Interspecific comparison of mushroom body synaptic complexes of dimorphic workers in the ant genus Pheidole

Gordon, Darcy G.; Zelaya, Alejandra; Ronk, Katherine; Traniello, James F. A.

doi:10.1016/j.neulet.2017.10.009

Cited by 11 publications

(13 citation statements)

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“…The organization of these microglomeruli, which may enable neural plasticity and support behavioral diversity, has been used as a proxy for information-processing abilities that appear to correlate with task performance demands [28–32]. However, MG structure may not be consistently associated with worker size-related behavioral differentiation [25,31–33].…”

Section: Introductionmentioning

confidence: 99%

Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

et al. 2019

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Strongly polyphenic social insects provide excellent models to examine the neurobiological basis of division of labor. Turtle ants, Cephalotes varians, have distinct minor worker, soldier, and reproductive (gyne/queen) morphologies associated with their behavioral profiles: small-bodied task-generalist minors lack the phragmotic shield-shaped heads of soldiers, which are specialized to block and guard the nest entrance. Gynes found new colonies and during early stages of colony growth overlap behaviorally with soldiers. Here we describe patterns of brain structure and synaptic organization associated with division of labor in C. varians minor workers, soldiers, and gynes. We quantified brain volumes, determined scaling relationships among brain regions, and quantified the density and size of microglomeruli, synaptic complexes in the mushroom body calyxes important to higher-order processing abilities that may underpin behavioral performance. We found that brain volume was significantly larger in gynes; minor workers and soldiers had similar brain sizes. Consistent with their larger behavioral repertoire, minors had disproportionately larger mushroom bodies than soldiers and gynes. Soldiers and gynes had larger optic lobes, which may be important for flight and navigation in gynes, but serve different functions in soldiers. Microglomeruli were larger and less dense in minor workers; soldiers and gynes did not differ. Correspondence in brain structure despite differences in soldiers and gyne behavior may reflect developmental integration, suggesting that neurobiological metrics not only advance our understanding of brain evolution in social insects, but may also help resolve questions of the origin of novel castes.

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Section: Introductionmentioning

confidence: 99%

Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

et al. 2019

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“…For an elaborate analysis of these aspects, however, it is essential to assess bouton numbers in a three‐dimensional environment and by combining the quantification of bouton densities with neuropil volume measurements to estimate total numbers of boutons rather than calculating densities from two‐dimensional counts (for a more detailed discussion see Rössler et al , ). This makes it difficult to directly compare the results from the studies by Kamhi et al (), Gordon and Traniello () and Gordon et al () and potential implications for our present results in the bumble bee. To further address the question of varying cognitive abilities and their potential consequences for differences in task performance across polymorphic workers, we definitely need more studies that combine manipulative behavioral assays such as learning experiments with quantitative analyses of both pre‐ and postsynaptic structures in the MB calyces across workers of different sizes and with different task allocations to obtain a more detailed knowledge about the functional significance of interindividual variation and composition of synaptic connections.…”

Section: Discussionmentioning

confidence: 74%

“…The results were, however, inconclusive. A comparison of two Pheidole ant species revealed that, in addition to an age‐related decrease in MG density in all subcastes, minor workers had significantly less MG than major soldiers, contradicting the authors' hypothesis that the higher task diversity of minor workers is reflected in a greater density of MG (Gordon et al , ). When comparing subcastes of trimorphic Pheidole dentata ants, the opposite trend was observed: supersoldiers had significantly less MG than task‐diverse minor workers (Gordon and Traniello, ).…”

Section: Discussionmentioning

confidence: 89%

“…Several comparative studies on polymorphic and monomorphic ant species have tried to correlate differences in the task repertoire of ant subcastes with neuronal differences (Kamhi et al , ; Gordon and Traniello, ; Gordon et al , ). The results were, however, inconclusive.…”

Section: Discussionmentioning

confidence: 99%

“…The authors concluded that caste‐ and size‐related differences in task repertoire might, in fact, arise from a more complex relationship between neuronal correlates rather than being reflected in MG numbers alone. By assessing the diameter of PN boutons, the authors included an interesting parameter in their studies, which has been neglected in most of the other studies on polymorphic social insects, even though no general trend in relation to body size was revealed (Kamhi et al , ; Gordon and Traniello, ; Gordon et al , ). PN boutons were found to increase in size during adult maturation in minor Pheidole ants (Seid et al , ) and honey bees, which was further accompanied by an increase in postsynaptic partners and active zones (Groh et al , ).…”

Section: Discussionmentioning

confidence: 99%

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Neuronal Plasticity in the Mushroom‐Body Calyx of Bumble Bee Workers During Early Adult Development

Kraft

Spaethe

Rößler

et al. 2019

Developmental Neurobiology

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Division of labor among workers is a key feature of social insects and frequently characterized by an age‐related transition between tasks, which is accompanied by considerable structural changes in higher brain centers. Bumble bees (Bombus terrestris), in contrast, exhibit a size‐related rather than an age‐related task allocation, and thus workers may already start foraging at two days of age. We ask how this early behavioral maturation and distinct size variation are represented at the neuronal level and focused our analysis on the mushroom bodies (MBs), brain centers associated with sensory integration, learning and memory. To test for structural neuronal changes related to age, light exposure, and body size, whole‐mount brains of age‐marked workers were dissected for synapsin immunolabeling. MB calyx volumes, densities, and absolute numbers of olfactory and visual projection neuron (PN) boutons were determined by confocal laser scanning microscopy and three‐dimensional image analyses. Dark‐reared bumble bee workers showed an early age‐related volume increase in olfactory and visual calyx subcompartments together with a decrease in PN‐bouton density during the first three days of adult life. A 12:12 h light‐dark cycle did not affect structural organization of the MB calyces compared to dark‐reared individuals. MB calyx volumes and bouton numbers positively correlated with body size, whereas bouton density was lower in larger workers. We conclude that, in comparison to the closely related honey bees, neuronal maturation in bumble bees is completed at a much earlier stage, suggesting a strong correlation between neuronal maturation time and lifestyle in both species.

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Heliconiini butterflies as a case study in evolutionary cognitive ecology: behavioural innovation and mushroom body expansion

Young,

Montgomery

2023

Behav Ecol Sociobiol

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The evolutionary relationships between ecology, cognition, and neurobiology remain elusive, despite important contributions from functional studies and comparative analyses. Recently, Heliconius butterflies and their Heliconiini allies have emerged as a promising system for investigating the evolution and ecology of cognition. In Heliconius, regions of the brain involved in learning and memory, called the mushroom bodies, have quadrupled in size and contain up to 8 times more neurons than closely related genera. This expansion, largely driven by increased dedication to processing visual input, occurred relatively recently (~12–18 Ma) and coincides with the evolution of a novel foraging behaviour — trapline foraging between pollen resources, which provide an adult source of amino acids. Behavioural experiments show that, relative to other Heliconiini, Heliconius exhibit superior visual long-term memory and non-elemental learning, behaviours which have putative relevance for visual learning during traplining, while exhibiting no differences in shape learning or reversal learning. These cognitive differences are also associated with changes in the plastic response of the mushroom body to learning and experience. Heliconius thus constitute a clear example of a suite of neural adaptations that coincides with a novel behaviour reliant on distinct cognitive shifts. We highlight the Heliconiini as a well-positioned, developing case study in cognitive ecology and evolution, where there is the possibility of synthesising comparative neuroanatomical, developmental and behavioural data with extensive genomic resources. This would provide a rich dataset linking genes, brains, behaviour, and ecology, and offer key insights into the mechanisms and selective pressures shaping the evolution of interspecific cognitive variation.

show abstract

Interspecific comparison of mushroom body synaptic complexes of dimorphic workers in the ant genus Pheidole

Cited by 11 publications

References 47 publications

Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

Neuronal Plasticity in the Mushroom‐Body Calyx of Bumble Bee Workers During Early Adult Development

Heliconiini butterflies as a case study in evolutionary cognitive ecology: behavioural innovation and mushroom body expansion

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