Regulative capacity for eye formation by first quartet micromeres of the polychaete Capitella teleta

Abstract

The stereotypic cleavage pattern shared by spiralian embryos provides unique opportunities to compare mechanisms of cell fate specification of homologous blastomeres, and can give insights into how changes in fate may have influenced the evolution of novel structures and morphological diversity. The potential of cells to undergo regulation and the timing of cell fate specification were investigated during early development in the polychaete annelid, Capitella teleta. Targeted laser deletions of the first quartet micromeres were performed, with a focus on the eye-forming cells 1a and 1c. Most of the larvae resulting from deletion of the 1a or 1c micromeres lack both the pigment cell and sensory cell of the eye as predicted by the C. teleta fate map. In a minority of cases, however, both left and right larval eye spots develop, suggesting that other blastomeres within the embryo regulate for loss of these cells. Deletion of the 1a and 1c derivatives, 1a1 or 1c1, also largely result in larvae with one pigment spot, although there are larvae with two eye spots, suggesting that the ability to regulate for loss of an eye-generating cell persists for an additional cell cycle. Cell deletion in conjunction with intracellular labeling indicates that all four quadrants retain the ability to generate eyes, including those that normally do not. Deletion of all four first quartet micromeres provides evidence that only the first quartet micromeres have eye-forming potential. Additionally, in contrast to the right side of the head where larval and adult eye sensory cells are derived from the same cell (1c), on the left side, the larval and adult eye sensory cells are generated by different embryonic lineages. We hypothesize that cell–cell interactions and cell position are important for regulative ability in Capitella. To our knowledge, this is one of the first detailed deletion studies of the first quartet micromeres and the first convincing example of regulation in polychaetes, which are often thought to be non-regulative in nature.