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.

Phototactic preference and its genetic basis in the planulae of the colonial Hydrozoan Hydractinia symbiolongicarpus

“…Thus, a sensory mechanism other than phototaxis, likely involving the perception of chemical and/or mechanical cues, is required for settlement on the proper substrate. Similarly, we recently described the interaction between light, chemical, and mechanical cues in larval settlement in another hydrozoan species Ectopleura crocea (23), furthering the idea that the integration of multiple sensory cues may be a common mechanism for larval settlement (60–62).…”

“…Orthology analyses utilized a dataset including the present data plus an additional five genome-scale protein coding datasets from cnidarian and bilaterian species, including human. Opsin-mediated photobehavior has been described in cnidarians previously (8,9, 44,12,16,23,[39][40][41][42][43]. We, therefore, identified between-day differentially expressed transcripts with membership in GSEA gene sets that contained opsin, which included the sensory perception of light (Fig 3) and sensory systems development (Fig 4) gene sets, the latter including genes involved in mechanoreception and chemoreception as well.…”

“…Larval phototaxis is widespread in the marine environment and has been implicated as a strategy for predator avoidance, dispersal, diel vertical migrations, and larval settlement (1, [53][54][55][56]. H. symbiolongicarpus planulae are phototactic and neuropeptides including RFamide play a role in relaying photosensory stimuli to epithelial muscular cells, directing the movement of the photoresponse (6,7).…”

Multisensory integration by polymodal sensory neurons dictates larval settlement in a brainless cnidarian larva

“…Our larval settlement study identified a sensory cue hierarchy, where the highest rates of settlement occurred in the presence of chemical, mechanical, and light cues, with green light being the most permissive to settlement (Figure 3). This is not surprising as marine invertebrate larvae are known to integrate information from different modalities (Birch et al, 2023;Crisp, 1974;Ettinger-Epstein et al, 2008;Hadfield, 2011;Hadfield & Paul, 2001;Hodin et al, 2018;Holst & Jarms, 2007;Morello & Yund, 2016;Müller & Leitz, 2002;Pawlik, 1992;Say & Degnan, 2020;Whalan et al, 2015;Woodson et al, 2007). This type of sensory integration, and the likelihood that some cues are more important than others, was the basis for the proposal that a hierarchy of sensory cues dictates larval settlement in a species-specific manner (Ettinger-Epstein et al, 2008;Hodin et al, 2018;Kingsford et al, 2002;Woodson et al, 2007).…”

“…All behavioural analyses and metadata can be found on Github (https://github.com/sjb10 61/Actin ula_Paper/ tree/ main/Settl ement_Behav ior_Analysis). Raw behavioural data, RNA FISH probe sequences, and the mechanosensory pilot study can be found on Dryad (https://doi.org/10.5061/dryad.tqjq2 bw3x) (Birch & Plachetzki, 2023). Multisensory integration by polymodal sensory neurons dictates larval settlement in a brainless cnidarian larva.…”