Ecdysone Antagonizes Growth and Juvenile Hormone-Dependent Soldier Caste Identity in Camponotus floridanus

From tardigrades to lobsters, ecdysone is the critical steroid hormone regulating ecdysis across Panarthropoda. In insects, the sesquiterpenoid hormone called juvenile hormone (JH) prolongs the juvenile state, and together, ecdysone and JH regulate growth and developmental timing. The complex worker caste system in ants has elaborated multiple times and is composed of individuals exhibiting an array of size and allometry variation. While we have accumulated a great deal of knowledge related to the role of JH in influencing size and caste identity in ants, the role of ecdysone in caste development remains poorly understood. Here we show in Camponotus floridanus that ecdysone negatively regulates size, can block soldier determination, and there is an antagonistic relationship between JH and ecdysone. First, we show that during the worker-soldier switchpoint sensitivity window of development, ecdysone is capable of negatively influencing head size, body size, head-to-body allometry, and unexpectedly extends developmental timing. We then show at the molecular level that as expected, developing soldiers upregulate ecdysone degradation, yet surprisingly, developing soldiers also upregulate ecdysone synthesis and the reception of ecdysone signalling. We next investigated the interaction between JH and ecdysone signaling and found that the two hormones antagonize each other at both the molecular and phenotypic levels. Furthermore, in contrast to other insects, we uncovered that ecdysone signaling is negatively regulated by temperature. Beyond its role in size regulation, we also provide preliminary data suggesting that the interaction of JH and ecdysone may have sex inducing properties, generating male-like anomalies. Altogether, our findings show that ecdysone blocks JH-dependent soldier development and we propose that the dynamic regulation of ecdysone synthesis, reception, and degradation may be the basis for the complex sigmoid-like head-to-body allometry found in this species as well as several others across ants. More generally, the evolutionary tinkering of antagonistic growth hormones, their regulation and interaction, and opposing responses to environmental cues, may be a major source for size diversity across developmentally plastic organisms.