The roles of adaptation and phenotypic plasticity in determining a coastal fish's response to climate change

Abstract

When organisms experience an environmental change, they can employ a broad suite of behavioral, phenotypic, and molecular responses, mediated through either phenotypic plasticity or adaptation. These alternatives differ in speed and scale, with plasticity occurring rapidly during an organism’s lifetime, and adaptation occurring more slowly, across multiple generations. While both plasticity and adaptation represent viable mechanisms for species to persist in the face of environmental change, the relative importance of each is not well- established, particularly for non-model organisms. In today’s world, organisms are experiencing environmental change at an unprecedented rate. Marine species are under particular threat from climate change, as Earth’s oceans are absorbing the bulk of the excess heat energy produced by anthropogenic climate change, leading to dramatic and extreme ocean warming. In this dissertation, I assess the potential roles of plasticity and adaptation in response to heat stress in a common, widely distributed bait fish that plays a key ecological role in food webs of the western Atlantic, the pinfish (Lagodon rhomboides). In chapter 1, I examined the molecular and physiological responses to an acute heat stressor in both juvenile and adult pinfish, and found high levels of molecular plasticity, particularly in juveniles, which showed major changes to their gene expression repertoire. I also saw increases in aerobic demand under elevated temperatures for both juveniles and adults, in line with predictions about the effects of acute heat stress on ectotherm physiology. In chapter 2, I carried out a long-term experiment aimed at understanding the potential for developmental plasticity in response to repeated heat stressors during the juvenile life stage. I found that pinfish which had been exposed to fluctuating temperatures during development showed better physiological and phenotypic performance at elevated temperatures than individuals that developed at constant, cooler temperatures. Additionally, I found that developmentally-exposed pinfish displayed distinct molecular responses to repeated heat stressors, including heightened activation of genes involved in the unfolded protein response and antioxidant activity. This suggests that exposure to elevated temperatures during the juvenile life stage can prime an individual to perform better under future warming. For chapter 3, I sequenced and analyzed a chromosome-scale genome for the pinfish, which provided insight into the evolutionary and demographic history of this species, including findings of historical population expansion and contraction which coincide with the timing of known ancient climatic shifts. Finally, chapter 4 leverages this newly developed genomic resource as a reference to evaluate the population genetic differentiation of this species. Here, I resequenced the genomes of 120 pinfish from six populations across the species’ broad range, to assess population connectivity, genetic diversity, and the potential for local adaptation to distinct environmental conditions across a latitudinal gradient. In general, I found that pinfish show high genetic diversity and strong population connectivity, with low average genome-wide differentiation. However, I did identify three clear regions that distinguish two populations (Florida Keys and Northern Florida) from the other four (Maryland, North Carolina, Alabama, and Texas), indicating that there is the potential for local adaptation to distinct conditions. These results shed light on the mechanisms employed by coastal fishes persisting in changing or novel environments, and they provide a strong foundational base of knowledge for future studies in coastal marine fishes.