Broad geographic sampling reveals the shared basis and environmental correlates of seasonal adaptation in Drosophila.

Heather E Machado ,Bernard Kim,Susanne Tilk,Iryna Kozeretska,Thomas Flatt,Josefa González,Svitlana Serga,Subhash Rajpurohit,Talia L Karasov ,John E Pool ,Thomas J S Merritt ,Daniel K Fabian ,Alan O Bergland ,Katherine R O’brien ,Paula R Roy ,Emily L Behrman ,Stephen W Schaeffer ,Brian P Lazzaro ,Kelly A Dyer ,Paul S Schmidt ,Ryan W Taylor ,Dmitri A Petrov

doi:10.7554/elife.67577

Abstract

To advance our understanding of adaptation to temporally varying selection pressures, we identified signatures of seasonal adaptation occurring in parallel among Drosophila melanogaster populations. Specifically, we estimated allele frequencies genome-wide from flies sampled early and late in the growing season from 20 widely dispersed populations. We identified parallel seasonal allele frequency shifts across North America and Europe, demonstrating that seasonal adaptation is a general phenomenon of temperate fly populations. Seasonally fluctuating polymorphisms are enriched in large chromosomal inversions, and we find a broad concordance between seasonal and spatial allele frequency change. The direction of allele frequency change at seasonally variable polymorphisms can be predicted by weather conditions in the weeks prior to sampling, linking the environment and the genomic response to selection. Our results suggest that fluctuating selection is an important evolutionary force affecting patterns of genetic variation in Drosophila.

Highlights

Fluctuations in the environment are an inescapable condition for all organisms
We show that allele frequency change between seasons is most predictable when taking into account the local temperature prior to sample collections both in the spring and in the fall, which hints at the complex and nonlinear nature of adaptation with adaptive tracking occurring at sub-seasonal timescales
Samples in the Core20 set are drawn from 15 localities in North America and Europe and we use at most 2 years of sampling from any one locality

Summary

Introduction

Fluctuations in the environment are an inescapable condition for all organisms. While many of these fluctuations are entirely unpredictable, some are predictable to a degree, including those that occur on diurnal and seasonal time scales. Classic quantitative genetic theory suggests that an optimal, plastic genotype will eventually dominate a population that is exposed to periodically changing environments (Burger and Gimelfarb, 1999; Korol et al, 1996; Lande, 2008; Scheiner, 1993). This is so when certain environmental cues are reliable indicators of changes in selection pressure (Levins, 1974; Via and Lande, 1985). Predictions from traditional population genetic models suggest that periodically changing environments will lead to the rapid loss of seasonally favored ecotypes as slight changes in selection pressure from one year to another eventually push allele frequencies at causal alleles to fixation (Hedrick, 1976)

Methods

Results

Conclusion