The ecological dominance of ants in terrestrial ecosystems is unparalleled in the animal kingdom (Wilson, 1971; Folgarait, 1998). Because no other group of social insects reaches equivalent levels of adaptive radiation and species-richness (Hölldobler and Wilson, 1990), it seems that factors in addition to social behavior and division of labor promoted ant diversification. The evolutionary success of ants is indisputably associated with a strong divergence between queens and workers. A caste of flightless workers specialized in non-reproductive activities is unique among social Hymenoptera. However, rather than being just simplified, wingless versions of the queen, the thorax of ant workers has its own specialization. Relative to the thoracic morphology of queens, which is typical of species of flying insects, worker ants have an unusually large T1 and T1-associated muscles, which provide superior strength and mobility to the neck controlling head movements.

Control of the head is of great importance for ant workers, which in some species singly hunt and carry prey up to 30-90 times their weight (Dejean, 2011; Dejean et al., 2012). Among insects, ant carrying behavior is unique in that workers lift their load off the ground. Many other insects can move relatively large objects, but by dragging (e.g., spider wasps) or rolling them (e.g., dung beetles) on the ground, or holding them while flying (e.g., robber flies). Biomechanical studies on grass-cutting ants have shown that workers perform controlled head movements at the neck articulation when transporting large objects (Moll et al., 2010). Precise head movements are essential to reduce displacement of the center of mass, and retain stability while carrying objects many times the workers’ weight and length. Our finding that worker ants differ from queens and other flying insects in the configuration and size of the T1-associated muscles suggests that ants can achieve this biomechanical feat by virtue of their specialized neck musculature. This represents a striking structural innovation, differentiating ant workers from the typical flying insects, which had not been recognized until now. Their distinctive internal skeletomuscular modifications presumably enhance their behavior as flightless foragers and heavy-load transporters. We propose that the modified T1 was an innovation that helped ants to use their heads and mandibles in novel ways, and hence exploit a broader spectrum of trophic resources. Compared to social bees and wasps (Hölldobler and Wilson, 1990), where worker morphology is constrained by the requirements of a winged thorax, mandibular morphology and function have specialized enormously across ant lineages (Paul and Gronenberg, 1999), in parallel with their much greater diversification of foraging habits.

Our analysis also showed that queens fall in two distinct anatomical types that evolved in association with the two strategies of independent colony founding. Foraging activity during independent foundation is high in non-claustral species vs absent in claustral species. Non-claustral queens have a T1 that is closer in size to that of workers, while claustral queens, which do not go through a worker-like phase, have a much more reduced T1. Unfortunately, biomechanical data of neck strength in queens are difficult to obtain because they are evasive and, especially in claustral species, cannot be induced to carry objects. Claustral queens have an enlarged T2 relative to non-claustral queens, reflecting the existence of massive wing muscles (Figure 2A). A correlation between increased wing muscle mass and claustral behavior has been suggested before: these larger muscles do not function to enhance flight, rather they are a solution for storing amino acids that are essential for feeding the first generation of workers without outside foraging (Jones et al., 1978; Peeters, 2012) . We speculate that, during the acquisition of claustral behavior, the decrease in foraging activity lessened the constraint on the size of T1, thus allowing T2 to expand and accommodate larger wing muscles as metabolic reserves. Differences in the nesting habits of queens, such as excavating a nest vs nesting in pre-existing cavities, might also impose variable muscle requirements. However, this type of behavioral differences occurs across species in a scattered pattern that does not match the anatomical categories we revealed. There are examples of nest excavating by queens with ‘intermediate’ (e.g., Amblyopone) and ‘reduced’ T1 (e.g., Pogonomyrmex), and of nesting in pre-existing cavities by ‘intermediate’ (e.g., Tetraponera) as well as ‘reduced’ T1 (e.g., Leptothorax) species.

While data on queen morphology is readily accessible from museum collections for many species, knowledge about their founding behavior remains sparse. There is no published information in many important genera, possibly because this requires field observations of behavior at an appropriate time of the year. Our findings provide a means of predicting colony foundation strategy from the morphology of the queen thorax, and thus guide field research on particular species of interest. For example, within the subfamily Myrmicinae (clade 14 in Figure 3), the genera Cataulacus and Metapone show independent reversals to an ‘intermediate T1’ in queens, suggesting that colony foundation is not claustral as in closely related genera. Importantly, the phylogenetic component of our correlation provides a powerful tool to infer the ecology of extinct clades for which behavioral observations are impossible. For example, we lack data on queens of two early lineages, the extinct Sphecomyrma† and the enigmatic Martialis, but based on our reconstructions we can predict that they will have an ‘intermediate T1’ and behave non-claustrally.

Our finding that the ratio of the lengths of T1 and T2 is inverted between queens and workers suggests that a morphological trade-off was at play in determining the relative size of these two segments. It is likely that T1 can become hypertrophied only at the expense of a reduced, non-functional T2. Indeed, our anatomical analysis showed that some of the internal modifications of T1 in workers are only possible in conjunction with a complete absence of wing muscles. Conversely, only queens with a highly reduced T1 have an expanded T2 that constitutes most of the thoracic dorsum (queens with intermediate T1 are also intermediate for T2, see Figure 1B). This morphological trade-off between adjacent body segments can occur due to competition for metabolic resources during pre-adult development (Nijhout and Emlen, 1998). It is possible that the functional cost of enlarging T2 (reserves for colony founding) at the expense of T1 (reduced neck strength and work performance), occurred when founding behavior gradually shifted to claustral, with a decreased need to forage outside the nest.