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.

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Multisensory integration (MSI) combines information from more than one sensory modality to elicit behaviours distinct from unisensory behaviours. MSI is best understood in animals with complex brains and specialized centres for parsing different modes of sensory information, but 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 mechanosensory cues each influenced the settlement response in a complex and hierarchical manner that was dependent on specific combinations of cues, an indication of MSI. Additionally, 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 photosensory 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 expressing putative chemo‐ and photosensitivity interface with mechanoreceptive cnidocytes. We propose a simple multisensory processing circuit, involving polymodal chemo/photosensory neurons and mechanoreceptive cnidocytes, that 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.

The ability of an animal to effectively capture prey and defend against predators is pivotal for its survival. Venom, a mixture of many toxin proteins, shapes predator-prey interactions. Here, we use the sea anemone Nematostella vectensis to test how toxin genotypes impact predator-prey interactions. We developed a new genetic manipulation tool which significantly reduces both RNA and protein levels of Nv1, a major neurotoxin. In concert we recently discovered a native population of Nematostella that has lost Nv1.We demonstrate that these anemones lacking Nv1, have reduced ability to defend themselves against grass shrimp, a native predator. Additionally, secreted Nv1 can act indirectly in defense by attracting mummichog fish, which are known to prey on grass shrimp. This unravels a tritrophic interaction acting in animal defense at the molecular level. Additionally, our work reveals an evolutionary tradeoff, as the reduction of Nv1 levels causes faster growth and increased sexual and asexual reproductive rates.

Multisensory integration (MSI) combines information from two or more sensory modalities and results in a different response from the individual sensory stimuli. Larvae of sessile marine invertebrates use environmental sensory stimuli to irreversibly settle and metamorphose. It can be expected that with such an important survival decision larvae leverage information from multiple sensory modalities. However, MSI has yet to be deeply investigated in marine larvae that lack complex nervous systems and brains. Here, we examined the settlement response of the actinula larva of the hydrozoan Ectopleura crocea, which possess a diffuse nerve net, and found that actinulae utilize MSI during larval settlement. We performed a factorial larval settlement study that revealed larvae are sensitive to photo- chemo- and mechanosensory cues and settle in complex ways to different combinations of cues, indicating MSI. In addition, a developmental transcriptome study revealed peak expression of a comprehensive set of candidate sensory genes at the developmental stage when larvae are competent to settle. Finally, RNA fluorescent in situ hybridization studies of candidate sensory genes showed that many of the sensory genes of interest are expressed in the same sensory neuron, suggesting that the process of MSI in E. crocea takes place within a sensory neuron and not between specialized neurons or neural regions as in other animals. Our results indicate that MSI plays an important role in mediating the larval settlement decision in E. crocea and suggests that this process may be accomplished by integrating different lines of sensory information within a polymodal sensory neuron.