Experience-expectant brain plasticity corresponds to caste-specific abiotic challenges in dampwood termites (Zootermopsis angusticollis and Z. nevadensis)

Abstract

Hypotheses for adaptive brain investment predict associations between the relative sizes of functionally distinct brain regions and the sensory/cognitive demands animals confront. We measured developmental differences in the relative sizes of visual processing brain regions (optic lobes) among dampwood termite castes to test whether optic lobe investment matches caste differences in exposure to visually complex environments. The winged primary reproductives (Kings/Queens) on mating flights are the only caste to leave the dark nest cavities and as predicted, Kings/Queens showed greater relative investment in optic lobe tissue than nestbound (neotenic) reproductives and soldiers in two dampwood termite species (Zootermopsis angusticollis and Z. nevadensis). Relative optic lobe size spanned more than an order of magnitude among the castes we studied, suggesting the growth of the optic lobes incurs substantial tissue costs. Optic lobe growth was experience-expectant: the optic lobes of Z. angusticollis brachypterous nymphs, which typically develop into Kings/Queens, were relatively larger than the optic lobes of apterous nymphs, which precede neotenics and soldiers, and relative optic lobe size of nestbound brachypterous nymphs was statistically similar to that of Kings/Queens. Experience-expectant brain tissue growth is rarely documented in insects, likely because it entails high potential costs of tissue production and maintenance and relatively low immediate sensory/cognitive benefits. We develop hypotheses for the conditions under which experience-expectant growth in brain regions could be favored by natural selection.