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

Background: Marine organisms with sessile adults commonly possess motile larval stages that make settlement decisions based on integrating environmental sensory cues. Phototaxis, the movement toward or away from light, is a common behavioral characteristic of aquatic and marine metazoan larvae, and of algae, protists, and fungi. In cnidarians, behavioral genomic investigations of motile planulae larvae have been conducted in anthozoans (corals and sea anemones) and scyphozoans (true jellyfish), but such studies are presently lacking in hydrozoans. Here, we examined the behavioral genomics of phototaxis in planulae of the hydrozoan Hydractinia symbiolongicarpus. Results: A behavioral phototaxis study of day 3 planulae indicated preferential phototaxis to green (523 nm) and blue (470 nm) wavelengths of light, but not red (625 nm) wavelengths. A developmental transcriptome study where planula larvae were collected from four developmental time points for RNA-seq revealed that many genes critical to the physiology and development of ciliary photosensory systems are dynamically expressed in planula development and correspond to the expression of phototactic behavior. Microscopical investigations using immunohistochemistry and in situ hybridization demonstrated that several transcripts with predicted function in photoreceptors, including cnidops class opsin, CNG ion channel, and CRX-like transcription factor, localize to ciliated bipolar sensory neurons of the aboral sensory neural plexus, which is associated with the direction of phototaxis and the site of settlement. Conclusions: The phototactic preference displayed by planulae is consistent with the shallow sandy marine habitats they experience in nature. Our genomic investigations add further evidence of similarities between cnidops-mediated photoreceptors of hydrozoans and other cnidarians and ciliary photoreceptors as found in the eyes of humans and other bilaterians, suggesting aspects of their shared evolutionary history.

Venom trade-off shapes interspecific interactions, physiology, and reproduction.

The ability of an animal to effectively capture prey and defend against predators is pivotal for survival. Venom is often a mixture of many components including toxin proteins that shape predator-prey interactions. Here, we used the sea anemone Nematostella vectensis to test the impact of toxin genotypes on predator-prey interactions. We developed a genetic manipulation technique to demonstrate that both transgenically deficient and a native Nematostella strain lacking a major neurotoxin (Nv1) have a reduced ability to defend themselves against grass shrimp, a native predator. In addition, secreted Nv1 can act indirectly in defense by attracting mummichog fish, which prey on grass shrimp. Here, we provide evidence at the molecular level of an animal-specific tritrophic interaction between a prey, its antagonist, and a predator. Last, this study reveals an evolutionary trade-off, as the reduction of Nv1 levels allows for faster growth and increased reproductive rates.

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

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.