Abstract
The crown-of-thorns starfish (COTS) has raised widespread concern due to its population outbreaks, which can inflict extensive damage on coral reefs. Although hypotheses regarding the causes of its outbreaks remain contentious, the early life-history stages are widely considered critical for understanding outbreak dynamics of this coral reef pest. Yet, a lack of fundamental insight regarding the molecular components that regulate physiological processes has impeded the development of novel biocontrol strategies. Therefore, in this study we profiled COTS gene expression (transcriptomics) and metabolite dynamics (metabolomics) across 7 early developmental stages, from fertilized egg to late-brachiolaria. Through sequential stage-pair comparisons, we identified stage-specific activation of complex organismal systems, including the marked up-regulation of digestive enzymes (e.g., sucrase-isomaltase and lactase) at the bipinnaria stage. Also, there was sustained up-regulation of opsin and olfactory receptor genes until late-brachiolaria, suggesting an increased ability to perceive their environment. Combining weighted gene co-expression network analysis and trend analysis, we pinpointed several metabolites, such as all-trans-4-ketoretinoic acid and 3,3'-diiodo-l-thyronine, which may regulate the metamorphosis of COTS larvae into benthic juveniles. Furthermore, transcriptome-metabolome association analysis revealed that the pyrimidine metabolism pathway was essential for planktonic larval development. Our findings delineate transcriptional regulation strategies and characterize the metabolome landscape across COTS early developmental stages, providing a foundational resource for developmental biology studies of this destructive coral reef pest.