Weak gene–gene interaction facilitates the evolution of gene expression plasticity

Hao-Chih Kuo, Cheng-Te Yao, Ben-Yang Liao, Meng-Pin Weng, Feng Dong, Yu-Cheng Hsu, Chih-Ming Hung

Individual organisms may exhibit phenotypic plasticity when they acclimate to different conditions. Such plastic responses may facilitate or constrain the adaptation of their descendant populations to new environments, complicating their evolutionary trajectories beyond the genetic blueprint. Intriguingly, phenotypic plasticity itself can evolve in terms of its direction and magnitude during adaptation. However, we know little about what determines the evolution of phenotypic plasticity, including gene expression plasticity. Recent laboratory-based studies suggest dominance of reversing gene expression plasticity-plastic responses that move the levels of gene expression away from the new optima. Nevertheless, evidence from natural populations is still limited. Here, we studied gene expression plasticity and its evolution in the montane and lowland populations of an elevationally widespread songbird-the Rufous-capped Babbler (Cyanoderma ruficeps)-with reciprocal transplant experiments and transcriptomic analyses; we set common gardens at altitudes close to these populations' native ranges. We confirmed the prevalence of reversing plasticity in genes associated with altitudinal adaptation. Interestingly, we found a positive relationship between magnitude and degree of evolution in gene expression plasticity, which was pertinent to not only adaptation-associated genes but also the whole transcriptomes from multiple tissues. Furthermore, we revealed that genes with weaker expressional interactions with other genes tended to exhibit stronger plasticity and higher degree of plasticity evolution, which explains the positive magnitude-evolution relationship. Our experimental evidence demonstrates that species may initiate their adaptation to new habitats with genes exhibiting strong expression plasticity. We also highlight the role of expression interdependence among genes in regulating the magnitude and evolution of expression plasticity. This study illuminates how the evolution of phenotypic plasticity in gene expression facilitates the adaptation of species to challenging environments in nature.