Date of Award
2024
Degree Type
Dissertation
Degree Name
Doctor of Philosophy in Biological and Environmental Sciences
Department
Biological Sciences
First Advisor
Hollie M. Putnam
Abstract
Coral reef ecosystems face extreme challenges due to increasing ocean temperatures caused by anthropogenically induced global climate change and require reproductive replenishment for reef persistence. Corals and other marine invertebrates have exhibited the capacity for environmental memory, or the retention of information from prior environmental experiences, which can be inherited by subsequent generations (e.g., via non-genetic mechanisms). However, less is known about how molecular modifications in the coral epigenome influence acclimatization and adaptive responses to environmental variation within and across generations. Here, I present three manuscripts testing different mechanisms involved in coral’s physiological, reproductive, and epigenetic response to environmental perturbation that can have consequences for reproductive capacity and development of stress tolerance. Manuscript 1: As corals and their algal endosymbionts engage in a nutritionally symbiotic relationship that allows for survival in rapidly changing environments, we leveraged an existing experiment where the in-situ exposure of Pocillopora meandrina in Mo'orea, French Polynesia to increased nutrients for 15 months drove increased endosymbiont densities and resulted in enhanced photosynthetic rates at increased temperatures. We tested the hypothesis that the changes in symbiont performance resulted in changes in coral host gene expression and gene expression regulation and that the expression regulation would be strongest in pathways related to holobiont nutrient cycling. We determined that in response to chronic nutrient exposure, the coral host displayed differential gene expression, specifically in stress response, nutrient metabolism, and symbiotic nutrient exchange and signaling pathways. Additionally, differential methylation was present, particularly in genes associated with stress response, DNA maintenance and function, and carbohydrate metabolism. We found that as DNA methylation increases, gene expression also increases for all genes, with slightly higher explanatory effects on differentially expressed genes and highest explanatory power from genes with key response functions of corals exposed to nutrients. Our results support that changing environmental conditions, such as nutrient exposure, can be modulated by the symbiont, responded to by the host through gene expression, and regulated epigenetically. Manuscript 2: To expand our understanding on the energetic demands of gametogenic development, we characterized gametogenesis and physiological state in Acropora pulchra colonies from Mo'orea, French Polynesia through the physiological and histological analysis of fragments collected monthly from December 2021 to October 2022. Adult symbiont physiological state (i.e., symbiont densities, total chlorophyll content, and symbiont biomass) contributed to early and late transitions in gametogenic state between stages in both oogenesis and spermatogenesis. A one-unit increase in cell densities resulted in a greater than 50% increase in the likelihood of transitioning earlier to a higher stage (I-III) in both gamete types, with symbiont biomass resulting in a greater than 8% increase in the likelihood of transitioning later to a higher stage (III-V) in both gamete types. At later stages, symbiont biomass more than doubled the odds of transitioning to Stage IV and V for oogenesis, indicating the impact of seasonal symbiont acclimation patterns on physiological demand over gametogenic development. Manuscript 3: The final study tested the hypothesis that spawning Acropora pulchra corals exposed to a simulated marine heatwave event during gametogenesis would result in cross-generational acclimatization through environmental memory. Negative effects of marine heatwaves have been documented on the resilience and survival of corals, yet conversely, beneficial transgenerational acclimatization has also been demonstrated in marine invertebrate offspring following exposure to environmental stress. Therefore, we studied the impacts of marine heatwaves on reef-building corals’ non-genetic inheritance of environmental memory during periods of stress. Adult colonies (n = 12 genets) collected from the north shore backreef in Mo'orea, French Polynesia were split in half and exposed to ambient conditions or a simulated marine heatwave for four weeks in March/April 2022. Under the heatwave, adult corals showed bleaching and declines in symbiont densities (-20%), chlorophyll content (-20%), and photosynthesis (-3%), and respiration (-11%). Gametes from the heatwave parental history showed cross-generational plasticity, with larger egg sizes and higher fertilization success. Larvae reared to the swimming stage from the heatwave parental history had significantly higher survivorship (30%) under thermal stress. Gene expression of protein synthesis processes was enriched following the parental heatwave treatment and, in the offspring, due to the heatwave parental history. These results demonstrate that the offspring of parents challenged by thermal stress exhibit enhanced fitness through “environmental memory”, which may allow early developmental stages to survive disturbances and facilitate reef recovery. By studying environmental perturbations such as marine heatwaves or nutrient enrichment, we can understand the complex dynamics between coral performance and capacity for physiological and molecular mechanisms of intra- and cross-generational acclimatization. Together, the results from this dissertation will be useful for both mechanistic understanding of coral response to environmental variation, as well as for informing forecasts of the contributions of reproduction and offspring performance on reefs of the future.
Creative Commons License
This work is licensed under a Creative Commons Attribution-Noncommercial-No Derivative Works 4.0 License.
Recommended Citation
Becker, Danielle M., "LEARNING FROM THE PAST: ENVIRONMENTAL IMPACTS ON CORAL PERFORMANCE, REPRODUCTION, AND EPIGENETIC INHERITANCE" (2024). Open Access Dissertations. Paper 1718.
https://digitalcommons.uri.edu/oa_diss/1718