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Data for: Limited genomic predictability of complex trait evolution despite genotype-phenotype stability

Smiley-Rhodes, Jessica1; Bitter, Mark1; Berardi, Skyler2; Beltz, Jack2; Petrov, Dmitri1; Schmidt, Paul2

Published Sep 28, 2026 on Dryad. https://doi.org/10.5061/dryad.pnvx0k73t

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Abstract

The extent to which adaptation can be predicted, particularly for traits with complex genetic bases, is unknown. We leveraged a model complex trait (abdominal pigmentation), a model species (Drosophila melanogaster), and a longitudinal sampling design to test the efficacy of genomic prediction of complex trait variation and evolution in an ecologically relevant setting. We monitored genome-wide allele frequencies and pigmentation variation in genetically diverse populations of D. melanogaster across seven generations of evolution in both field mesocosms exposed to natural environmental fluctuations and mesocosms housed in a controlled, lab-based setting. At two time points throughout trait evolution, we conducted a high-powered, tail-based mapping of pigmentation, producing a well-resolved genotype-phenotype map that reaffirms canonical pigmentation genes and unveils novel loci. While we were able to use this map to correctly infer the direction of pigmentation evolution in both the field and lab mesocosms, the particular loci responding to selection, and thus the architecture of adaptation itself, were largely unpredictable. We suggest this unpredictability to be a result of pleiotropic constraint and genotype-by-environment interactions, which were more pronounced in the field mesocosm, relative to the lab-based environment. Finally, we quantified a striking stability of the genotype-phenotype map across genetically diverged populations, demonstrating that shifting epistatic landscapes throughout the evolutionary process did not alter trait architecture to a degree that precluded phenotypic prediction among independent populations. In concert, our results highlight both the promise and limitations of genomic prediction, and exemplify the challenges of extrapolating from lab-based studies of complex traits to their evolutionary dynamics in the wild.