Recent progress narrowing the gaps between molecular biology, studies of larval settlement and metamorphosis, and field studies of recruitment of benthic invertebrates is discussed. Evidence is presented that the stringent and specific requirements of developmentally arrested larvae
for exogenous chemical inducers in many cases determine the site-specificity of settlement, metamorphosis and recruitment in the ocean environment. The complexity of recently revealed larval chemosensory mechanisms controlling metamorphosis in response to both substratum-associated and water-borne
chemical cues, and the sensitivity of these systems to regulation at multiple levels, confer on the larvae of some species a capacity for fine-scale discrimination of (and responsiveness to) chemical features of the environment that had not been anticipated a few years ago. Larval settlement
and metamorphosis in stringently cue-dependent species are not largely random events, as first had been widely thought, but instead are highly determined by chemosensory recognition of morphogenic and regulatory molecules in the environment. A new synthesis incorporating the role of these
mechanisms is required to better understand the ecology of recruitment and reproductive success in such species, and their evolution. A summary of what is known at the molecular level about the control of settlement and metamorphosis in Phragmalopoma californica (polychaete annelid)
and Haliolis rufescens (gastropod mollusc) larvae, and of the multiple, independent lines of evidence by which it is known, is presented. Recent evidence casting doubt on the relevance of fatty acids (known effectors of cyclic AMP in many systems) as environmentally important inducers
of P. californica is summarized. New developments in the identification, partial purification, and analyses (both in vitro and in vivo) of the larval Haliolis receptors and signal transducers responsible for the recognition of environmentally deployed morphogens and regulatory
molecules, and studies of their roles in the control of settlement and metamorphosis, are reviewed. Thus far, 10 of the 13 separate receptor-dependent and signal-transduction reactions and pathways that were first identified or deduced from experiments performed in vivo have now been verified
in vitro, in analyses conducted with purified epithelia cilia containing populations of chemosensory cilia from the larvae. These recent in vitro observations thus substantially confirm the mechanisms controlling metamorphosis that had been suggested from experiments in vivo. At the molecular
and cellular levels, the receptors and signal transducers that control metamorphosis are proving to be structually, functionally, and evolutionarily closely related to receptors and transducers that control developmental, sensory, neuronal and hormonal processes in numerous other systems.
Information learned from analyses of these components and their mechanisms of action in marine invertebrate larvae thus should be widely applicable to the understanding of developmental and sensory processes in other animals. The need for a coordinated genetic and molecular dissection of the
complex processes controlling the differential activation of gene expression and development in marine invertebrate larvae in response to environmental morphogens, in experimentally tractable systems, is discussed.
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