Abstract
Social insects control brood development by using different thermoregulatory strategies. Camponotus mus ants expose their brood to daily temperature fluctuations by translocating them inside the nest following a circadian rhythm of thermal preferences. At the middle of the photophase brood is moved to locations at 30.8°C; 8 h later, during the night, the brood is transferred back to locations at 27.5°C. We investigated whether daily thermal fluctuations experienced by developing pupae affect the neuroarchitecture in the adult brain, in particular in sensory input regions of the mushroom bodies (MB calyces). The complexity of synaptic microcircuits was estimated by quantifying MB-calyx volumes together with densities of presynaptic boutons of microglomeruli (MG) in the olfactory lip and visual collar regions. We compared young adult workers that were reared either under controlled daily thermal fluctuations of different amplitudes, or at different constant temperatures. Thermal regimes significantly affected the large (non-dense) olfactory lip region of the adult MB calyx, while changes in the dense lip and the visual collar were less evident. Thermal fluctuations mimicking the amplitudes of natural temperature fluctuations via circadian rhythmic translocation of pupae by nurses (amplitude 3.3°C) lead to higher numbers of MG in the MB calyces compared to those in pupae reared at smaller or larger thermal amplitudes (0.0, 1.5, 9.6°C), or at constant temperatures (25.4, 35.0°C). We conclude that rhythmic control of brood temperature by nursing ants optimizes brain development by increasing MG densities and numbers in specific brain areas. Resulting differences in synaptic microcircuits are expected to affect sensory processing and learning abilities in adult ants, and may also promote interindividual behavioral variability within colonies.
Highlights
Temperature has a major impact on the development and life history of insects
We show that daily thermal fluctuations experienced by developing pupae and mediated by circadian rhythmic broodtending behaviors of nurse ants affect the postembryonic development of the mushroom bodies (MBs) calyces in C. mus ants
Effects of daily fluctuating temperatures on young adult ants were most evident at the level of density and number of synaptic boutons (MG) of the MB calyx
Summary
Temperature has a major impact on the development and life history of insects. The thermal range preferred during development is species-specific, and substantial deviations from its boundaries can cause brood abnormalities, increase mortality, or influence developmental times. Under starvation, when protein necessary for larval growth is not available, only pupae and last instar larvae (i.e., in which pupation has already been triggered) are translocated (Roces and Núñez, 1989) This indicates that fluctuating temperature regimes as actively provided by nurse ants to the brood are of particular relevance for postembryonic development during the pupal phase. Their specific effects remain elusive, and differential effects of fluctuating and constant temperatures are not evident in growth parameters such as developmental time or mortality in C. mus (Roces and Núñez, 1989). Using immunolabeling of large presynaptic boutons in complete brains (whole-mounts), we compared neuropil volumes together with synaptic bouton densities in olfactory and visual MB regions of young adult ants reared at different thermal regimes
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