Adaptation of plasticity to projected maximum temperatures and across climatically defined bioregions

Significance

Adaptation to climate change is expected to be influenced by thermal conditions experienced by species during their evolutionary history. We studied plastic capacity as a target of climatic selection, hypothesizing that populations that evolved under warmer climates have greater plastic adaptive resilience to climate change. This was tested experimentally by comparing upper thermal tolerance and gene expression in fish populations from desert, temperate, and subtropical regions of Australia. Divergent adaptive plastic responses to future climates were found across different bioregions, including in key heat stress genes. The greatest adaptive resilience was shown by the subtropical ecotype, followed by the desert and temperate ecotypes. These results have implications for large-scale assessments of climate impacts and for predictions of species distribution changes.

Abstract

Resilience to environmental stressors due to climate warming is influenced by local adaptations, including plastic responses. The recent literature has focused on genomic signatures of climatic adaptation, but little is known about how plastic capacity may be influenced by biogeographic and evolutionary processes. We investigate phenotypic plasticity as a target of climatic selection, hypothesizing that lineages that evolved in warmer climates will exhibit greater plastic adaptive resilience to upper thermal stress. This was experimentally tested by comparing transcriptomic responses within and among temperate, subtropical, and desert ecotypes of Australian rainbowfish subjected to contemporary and projected summer temperatures. Critical thermal maxima were estimated, and ecological niches delineated using bioclimatic modeling. A comparative phylogenetic expression variance and evolution model was used to assess plastic and evolved changes in gene expression. Although 82% of all expressed genes were found in the three ecotypes, they shared expression patterns in only 5 out of 236 genes that responded to the climate change experiment. A total of 532 genes showed signals of adaptive (i.e., genetic-based) plasticity due to ecotype-specific directional selection, and 23 of those responded to projected summer temperatures. Network analyses demonstrated centrality of these genes in thermal response pathways. The greatest adaptive resilience to upper thermal stress was shown by the subtropical ecotype, followed by the desert and temperate ecotypes. Our findings indicate that vulnerability to climate change will be highly influenced by biogeographic factors, emphasizing the value of integrative assessments of climatic adaptive traits for accurate estimation of population and ecosystem responses.