Cosmopolitan gene families with known functions are hotspots for the evolution of novel genes in stony corals

Climate change has accelerated research on biodiverse coral reef ecosystems. However, this area of investigation is limited by our understanding of the biology of these organisms, with many of the genes identified as important for stress response in corals being "dark", that is, with no ascribable biological function. To aid reverse genetic efforts, and help explore dark gene evolution in this lineage, we analyzed available genomic and transcriptomic data from corals with the goal of identifying well conserved (often lineage specific) dark gene families and interrogating their putative roles in coral biology using available multi-omics data and bioinformatic approaches. Many of the well conserved dark gene families are stress responsive, enriched in specific cell types, or have predicted 3D protein structures with significant similarity to known proteins that may be adaptive in corals. We demonstrate that dark genes form cosmopolitan (broadly shared) families which originated via bursts of lineage specific duplication, often involving genes with known functions. Analysis of single cell gene expression data suggests that dark gene provenance may have precipitated or been concomitant with the origin of novel coral functions such as biomineralization. Our results open a new window into coral evolution that integrates knowledge from known and dark genes to elucidate how these species achieved their remarkable success in diverse marine environments. The dark gene families we identified also provide a significant resource for future studies into the role of novel genes in coral biology and adaptation to climate change.