Juvenile Hormone Signalling Underlies the Switchpoint and Differentiation of Soldiers in Camponotus floridanus

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Abstract

Multicellular organisms are composed of various cell types derived from cellular determination and differentiation, which carry out specialized functions in the individual. Ant societies are composed of various castes of individuals derived from caste determination and differentiation, which divide specialized tasks in the colony. From cells to societies, the underlying mechanisms orchestrating determination and differentiation at different biological levels are fundamental in generating biological diversity. While past work has described the developmental process of caste determination and differentiation in ants, the endocrinological and molecular basis for these processes in the genus Camponotus remains unknown. Here we show that minor worker and soldier development is determined by a Juvenile hormone (JH)-mediated minor-soldier switchpoint in C. floridanus . Hormonal treatments identified a sensitivity period when JH can induce bipotential larvae to become soldiers. Induced soldiers phenocopy natural soldiers in size and soldier-specific head-to-body allometry and this is associated with a heterochronic shift in metamorphosis. Furthermore, we molecularly characterize the activity of the JH pathway at the level of synthesis, degradation, reception, and downstream effectors during caste determination and differentiation. Surprisingly, rather than JH synthesis, we found JH reception and JH degradation are the major signalling processes differentially regulated across castes and RNAi of juvenile hormone degradation enzymes generates soldiers. Finally, our data suggests that the hyperdiverse genus Camponotus has independently evolved a JH-mediated minor-soldier switchpoint similar to that known in Pheidole . More generally, the evolution of plastic hormonal regulation may facilitate the origin of developmental determination and differentiation processes underlying complex adaptive phenotypes.

Significance Statement

Ants live in complex societies like a superorganism where individuals divide reproductive and various non-reproductive labors, which are analogous to the array of functions of germ cells and highly differentiated somatic cells in an organism. While there are over 1500 species of the hyperdiverse genus Camponotus , a genus whose diversity reflects their complex caste system including minor workers and soldiers, the molecular and endocrinological basis for how these castes develop remains unknown. Here we have identified a juvenile hormone (JH) mediated minor-soldier switchpoint during larval development, and have characterized components of the JH signalling pathway that regulate soldier development. This work enables further understanding of how castes are regulated across ants and social insects more broadly.

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