Cell fate specification modes shape transcriptome evolution in the highly conserved spiral cleavage

Early animal development can be remarkably variable, influenced by lineage-specific reproductive strategies and adaptations. Yet, early embryogenesis is also strikingly conserved in some groups, like Spiralia (e.g., snails, clams, and many marine worms). In this large clade, a shared cleavage program –– the so-called spiral cleavage –– and similar cell lineages are ancestral to at least seven animal phyla. Why early development is so conserved in specific groups and plastic in others is not fully understood. Here, we investigated two annelid species –– Owenia fusiformi s and Capitella teleta –– with spiral cleavage but different modes of specifying their primary progenitor cells. By generating high-resolution transcriptomic time courses from the oocyte and fertilisation until gastrulation, we show transcriptional dynamics are markedly different between these species during spiral cleavage and instead reflect their distinct timings of embryonic organiser specification. However, the end of cleavage and gastrulation exhibit high transcriptomic similarity. At these stages, orthologous transcription factors share gene expression domains, suggesting this period is a previously overlooked mid-developmental transition in annelid embryogenesis. Together, our data reveal hidden developmental plasticity in the genetics underpinning spiral cleavage, indicating an evolutionary decoupling of morphological and transcriptomic conservation during early animal embryogenesis.