From tropical rainforests to scorching deserts: biogeography shapes climate-change plasticity in Australian rainbowfishes

Thermal tolerance and the plasticity of regulatory mechanisms are likely to influence biodiversity persistence under global warming. Continental-scale assessments of physiological resilience and gene expression plasticity within a closely related clade are rare, yet they could reveal how bioregional climatic history shapes vulnerability to climate warming. We used a comparative approach across five climatic ecotypes of Australian rainbowfishes (tropical rainforest, tropical savannah, subtropical, desert, and temperate) to investigate variation in thermal tolerance and gene expression plasticity in response to warming. We reconstructed phylogenetic relationships among these ecotypes, estimated their ecological niches and environmental warming tolerance, and experimentally measured CTMAX and global gene expression responses to a projected summer heat event. Closely related ecotypes showed divergent bioclimatic niches, contrasting sensitivities to warming, and extensive but idiosyncratic expression responses to heat stress. Plastic responses to warming, including in key heat stress genes, were positively associated with thermal tolerance across ecotypes. The tropical savannah and subtropical ecotypes, both from environmentally variable bioregions, showed extensive transcriptional responses to warming and high thermal tolerance. The desert ecotype was intermediate for both traits, whereas the temperate ecotype showed the most limited transcriptional response and lowest thermal tolerance. In contrast, the tropical rainforest ecotype showed limited plasticity, potentially reflecting local adaptation to milder, more stable conditions and more specialised thermal responses. Our findings support the hypothesis that bioregional climatic history shapes broad patterns of climate resilience, including thermal tolerance and transcriptional plasticity, and may influence which combinations of traits are favoured under future climates.