Freshwater Transitions and the Evolution of Osmoregulation in the Alewife

The transition from seawater to freshwater is deeply rooted in the evolutionary history of animals, initiating the radiation and speciation of many taxa. However, crossing the boundary into freshwater from the sea represents a considerable physiological challenge for animals that maintain a near constant internal ion concentration. Because seawater and freshwater differ strongly in solute concentration, the transition into freshwater must involve the evolution of ion and water balance; yet, we have a limited understanding of the physiological modifications that facilitate this transition. Here, I investigate the evolution of the osmoregulatory system upon transition to freshwater using populations of an ancestrally anadromous fish, the Alewife (Alosa pseudoharengus), which has become landlocked on multiple, independent occasions. I take an integrative approach, exploring the molecular, physiological, and whole-organism level consequences of the freshwater transition. Overall, my dissertation demonstrates that the transition to freshwater in the Alewife leads to evolutionary shifts in osmoregulatory capacity, which may be driven by changes in the mechanisms of ion exchange at the gill. In chapter 2, I show that landlocking leads to the partial loss of seawater tolerance and hypoosmoregulatory performance, which may be mediated through reductions in expression and activity of genes for gill ion secretion. Chapter 3 demonstrates that several independently derived landlocked populations vary in the degree of seawater tolerance loss, and that this variation is negatively correlated with freshwater tolerance. This suggests that trade-offs in osmoregulation follow local adaptation to freshwater. In chapter 4, I use next generation sequencing to show that thousands of genes have differentiated in expression between Alewife life history forms. Comparison of gill transcriptomes of anadromous and landlocked Alewives reveals that changes in the regulation of transcription of genes in gill ion exchange pathways may underlie evolutionary changes in osmoregulation. In chapter 5, I demonstrate that landlocked Alewives are poor swimmers compared to anadromous Alewives, and that differences in swimming ability are not explained by differences in osmoregulatory performance or body shape. These results suggest that reductions in swimming performance among landlocked Alewives may be a function of relaxed selection on migration capacity