Evolutionary innovation within conserved gene regulatory networks underlying biomineralized skeletons in Bilateria

Abstract

Biomineralized skeletons have evolved convergently across animals, yet exhibit remarkable diversity in structure and development. However, the evolutionary origins of gene regulatory networks underlying biomineralized skeletons remains elusive. Here, we report comprehensive developmental profiling of transcriptomic and chromatin dynamics in a bivalve mollusc, Crassostrea nippona. We provide evidence for a biphasic regulatory program orchestrating larval and adult shell formation, involving the coordinated activity of ancient transcription factors and dynamic chromatin remodeling. Comparative analyses suggest a conserved developmental toolkit was co-opted for larval exoskeleton formation in the common lophotrochozoan ancestor. In contrast, limited regulatory conservation was observed between lophotrochozoans and echinoderms with regards to the formation of biomineralized skeletons, despite both relying on a heterochronic activation of ancestral regulators. Together, our findings support a hierarchical model where dynamic chromatin decouples rapidly evolving effectors from deeply conserved regulators, allowing modular innovations within conserved gene regulatory networks. This study highlights how epigenetic dynamics bridge evolutionary conservation and novelty, offering a framework for understanding the independent evolution of biomineralization across Bilateria through combinatorial regulatory evolution.