Multisensory integration by polymodal sensory neurons dictates larval
settlement in a brainless cnidarian larva
Abstract
Multisensory integration (MSI) combines information from more than one
sensory modality to elicit behaviors distinct from unisensory behaviors.
MSI is best understood in animals with complex brains and specialized
centers for parsing sensory information, but the dispersive larvae of
sessile marine invertebrates utilize multimodal environmental sensory
stimuli to base irreversible settlement decisions on, and most lack
complex brains. Here, we examined the sensory determinants of settlement
in actinula larvae of the hydrozoan Ectopleura crocea (Cnidaria),
which possess a diffuse nerve net. A factorial settlement study revealed
that photo-, chemo-, and mechano-sensory cues each influence the
settlement response, which was complex and dependent on specific
combinations of cues, therefore indicating MSI. Mechanosensory cues
either inhibited or enhanced settlement rates depending on the presence
or absence of chemical and light cues in the environment. Sensory gene
expression over development peaked with developmental competence to
settle, which in actinulae, requires cnidocyte discharge. Transcriptome
analyses also highlighted several deep homological links between
cnidarian and bilaterian mechano- chemo- and photo-sensory pathways.
Fluorescent in situ hybridization studies of candidate transcripts
suggested cellular partitioning of sensory function among the few cell
types that comprise the actinula nervous system, where ubiquitous
polymodal sensory neurons with putative chemo- and photo-sensitivity
interface with mechanoreceptive cnidocytes. We propose that a simple
multisensory processing circuit, involving polymodal chemo/photosensory
neurons and mechanoreceptive cnidocytes, is sufficient to explain MSI in
actinulae settlement. Our study demonstrates that MSI is not exclusive
to complex brains, but likely predated and contextualized their
evolution.