Abstract
BackgroundDuring larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology. This change between life-cycle stages is often associated with a change in diet or a transition between a non-feeding and a feeding form. How larvae regulate changes in feeding during this life-cycle transition is not well understood. Neuropeptides are known to regulate several aspects of feeding, such as food search, ingestion and digestion. The marine annelid Platynereis dumerilii has a complex life cycle with a pelagic non-feeding larval stage and a benthic feeding postlarval stage, linked by the process of settlement. The conserved neuropeptide myoinhibitory peptide (MIP) is a key regulator of larval settlement behavior in Platynereis. Whether MIP also regulates the initiation of feeding, another aspect of the pelagic-to-benthic transition in Platynereis, is currently unknown.ResultsHere, we explore the contribution of MIP to the regulation of feeding behavior in settled Platynereis postlarvae. We find that in addition to expression in the brain, MIP is expressed in the gut of developing larvae in sensory neurons that densely innervate the hindgut, the foregut, and the midgut. Activating MIP signaling by synthetic neuropeptide addition causes increased gut peristalsis and more frequent pharynx extensions leading to increased food intake. Conversely, morpholino-mediated knockdown of MIP expression inhibits feeding. In the long-term, treatment of Platynereis postlarvae with synthetic MIP increases growth rate and results in earlier cephalic metamorphosis.ConclusionsOur results show that MIP activates ingestion and gut peristalsis in Platynereis postlarvae. MIP is expressed in enteroendocrine cells of the digestive system suggesting that following larval settlement, feeding may be initiated by a direct sensory-neurosecretory mechanism. This is similar to the mechanism by which MIP induces larval settlement. The pleiotropic roles of MIP may thus have evolved by redeploying the same signaling mechanism in different aspects of a life-cycle transition.Electronic supplementary materialThe online version of this article (doi:10.1186/s12983-014-0093-6) contains supplementary material, which is available to authorized users.
Highlights
During larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology
Platynereis myoinhibitory peptide (MIP) is expressed in the brain and gut of postlarvae, juveniles and adults Expression profiling of the MIP precursor gene by RNA in situ hybridization showed that MIP is expressed during both larval and postlarval development and continues to be expressed after cephalic metamorphosis, in the early adult stage (Figure 1A-C, G-H; Additional file 1)
MIP treatment has a myostimulatory effect on the digestive system of Platynereis postlarvae In order to understand how the morpholino knockdown of MIP resulted in reduced larval feeding, we examined the effect of synthetic MIP treatment on postlarvae, focusing on the digestive system
Summary
During larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology. This change between life-cycle stages is often associated with a change in diet or a transition between a non-feeding and a feeding form. The marine annelid Platynereis dumerilii has a complex life cycle with a pelagic non-feeding larval stage and a benthic feeding postlarval stage, linked by the process of settlement. Marine invertebrate larval settlement is often coupled to the initiation of feeding or a change in diet [2] These behavioral, physiological and morphological changes have to be tightly coordinated for the successful transition to a benthic life style. In which the first pair of parapodia are transformed into a second pair of tentacular cirri
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