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

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.

Keywords: climate change; climatic variability hypothesis; ecological genomics; teleosts; thermal biology.

Fig. 1.

(A) Map of Australia showing spatially and taxonomically validated records that depict the range of the three Melanotaenia ecotypes. The black circles show sampling localities for the transcriptomic and physiological experiments. (B) Maximum-likelihood tree depicting evolutionary relationships among 36 individuals of the three ecotypes based on ddRAD sequences of 1,799 loci and 156,581 bp. Numbers above nodes denote bootstrap support values. (C) Ecotype niche model based on 1,279 unique distribution records and nine bioclimatic variables generated in MaxEnt 3.4.1. Color tone indicates habitat suitability of each ecotype. (D) Physiological sensitivity of ecotypes across their ranges estimated by the warming tolerance quantity (41). Modern days are based on monthly average maximum temperature (BIOCLIM 2010 to 2018 data) and climatic projections are based on a global climate model (BCC-CSM2-MR) and on three shared socioeconomic pathways (SSPs) (mild, SSP126; moderate, SSP245; severe, SSP585).

Fig. 2.

Experimental design and pipeline of the comparative transcriptomic section. Wild-caught individuals from each Melanotaenia ecotype (subtropical, temperate, and desert) were subjected to control (21 °C) and experimental (33 °C) treatments. Their transcriptomes were assembled de novo. Expression profiles of 34,815 unigenes were used to identify 2,409 differentially expressed (DE) genes in all pairwise comparisons (blue shading, 15 comparisons), and 236 genes DE between temperature treatments for the same ecotype (orange shading, three comparisons). In parallel, an expression variance and evolution (EVE) model was used to identify genes for which expression plasticity is under divergent selection. Under a neutral model, the ratio of the expression variance between vs. within lineages (i.e., ecotypes) is the same for all genes, compared to a higher relative ratio for genes under divergent selection. This resulted in 532 EVE candidates for divergent selection on expression between ecotypes. Twenty-three genes (overlapping gray and orange area) that were DE between temperature treatments for the same ecotype and also identified by EVE were considered candidates for adaptation to projected upper thermal stress.

Fig. 3.

(A) Venn diagram of unigenes identified in each ecotype of Melanotaenia as well as shared among ecotypes (based on a total of 34,815 unigenes). (B) Heatmap summarizing correlation among ecotypes in log₂ gene expression profiles. This analysis was based on 2,409 DE transcripts. The colored bars under the sample dendrograms represent the climate change experimental (Exp) and control (Cont) groups. (C) Heatmap summarizing correlation between treatments (control vs. experiment) in log₂ gene expression profiles. This analysis was based on 236 DE unigenes identified between control and experiment samples. Colored bars under the sample dendrograms represent the ecotypes, with climate change experimental groups represented by dark color variation and control groups represented by light color variation. (D) Venn diagram of DE unigenes shared between ecotypes.

Fig. 4.

(A) Hierarchical clusters of 23 transcripts identified as candidates for divergent selection on expression level and also showing significant differential expression between control and experiment. Color bars indicate the ecotype of the samples. DesCont, desert control (20 °C); DesExp, desert experimental (33 °C); SubCont, subtropical control (20 °C); SubExp, subtropical experimental (33 °C); TemCont, temperate control (20 °C); TemExp, temperate experimental (33 °C). (B) Protein interaction network containing 137 heat stress-associated proteins linked via 1,114 interactions. Size of node is proportional to its centrality in the network, color of node indicates the relative number of interactions it is directly involved in (blue, lower, to red, higher number of interactions), and both color and size of the node indicate relative importance of the protein in Melanotaenia heat stress response.

Fig. 5.

Association between CT_MAX and number of genes differentially expressed in response to projected climate in three ecotypes of Melanotaenia (r = 0.998). The box plots display the upper and lower quartiles, whiskers represent 95th and 5th percentiles, and their intersections represent the median.