How predictable is adaptation from standing genetic variation? Experimental evolution in Drosophila highlights the central role of redundancy and linkage disequilibrium

Abstract

Experimental evolution is well-suited to test the predictability of evolution without the confounding effects of inaccurate forecasts about future environments. Most of the literature about parallel (and thus predictable) evolution has been carried out in asexual microorganisms, which adapt by de novo mutations. Nevertheless, parallel evolution has also been studied in sexual species at the genomic level. Here, I review the evidence for parallel evolution in Drosophila , the best-studied obligatory outcrossing model for adaptation from standing genetic variation in the laboratory. Similar to asexual microorganisms, evidence for parallel evolution varies between the focal hierarchical levels. Selected phenotypes consistently respond in a very predicable way, but the underlying allele frequency changes are much less predictable. The most important insight is that the predictability of the genomic selection response for polygenic traits depends highly on the founder population and to a much lesser extent on the selection regime. This implies that predicting adaptive genomic response is challenging and requires a good understanding of the adaptive architecture (including linkage disequilibrium) in the ancestral populations. This article is part of the theme issue ‘Interdisciplinary approaches to predicting evolutionary biology’.

Polygenic adaptation to overnutrition reveals a role for cholinergic signaling in longevity

“…Beneficial alleles, especially for a highly polygenic trait like lifespan, might easily be lost due to chance under strong selection. These data are consistent with other studies showing that stochasticity plays an important role (79)(80)(81), especially in populations with extensive standing variation (79,82,83). Interestingly, among the neuronal GO terms, genes associated with development were the most enriched in our SNP gene lists despite our selective pressure being applied exclusively to adults.…”

“…Evidence for parallel evolution Understanding whether adaptation is predictable and can proceed via parallel evolution from standing variation is a major question in evolutionary genetics. Our results support the hypothesis that the predictability of evolution depends upon the hierarchical level being tested (79). All Selected populations showed significant increases in lifespan on HS as compared to Controls, suggesting parallelism at the level of overall fitness.…”

Genomic evidence for domestication selection in three hatchery populations of Chinook salmon, Oncorhynchus tshawytscha

“…More specifically, parallel adaptation to similar environments has been shown to occur via variable genomic architectures (Ament-Velásquez et al, 2022;Barghi et 2019;Bolnick et al, 2018;Schlötterer, 2023;Therkildsen et al, 2019). For example, ten Drosophila lines exposed to the same selective pressure evolved similar phenotypes but had unique genetic architectures underlying adaptation (Barghi et al, 2019) Another possible difference between Unuk and the other two population pairs is the average body size at release between the hatcheries.…”

Interdisciplinary approaches to predicting evolutionary biology

“…An exciting approach to forecasting evolutionary change is the use of laboratory evolution for systems that can be run in multiple replicates and be fully sequenced. To this end, Schlötterer [ 17 ] reviews the evidence for parallel evolution in the fruit fly Drosophila , the best-studied obligatory outcrossing model for adaptation from standing genetic variation. He argues that selected phenotypes consistently respond in a very predictable way, but allele frequency changes are much less predictable.…”