HSP90 as an evolutionary capacitor drives adaptive eye size reduction via atonal.

Abstract

Genetic variation fuels evolution, and the release of cryptic variation is key for adaptation. The heat shock protein 90 (HSP90) has been proposed to act as an evolutionary capacitor by revealing such hidden variation under stress. However, this idea remains debated, as the genetic basis of HSP90-regulated traits is often unknown, and many observed phenotypes are deleterious. Here, we show in Tribolium castaneum that HSP90 shapes evolution by unmasking a hidden trait providing enhanced fitness under specific conditions. Using RNA interference and chemical inhibition, we consistently reveal a reduced-eye phenotype that persists in descendant lines across generations without continued HSP90 disruption. Under constant light, reduced-eye beetles had higher reproductive success and greater trait penetrance than normal-eyed siblings, suggesting a selective advantage. Whole-genome sequencing and functional analysis identify the transcription factor atonal (ato) as the underlying gene. These results provide the first direct genetic link between an HSP90-buffered trait and context-dependent fitness benefits in animals, highlighting a potential mechanism by which cryptic variation contributes to adaptation.