Pervasive and dynamic release of Cryptic Genetic Variation in Chironomus riparius: Rethinking adaptation in fluctuating environments

Abstract

The interplay between phenotypic plasticity and cryptic genetic variation (CGV) is crucial for understanding adaptation, yet the prevailing paradigm suggests CGV is primarily exposed under novel or extreme conditions. By examining gene expression responses along a natural temperature gradient in Chironomus riparius, we challenged this view. We found that the vast majority of expressed genes (63%) exhibit dynamic CGV, where interindividual expression variability scales continuously with distance from the selectively optimal temperature, a pattern also observed in higher-level traits like mutation rate and ROS levels. Genes with lower overall expression levels were less temperature-regulated, and thermal reaction norm shapes varied with gene function. Unexpectedly, thermally plastic genes were more pleiotropic, often acting as hub genes, while CGV in gene expression was associated with lower pleiotropy. This pattern, and the observed strong recurrent selection on plastic genes with CGV, aligns with C. ripariuss adaptation to its highly fluctuating environment through selective tracking. We propose that this continuous, dynamic release of genetic variation is a necessary and inherent outcome of the polygenic nature of traits. This model fundamentally reshapes our understanding of adaptation, implying that populations can gradually and continuously adapt without requiring harsh conditions to expose hidden diversity. This leads to smoother adaptive landscapes, enhancing rapid adaptation and facilitating evolutionary innovation in the face of ongoing environmental change.