The Environmental, Endocrine, and Epigenetic Basis of Size Plasticity in a Superorganism

From plants to animals, genomes are responsive to environmental variation, the interaction of which can influence developmental processes and facilitate profound consequences on life-history and evolution. The interplay between genes and the environment is known to be mediated by the action of endocrine and epigenetic mechanisms including histone modifications. Ant development is plastic: environmental changes can induce diverse phenotypes, generating different castes that distinguish individuals by size, behaviour, and reproduction. While recent work has demonstrated that hormonal and epigenetic mechanisms underlie caste-specific trait variation in ants, the interplay of these mechanisms, and the process by which they mediate environmental changes to produce distinct trait variation, remains enigmatic. Here, we use the invasive fire ant Solenopsis invicta, dubbed a superorganism and known for its extreme worker caste size variation, to investigate the interplay between endocrine and epigenetic mechanisms in response to environmental variation. We found that sizing and developmental timing are both thermally and nutritionally plastic, influenced by juvenile hormone, ecdysone, histone (de)acetylation, and histone (de)methylation, and that these mediators interact and are thermally and nutritionally plastic. Surprisingly, fire ants break the Temperature-Size Rule, ecdysone makes ants bigger faster, and histone methylation disruption unexpectedly makes ants smaller. These and other findings suggest that an endocrine-epigenetic axis mediates thermal and nutritional plasticity underlying the extreme size variation that has evolved in the complex worker caste system in fire ants. More generally, we propose that an environment-endocrine-epigenetic (E3) approach will provide an integrative perspective on the development and evolution of adaptive phenotypes.