Glandular innovations for a tunnelling life: Silk and associated leg glands in Melissotarsus and Rhopalomastix queen and worker ants

As in other Hymenoptera, adult ants cannot secrete silk, unlike the larvae that spin a cocoon prior to metamorphosis. Fisher and Robertson (1999) first showed the existence of a silk gland in the head of adult Melissotarsus beccarii workers, and we confirm this with detailed histology and ultrastructural comparisons of both queens and workers. This African genus exhibits extreme morphological adaptations (legs, head shape and mandibular muscles) for tunnelling behaviour inside living trees, that underlie an obligate mutualism with scale insects. Rhopalomastix is its sister genus distributed across Asia, and we show that queens and workers also have a silk gland. This lineage of minute workers relies on silk to secure their network of tunnels against other arboreal ants. We show striking differences between these genera in the anatomy and ultrastructure of the cells that secrete silk, especially numerous vacuoles and an unexpectedly branched end apparatus in Melissotarsus. Moreover, the legs of Melissotarsus are much more specialized for tunnelling, and this includes highly expanded basitarsi. The latter house the novel ‘Delage-Darchen gland’, and we document its anatomy and ultrastructure, suggesting a proteinaceous secretion to harden roofs made of silk combined with wood fragments. The restriction of the Delage-Darchen gland to Melissotarsus, combined with a modified silk gland (an almost three-fold increase in the number of secretory cells, and ultrastructural differences suggestive of higher secretory activity), are evidence of an outstanding evolutionary divergence relative to Rhopalomastix. Synthesis of silk by adults is a significant innovation among ants, but its augmented production in Melissotarsus makes them better adapted for the hazards of arboreal life. [Display omitted] •Melissotarsus and Rhopalomastix ants chew network of tunnels in live trees to house scale insects.•Both workers and queens have head glands producing silk to secure tunnel roofs.•Ultrastructure of silk glands differs between genera, suggesting increased synthesis in Melissotarsus.•Enlarged basitarsus in Melissotarsus workers houses exocrine gland that may bind silk and wood in tunnel roofs.•Evolutionary divergence in glands between genera underlies more extreme tunnelling of Melissotarsus.