Patterns of Autonomous and Conditional Neural Specification for the Brain and Ventral Nerve Cord in Annelida

ABSTRACT

Evolution of central nervous systems is a long‐debated topic. Similar mechanisms of conditional neural specification linked to dorsal‐ventral (D–V) axis formation have been used to support homology across several taxa. We tested for autonomous versus conditional neural specification in two distantly related annelids, Capitella teleta and Platynereis dumerilii , using blastomere isolations and ablations. Our results demonstrate autonomous specification of anterior neural tissue in isolated first‐quartet (1q) micromeres for both annelids. In both annelids, partial larvae derived from isolation of the somatoblast, micromere 2d, also resulted in the formation of trunk neural tissue (ventral nerve cord or VNC), suggesting that this cell has intrinsic neural fate. However, at least in C. teleta , we found evidence that additional external proneural and anti‐neural signals affect specification of trunk neural fate in 2d. Ablation of the vegetal macromeres at the 16‐cell stage (leaving 1q + 2q) resulted in partial larvae that failed to form trunk neural tissue although they did have anterior neural tissue and a D–V axis, suggesting that micromeres other than 2d may repress the intrinsic neural fate of 2d. Conversely, ablation of only three of four vegetal macromeres at the 16‐cell stage (e.g., leaving 1 macromere with 1q + 2q) “rescues” trunk neural fate, suggesting the presence of a vegetal proneural signal in all four quadrants. Taken together, these results imply that VNC fate is specified by a complex interplay of signaling that is decoupled from D–V axis formation in C. teleta . Our results suggest that the distinct neural specification mechanisms between the head and trunk may be conserved in Annelida and that annelid CNS specification may operate independently of D–V axis formation. These findings will broaden our understanding of how neural specification mechanisms evolved and diversified in Spiralia in comparison to other bilaterians.