Adaptation of plasticity to predicted climates in Australian rainbowfishes (Melanotaenia) across climatically defined bioregions

Abstract

Resilience to environmental stressors due to climate warming is influenced by local adaptations, including the capacity for plastic responses. The recent literature has focussed on genomic signatures of climatic adaptation, however little work has been done to address how plastic capacity may be influenced by biogeographic history and evolutionary processes. Here, we investigate phenotypic plasticity as a target of climatic selection, hypothesising that lineages that evolved under warmer climate will exhibit greater plastic adaptive resilience to thermal stress. This was tested using common garden experiments to compare gene expression regulation within and among a temperate, a subtropical and a desert ecotype of Australian rainbowfish. Individuals from each ecotype were subjected to contemporary and projected summer thermal conditions for 2070, and their global patterns of gene expression were characterized using liver transcriptomes. Critical thermal maximums were also determined for each ecotype to assess thermal tolerance. A comparative phylogenetic expression variance and evolution model framework was used to assess plastic and evolved changes in gene expression. Similar changes in both the direction and the magnitude of expressed genes were found within ecotypes. Although most expressed genes were identified in all ecotypes, 532 genes were identified as candidates subject to ecotype-specific directional selection. Twenty-three of those genes showed signal of adaptive (i.e. genetic-based) plastic response to future increases in temperature. Network analyses demonstrated centrality of these genes in thermal response pathways, along with several highly conserved hub genes thought to be integral for heat stress responses. The greatest adaptive resilience to warming 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, and we stress the need for integrative assessments of climatic adaptive traits for accurate estimations of population and ecosystem responses.