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Abstract

Candidate gene approaches have positioned the Platynereis dumerilii mushroom bodies as an interesting evolutionary case study. With resemblances to both the vertebrate telencephalon and to similarly structured insect mushroom bodies, the neurons making up these brain regions have been thought to stem from an ancestral cell type family. Single cell transcriptomics is enabling the investigation of such evolutionary questions based on a cell's entire repertoire of expressed genes. The present investigation used single nucleus RNA sequencing to characterise the neurons of this structure in adult P.dumerilii. This revealed a gene signature comprising known and novel genes that can now be compared to closely and more evolutionarily distant species. This approach also uncovered the stage - specific expression of a ciliary opsin - cOpsin1 - and a possible emx paralog - emx2 - in a subset of these neurons, which appear to undergo dramatic restructuring upon sexual metamorphosis. Incorporating publicly available datasets of similar stages further showed that this subset of neurons may reflect vertebrate - like mechanisms of adult neurogenesis influenced - either directly or indirectly - by cOpsin1. These findings are interpreted in light of recent work characterising a neurogenic region adjacent to the rhabdomeric eyes and responsible for their growth during sexual metamorphosis, a process that also seems to involve the expression of cOpsin1 (Milivojev et al., 2024). In addition to this unexpected finding, the present work attempts to compare the overall mushroom body gene signature across distant species, finding mef2c to be a common gene shared among P.dumerilii and insect mushroom bodies, as well as cephalopod vertical lobe neurons. It also highlights how the diversity within Annelida can help resolve outstanding questions of whether these neurons represent an ancestral cell type and how future transcriptomic investigations on diverse annelid brains will provide macro- and microevolutionary insights.