Direct observation of evolution in response to natural environmental change can resolve fundamental questions about adaptation, including its pace, temporal dynamics, and underlying phenotypic and genomic architecture. We tracked the evolution of fitness-associated phenotypes and allele frequencies genome-wide in 10 replicate field populations of Drosophila melanogaster over 10 generations from summer to late fall. Adaptation was evident over each sampling interval (one to four generations), with exceptionally rapid phenotypic adaptation and large allele frequency shifts at many independent loci. The direction and basis of the adaptive response shifted repeatedly over time, consistent with the action of strong and rapidly fluctuating selection. Overall, we found clear phenotypic and genomic evidence of adaptive tracking occurring contemporaneously with environmental change, thus demonstrating the temporally dynamic nature of adaptation.

Diapause is the classic adaptation to seasonality in arthropods, and its expression can result in extreme lifespan extension as well as enhanced resistance to environmental challenges. Little is known about the underlying evolutionary genetic architecture of diapause in any organism. Drosophila melanogaster exhibits a reproductive diapause that is variable within and among populations; the incidence of diapause increases with more temperate climates and has significant pleiotropic effects on a number of life history traits. Using quantitative trait mapping, we identified the RNA-binding protein encoding gene couch potato ( cpo ) as a major genetic locus determining diapause phenotype in D. melanogaster and independently confirmed this ability to impact diapause expression through genetic complementation mapping. By sequencing this gene in samples from natural populations we demonstrated through linkage association that variation for the diapause phenotype is caused by a single Lys/Ile substitution in one of the six cpo transcripts. Complementation analyses confirmed that the identified amino acid variants are functionally distinct with respect to diapause expression, and the polymorphism also shows geographic variation that closely mirrors the known latitudinal cline in diapause incidence. Our results suggest that a naturally occurring amino acid polymorphism results in the variable expression of a diapause syndrome that is associated with the seasonal persistence of this model organism in temperate habitats.

Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterize variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.

In Drosophila melanogaster, exposure of females to low temperature and shortened photoperiod can induce the expression of reproductive quiescence or diapause. Diapause expression is highly variable within and among natural populations and has significant effects on life-history profiles, including patterns of longevity, fecundity, and stress resistance. We hypothesized that if diapause expression is associated with overwintering mechanisms and adaptation to temperate environments, the frequency of diapause incidence would exhibit a latitudinal cline among natural populations. Because stress resistance and reproductive traits are also clinal in this species, we also examined how patterns of fecundity and longevity varied with geography and how stress resistance and associated traits differed constitutively between diapause and nondiapause lines. Diapause incidence was shown to vary predictably with latitude, ranging from 35% to 90% among natural populations in the eastern United States Survivorship under starvation stress differed between diapause and nondiapause lines; diapause phenotypes were also distinct for total body triglyceride content and the developmental distribution of oocytes in the ovary following stress exposure. Patterns of longevity, fecundity, and ovariole number also varied with geography. The data suggest that, for North American populations, diapause expression is functionally associated with overwintering mechanisms and may be an integral life-history component in natural populations.