Brain plasticity indicates key cognitive demands in an animal society: caste comparisons in dampwood termites

Neuroecology theory predicts relative investment in brain regions will vary to match differences in behavior. Social insect castes provide exceptional opportunities to test for adaptive brain investment because castes differ in behavior and in cognitive demands. Caste development in dampwood termites (genus Zootermopsis) is complex, providing multiple caste comparisons for testing neuroecological predictions: Zootermopsis termites can remain in a worker-like sterile nymphal caste, develop into sterile defensive soldiers, or follow three distinct pathways to reproductive status (wingless neotenic reproductives, reproductive soldiers, and winged primary reproductives [Queens/Kings]). We measured differences in the relative sizes of key brain neuropils among Zootermopsis termite castes to test which caste-specific behavioral and cognitive demands (reproduction versus worker behavior) best predicted patterns of brain investment. We focused on the Antennal Lobes (centers of chemosensory processing) and the Mushroom Bodies (centers of learning, memory, and sensory integration). There was no evidence that reproductive status was associated with increased investment in either the Antennal Lobes or the Mushroom Bodies. Instead, several caste comparisons supported the hypothesis that labor/task performance was a positive predictor of brain region investment: nymphs (workers) had the greatest relative investment in both Antennal Lobes and Mushroom Bodies, compared to developmentally preceding stages (immature instars I-III) and later castes (soldiers and reproductives). These findings suggest that task performance demands were the main drivers of caste-specific adaptive brain investment in Zootermopsis, and that reproductive status entailed relatively few cognitive challenges.