Carry-over effect of larval settlement cue on postlarval gene expression in the marine gastropod Haliotis asinina

The drastic shift from pelagic larvae to benthic adult form that occurs during marine invertebrate metamorphosis is often induced by intimate interactions between settling larvae and their benthic environment. Larval experience prior to and during metamorphosis can significantly affect adult fitness, but it is presently unknown whether the exact nature of the inductive cue is an experience that matters, or by what mechanism such carry-over effects are mediated. Here we test for carry-over effects of the specific nature of inductive cues on gene expression in metamorphosing postlarvae of the tropical abalone, Haliotis asinina. Postlarvae induced by three different species of coralline algae all successfully undergo metamorphosis, yet the expression profiles of 11 of 17 metamorphosis-related genes differ according to which species of algae the larvae settled upon. Significantly, several genes continue to be differentially expressed for at least 40 h after removal of the algae from the postlarvae, clearly demonstrating a carry-over effect of inductive cue on gene expression. We observe a carryover effect in several genes with varying functions and spatial expression patterns, indicating that each algal species impacts global gene expression in a unique manner. These data unexpectedly reveal that transcriptional modulation of metamorphosis-related genes is contingent upon the precise composition of the benthic microenvironment experienced directly at induction of settlement, and highlight transcription as a mechanism that can mediate between larval and postlarval experiences. For new recruits into an abalone population, metamorphosis clearly does not represent a new transcriptional beginning.