Closing the oral cavity: Evolution of a novel labro-maxillary interlocking mechanism in ants (Hymenoptera: Formicidae)

Ants are dominant animals in terrestrial ecosystems. Their success is arguably related to their unique combination of a eusocial, ground-oriented, and predatory lifestyle. A suite of morphological features has been related to ants’ eusocial life on the ground, including the wingless worker caste and an antibiotic gland. However, these characters do not necessarily correlate functionally with the ant’s major ecological role as predators and territory/ nest defenders. Here we describe a mechanical innovation that may be crucial for this role: when ants retract their mouthparts, the labrum interlocks with both maxillae through cuticular outgrowths. The maxillae push onto labral arms, which in turn pushes the labrum onto maxillae and labium, tightly holding the pieces inside the oral cavity. We hypothesize that this mechanism effectively shields the feeding apparatus when not in use, leaving the mandibles free to be used as tools during predation and combat. Examination of 170 species representing all ant subfamilies and several outgroups suggests that the mechanism is autapomorphic for Formicidae and comes in various modifications of distal maxilla and labral arm shape. We reconstruct the evolution of the interaction and attempt to relate different levels of interlocking to ant ecology. We do find support using several lines of evidence for dependent evolution between ant diet and the ability to interlock the mouthparts, supporting our hypothesis for improved protection. We call for focused biomechanical study of ant mouthparts to better understand the mechanical consequences of the interlocking and its potential role in the ecological dominance of ants.