but it also has a novel origin for trunk mesoderm (3c and 3d micromeres). Studies have identified an inductive signal in spiralians that has “organizing activity” and that influences cell fates in the surrounding embryo. Capitella teleta also has an organizing activity; however, surprisingly, it is localized to a different cell, it signals at a different developmental stage, and likely utilizes a distinct molecular signaling pathway compared with that in molluscs. A model is presented to provide a mechanistic explanation of evolutionary changes in the cellular identity of the organizer. Detailed experimental investigations in spiralian embryos demonstrate variation in developmental features that may influence the evolution of novel forms.