Contrasting temperature-induced gene network rewiring and isoform switching underlie relative thermal tolerance of coral species

Organismal thermal tolerance will shape future coral reef diversity and abundance, as ocean warming drives extensive bleaching and mortality through increasingly frequent marine heatwaves. Coral thermal tolerance varies markedly among species, reflecting differences in physiology underpinned by molecular regulatory mechanisms. Gene expression plasticity enables transcriptional adjustments to environmental stress, while alternative splicing and isoform switching further expand molecular adaptability by altering transcript diversity and abundance. Because genes function within combinatorial networks, changes in these network members and in the identity of highly influential hub genes can reveal higher-order biological reorganization under stress. Yet, the contribution of isoform switching to gene network dynamics remains unknown in corals. Here we integrate physiology, gene network topology, hub genes dynamics, and isoform switching across three Hawaiian corals, Porites compressa, Montipora capitata, and Pocillopora acuta, to identify molecular processes shaping thermal performance. We show that the interplay between expression plasticity, hub gene rearrangement, and isoform switching drives species-specific thermal tolerance. Network analysis uncovered extensive rewiring and temperature-responsive hub genes turnover regulated by switches in isoform usage. The most thermally tolerant species, P. compressa, shows high energy reserves, stable constitutive gene expression and continuous isoform adjustments across temperatures, while fine-tuning thermal response through dedicated hub genes. In contrast, the most thermally sensitive species, P. acuta, shows lowest energy reserves, with broad transcriptomic shifts and isoform switching controlling the reorganization of network leadership at high temperatures. Together, these findings identify isoform switching as a newly recognized regulatory mechanism contributing to coral thermal resilience and species persistence in warming oceans.