Does local adaptation influence thermal responses in red coral populations across depth gradients? Transcriptomic insights for effective conservation.

Abstract

Marine heatwaves (MHWs) pose significant threats to marine biodiversity, including Mediterranean octocorals. Using a common garden experiment, we test whether differential transcriptomic responses to thermal stress between shallow and mesophotic populations of Corallium rubrum are shaped by their adaptation to the local environment, i.e. local adaptation. Six individuals from one shallow (15m) and one mesophotic (48m) population were exposed to control (18{degrees}C) and thermal stress (25{degrees}C) treatments, with samples collected at day 0 (T0), day 5 (T5), and day 10 (T10) for RNA sequencing (N=36). We revealed 1,957 differentially expressed genes (DEGs) in response to heat stress. Mild transcriptomic responses were observed in the shallow population (441 DEGs) characterized by heat shock proteins (HSPs) and developmental regulation. Conversely, a stronger and extensive response was observed in the mesophotic population with more than twice as many DEGs (1,081), predominantly associated with enhanced stress and wound healing mechanisms. Temporal transcriptional shifts were larger between T5 to T10 in the mesophotic population (1,497 vs 241), while more stable in the shallow (265 vs 271). Additionally, 172 DEGs, including HSPs, apoptosis and collagen, were found in the shallow population under control conditions, indicating transcriptional frontloading. The contrasting thermal stress responses between populations suggest distinct adaptative strategies potentially driven by local adaptation. These insights challenge the deep refugia hypothesis that considered mesophotic populations as potential sources for recolonization and active restoration of shallow populations threatened by MHWs. Our results support the need to integrate population-specific adaptive responses into conservation and restoration strategies for C. rubrum.