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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

(A,B) Pupal developmental time and (C,D) mortality rates of individuals reared at (A,C) different amplitudes of fluctuating temperature or (B,D) constant temperature regimes. Developmental time is shown as boxplots: boxes show quartiles, whiskers provide the minimum and maximum values, and small squares represent medians. Percentage of pre- and post- eclosion mortality for each group is indicated by black and white bars, respectively. Gray area indicates the temperature regime selected by nurses for brood translocation. Different letters show significant differences among different amplitudes of fluctuating temperature or between constant temperatures regimes. Developmental time: N0 = 15, N1.5 = 14, N3.3 = 13, N9.6 = 16, N25.4 = 18, N35 = 18. Mortality: N0 = 15, N1.5 = 16, N3.3 = 15, N9.6 = 16, N25.4 = 20, N35 = 23.
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Figure 2: (A,B) Pupal developmental time and (C,D) mortality rates of individuals reared at (A,C) different amplitudes of fluctuating temperature or (B,D) constant temperature regimes. Developmental time is shown as boxplots: boxes show quartiles, whiskers provide the minimum and maximum values, and small squares represent medians. Percentage of pre- and post- eclosion mortality for each group is indicated by black and white bars, respectively. Gray area indicates the temperature regime selected by nurses for brood translocation. Different letters show significant differences among different amplitudes of fluctuating temperature or between constant temperatures regimes. Developmental time: N0 = 15, N1.5 = 14, N3.3 = 13, N9.6 = 16, N25.4 = 18, N35 = 18. Mortality: N0 = 15, N1.5 = 16, N3.3 = 15, N9.6 = 16, N25.4 = 20, N35 = 23.

Mentions: Temperature experienced during the pupal phase affected the time of pupal development until eclosion. Under temperature regimes fluctuating around the same mean yet with different amplitudes, pupal developmental time varied with the thermal amplitude (H3, N = 58 = 20.93, p = 0.0001, Kruskal–Wallis, Figure 2A). Pupae reared at 0.0 and 1.5°C amplitude regimes required shorter developmental times (between 16 and 18 days) than those reared under a 9.6°C amplitude of thermal fluctuation but the same mean temperature (between 17 and 19 days). Pupae reared at temperature fluctuations selected by nurses (amplitude 3.3°C) required between 17 and 19 days to complete their development and, on average, this group did not significantly differ from the others. Under constant temperatures, a large difference was evident between groups of pupae reared at 25.4 and 35.0°C (21–24 and 12–13 days, respectively, H1, N = 36 = 26.27, p < 0.0001, Kruskal–Wallis, Figure 2B).


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)

(A,B) Pupal developmental time and (C,D) mortality rates of individuals reared at (A,C) different amplitudes of fluctuating temperature or (B,D) constant temperature regimes. Developmental time is shown as boxplots: boxes show quartiles, whiskers provide the minimum and maximum values, and small squares represent medians. Percentage of pre- and post- eclosion mortality for each group is indicated by black and white bars, respectively. Gray area indicates the temperature regime selected by nurses for brood translocation. Different letters show significant differences among different amplitudes of fluctuating temperature or between constant temperatures regimes. Developmental time: N0 = 15, N1.5 = 14, N3.3 = 13, N9.6 = 16, N25.4 = 18, N35 = 18. Mortality: N0 = 15, N1.5 = 16, N3.3 = 15, N9.6 = 16, N25.4 = 20, N35 = 23.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4835446&req=5

Figure 2: (A,B) Pupal developmental time and (C,D) mortality rates of individuals reared at (A,C) different amplitudes of fluctuating temperature or (B,D) constant temperature regimes. Developmental time is shown as boxplots: boxes show quartiles, whiskers provide the minimum and maximum values, and small squares represent medians. Percentage of pre- and post- eclosion mortality for each group is indicated by black and white bars, respectively. Gray area indicates the temperature regime selected by nurses for brood translocation. Different letters show significant differences among different amplitudes of fluctuating temperature or between constant temperatures regimes. Developmental time: N0 = 15, N1.5 = 14, N3.3 = 13, N9.6 = 16, N25.4 = 18, N35 = 18. Mortality: N0 = 15, N1.5 = 16, N3.3 = 15, N9.6 = 16, N25.4 = 20, N35 = 23.
Mentions: Temperature experienced during the pupal phase affected the time of pupal development until eclosion. Under temperature regimes fluctuating around the same mean yet with different amplitudes, pupal developmental time varied with the thermal amplitude (H3, N = 58 = 20.93, p = 0.0001, Kruskal–Wallis, Figure 2A). Pupae reared at 0.0 and 1.5°C amplitude regimes required shorter developmental times (between 16 and 18 days) than those reared under a 9.6°C amplitude of thermal fluctuation but the same mean temperature (between 17 and 19 days). Pupae reared at temperature fluctuations selected by nurses (amplitude 3.3°C) required between 17 and 19 days to complete their development and, on average, this group did not significantly differ from the others. Under constant temperatures, a large difference was evident between groups of pupae reared at 25.4 and 35.0°C (21–24 and 12–13 days, respectively, H1, N = 36 = 26.27, p < 0.0001, Kruskal–Wallis, Figure 2B).

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