Rethinking competence in marine life cycles: ontogenetic changes in the settlement response of sand dollar larvae exposed to turbulence

Abstract

Complex life cycles have evolved independently numerous times in marine animals as well as in disparate algae. Such life histories typically involve a dispersive immature stage followed by settlement and metamorphosis to an adult stage on the sea floor. One commonality among animals exhibiting transitions of this type is that their larvae pass through a ‘precompetent’ period in which they do not respond to localized settlement cues, before entering a ‘competent’ period, during which cues can induce settlement. Despite the widespread existence of these two phases, relatively little is known about how larvae transition between them. Moreover, recent studies have blurred the distinction between the phases by demonstrating that fluid turbulence can spark precocious activation of competence. Here, we further investigate this phenomenon by exploring how larval interactions with turbulence change across ontogeny, focusing on offspring of the sand dollar Dendraster excentricus (Eschscholtz). Our data indicate that larvae exhibit increased responsiveness to turbulence as they get older. We also demonstrate a likely cost to precocious competence: the resulting juveniles are smaller. Based upon these findings, we outline a new, testable conception of competence that has the potential to reshape our understanding of larval dispersal and connectivity among marine populations.

Interdependent photo- and chemosensory systems regulate larval settlement in a marine sponge

“…However, we find that constant light prevents larval settlement, demonstrating deep interdependencies between photo-and chemosensory systems. Our transcriptome data also provide the first molecular evidence to support a recent hypothesis that active inhibition of inducer-signal transduction prevents settlement until such time as larvae detect a physical cue from the environment (8). We hypothesise that the photosensory cryptochrome and chemosensory GPCRs may both converge on the NO-cGMP pathway to regulate the pelago-benthic transition in A. queenslandica, via mechanisms as yet undiscovered.…”

“…We hypothesise that the photosensory cryptochrome and chemosensory GPCRs may both converge on the NO-cGMP pathway to regulate the pelago-benthic transition in A. queenslandica, via mechanisms as yet undiscovered. The results presented here, for this sponge, phylogenetically extend the importance of interdependent physical and biochemical cues for the pelago-benthic transition far beyond the echinoderms (7,8) to one of the earliestbranching phyletic animal lineages. In doing so, this study raises the possibility that the requirement of multiple, interdependent sensory systems for regulating larval settlement can be traced back to the last common animal ancestor.…”

“…Competence has long been hypothesised to be acquired upon the accumulation of a threshold concentration of chemosensory G-protein coupled receptors (GPCRs) (6). More recently, it has also been suggested that the acquisisiton of competence can be accelerated by an environmental physical cue (7,8), but the underlying molecular mechanisms remain to be explored. Here, we combine behavioural and molecular assays to explore, for the first time, how responses to physical and biochemical cues are integrated during larval ontogeny, using a representative of an early-branching animal lineage, the demosponge Amphimedon queenslandica.…”

A microbial perspective on the life‐history evolution of marine invertebrate larvae: If, where and when to feed

“…The sensory systems of larvae from disparate phyla, for example, use physical and chemical features of the sea spanning several orders of magnitude in spatial scale, such as sound, turbulence and chemical cues, for navigation (Fuchs, Gerbi, Hunter, Christman, & Diez, ; Gaylord, Hodin, & Ferner, ; Hodin, Ferner, Heyland, & Gaylord, ; Hodin, Ferner, Ng, Lowe, & Gaylord, ; Lillis, Bohnenstiehl, & Eggleston, ; Stanley, Radford, & Jeffs, ). Some sea urchin larvae (e.g.…”

An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge

“…Settlement and metamorphosis typically requires that the larva first obtains “competence” to be able to detect and respond to a local inductive environmental cue45. Acquisition of competence may require that the larva first encounters a broad-scale environmental condition indicative of a generally appropriate habitat67. A competent larva in the presence of an appropriate local inductive cue will generally settle and initiate metamorphosis.…”