HSP90 as an Evolutionary Capacitor Drives Adaptive Eye Size Reduction via atonal

Kurtz, Joachim; Sayed, Rascha; Şahin, Özge; Errbii, Mohammed; Prüser, Tobias; Schrader, Lukas; Schulz, Nora

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 revealed a reduced-eye phenotype that was stably inherited 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 identified the transcription factor atonal as the underlying gene. These results provide the first direct genetic link between an HSP90-released trait and increased fitness, highlighting a mechanism by which hidden variation contributes to adaptation.