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Rapid changes in gene expression can result in physiological plasticity that assists animals in coping with environmental stressors. Increased capacity for physiological plasticity may then facilitate adaptation to stressful habitats like urban heat islands or invasion into novel ranges. Currently, temperature stress is a leading threat to organisms, especially ectotherms. While exposure to changing temperatures is known to shift gene expression patterns in ectothermic animals, many studies are conducted after lengthy acclimation times. However, exposure to thermal stress in nature can occur rapidly. We assessed the capacity for gene expression plasticity in response to a brief exposure to extreme thermal stress in an urban, introduced species, the common wall lizard (Podarcis muralis). Lizards were ramped to their critical thermal maximum (CTmax) or minimum (CTmin) followed by rapid recovery. We used RNA-sequencing to compare the transcriptomes of lizards exposed to CTmax, CTmin, or control conditions using heart, liver, and large intestine tissue. Exposure to heat stress induced a much stronger gene expression response across tissues than cold exposure. In response to heat, there was systemic upregulation of heat shock proteins and stress response pathways. Heat also induced changes in transcription, translation, and metabolic processes but these effects were more tissue specific. Although fewer gene expression changes were observed in response to cold, some genes were upregulated that could be beneficial under cooling stress. Our data suggests gene expression plasticity could facilitate range expansion in this species, but more work is needed to assess the transcriptomic response to temperature stress in nature.
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Synergistic response to climate stressors in coral is associated with genotypic variation in baseline expression
As environments are rapidly reshaped due to climate change, phenotypic plasticity plays an important role in the ability of organisms to persist and is considered an especially important acclimatization mechanism for long-lived sessile organisms such as reef-building corals. Often, this ability of a single genotype to display multiple phenotypes depending on the environment is modulated by changes in gene expression, which can vary in response to environmental changes via two mechanisms: baseline expression and expression plasticity. We used transcriptome-wide expression profiling of eleven genotypes of common-gardenedAcropora cervicornisto explore genotypic variation in the expression response to thermal and acidification stress, both individually and in combination. We show that the combination of these two stressors elicits a synergistic gene expression response, and that both baseline expression and expression plasticity in response to stress show genotypic variation. Additionally, we demonstrate that frontloading of a large module of coexpressed genes is associated with greater retention of algal symbionts under combined stress. These results illustrate that variation in the gene expression response of individuals to climate change stressors can persist even when individuals have shared environmental histories, affecting their performance under future climate change scenarios.
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- Award ID(s):
- 1452538
- PAR ID:
- 10503481
- Publisher / Repository:
- Royal Society Publishing
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 291
- Issue:
- 2019
- ISSN:
- 0962-8452
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Phenotypic plasticity can play an important role in the ability of animals to tolerate environmental stress, but the nature and magnitude of plastic responses are often specific to the developmental timing of exposure. Here, we examine changes in gene expression in the diaphragm of highland deer mice (Peromyscus maniculatus) in response to hypoxia exposure at different stages of development. In highland deer mice, developmental plasticity in diaphragm function may mediate changes in several respiratory traits that influence aerobic metabolism and performance under hypoxia. We generated RNAseq data from diaphragm tissue of adult deer mice exposed to (1) life‐long hypoxia (before conception to adulthood), (2) post‐natal hypoxia (birth to adulthood), (3) adult hypoxia (6–8 weeks only during adulthood) or (4) normoxia. We found five suites of co‐regulated genes that are differentially expressed in response to hypoxia, but the patterns of differential expression depend on the developmental timing of exposure. We also identified four transcriptional modules that are associated with important respiratory traits. Many of the genes in these transcriptional modules bear signatures of altitude‐related selection, providing an indirect line of evidence that observed changes in gene expression may be adaptive in hypoxic environments. Our results demonstrate the importance of developmental stage in determining the phenotypic response to environmental stressors.more » « less
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Synopsis Ectothermic species in lowland tropical forests have evolved in historically stable climates, leading to the prediction that transcriptomic and phenotypic plasticity do not play major roles in their responses to changes in environmental temperature. However, these species are often thermoconformers and are therefore exposed to short-term temporal fluctuations in temperature. Hence, transcriptomic plasticity in tropical forest ectotherms might replace behavioral thermoregulation as a mechanism to buffer against thermal stress. In particular, upregulation of heat shock proteins can occur during thermal stress in a range of organisms. However, while many studies have explored gene expression plasticity in response to heat stress in model organisms, little is known about transcriptomic plasticity in the tropical, non-model species that will be the most impacted by climate change. We studied the effects of moderate and severe acute heat stress events in the Panamanian slender anole (Anolis apletophallus) to gain insight into a mechanism that might allow tropical ectotherms to withstand the heat waves that are likely to rise in frequency over the coming decades under anthropogenic climate change. We found that multiple genes were upregulated across several heat shock protein networks in three tissues, and the magnitude of the expression response was similar irrespective of whether heat stress was moderate or severe. Overall, our results indicate a potentially crucial role for heat shock protein networks in the ability of tropical ectotherms to resist the negative effects of rising temperatures.more » « less
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Gene expression can be highly plastic in response to environmental variation. However, we know little about how expression plasticity is shaped by natural selection and evolves in wild and domesticated species. We used genotypic selection analysis to characterize selection on drought-induced plasticity of over 7,500 leaf transcripts of 118 rice accessions (genotypes) from different environmental conditions grown in a field experiment. Gene expression plasticity was neutral for most gradually plastic transcripts, but transcripts with discrete patterns of expression showed stronger selection on expression plasticity. Whether plasticity was adaptive and co-gradient or maladaptive and counter-gradient varied among varietal groups. No transcripts that experienced selection for plasticity across environments showed selection against plasticity within environments, indicating a lack of evidence for costs of adaptive plasticity that may constrain its evolution. Selection on expression plasticity was influenced by degree of plasticity, transcript length and gene body methylation. We observed positive selection on plasticity of co-expression modules containing transcripts involved in photosynthesis, translation and responsiveness to abiotic stress. Taken together, these results indicate that patterns of selection on expression plasticity were context-dependent and likely associated with environmental conditions of varietal groups, but that the evolution of adaptive plasticity would likely not be constrained by opposing patterns of selection on plasticity within compared to across environments. These results offer a genome-wide view of patterns of selection and ecological constraints on gene expression plasticity and provide insights into the interplay between plastic and evolutionary responses to drought at the molecular level.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1098/rspb.2023.2447
