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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

Temperature effects on synaptic bouton densities. (A) Examples of synapsin-IR bouton quantification in the ND lip of ants reared at 0.0, 1.5, 3.3, and 9.6°C of thermal amplitude (mean temperature, Tm: 28.6°C). Single confocal image of a 10 × 10 μm2 synapsin-stained area in the ND lip (bottom) and 3D reconstruction (top) of the position of the boutons visualized by AMIRA in a 1000 μm3–volume (10 × 10 × 10 μm3). Each yellow sphere marks the center of a synapsin-IR bouton. (B–E) Presynaptic bouton densities in (B,C) the olfactory D and ND lip and (D,E) the visual collar input regions of the MB calyces of ants (B,D) reared at different amplitudes of fluctuating temperature but the same mean temperature or (C,E) different constant temperature regimes. 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. Lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 11; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 10, N25.4 = 11, N35 = 10.
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Figure 4: Temperature effects on synaptic bouton densities. (A) Examples of synapsin-IR bouton quantification in the ND lip of ants reared at 0.0, 1.5, 3.3, and 9.6°C of thermal amplitude (mean temperature, Tm: 28.6°C). Single confocal image of a 10 × 10 μm2 synapsin-stained area in the ND lip (bottom) and 3D reconstruction (top) of the position of the boutons visualized by AMIRA in a 1000 μm3–volume (10 × 10 × 10 μm3). Each yellow sphere marks the center of a synapsin-IR bouton. (B–E) Presynaptic bouton densities in (B,C) the olfactory D and ND lip and (D,E) the visual collar input regions of the MB calyces of ants (B,D) reared at different amplitudes of fluctuating temperature but the same mean temperature or (C,E) different constant temperature regimes. 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. Lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 11; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 10, N25.4 = 11, N35 = 10.

Mentions: Brains of ants reared at different amplitudes of fluctuating temperature significantly differed in the density of synapsin-IR boutons in the ND subregion of the olfactory lip of the MB calyces (Figure 4). ND lip boutons had the highest packing density in those ants reared at 3.3°C thermal amplitude [amplitude: F(3, 38) = 6.31, p = 0.0014; covariate size: F(1, 38) = 19.75, p = 0.0001; ANCOVA; Figures 4A,B], the regime that resembled the daily thermal preferences of nurses for brood rearing. Workers reared under a constant temperature of 28.6°C (amplitude 0.0°C) or under a high temperature variation (amplitude 9.6°C) showed significantly lower ND lip bouton densities than those under a thermal amplitude of 3.3°C. Workers reared under 1.5°C thermal amplitude showed intermediate values. Furthermore, bouton densities in the ND lip significantly correlated with ant size (Table 3). In the constant temperature series, the ND lip bouton density was significantly higher in ants reared at 35.0°C compared to those reared at 25.4°C [temperature: F(1, 19) = 7.59, p = 0.013; covariate size: F(1, 19) = 0.69, p = 0.42; ANCOVA; Figure 4C]. Most interestingly, variations in bouton densities was subregion-specific within the lip as no significant differences among fluctuating temperature treatments were found for the D lip subregion [amplitude: F(3, 38) = 2.86, p = 0.05; covariate size: F(1, 38) = 2.00, p = 0.17; ANCOVA; Figure 4B], nor between groups that had experienced constant temperatures [temperature: F(1, 19) = 1.08, p = 0.31; covariate size: F(1, 19) = 3.99, p = 0.06; ANCOVA; Figure 4C]. D lip bouton density was lower in ants reared under a 9.6°C amplitude, but differences were not statistically significant in comparison with those ants reared under smaller thermal amplitudes.


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)

Temperature effects on synaptic bouton densities. (A) Examples of synapsin-IR bouton quantification in the ND lip of ants reared at 0.0, 1.5, 3.3, and 9.6°C of thermal amplitude (mean temperature, Tm: 28.6°C). Single confocal image of a 10 × 10 μm2 synapsin-stained area in the ND lip (bottom) and 3D reconstruction (top) of the position of the boutons visualized by AMIRA in a 1000 μm3–volume (10 × 10 × 10 μm3). Each yellow sphere marks the center of a synapsin-IR bouton. (B–E) Presynaptic bouton densities in (B,C) the olfactory D and ND lip and (D,E) the visual collar input regions of the MB calyces of ants (B,D) reared at different amplitudes of fluctuating temperature but the same mean temperature or (C,E) different constant temperature regimes. 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. Lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 11; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 10, N25.4 = 11, N35 = 10.
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Figure 4: Temperature effects on synaptic bouton densities. (A) Examples of synapsin-IR bouton quantification in the ND lip of ants reared at 0.0, 1.5, 3.3, and 9.6°C of thermal amplitude (mean temperature, Tm: 28.6°C). Single confocal image of a 10 × 10 μm2 synapsin-stained area in the ND lip (bottom) and 3D reconstruction (top) of the position of the boutons visualized by AMIRA in a 1000 μm3–volume (10 × 10 × 10 μm3). Each yellow sphere marks the center of a synapsin-IR bouton. (B–E) Presynaptic bouton densities in (B,C) the olfactory D and ND lip and (D,E) the visual collar input regions of the MB calyces of ants (B,D) reared at different amplitudes of fluctuating temperature but the same mean temperature or (C,E) different constant temperature regimes. 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. Lip: N0 = 13, N1.5 = 9, N3.3 = 10, N9.6 = 11, N25.4 = 11, N35 = 11; collar: N0 = 10, N1.5 = 8, N3.3 = 11, N9.6 = 10, N25.4 = 11, N35 = 10.
Mentions: Brains of ants reared at different amplitudes of fluctuating temperature significantly differed in the density of synapsin-IR boutons in the ND subregion of the olfactory lip of the MB calyces (Figure 4). ND lip boutons had the highest packing density in those ants reared at 3.3°C thermal amplitude [amplitude: F(3, 38) = 6.31, p = 0.0014; covariate size: F(1, 38) = 19.75, p = 0.0001; ANCOVA; Figures 4A,B], the regime that resembled the daily thermal preferences of nurses for brood rearing. Workers reared under a constant temperature of 28.6°C (amplitude 0.0°C) or under a high temperature variation (amplitude 9.6°C) showed significantly lower ND lip bouton densities than those under a thermal amplitude of 3.3°C. Workers reared under 1.5°C thermal amplitude showed intermediate values. Furthermore, bouton densities in the ND lip significantly correlated with ant size (Table 3). In the constant temperature series, the ND lip bouton density was significantly higher in ants reared at 35.0°C compared to those reared at 25.4°C [temperature: F(1, 19) = 7.59, p = 0.013; covariate size: F(1, 19) = 0.69, p = 0.42; ANCOVA; Figure 4C]. Most interestingly, variations in bouton densities was subregion-specific within the lip as no significant differences among fluctuating temperature treatments were found for the D lip subregion [amplitude: F(3, 38) = 2.86, p = 0.05; covariate size: F(1, 38) = 2.00, p = 0.17; ANCOVA; Figure 4B], nor between groups that had experienced constant temperatures [temperature: F(1, 19) = 1.08, p = 0.31; covariate size: F(1, 19) = 3.99, p = 0.06; ANCOVA; Figure 4C]. D lip bouton density was lower in ants reared under a 9.6°C amplitude, but differences were not statistically significant in comparison with those ants reared under smaller thermal amplitudes.

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