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Abstract

Biological systems have a remarkable dual capacity: they are robust to mutations and developmental noise, while also evolving and responding dynamically to their environment. To gain a better understanding of robustness and evolvability, we conducted a comparative analysis of wild-type Drosophila reared under control conditions and those exposed to a sucrose and glucose-rich diet. Our focus encompassed three key components of phenotypic robustness: population-level analysis of wing shape morphology, developmental stability reflected in wing asymmetry, and flying performance. Surprisingly, we observed a reduction in behavioral variation in populations reared on high-sugar diets that exhibited robust flight performance. Our results indicate that individuals exposed to stressful dietary conditions also demonstrate rapid and substantial changes in morphology and fluctuating asymmetry. Despite these alterations, functional capacity for flight was maintained, highlighting a remarkable resilience in the face of underlying morphological shifts. Tracking these phenotypic traits over 15 generations allowed us to discern both immediate and delayed adaptive responses to environmental stress. To further probe the environmental role in adaptability, we initiated experiments implementing stabilizing selection on flies raised under two distinct conditions. In each generation, we artificially reduced variation in flight performance by selecting flies close to the mean. Remarkably, flies reared on control food exhibited faster adaptation to truncating selection, manifesting in reduced flight variation within just five generations. In contrast, flies subjected to food enriched with sugar displayed a noisier and less predictable response, suggesting a diminished adaptability to artificial selection. The fluctuations in variation observed are likely a result of genotype-by-environment interactions (GxE), influencing the heritability pattern for flight performance. In conclusion, our study sheds light on the dynamic nature of phenotypic responses to environmental stress and the subsequent implications for adaptive evolution. The ability of organisms to maintain functional traits amidst morphological and symmetrical alterations underscores the complexity of the relationship between genotype and phenotype. These findings detangle the speed of adaptive responses in terms of behavior, morphology, and developmental stability, with potential applications in understanding and managing evolutionary processes in response to stress.