Abstract
BackgroundA metamorphic life-history is present in the majority of animal phyla. This developmental mode is particularly prominent among marine invertebrates with a bentho-planktonic life cycle, where a pelagic larval form transforms into a benthic adult. Metamorphic competence (the stage at which a larva is capable to undergo the metamorphic transformation and settlement) is an important adaptation both ecologically and physiologically. The competence period maintains the larval state until suitable settlement sites are encountered, at which point the larvae settle in response to settlement cues. The mechanistic basis for metamorphosis (the morphogenetic transition from a larva to a juvenile including settlement), i.e. the molecular and cellular processes underlying metamorphosis in marine invertebrate species, is poorly understood. Histamine (HA), a neurotransmitter used for various physiological and developmental functions among animals, has a critical role in sea urchin fertilization and in the induction of metamorphosis. Here we test the premise that HA functions as a developmental modulator of metamorphic competence in the sea urchin Strongylocentrotus purpuratus.ResultsOur results provide strong evidence that HA leads to the acquisition of metamorphic competence in S. purpuratus larvae. Pharmacological analysis of several HA receptor antagonists and an inhibitor of HA synthesis indicates a function of HA in metamorphic competence as well as programmed cell death (PCD) during arm retraction. Furthermore we identified an extensive network of histaminergic neurons in pre-metamorphic and metamorphically competent larvae. Analysis of this network throughout larval development indicates that the maturation of specific neuronal clusters correlates with the acquisition of metamorphic competence. Moreover, histamine receptor antagonist treatment leads to the induction of caspase mediated apoptosis in competent larvae.ConclusionsWe conclude that HA is a modulator of metamorphic competence in S. purpuratus development and hypothesize that HA may have played an important role in the evolution of settlement strategies in echinoids. Our findings provide novel insights into the evolution of HA signalling and its function in one of the most important and widespread life history transitions in the animal kingdom - metamorphosis.
Highlights
A metamorphic life-history is present in the majority of animal phyla
Pre-treatment of S. purpuratus larvae with histamine leads to attainment of metamorphic competence based on a settlement induction assay We used the settlement induction assay to test for metamorphic competence in S. purpuratus larvae
If larvae were pretreated with HA they settled at a higher rate upon exposure to settlement plates compared to larvae that were not pre-treated (23.3% ± 10.3, p = 0.05)
Summary
A metamorphic life-history is present in the majority of animal phyla. This developmental mode is prominent among marine invertebrates with a bentho-planktonic life cycle, where a pelagic larval form transforms into a benthic adult. Metamorphosis is a life history transition that is widespread in the animal kingdom and is abundantly present in marine invertebrate species [1,2] Metamorphoses in these groups are often characterized by a rapid transition from a planktonic larval form to a benthic adult form (settlement). Echinoids (sea urchins and sand dollars) have evolved a broad range of life history strategies including significant variations in reproductive and developmental modes (reviewed in [2]). Understanding such evolutionary patterns requires detailed insights into the mechanistic bases of these processes [8,9]. Developmental mechanisms regulating the acquisition of competence and the physiological, cellular, and molecular processes regulating the metamorphic transition have been understudied [8,9]
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