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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.

Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental variation across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than 15 generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic axes. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified at each scale were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with distinct components of the polygenic architecture shifting across each environmental axis to produce redundant adaptive patterns.

Temporally fluctuating environmental conditions are a ubiquitous feature of natural habitats. Yet, how finely natural populations adaptively track fluctuating selection pressures via shifts in standing genetic variation is unknown. We generated high-frequency, genome-wide allele frequency data from a genetically diverse population of in extensively replicated field mesocosms from late June to mid-December, a period of ∼12 generations. Adaptation throughout the fundamental ecological phases of population expansion, peak density, and collapse was underpinned by extremely rapid, parallel changes in genomic variation across replicates. Yet, the dominant direction of selection fluctuated repeatedly, even within each of these ecological phases. Comparing patterns of allele frequency change to an independent dataset procured from the same experimental system demonstrated that the targets of selection are predictable across years. In concert, our results reveal fitness-relevance of standing variation that is likely to be masked by inference approaches based on static population sampling, or insufficiently resolved time-series data. We propose such fine-scaled temporally fluctuating selection may be an important force maintaining functional genetic variation in natural populations and an important stochastic force affecting levels of standing genetic variation genome-wide.

Pigmentation has been widely studied by evolutionary biologists due to both ease of measure and relationship to fitness. pigmentation has represented a particularly useful avenue of investigation, as extensive genetic tools have enabled the characterization of the trait's complex architecture. pigmentation also varies predictably across space and time in wild populations, suggesting pigmentation is a component of adaptation to local environmental conditions. Despite this, the impact of pigmentation on fitness, and the environmental factors that drive the evolution of pigmentation, are not well understood. To address this gap, we experimentally evolved replicated populations in field mesocosms to determine whether and how pigmentation evolves in response to environmental variation. We found that pigmentation rapidly and predictably adapted to a direct manipulation of temperature, supportive of melanization playing a role in thermoregulation. However, we also determined that pigmentation responded adaptively to direct manipulations of numerous additional factors, including intraspecific competition, diet, and the microbiome. These findings suggest that the selective landscape acting on pigmentation is complex and multifaceted, and that patterns of melanization may be driven, at least in part, by indirect selection due to correlations with other fitness-related traits.

Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that pigmentation evolves as a highly parallel and deterministic response to shared environmental gradients across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than ten generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic gradients. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified in each context were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with an unpredictable genomic response, with distinct components of the polygenic architecture shifting across each environmental gradient to produce redundant adaptive patterns. Shifts in global climate conditions have heightened our need to understand the dynamics and pace of adaptation in natural populations. In order to anticipate the population-level response to rapidly changing environmental conditions, we need to understand whether trait evolution is predictable over short timescales, and whether the genetic basis of adaptation is shared or distinct across multiple timescales. Here, we explored parallelism in the adaptive response of a complex phenotype, pigmentation, to shared conditions that varied over multiple spatiotemporal scales. Our results demonstrate that while phenotypic adaptation proceeds as a predictable response to environmental gradients, even over short timescales, the genetic basis of the adaptive response is variable and nuanced across spatial and temporal contexts.

Populations are capable of responding to environmental change over ecological timescales via adaptive tracking. However, the translation from patterns of allele frequency change to rapid adaptation of complex traits remains unresolved. We used abdominal pigmentation in Drosophila melanogaster as a model phenotype to address the nature, genetic architecture, and repeatability of rapid adaptation in the field. We show that D. melanogaster pigmentation evolves as a highly parallel and deterministic response to shared environmental gradients across latitude and season in natural North American populations. We then experimentally evolved replicate, genetically diverse fly populations in field mesocosms to remove any confounding effects of demography and/or cryptic structure that may drive patterns in wild populations; we show that pigmentation rapidly responds, in parallel, in fewer than fifteen generations. Thus, pigmentation evolves concordantly in response to spatial and temporal climatic gradients. We next examined whether phenotypic differentiation was associated with allele frequency change at loci with established links to genetic variance in pigmentation in natural populations. We found that across all spatial and temporal scales, phenotypic patterns were associated with variation at pigmentation-related loci, and the sets of genes we identified in each context were largely nonoverlapping. Therefore, our findings suggest that parallel phenotypic evolution is associated with distinct components of the polygenic architecture shifting across each environmental gradient to produce redundant adaptive patterns.Competing Interest StatementThe authors have declared no competing interest.Footnotes* Edits were made to the interpretation of genomic analysis results.