Larvae of a marine gastropod and a marine bivalve share common gene expression signatures during metamorphic competence

Abstract

Many aquatic invertebrates undergo an indirect development, a biphasic life cycle which encompasses the transformation of free-swimming larvae into benthic juveniles via settlement and metamorphosis. During this transition, metamorphic competence is a crucial developmental stage that allows larvae to swim and feed in the planktonic realm while retaining the ability to settle and metamorphose in response to environmental cues. Although there have been substantial efforts to decipher the molecular mechanisms underlying this event in several molluscan species, the conserved biological pathways that are crucial to enable this transition across species are not well understood. Here, we performed a comparative analysis of the developmental transcriptomes between bivalve Crassostrea gigas and gastropod Rapana venosa. We particularly explored the common gene expression signatures that may underlie their larval competence. We showed that, although the developmental transcriptomes differed remarkably between C. gigas and R. venosa, they likely shared a plethora of genes (n = 690) that exhibited similar expression signatures during their larval competence. Gene Ontology enrichment and expression analyses further indicated that competent larvae of both species exhibited up-regulation of pathways associated with response to stimuli, metal ion binding and transport, and neuronal development, but showed down-regulation of pathways that were mainly involved in cilium assembly and organ development. Using oyster and whelk as models, our study suggests that regulation of these conserved pathways is crucial for their subsequent settlement and metamorphosis and may represent a universal mechanism that enables the pelagic-to-benthic transition in a broader range of marine invertebrates.