Structural, molecular and developmental evidence for cell-type diversity in cnidarian mechanosensory neurons

Deploying a conserved mechanosensory neuron known as the concentric hair cell, cnidarians have evolved diverse mechanoreceptors from hydroid filiform tentacles to jellyfish statocysts. However, it is unknown whether cnidarian mechanoreceptor evolution has relied solely on repurposing a single ancestral mechanosensory neuron type. Here we report evidence for cell-type diversity of mechanosensory neurons in sea-anemone cnidarian Nematostella vectensis. Uncovered in the ectoderm of feeding tentacles are conventional type I hair cells and previously unrecognized type II hair cells differing in the structure of apical sensory apparatus and synapses. Moreover, we identify TRP channel-encoding gene polycystin-1 as a type-II-hair-cell-specific essential mediator of gentle touch response. Ontogenically, type I and type II hair cells derive from distinct postmitotic precursors that begin forming at different phases of larval development. Taken together, our findings suggest that anatomically, molecularly, and developmentally distinct mechanosensory neurons diversified within Cnidaria, or prior to the divergence of Cnidaria and Bilateria.