Specialization and group size: brain and behavioural correlates of colony size in ants lacking morphological castes

Abstract

Group size in both multicellular organisms and animal societies can correlate with the degree of division of labour. For ants, the task specialization hypothesis (TSH) proposes that increased behavioural specialization enabled by larger group size corresponds to anatomical specialization of worker brains. Alternatively, the social brain hypothesis proposes that increased levels of social stimuli in larger colonies lead to enlarged brain regions in all workers, regardless of their task specialization. We tested these hypotheses in acacia ants (Pseudomyrmex spinicola), which exhibit behavioural but not morphological task specialization. In wild colonies, we marked, followed and tested ant workers involved in foraging tasks on the leaves (leaf-ants) and in defensive tasks on the host tree trunk (trunk-ants). Task specialization increased with colony size, especially in defensive tasks. The relationship between colony size and brain region volume was task-dependent, supporting the TSH. Specifically, as colony size increased, the relative size of regions within the mushroom bodies of the brain decreased in trunk-ants but increased in leaf-ants; those regions play important roles in learning and memory. Our findings suggest that workers specialized in defence may have reduced learning abilities relative to leaf-ants; these inferences remain to be tested. In societies with monomorphic workers, brain polymorphism enhanced by group size could be a mechanism by which division of labour is achieved.

Keywords: Pseudomyrmex spinicola; acacia ants; brain anatomy; division of labour; task specialization.

Figure 1.

Acacia ant (Pseudomyrmex spinicola) transverse brain section and ventral view of head. (a) Brain section highlighting some of the measured neuropiles including: the lamina (la), lobula (lo) and medulla (me) of the optic lobe and the olfactory lobe (ol). In the mushroom bodies, we measured the lip and collar of the lateral (llip and lco) and medial calyces (mlip and mco); the vertical lobe (alpha; not visible) and medial lobe (mlo, beta). (b) Neuropile dimensions of brain sections were used to generate three-dimensional reconstructions of the brain regions to obtain volumetric measurements. Colours correspond to the neuropiles shown in the section; the vertical lobe (vlo), not visible in the two-dimensional section, is shown here. (c) Ventral view of the head showing in blue the contour used to calculate the head area, excluding eyes and mouthparts. (Online version in colour.)

Figure 2.

Proportion of trunk-ants or leaf-ants that were re-sighted working on the same tasks as on the previous day, in relation to colony-size parameters (n = 17 colonies). Re-sighting of an ant performing the same task is a measure of behavioural specialization. The specialization of trunk-ants increased with number of (a) tree spines, (b) workers and (c) tree diameter. Leaf-ants were not more specialized (d) in trees with more spines, nor (e) in colonies with more workers, nor (f) in trees with greater trunk diameter. Correlations of foraging specialization with number of spines and workers are statistically significant when excluding the largest colony (see text).

Figure 3.

Absolute (a) brain volume (n = 63 brains, eight colonies) and (b) head area (n = 98, eight colonies) of acacia ants performing tasks on the trunk (triangles) or foraging on leaves (circles) of the host tree, as a function of colony-size-related traits (see text). The shaded area represents 95% CI for the linear fit. As colony size and task specialization increased, absolute brain volume tended to increase more for trunk- than for leaf-ants, while head size increased equally for both types of ants. (Online version in colour.)

Figure 4.

Relative volume of regions within the mushroom body's calyces, for trunk (triangles) and leaf-ants (circles), as a function of colony-size-related traits (see text). Trunk-ants in smaller colonies have relatively larger volume of (a) lateral lip, (b) medial lip and (c) lateral collar than when living in larger societies. Conversely, those same brain regions are relatively larger in leaf-ants living in larger societies. (d) The medial collar did not change with colony-size-related traits for either of the two types of ants. (Online version in colour.)