Genetic redundancy fuels polygenic adaptation in Drosophila

The genetic architecture of adaptive traits is of key importance to predict evolutionary responses. Most adaptive traits are polygenic—i.e., result from selection on a large number of genetic loci—but most molecularly characterized traits have a simple genetic basis. This discrepancy is best explained by the difficulty in detecting small allele frequency changes (AFCs) across many contributing loci. To resolve this, we use laboratory natural selection to detect signatures for selective sweeps and polygenic adaptation. We exposed 10 replicates of a Drosophila simulans population to a new temperature regime and uncovered a polygenic architecture of an adaptive trait with high genetic redundancy among beneficial alleles. We observed convergent responses for several phenotypes—e.g., fitness, metabolic rate, and fat content—and a strong polygenic response (99 selected alleles; mean s = 0.059). However, each of these selected alleles increased in frequency only in a subset of the evolving replicates. We discerned different evolutionary paradigms based on the heterogeneous genomic patterns among replicates. Redundancy and quantitative trait (QT) paradigms fitted the experimental data better than simulations assuming independent selective sweeps. Our results show that natural D. simulans populations harbor a vast reservoir of adaptive variation facilitating rapid evolutionary responses using multiple alternative genetic pathways converging at a new phenotypic optimum. This key property of beneficial alleles requires the modification of testing strategies in natural populations beyond the search for convergence on the molecular level.Replicate populations of the fruit fly Drosophila simulans exposed to a novel temperature environment showed convergent evolution on the phenotypic level. On the genetic level, however, no convergence was observed. These results support the “trait optimum” paradigm as the predominant mode of adaptation.Author summary: It is widely assumed that adaptation is mainly polygenic, with the underlying frequency changes being so small that they are difficult to detect and characterize. Taking advantage of laboratory-based natural selection of replicated populations of the fruit fly Drosophila simulans exposed to a high temperature regime, we identified a polygenic response with many (99) selected alleles having pronounced allele frequency changes (AFCs). Despite phenotypic convergence across the 10 replicates, the genomic response was highly heterogeneous, with different subsets of the selected alleles contributing to the convergent phenotype in each of the replicate populations. The observed genetic redundancy not only indicates lack of genetic constraint but also demonstrates that multiple genetic pathways lead to convergent phenotypic outcomes.