The Predictability of Complex Trait Adaptation Over Ecological Timescales
Degree type
Graduate group
Discipline
Biology
Genetics and Genomics
Subject
Complex traits
Drosophila
Experimental evolution
Genomics
Pigmentation
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Abstract
Understanding whether patterns of adaptation arise as a repeatable, or distinct, response to recurrent environmental shifts remains an open question in the field of evolutionary biology. It is of particular importance to define the predictability of rapid adaptation, which is a process central to modeling key issues such as responses to climate change, dynamics of pathogen outbreaks, the evolution of drug resistance, cancer proliferation, and the spread of invasive species. Therefore, I investigated the predictability of rapid adaptation by exploring responses to the seasonal environment in temperate Drosophila melanogaster populations. I specifically examined whether predictability emerges across scales of observation (i.e., from genotype to phenotype), and I characterized how complex selective landscapes and genetic architectures inform predictability. I first identified temperature and population density as primary drivers of seasonal adaptation in D. melanogaster by manipulating these factors in field mesocosm populations. Each manipulation produced differential patterns of genomic and phenotypic adaptation, but neither factor appeared to be the dominant driver of trait patterns; this underscored the complexity of the seasonal selective landscape. I next utilized pigmentation as a focal trait to characterize genomic and phenotypic predictability in wild populations. I show for the first time that pigmentation adapts as a rapid and repeatable response to spatiotemporal environmental variation, but these parallel phenotypic patterns were associated with distinct shifts in the genetic architecture across each spatial or temporal axis. Thus, predictability appears to emerge more readily at the phenotypic level for this polygenic trait. Subsequent analyses revealed that this phenotypic predictability hinges on the summed effects of a multidimensional selective landscape and complex genetic architecture. I found that numerous abiotic and biotic factors modulate adaptive trajectories of melanization, which suggests pigmentation is influenced indirectly by selection on correlated traits. Finally, I demonstrate that melanization rapidly adapts as a differential response across individual segments of the fly cuticle, and this modular response contributes additional complexity to the predictability of phenotypic adaptation.