Molecular and behavioural evidence that interdependent photo - and chemosensory systems regulate larval settlement in a marine sponge

Marine pelagic larvae use a hierarchy of environmental cues to identify a suitable benthic habitat on which to settle and metamorphose into the adult phase of the life cycle. Most larvae are induced to settle by biochemical cues and many species have long been known to preferentially settle in the dark. Combined, these data suggest that larval responses to light and biochemical cues may be linked, but this has yet to be explored at the molecular level. Here, we track the vertical position of larvae of the sponge Amphimedon queenslandica to show that they descend to the benthos at twilight, by which time they are competent to respond to biochemical cues, consistent with them naturally settling in the dark. We use larval settlement assays under three different light regimes, combined with transcriptomics on individual larvae, to identify candidate molecular pathways underlying larval settlement. We find that larvae do not settle in response to biochemical cues if maintained in constant light. Our transcriptome data suggest that constant light actively represses settlement via the sustained up-regulation of two putative inactivators of chemotransduction in constant light only. Our data suggest that photo- and chemosensory systems interact to regulate larval settlement via nitric oxide and cyclic guanosine monophosphate signalling in this sponge, which belongs to one of the earliest-branching animal phyla.