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.

BackgroundPopulation genetic theory predicts that rapid adaptation is largely driven by complex traits encoded by many loci of small effect. Because large-effect loci are quickly fixed in natural populations, they should not contribute much to rapid adaptation.ResultsTo investigate the genetic architecture of thermal adaptation — a highly complex trait — we performed experimental evolution on a natural Drosophila simulans population. Transcriptome and respiration measurements reveal extensive metabolic rewiring after only approximately 60 generations in a hot environment. Analysis of genome-wide polymorphisms identifies two interacting selection targets, Sestrin and SNF4Aγ, pointing to AMPK, a central metabolic switch, as a key factor for thermal adaptation.ConclusionsOur results demonstrate that large-effect loci segregating at intermediate allele frequencies can allow natural populations to rapidly respond to selection. Because SNF4Aγ also exhibits clinal variation in various Drosophila species, we suggest that this large-effect polymorphism is maintained by temporal and spatial temperature variation in natural environments.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1503-4) contains supplementary material, which is available to authorized users.

Individuals can adapt to heterogeneity in their environment through either local adaptation or phenotypic plasticity. Colour forms of the ladybird Harmonia axyridis are a classic example of local adaptation, in which the frequency of melanic forms varies greatly between populations. In some populations, there are also large seasonal changes in allele frequency, with melanism being costly in summer and beneficial in winter. We report that the non‐melanic morph of H. axyridis dramatically increases its degree of melanization at cold temperatures. Furthermore, there is genetic variation in reaction norms, with different families responding to temperature in different ways. Variation at different spatial and temporal scales appears to have selected for either genetic or phenotypically plastic adaptations, which may be important in thermoregulation. As melanism is known to have a large effect on fitness in H. axyridis, this plasticity of melanization may have hastened its spread as an invasive species.

Background: Population genetic theory predicts that rapid adaptation is largely driven by complex traits encoded by many loci of small effect. Because large-effect loci are quickly fixed in natural populations, they should not contribute much to rapid adaptation. Results: To investigate the genetic architecture of thermal adaptation -a highly complex trait -we performed experimental evolution on a natural Drosophila simulans population. Transcriptome and respiration measurements reveal extensive metabolic rewiring after only approximately 60 generations in a hot environment. Analysis of genome-wide polymorphisms identifies two interacting selection targets, Sestrin and SNF4Aγ, pointing to AMPK, a central metabolic switch, as a key factor for thermal adaptation.Conclusions: Our results demonstrate that large-effect loci segregating at intermediate allele frequencies can allow natural populations to rapidly respond to selection. Because SNF4Aγ also exhibits clinal variation in various Drosophila species, we suggest that this large-effect polymorphism is maintained by temporal and spatial temperature variation in natural environments.

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