Extreme morphological adaptations in Melissotarsus worker ants counterbalanced by flying queens
Adam Khalife, Roberto Keller , Johan Billen , Francisco Hita Garcia , Evan Economo , Christian Peeters
Sorbonne Université, CNRS, Institut d'Ecologie et des Sciences de l'Environnement, 75005 Paris, France; MUHNAC/cE3c – Centre for Ecology, Evolution and Environmental Changes, Faculdade de Ciências da Universidade de Lisboa, Lisbon, Portugal ; Laboratory of Entomology, K.U. Leuven, Belgium ; Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology, Japan ; Biodiversity and Biocomplexity Unit, Okinawa Institute of Science and Technology, Japan ; Sorbonne Université, CNRS, Institut d’Écologie et des Sciences de l’Environnement, 75005 Paris, France
Melissotarsus ants are highly specialized parasites of living trees, chewing extensive galleries under bark that allow thousands of diaspidid scale insects to feed in a protected environment. Direct observations are problematic in situ, but morphology (SEM, histology, microCT) allows strong predictions about behavior. The minute workers (2-2.5mm long) have dorsoventrally enlarged heads packed with muscles powering short conical mandibles with sharp teeth. Their mid- and hindlegs are strikingly modified for tunnelling activities, hence they cannot walk outside the host trees. A commitment to life with diaspidids explains reduced eyes (12 ommatidia) and loss of the sting (together with most petiole muscles). Specialisation for parasitism is commonly associated with a reduced task repertoire, but there is a twist in ants with a queen caste capable of independent colony foundation. Melissotarsus queens have large eyes (about 138 ommatidia) and normal legs; after flying to a suitable tree, they initiate a shelter under bark and gather appropriate diaspidid partners. Chewing wood abrades the zinc-reinforced mandibles so that old workers become incapable of tunnelling. Given the lack of outside foraging, the activities of old workers are a puzzle. Single eggs, larvae and pupae are scattered in the galleries, and larvae feed individually on diaspidid secretions, so workers engage little in brood care except for moving eggs from ovipositing queens to diaspidid aggregates. Melissotarsus adults are unique among ants for the ability to secrete and spin silk, which is used to close breaches in galleries. Emergency repairs are the sole defence against other ants and insects, and it appears that young and old workers are involved. Idiosyncracies of workers in this genus have intriguing consequences on age polyethism. Although queen-worker divergence in body size is limited, flying compensates for reduced behavioral repertoires resulting from extreme adaptations in morphology.