Clinal and seasonal changes are correlated in Drosophila melanogaster natural populations

Abstract

Spatial and seasonal variations in the environment are ubiquitous. Environmental heterogeneity can affect natural populations and lead to covariation between environment and allele frequencies. Drosophila melanogaster is known to harbor polymorphisms that change both with latitude and seasons. Identifying the role of selection in driving these changes is not trivial, because nonadaptive processes can cause similar patterns. Given the environment changes in similar ways across seasons and along the latitudinal gradient, one promising approach may be to look for parallelism between clinal and seasonal changes. Here, we test whether there is a genome‐wide correlation between clinal and seasonal changes, and whether the pattern is consistent with selection. Allele frequency estimates were obtained from pooled samples from seven different locations along the east coast of the United States, and across seasons within Pennsylvania. We show that there is a genome‐wide correlation between clinal and seasonal variations, which cannot be explained by linked selection alone. This pattern is stronger in genomic regions with higher functional content, consistent with natural selection. We derive a way to biologically interpret these correlations and show that around 3.7% of the common, autosomal variants could be under parallel seasonal and spatial selection. Our results highlight the contribution of natural selection in driving fluctuations in allele frequencies in natural fly populations and point to a shared genomic basis to climate adaptation that happens over space and time in D. melanogaster.

Seasonal variation in wing size and shape of Drosophila melanogaster reveals rapid adaptation to environmental changes

“…In the same manner, temperate populations from North America and Europe demonstrate parallel seasonal allele frequency change across the two continents 13 . Together, these results support that seasonal adaptation could be a general phenomenon of temperate Drosophila populations 12 – 14 .…”

“…Seasonal fluctuations are main sources for rapidly changing environments in temperate regions and recent studies provided evidence for rapid change in SNP frequencies among seasons 12 – 14 . Previous studies also revealed that seasonal variation in adaptive phenotypic traits like thermal and starvation tolerance 22 , and innate immunity 25 in D. melanogaster populations and all together suggesting that many loci respond to seasonal selection.…”

“…For example, some individuals of an inbred line might have outliers within a month, however a general pattern persists. Previous studies showed that SNP frequencies in D. melanogaster populations vary seasonally 12 – 14 and transposable elements (TEs) were significantly associated with seasons 80 . Thus, it is possible that selection favors size and / or size related traits depended on changing environmental variables as our wing size and shape results support.…”

“…Environmental variables such as temperature, photoperiod and food availability vary over spatial and temporal scales, driving adaptive divergence among populations, and providing information concerning adaptive evolution. Because of this fact, the ecological and evolutionary impact of latitude 1 – 4 , altitude 4 – 9 and seasons ( 10 , 11 and references therein 12 – 14 ), on organisms’ life history have long been a topic of interest. Natural populations distributed along latitudinal or altitudinal gradients have been widely used for studies of spatial selection, where the most predictable abiotic factor is the temperature between several climatic and ecological factors.…”

“…The organism’s evolutionary response to seasonality, which is triggered by a complex and fluctuating environmental pressure, ensures that existing genetic polymorphisms are preserved. In multivoltine species, seasonal selective pressures can change across generations; in this case, natural selection can cause cyclical changes in allele frequencies 12 – 14 , 24 – 28 . The first findings of genetic differences related to seasonal variation reported in Drosophila pseudoobscura 29 and Drosophila funebris 30 .…”