The mechanisms of seasonal adaptation in Drosophila melanogaster

Environmental heterogeneity is ubiquitous across space and time and can be a form of balancing selection that maintains genetic variation. Deciphering the mechanisms and traits associated with adaptation to environmental heterogeneity is an important task in evolutionary biology. Adaptive evolution and phenotypic plasticity are two important adaptive mechanisms. Gene expression traits provide a great opportunity to study how populations cope with environmental heterogeneity since they allow us to infer physiological functions and assess the adaptive mechanisms. In my dissertation, I address the adaptive mechanisms under seasonal adaptation in the model organism Drosophila melanogaster from three perspectives, including genetics, gene expression and ecologically important traits. In Chapter 1, I utilized publicly available datasets to compare the adaptive signals at expression quantitative trait loci (eQTLs) between space and time. I find that the adaptive signals between space and time differ at eQTLs. While adaptation to space across latitudinal clines show strong signals at eQTLs, there is weak seasonal adaptive signal. In addition, seasonal adaptation at eQTLs show idiosyncratic patterns across different populations. These results suggest that adaptation at eQTLs across seasons is likely distinct from that across latitudinal clines. In Chapter 2, I investigate the plasticity in gene expression across 10 seasonal time points using flies reared in an experimental orchard. By modeling gene expression variation across seasons and across associated temperature ranges, I find that seasonal gene expression plasticity is prevalent and that the plastic genes are functionally enriched. Interestingly, the direction of plastic gene expression changes across seasons shows maladaptive signal. In addition, eQTLs associated with plastic genes are depleted for seasonal SNPs, suggesting that plasticity and genetic evolution have limited overlap at the eQTLs. In Chapter 3, I investigate the seasonal plasticity of three fitness traits (body size, developmental time, fecundity) and assessed whether temperature is associated with their plasticity. I find that seasonal developmental temperatures can elicit phenotypic plasticity in wild seasonal environments. Moreover, I show evidence that seasonal phenotypic plasticity in developmental time and body size are likely adaptive. In general, my work challenges the previous assumption that seasonal adaptation parallels clinal adaptation by showing distinct adaptive signals between space and time at eQTLs. In addition, I show that plasticity in gene expression is prevalent across seasons and that plasticity and genetic evolution likely have limited overlap at eQTLs. However, seasonal plasticity in gene expression shows maladaptive signal. Finally, I show that seasonal developmental temperature in the wild can elicit plastic response in fitness traits and such plasticity could contribute to seasonal population size dynamics. Taken together, my dissertation can advance our understanding of how populations cope with temporal environmental heterogeneity across seasons from the genetics, gene expression, and fitness-related phenotypic levels.