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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 the adult MB calyx volume. (A,B) Volume of the olfactory lip and (C,D) the visual collar input regions of the MB calyces of ants reared at (A,C) different amplitudes of fluctuating temperature but the same mean temperature or (B,D) 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 treatments with different amplitudes or between those with different constant temperatures. Lip and collar: N0 = 13, N1.5 = 9, N3.3 = 12, N9.6 = 10, N25.4 = 14, N35 = 12.
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Figure 3: Temperature effects on the adult MB calyx volume. (A,B) Volume of the olfactory lip and (C,D) the visual collar input regions of the MB calyces of ants reared at (A,C) different amplitudes of fluctuating temperature but the same mean temperature or (B,D) 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 treatments with different amplitudes or between those with different constant temperatures. Lip and collar: N0 = 13, N1.5 = 9, N3.3 = 12, N9.6 = 10, N25.4 = 14, N35 = 12.

Mentions: An example of a 2-day old adult ant brain labeled with anti-synapsin and its 3D reconstruction is shown in Figure 1. The olfactory lip region of the MBs showed no statistically significant volumetric differences among ants that had experienced different fluctuating temperature treatments [total lip volume, amplitude: F(3, 39) = 2.66, p = 0.06; covariate size: F(1, 39) = 0.04, p = 0.85; ANCOVA; Figure 3A]. Those ants that experienced a high thermal amplitude (9.6°C) during the pupal phase tended to develop bigger lip regions, but differences were not statistically significant in comparison with those reared under smaller thermal amplitudes. No differences were found for the total lip volume between different constant temperatures [temperature: F(1, 23) = 1.11, p = 0.30; covariate size: F(1, 23) = 0.01, p = 0.93; ANCOVA; Figure 3B].


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 the adult MB calyx volume. (A,B) Volume of the olfactory lip and (C,D) the visual collar input regions of the MB calyces of ants reared at (A,C) different amplitudes of fluctuating temperature but the same mean temperature or (B,D) 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 treatments with different amplitudes or between those with different constant temperatures. Lip and collar: N0 = 13, N1.5 = 9, N3.3 = 12, N9.6 = 10, N25.4 = 14, N35 = 12.
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Related In: Results  -  Collection

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Figure 3: Temperature effects on the adult MB calyx volume. (A,B) Volume of the olfactory lip and (C,D) the visual collar input regions of the MB calyces of ants reared at (A,C) different amplitudes of fluctuating temperature but the same mean temperature or (B,D) 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 treatments with different amplitudes or between those with different constant temperatures. Lip and collar: N0 = 13, N1.5 = 9, N3.3 = 12, N9.6 = 10, N25.4 = 14, N35 = 12.
Mentions: An example of a 2-day old adult ant brain labeled with anti-synapsin and its 3D reconstruction is shown in Figure 1. The olfactory lip region of the MBs showed no statistically significant volumetric differences among ants that had experienced different fluctuating temperature treatments [total lip volume, amplitude: F(3, 39) = 2.66, p = 0.06; covariate size: F(1, 39) = 0.04, p = 0.85; ANCOVA; Figure 3A]. Those ants that experienced a high thermal amplitude (9.6°C) during the pupal phase tended to develop bigger lip regions, but differences were not statistically significant in comparison with those reared under smaller thermal amplitudes. No differences were found for the total lip volume between different constant temperatures [temperature: F(1, 23) = 1.11, p = 0.30; covariate size: F(1, 23) = 0.01, p = 0.93; ANCOVA; Figure 3B].

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