Organisms must respond to environmental cues to maintain homeostasis, with gene expressiondriving phenotypic variation. Variation in gene expression response to environmental stress varies across individuals, populations, and species and can determine tolerance to stressors. Understanding links between gene expression and tolerance is especially urgent in species vulnerable to climate change, such as reef-building corals. Acropora, the largest genus of corals, are ecologically significant, as reefs support marine biodiversity and human communities, yet are particularly vulnerable to climate-induced warming. Previous research linked gene expression variation to thermal tolerance, making Acropora an ideal system for exploring two fundamental questions, which I investigate in this dissertation: 1) What epigenetic mechanisms explain variation in gene expression at the individual level? and 2) How does the evolution of gene expression responses affect thermal tolerance across species?
In Chapter 1, I investigated the role of the epigenetic mechanism, DNA methylation, in driving gene expression changes coupled with enhanced thermal tolerance. In A. nana, individuals exhibiting thermal tolerance plasticity, or thermal acclimation, also have a reduced gene expression response to heat stress, a form of gene expression plasticity. DNA methylation is a chemical modification of DNA associated with overall mean gene expression and gene expression variability in invertebrates. I integrated RNA-seq and WGBS data to test the hypothesis that the heat stress genes with reduced expression responses to heat stress in acclimated individuals undergo a shift in DNA methylation throughout the thermal acclimation period. I found no relationship between the change in the heat-stress gene expression response in acclimated individuals and changes in DNA methylation following thermal acclimation. This result is likely due to the complexities of molecular interactions of DNA methylation with other gene expression regulators.
In Chapter 2, I explored the role of chromatin accessibility in the gene expression response to heat stress using the species A. millepora. Chromatin accessibility is unexplored in reef-building coral species but is an epigenetic mechanism that plays a role in higher-level gene expression regulation in other species. I performed 3'TagSeq on samples subject to a heat stress assay to evaluate the gene
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expression response to heat stress. In parallel, I performed ATAC-seq on samples from ambient conditions (i.e., no stress treatment) to investigate baseline regions of open chromatin regions in A. millepora. By integrating these two data sets, I found a relationship between chromatin accessibility and gene expression and gene expression variation. Further, open chromatin promoters play a small but significant role in promoting a rapid gene expression response to heat stress.
In Chapter 3, I investigated the evolution of thermal tolerance and gene expression responses across eight Acropora species. Gene expression responses to heat stress are reduced in heat-tolerant individuals and populations, suggesting that this reduced response is a general thermal tolerance mechanism in corals. I estimated the relative thermal tolerances of multiple individuals across species and, using 3'TagSeq, found that thermally tolerant species exhibit a reduced gene expression response compared to thermally sensitive species. This suggests that similar mechanisms may be leading to thermal tolerance across levels of organization.
Overall, my findings lead to a better understanding of the mechanisms governing gene expression variation and thermal tolerance in corals, and phenotypic plasticity more broadly. These insights are critical for understanding organismal resilience to climate change and can inform conservation strategies at the molecular level.
