Transcriptional plasticity and environmental change in marine fishes

Abstract

How organisms respond to environmental changes is crucial for their survival, especially in the face of rapid climate change. One of the mechanisms facilitating acclimation to novel environments is phenotypic plasticity, the ability of a single genotype to produce multiple phenotypes in different environments. Phenotypic plastic responses are influenced by various factors like environmental stability, parental experiences, and genetic factors and can be classified as acute, developmental, or intergenerational responses based on the timeframe involved. This dissertation investigates molecular basis of all these three types of plasticity in marine fishes in response to changes in their physical and social environment. Physical environmental changes mediated by ocean acidification negatively affects various fish species however, some thrive in naturally occurring CO2 seeps, potentially benefiting from habitat shifts induced by reduced pH levels. In the anemone goby, a species that has increased population density at CO2 seeps in Vulcano Island, Italy, differential regulation of key pathways resulting in acclimation to acidified waters, potentially mediated by developmental plasticity, were identified. While overall increase in CO2 levels elicits molecular responses in fish, the stability of CO2 concentration is crucial. Exposure of spiny damselfish to both stable and fluctuating CO2 conditions resulted in loss of natural rhythmic splicing events however, fish in fluctuating CO2 conditions alone showed increased capability of time-dependent regulation of splicing events in genes associated with synaptic plasticity and neuronal functioning. This might be mediated by the observed amplitude change in circadian rhythm genes in the fluctuating CO2 treatment enabling the fish to coordinate biological processes in anticipation of periodic changes in CO2 levels. Furthermore, the spiny damselfish showed molecular signatures of intergenerational plasticity to ocean acidification conditions, particularly in the brain and liver. Specifically, within-generation transcriptional responses indicating altered neural signaling in the brain and metabolic depression in the liver returned to control levels when parents were also exposed to elevated CO2 conditions. Interestingly, these signatures indicating intergenerational acclimation were predominant in offspring of parents behaviourally tolerant to elevated CO2 conditions. This shows that parental phenotype and parental environment play a role in mediating offspring transcriptional response to ocean acidification. An organisms’ environment encompasses not only its physical environment but also the social environment. The last chapter of this thesis explores molecular processes underlying plastic responses of organisms to changes in their social environment by using the anemone-anemonefish mutualistic system. Significant changes in the transcriptome of both species were identified during the acclimation period of mutualistic association. Anemonefish showed activation of sensory pathways in response to cues received from the anemone, while the anemone showed upregulation of genes associated with nematocyst discharge and venom production, potentially in response to sensing fish movements. This study reveals an interplay of molecular events underlying mutualistic association in both partners. Taken together, the findings reported in this thesis furthers our understanding of the molecular processes underlying various types of phenotypic plastic responses to environmental changes and provides key information regarding the acclimation potential of marine fishes to global change.