Transcriptomic analysis of three annelid species: looking for markers of positional information

Positional information, classically defined through morphogen gradients, underlies the establishment and maintenance of spatial coordinates in developing organisms and remains essential throughout post-embryonic growth and regeneration. Many conserved developmental regulators, including components of the Wnt, FGF, retinoid, caudal, Hox, and ParaHox pathways, continue to function after embryogenesis, supporting posterior growth, segmentation, stem cell activity, and regenerative responses. Studies across metazoans demonstrate that gradients of these factors are maintained in adult tissues and are reorganized after injury, thereby guiding correct pattern restoration. Annelids provide a powerful model for investigating post-embryonic patterning and the maintenance of positional information. They grow by adding segments from a posterior growth zone, exhibit dynamic shifts in segment position throughout life, and show diverse regenerative capacities, offering an opportunity to identify molecular correlates of these differences. We generated spatially resolved transcriptomes for three annelid species with distinct regenerative potentials – Pygospio elegans, Platynereis dumerilii, and Arenicola marina. By analyzing differential gene expression across body fragments, we reconstructed expression patterns along the anterior-posterior axis and examined genes involved in organogenesis, growth zone function, and potential positional information. This comparative transcriptomic study shows that spatial gene expression in three annelid species broadly corresponds to major anatomical territories but also reflects deeper developmental origins. The clear transcriptional differences between larval and postlarval segments in P. elegans and P. dumerilii suggest that segment ontogeny, not anatomy alone, contributes to regional molecular identity. The posterior growth zones of these two species exhibit strong activation of Wnt, cad, Hox, and GMP genes, consistent with an active stem-cell–based growth program. In contrast, the posterior region of A. marina lacks these signatures, supporting previous evidence for an inactive growth zone and the absence of posterior regeneration. Gradient-like expression of Hox, ParaHox, and Wnt genes in P. elegans and P. dumerilii indicates that these factors may encode positional information along the body axis and facilitate regeneration. Their truncated expression in A. marina likely reflects functional specialization of the adult body. Overall, our findings highlight conserved molecular systems involved in posterior growth and positional identity, while revealing species-specific modifications associated with reduced regenerative capacity.