Energetic misfires: Hybridization drives transgressive expression in metabolic pathways in thermally divergent Icelandic stickleback

Climate change is causing rapid changes to freshwater environments, driving selection for phenotypes that can cope with altered thermal conditions, while also changing developmental environments. This may promote local adaptation, migration to new habitats, and/or phenotypic plasticity. Climate change may also increase hybridization rates between locally adapted phenotypes, as populations migrate and spatially mix in new ways. Consequently, these conditions may facilitate the production of variation, including both adaptive and maladaptive outcomes. To examine this, we leveraged threespine stickleback (Gasterosteus aculeatus) that have locally adapted to either geothermally warmed or ambient environments in Iceland. We tested the effects of hybridization between thermal ecotypes on gene expression using a common garden experiment, where pure-strain ecotypes and their hybrids were reared under 12 and 18 degrees. We performed RNA-seq on brain and liver to assess 1) ecotype divergence, 2) plasticity, and 3) the effects of hybridization and inheritance patterns. We identified a low degree of expression divergence between locally adapted ecotypes, despite a high degree of plasticity across rearing environments. Hybrid ecotypes were highly divergent from both geothermal and ambient ecotypes and exhibited transgressive expression under both rearing temperatures. Transgressive expression disrupted gene networks extensively, with broader effects at 18 degrees than at 12 degrees, primarily associated with metabolism and mitochondrial function. Hybridization between locally adapted thermal ecotypes appears to largely disrupt genes associated with energy balance and metabolic function. While demonstrating mechanisms underlying the rapid evolution of reproductive isolation, these findings also provide insights for how populations may cope or fail within a warming world.