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Daily Thermal Fluctuations Experienced by Pupae via Rhythmic Nursing Behavior Increase Numbers of Mushroom Body Microglomeruli in the Adult Ant Brain.

Falibene A, Roces F, Rössler W, Groh C - Front Behav Neurosci (2016)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg Würzburg, Germany.

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.

No MeSH data available.


Related in: MedlinePlus

Pupal thermal experience effects on the number of MB calyx synaptic boutons in the adult brain. Pupae reared at (A) different amplitudes of fluctuating temperature but the same mean temperature or (B) different constant temperature regimes. Number of synaptic boutons per calyx in the D lip, ND lip, collar, and the sum of all three regions (total number of boutons per calyx). Gray area shows the temperature regime selected by nurses for brood translocation. Symbols represent the mean value of each group and lines the S.E. Different letters indicate significant differences among amplitudes or between constant temperatures. D and ND lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 10; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 9, N25.4 = 11, N35 = 9; total: N0 = 10, N1.5 = 8, N3.3 = 10, N9.6 = 9, N25.4 = 11, N35 = 9.
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Figure 5: Pupal thermal experience effects on the number of MB calyx synaptic boutons in the adult brain. Pupae reared at (A) different amplitudes of fluctuating temperature but the same mean temperature or (B) different constant temperature regimes. Number of synaptic boutons per calyx in the D lip, ND lip, collar, and the sum of all three regions (total number of boutons per calyx). Gray area shows the temperature regime selected by nurses for brood translocation. Symbols represent the mean value of each group and lines the S.E. Different letters indicate significant differences among amplitudes or between constant temperatures. D and ND lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 10; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 9, N25.4 = 11, N35 = 9; total: N0 = 10, N1.5 = 8, N3.3 = 10, N9.6 = 9, N25.4 = 11, N35 = 9.

Mentions: Extrapolation of the total number of synaptic boutons per calyx showed significant differences among ants reared at different thermal regimes (Figure 5). As observed for the bouton densities, temperature experienced during the pupal phase had the greatest effect on the ND subregion of the MB calyx olfactory lip in both the fluctuating [amplitude: F(3, 37) = 4.68, p = 0.0072; covariate size: F(1, 37) = 10.82, p = 0.0022; ANCOVA; Figure 5A] and constant temperature series [temperature: F(1, 18) = 6.50, p = 0.02; covariate size: F(1, 18) = 0.34, p = 0.56; ANCOVA; Figure 5B]. The largest total number of ND lip boutons was found in those ants reared under a 3.3°C amplitude (~104,000 boutons per calyx lip), while ants reared under 0.0, 1.5, and 9.6°C amplitude showed on average 73, 82, and 81% of this number. Ants reared at 25.4°C constant temperature had on average 69% of the ND lip boutons when compared with ants reared at 35.0°C (~96,000 boutons per calyx). The total number of boutons in the D lip was not affected by the experienced temperature [fluctuating temperature: amplitude: F(3, 37) = 1.26, p = 0.30; covariate size: F(1, 37) = 1.27, p = 0.27; constant temperature: temperature: F(1, 18) = 0.71, p = 0.41; covariate size: F(1, 18) = 1.44, p = 0.25; ANCOVA]. Assuming that calyx volumes and bouton densities are equal for the medial and the lateral calyx, and for both brain hemispheres, we then estimated a rough total number of lip boutons per brain (extrapolated to all four calyces) of ~508,000 in those ants reared under a 3.3°C amplitude, whereas in those reared at 0.0, 1.5, and 9.6°C amplitude the estimated total numbers averaged ~391,000, ~428,000, and ~443,000 boutons, respectively.


Daily Thermal Fluctuations Experienced by Pupae via Rhythmic Nursing Behavior Increase Numbers of Mushroom Body Microglomeruli in the Adult Ant Brain.

Falibene A, Roces F, Rössler W, Groh C - Front Behav Neurosci (2016)

Pupal thermal experience effects on the number of MB calyx synaptic boutons in the adult brain. Pupae reared at (A) different amplitudes of fluctuating temperature but the same mean temperature or (B) different constant temperature regimes. Number of synaptic boutons per calyx in the D lip, ND lip, collar, and the sum of all three regions (total number of boutons per calyx). Gray area shows the temperature regime selected by nurses for brood translocation. Symbols represent the mean value of each group and lines the S.E. Different letters indicate significant differences among amplitudes or between constant temperatures. D and ND lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 10; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 9, N25.4 = 11, N35 = 9; total: N0 = 10, N1.5 = 8, N3.3 = 10, N9.6 = 9, N25.4 = 11, N35 = 9.
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Figure 5: Pupal thermal experience effects on the number of MB calyx synaptic boutons in the adult brain. Pupae reared at (A) different amplitudes of fluctuating temperature but the same mean temperature or (B) different constant temperature regimes. Number of synaptic boutons per calyx in the D lip, ND lip, collar, and the sum of all three regions (total number of boutons per calyx). Gray area shows the temperature regime selected by nurses for brood translocation. Symbols represent the mean value of each group and lines the S.E. Different letters indicate significant differences among amplitudes or between constant temperatures. D and ND lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 10; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 9, N25.4 = 11, N35 = 9; total: N0 = 10, N1.5 = 8, N3.3 = 10, N9.6 = 9, N25.4 = 11, N35 = 9.
Mentions: Extrapolation of the total number of synaptic boutons per calyx showed significant differences among ants reared at different thermal regimes (Figure 5). As observed for the bouton densities, temperature experienced during the pupal phase had the greatest effect on the ND subregion of the MB calyx olfactory lip in both the fluctuating [amplitude: F(3, 37) = 4.68, p = 0.0072; covariate size: F(1, 37) = 10.82, p = 0.0022; ANCOVA; Figure 5A] and constant temperature series [temperature: F(1, 18) = 6.50, p = 0.02; covariate size: F(1, 18) = 0.34, p = 0.56; ANCOVA; Figure 5B]. The largest total number of ND lip boutons was found in those ants reared under a 3.3°C amplitude (~104,000 boutons per calyx lip), while ants reared under 0.0, 1.5, and 9.6°C amplitude showed on average 73, 82, and 81% of this number. Ants reared at 25.4°C constant temperature had on average 69% of the ND lip boutons when compared with ants reared at 35.0°C (~96,000 boutons per calyx). The total number of boutons in the D lip was not affected by the experienced temperature [fluctuating temperature: amplitude: F(3, 37) = 1.26, p = 0.30; covariate size: F(1, 37) = 1.27, p = 0.27; constant temperature: temperature: F(1, 18) = 0.71, p = 0.41; covariate size: F(1, 18) = 1.44, p = 0.25; ANCOVA]. Assuming that calyx volumes and bouton densities are equal for the medial and the lateral calyx, and for both brain hemispheres, we then estimated a rough total number of lip boutons per brain (extrapolated to all four calyces) of ~508,000 in those ants reared under a 3.3°C amplitude, whereas in those reared at 0.0, 1.5, and 9.6°C amplitude the estimated total numbers averaged ~391,000, ~428,000, and ~443,000 boutons, respectively.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Würzburg Würzburg, Germany.

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.

No MeSH data available.


Related in: MedlinePlus