Comparative larval single-cell transcriptomics provides insights into the evolutionary origins of sensory-neural programmes in Porifera and Cnidaria

Abstract

Understanding how specialised cell types emerged and diversified is fundamental to reconstructing animal evolution. The origins of neural and sensory-secretory cell types are particularly intriguing, and early diverging non-neuronal metazoans, such as sponges, provide critical insights into pre-neural molecular toolkits. Free-swimming larval stages of sponges and cnidarians provide an unique context for investigating these questions, as these larvae rely on specialised sensory and signalling systems to detect environmental cues and coordinate behaviour during dispersal and settlement. Here, we integrated larval single-cell transcriptomic datasets from the demosponge Amphimedon queenslandica and four cnidarian species (Nematostella vectensis, Astroides calycularis, Pocillopora acuta and Clytia hemisphaerica). Cross-species mapping using Self-Assembling Manifold mapping (SAMap) recovered broad conservation of major cell-type identities among cnidarians, including neural, secretory, cnidocyte, epithelial, gastrodermal and apical populations. Extending these comparisons to A. queenslandica displayed transcriptional similarities between several sponge larval cell populations and cnidarian neural, sensory and progenitor-associated cell types. Within-species analyses showed that these cell populations remained transcriptionally integrated within the broader epithelial and sensory cell type of the sponge larva. Neural-associated gene modules, including conserved families associated with photoreception, neural fate specification and postsynaptic scaffolding, were distributed across distinct epithelial and sensory-like sponge larval cell populations rather than being restricted to a single proto-neural cell type. Our findings suggest that molecular components subsequently incorporated into neural systems were already deployed across diverse cell types in a common ancestor of sponges & cnidarians. Our work supports an evolutionary scenario in which extant neural and sensory-secretory cell types arose through the diversification and reorganisation of molecular programmes distributed across multiple ancestral sensory-secretory cell types.