The genetic architecture of temperature adaptation is shaped by population ancestry and not by selection regime

Kathrin A Otte,François Mallard,Viola Nolte,Christian Schlötterer

doi:10.1186/s13059-021-02425-9

Abstract

BackgroundUnderstanding the genetic architecture of temperature adaptation is key for characterizing and predicting the effect of climate change on natural populations. One particularly promising approach is Evolve and Resequence, which combines advantages of experimental evolution such as time series, replicate populations, and controlled environmental conditions, with whole genome sequencing. Recent analysis of replicate populations from two different Drosophila simulans founder populations, which were adapting to the same novel hot environment, uncovered very different architectures—either many selection targets with large heterogeneity among replicates or fewer selection targets with a consistent response among replicates.ResultsHere, we expose the founder population from Portugal to a cold temperature regime. Although almost no selection targets are shared between the hot and cold selection regime, the adaptive architecture was similar. We identify a moderate number of targets under strong selection (19 selection targets, mean selection coefficient = 0.072) and parallel responses in the cold evolved replicates. This similarity across different environments indicates that the adaptive architecture depends more on the ancestry of the founder population than the specific selection regime.ConclusionsThese observations will have broad implications for the correct interpretation of the genomic responses to a changing climate in natural populations.

Highlights

Adaptation of natural populations to environmental change may either occur from standing genetic variation or by the acquisition of new mutations
The adaptive architecture differs from the genetic architecture, which is inferred by QTL mapping and GWAS [2, 3], by accounting for pleiotropic constraints as well as for the large body of deleterious mutations [4, 5]
We studied the genetic architecture of cold adaptation in Drosophila simulans by combining experimental evolution with whole genome re-sequencing (Evolve and Resequence, E&R)

Summary

Introduction

Adaptation of natural populations to environmental change may either occur from standing genetic variation or by the acquisition of new mutations. Selection targets (Table 1) are identified with genomic selection scans, which apply statistical tests to detect selection signatures from population polymorphism data [7, 8]. [11,12,13,14,15]) It is, not apparent to what extent these results can be generalized, because most adaptive traits have a polygenic basis [16, 17] and either only small allele frequency changes [17] or non-parallel responses are expected [1]. Understanding the genetic architecture of temperature adaptation is key for characterizing and predicting the effect of climate change on natural populations. Recent analysis of replicate populations from two different Drosophila simulans founder populations, which were adapting to the same novel hot environment, uncovered very different architectures—either many selection targets with large heterogeneity among replicates or fewer selection targets with a consistent response among replicates

Methods

Results

Conclusion