Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

Abstract

Life-cycle transitions connecting larval and juvenile stages in metazoans are orchestrated by neuroendocrine signals including neuropeptides and hormones. In marine invertebrate life cycles, which often consist of planktonic larval and benthic adult stages, settlement of the free-swimming larva to the sea floor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory-neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not yet understood. Here we show that myoinhibitory peptide (MIP)/allatostatin-B, a pleiotropic neuropeptide widespread among protostomes, regulates larval settlement in the marine annelid Platynereis dumerilii. MIP is expressed in chemosensory-neurosecretory cells in the annelid larval apical organ and signals to its receptor, an orthologue of the Drosophila sex peptide receptor, expressed in neighboring apical organ cells. We demonstrate by morpholino-mediated knockdown that MIP signals via this receptor to trigger settlement. These results reveal a role for a conserved MIP receptor-ligand pair in regulating marine annelid settlement.M etazoan life cycles show great diversity in larval, juvenile, and adult forms, as well as in the timing and ecological context of the transitions between these forms. In many animal species, neuroendocrine signals involving hormones and neuropeptides regulate life cycle transitions (1-3). Environmental cues are often important instructors of the timing of life cycle transitions (4), and can affect behavioral, physiological, or morphological change via neuroendocrine signaling (5).Marine invertebrate larval settlement is a prime example of the strong link between environmental cues and the timing of life-cycle transitions. Marine invertebrate life cycles often consist of a free-swimming (i.e., pelagic) larval stage that settles to the ocean floor and metamorphoses into a bottom-dwelling (i.e., benthic) juvenile (6-8). In many invertebrate larvae, a pelagicbenthic transition is induced by chemical cues from the environment (9, 10). Larval settlement commonly includes the cessation of swimming and the appearance of substrate exploratory behavior, including crawling on or attachment to the substrate (11-14). In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17-20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22-24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.Here, we identify a conserved myoinhibitory peptide (MIP)/ allatostatin-B receptor-ligand pair as a regulator of larval settlement behavior in the marine polychaete annelid Platynereis dumerilii. MIPs are pleiotro...

Global view of the evolution and diversity of metazoan neuropeptide signaling

“…In cnidarians, external stimuli are directly translated into neuroendocrine signals by chemosensory-neurosecretory cells releasing small amidated peptides to regulate growth and metamorphosis (72). Wamides may have been ancestrally involved in mediating life-cycle transitions triggered by chemosensory cues (73). RFamides may have ancient roles in muscle control (74), ciliary locomotion (27,62), and food intake (75).…”

An immunocytochemical window into the development of Platynereis massiliensis (Annelida, Nereididae)

“…Solely, the sparse ciliary distribution of these embryos can be interpreted as remnants of the prototroch. Interestingly, in P. dumerilii larval settlement is regulated by a myoinhibitory neuropeptide (MIP) receptor-ligand pair that is expressed in the larval apical organ and neighboring cells (Conzelmann et al, 2013).…”

Myoinhibitory peptide regulates feeding in the marine annelidPlatynereis

“…The marine annelid Platynereis dumerilii has recently proven to be a useful marine invertebrate model for studying the molecular details of marine larval behavior, including settlement [9][10][11][12]. Platynereis has a biphasic life cycle with free-swimming, non-feeding larval (trochophore and nectochaete) stages and bottom-dwelling, feeding postlarval, juvenile and adult stages [13].…”

“…Recently, we identified myoinhibitory peptide (MIP) as an inducer of rapid larval settlement behavior in Platynereis [11]. MIP is expressed in anterior chemosensoryneurosecretory neurons of the larva.…”