Expression and function of a limb-patterning gene Distal-less in the soldier-specific morphogenesis in the nasute termite Nasutitermes takasagoensis

One of the major foci in evolutionary developmental biology is to understand developmental mechanisms that underlie the acquisition of morphological novelties. Termite soldiers, the highly specialized defensive caste, show exaggerated species-specific morphologies, mostly enlarged mandibles. Soldiers of the subfamily Nasutitermitinae (Termitidae), however, possess a novel structure for defense in their heads, that is a horn-like frontal projection (nasus) from which defensive chemicals are discharged. Just prior to the molt into presoldiers (the preceding stage to soldiers) from workers, a nasus disc, or a nasus primordium, is observed under the worker head cuticle. In order to understand the developmental underpinnings of this evolutionarily novel structure, the role of a homeobox gene Distal-less (Dll) during nasus development was examined in this study, using a nasute termite Nasutitermes takasagoensis. Histological observations showed that complex developmental processes comprising epidermal evagination and invagination through changes in cell shape and cell proliferation formed the projection and the gland. Immunohistochemistry showed that Dll was localized in the developing nasus disc, but not in the frontal-gland primordium. Consistent with this finding, Dll RNA interference only repressed nasus growth not the frontal-gland formation. Taken together, the co-option of Dll is suggested to contribute to the acquisition of a novel defensive structure in a termite lineage, coupled with the acquisition of adaptive defensive behaviors.