From spiral cleavage to bilateral symmetry: the developmental cell lineage of the annelid brain

Abstract Background During early development, patterns of cell division—embryonic cleavage—accompany the gradual restriction of blastomeres to specific cell fates. In Spiralia, which include annelids, mollusks, and flatworms, “spiral cleavage” produces a highly stereotypic, spiral-like arrangement of blastomeres and swimming trochophore-type larvae with rotational (spiral) symmetry. However, starting at larval stages, spiralian larvae acquire elements of bilateral symmetry, before they metamorphose into fully bilateral juveniles. How this spiral-to-bilateral transition occurs is not known and is especially puzzling for the early differentiating brain and head sensory organs, which emerge directly from the spiral cleavage pattern. Here we present the developmental cell lineage of the Platynereis larval episphere. Results Live-imaging recordings from the zygote to the mid-trochophore stage (~ 30 hpf) of the larval episphere of the marine annelid Platynereis dumerilii reveal highly stereotypical development and an invariant cell lineage of early differentiating cell types. The larval brain and head sensory organs develop from 11 pairs of bilateral founders, each giving rise to identical clones on the right and left body sides. Relating the origin of each bilateral founder pair back to the spiral cleavage pattern, we uncover highly divergent origins: while some founder pairs originate from corresponding cells in the spiralian lineage on each body side, others originate from non-corresponding cells, and yet others derive from a single cell within one quadrant. Integrating lineage and gene expression data for several embryonic and larval stages, we find that the conserved head patterning genes otx and six3 are expressed in bilateral founders representing divergent lineage histories and giving rise to early differentiating cholinergic neurons and head sensory organs, respectively. Conclusions We present the complete developmental cell lineage of the Platynereis larval episphere, and thus the first comprehensive account of the spiral-to-bilateral transition in a developing spiralian. The bilateral symmetry of the head emerges from pairs of bilateral founders, similar to the trunk; however, the head founders are more numerous and show striking left-right asymmetries in lineage behavior that we relate to differential gene expression.