Adaptation of Plasticity to Projected Maximum Temperatures and Across Climatically Defined Bioregions
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Adaptation of plasticity to projected maximum temperatures and across climatically defined bioregions Jonathan Sandoval-Castilloa, Katie Gatesa, Chris J. Brauera, Steve Smitha,b, Louis Bernatchezc, and Luciano B. Beheregaraya,1 aMolecular Ecology Lab, Flinders University, Bedford Park, SA 5042, Australia; bKonrad Lorenz Institute of Ethology, University of Veterinary Medicine, 1160 Vienna, Austria; and cInstitut de Biologie Intégrative et des Systèmes, Université Laval, Québec, QC G1V 0A6, Canada Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved June 2, 2020 (received for review December 2, 2019) Resilience to environmental stressors due to climate warming is the environment on allelic expression, as well as changes in in- influenced by local adaptations, including plastic responses. The teractions among loci (14, 15). Here, we focus on plasticity as the recent literature has focused on genomic signatures of climatic ability or tendency of an individual to up- or down-regulate genes adaptation, but little is known about how plastic capacity may be in response to the environment and, particularly, on how plas- influenced by biogeographic and evolutionary processes. We ticity might provide adaptive resilience to climate change. For investigate phenotypic plasticity as a target of climatic selection, many genes, this occurs primarily at the level of transcription, hypothesizing that lineages that evolved in warmer climates will and a complexity of responses (i.e., adaptive, maladaptive, or exhibit greater plastic adaptive resilience to upper thermal stress. neutral) has been documented (16, 17). For instance, plasticity This was experimentally tested by comparing transcriptomic can act as a buffer against environmental pressures (16, 18) and responses within and among temperate, subtropical, and desert can be a target of selection if genotypes differ in environmental ecotypes of Australian rainbowfish subjected to contemporary sensitivity (19). Alternatively, initial plastic responses could be and projected summer temperatures. Critical thermal maxima nonadaptive under novel environmental conditions (20). In the were estimated, and ecological niches delineated using bioclimatic context of climate, gene expression can inform about the func- modeling. A comparative phylogenetic expression variance and tional pathways relevant for persistence under given conditions, EVOLUTION evolution model was used to assess plastic and evolved changes in as well as the likely targets of selection (11, 21). This is especially gene expression. Although 82% of all expressed genes were important where phenotypes of ecological relevance are not found in the three ecotypes, they shared expression patterns in obvious and may be difficult to distinguish using traditional ap- only 5 out of 236 genes that responded to the climate change proaches (22, 23). Relatively few studies have attempted to find experiment. A total of 532 genes showed signals of adaptive signals of selection acting on gene expression. Challenges include (i.e., genetic-based) plasticity due to ecotype-specific directional controlling for internal and external environmental variables selection, and 23 of those responded to projected summer tem- peratures. Network analyses demonstrated centrality of these genes in thermal response pathways. The greatest adaptive resil- Significance ience to upper thermal stress was shown by the subtropical eco- type, followed by the desert and temperate ecotypes. Our findings Adaptation to climate change is expected to be influenced by indicate that vulnerability to climate change will be highly influ- thermal conditions experienced by species during their evolu- enced by biogeographic factors, emphasizing the value of integra- tionary history. We studied plastic capacity as a target of cli- tive assessments of climatic adaptive traits for accurate estimation matic selection, hypothesizing that populations that evolved of population and ecosystem responses. under warmer climates have greater plastic adaptive resilience to climate change. This was tested experimentally by compar- climate change | ecological genomics | teleosts | thermal biology | climatic ing upper thermal tolerance and gene expression in fish pop- variability hypothesis ulations from desert, temperate, and subtropical regions of Australia. Divergent adaptive plastic responses to future cli- haracterizing mechanisms underpinning variation in ecolog- mates were found across different bioregions, including in key Cical adaptation can assist in identifying biogeographic pat- heat stress genes. The greatest adaptive resilience was shown terns of vulnerability and resilience to environmental change. by the subtropical ecotype, followed by the desert and tem- Climate change has promoted numerous range shifts and local perate ecotypes. These results have implications for large-scale extinctions due to exposure of populations to conditions outside assessments of climate impacts and for predictions of species their zones of tolerance (1–3). However, it is expected that some distribution changes. populations will be able to persist in situ if they are not already Author contributions: L.B. and L.B.B. designed research; J.S.-C., K.G., C.J.B., S.S., L.B., and living at the edge of their tolerance limits or if they are able to L.B.B. performed research; L.B.B. contributed new reagents/analytic tools; J.S.-C., C.J.B., acclimatize or adapt outside their current range of tolerance and S.S. analyzed data; and J.S.-C., K.G., and L.B.B. wrote the paper. – ’ (4 7). Species distributions are strongly influenced by thermal The authors declare no competing interest. conditions in their native climates; it is expected that tolerance This article is a PNAS Direct Submission. ranges and vulnerability to change will also be influenced by – This open access article is distributed under Creative Commons Attribution-NonCommercial- biogeographic factors (8 10). Exploring how molecular mecha- NoDerivatives License 4.0 (CC BY-NC-ND). nisms influence upper thermal resilience is an important step for Data deposition: The sequences for all the transcripts and ddRAD loci have been depos- inferring responses to a warming environment (11). While plastic ited to the Figshare repository, https://doi.org/10.6084/m9.figshare.12110991. regulation of gene expression is expected to play an important role in 1To whom correspondence may be addressed. Email: luciano.beheregaray@flinders. adaptation, the effects of selection on plasticity are poorly understood edu.au. and untangling them requires integrative approaches (12, 13). This article contains supporting information online at https://www.pnas.org/lookup/suppl/ Plasticity refers to a change in expressed phenotype as a doi:10.1073/pnas.1921124117/-/DCSupplemental. function of the environment and occurs through direct effects of www.pnas.org/cgi/doi/10.1073/pnas.1921124117 PNAS Latest Articles | 1of10 Downloaded by guest on September 30, 2021 influencing expression (24), as well as for the effect of genetic Results distance on the variation in transcription between lineages (25). Differential Gene Expression. Sequencing and de novo assemblies Climatically defined bioregions provide a scale at which en- produced transcriptomes with high percentages of gene com- vironmental variation drives meaningful differences in evolu- pleteness for the three rainbowfish ecotypes (SI Appendix, Fig. tionary and ecological processes (26, 27). The ability of S1 and Table S1). Of the 34,815 identified unigenes, 82% populations to persist in a warmer climate is predicted to vary (28,483) were present in all ecotypes (Fig. 3A). Comparison of geographically (6, 28–31), making climatic bioregions valuable gene expression profiles among ecotypes and between climate systems for comparative studies of adaptation. For instance, the change treatments identified 2,409 differentially expressed (DE) climatic variability hypothesis (CVH) predicts a positive re- unigenes. Expression profiles showed a strong phylogenetic lationship between breadth of thermal tolerance and the level of pattern (i.e., transcription responses are most highly correlated climatic variability experienced by organisms as latitude in- among individuals within ecotypes), followed by high correlation creases (32). Studies of climate change impacts are increasingly between experimental and control groups within each ecotype seeking to integrate spatial modeling (e.g., climatic envelopes) to (Fig. 3B; see also below). On the other hand, when gene ex- uncover associations between landscape features and evolu- pression was compared exclusively between climate change – tionary processes such as temperature adaptation (33 35). While treatments, 236 unigenes were identified (Fig. 3 C and D). Of a majority of species distribution models are primarily correla- these 236 unigenes responding plastically to climate change, 10 tive, there has been an urgent call for an increase in mechanistic were shared by at least two ecotypes, with only five shared re- ’ approaches for predicting species responses to climate change sponses among all three ecotypes (Fig. 3D). In contrast, unique – (36 39). Mechanistic approaches have the advantage of explaining plastic responses to the projected summer temperature were the underlying processes associated with observed trends, allowing observed for the temperate ecotype in 27 unigenes, the desert for findings to be interpreted more generally (40). ecotype in 84 unigenes, and the subtropical