Ecdysone coordinates plastic growth with robust pattern in the developing wing

Abstract

Animals develop in unpredictable, changing environments. To do this, they adjust their development according to environmental conditions to generate plastic variation in traits, while also buffering against environmental change to produce robust phenotypes. However, how organ development is coordinated to accommodate both plastic and robust developmental responses is poorly understood. Here, we propose that the steroid hormone ecdysone coordinates both plasticity in organ size and robustness of organ pattern in the developing wings of the fruit fly Drosophila melanogaster. Ablating the prothoracic glands (PGX), which synthesise and secrete ecdysone, resulted in wing discs that were reduced in size and delayed in the progression of Achaete and Senseless pattern. These effects were rescued by adding ecdysone to the food. Further, while wing growth was driven by both ecdysone and nutrition, ecdysone alone induced the progression of wing patterning. To further explore this difference in response, we quantified wing growth and patterning in PGX larvae that were either fed on standard diet or starved of yeast across a range of ecdysone concentrations. Disc growth rates increased in a graded, linear manner with ecdysone concentration in starved larvae. In contrast, Achaete and Senseless patterning rates showed threshold responses regardless of diet. This means that ecdysone confers robustness by turning on patterning once it exceeds threshold concentrations, while inducing graded responses for disc growth, tuning growth to environmental conditions. This potentially represents a generalizable mechanism through which hormones coordinate plastic growth with robust patterning in the face of environmental change.