Diversification of Cnidarian Mechanosensory Neurons Across Life Cycle Phases: Evidence from Hydrozoa

Over the course of more than half a billion years of independent evolution, cnidarians (e.g., sea anemones, corals, and jellyfishes) have evolved diverse, multicellular, mechanosensory structures ranging from tentacles of hydroids to gravity sensors of moon jellyfish. The ectodermal epithelium of mechanosensory structures houses the mechanosensory neuron-known as the concentric hair cell-characterized by an apical mechanosensory apparatus consisting of a single cilium surrounded by one or multiple rings of microvilli/stereovilli. While distinct concentric hair cell types are known to occur within life-cycle-stage-specific structures such as the sea anemone tentacles, it is unclear whether diverse concentric hair cell types exist across life cycle phases of any cnidarian. Here, we report evidence from the hydrozoan Cladonema pacificum that concentric hair cells of sedentary polyps are distinct from those of free-swimming medusae. By carrying out touch assays, we demonstrate that polyps and medusae exhibit distinct mechanosensory behaviors. Moreover, we find that concentric hair cells in the ectodermal epithelium of touch-sensitive regions in polyps differ from those in medusae in the morphology of apical sensory apparatuses. Furthermore, polyp-type concentric hair cells are not retained in the ectoderm of medusa buds, and medusa-type concentric hair cells begin to form de novo during medusa formation. Taken together, these findings suggest that distinct mechanosensitive behaviors of polyps and medusae are mediated by morphologically different sets of mechanosensory neurons that develop via life-cycle-stage-specific mechanisms. We propose that cell type diversification of mechanosensory neurons occurred not only within a given life cycle phase but across life cycle phases in cnidarian evolution.