Abstract
Brain evolution is hypothesized to be driven by behavioral selection on neuroarchitecture. We developed a novel metric of relative neuroanatomical investments involved in performing tasks varying in sensorimotor and processing demands across polymorphic task-specialized workers of the leafcutter ant Atta cephalotes and quantified brain size and structure to examine their correlation with our computational approximations. Investment in multisensory and motor integration for task performance was estimated to be greatest for media workers, whose highly diverse repertoire includes leaf-quality discrimination and leaf-harvesting tasks that likely involve demanding sensory and motor processes. Confocal imaging revealed that absolute brain volume increased with worker size and functionally specialized compartmental scaling differed among workers. The mushroom bodies, centers of sensory integration and learning and memory, and the antennal lobes, olfactory input sites, were larger in medias than in minims (gardeners) and significantly larger than in majors (“soldiers”), both of which had lower scores for involvement of olfactory processing in the performance of their characteristic tasks. Minims had a proportionally larger central complex compared to other workers. These results support the hypothesis that variation in task performance influences selection for mosaic brain structure, the independent evolution of proportions of the brain composed of different neuropils.
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Availability of data and material
All data used in this study are included as supplementary tables. Additionally, data are available via: https://doi.org/10.5061/dryad.wm37pvmnq.
Code availability
Code used is available via: https://github.com/Imuratore-bio/ant-brains.
Abbreviations
- AL:
-
Antennal lobe
- CX:
-
Central complex
- DMSO:
-
Dimethylsulfoxide
- HEPES:
-
4-(2-Hydroxyethyl)-1-piperazineethanesulfonic acid
- MB:
-
Mushroom body
- OL:
-
Optic lobe
- PBS:
-
Phosphate-buffered saline
- PBST:
-
Phosphate-buffered saline with Triton
- ROCB:
-
Remainder of central brain
- SEZ:
-
Subesophageal zone
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Acknowledgements
We gratefully acknowledge the assistance of Dr. Wulfila Gronenberg, Dr. Sam Beshers and Dr. Sean Mullen (manuscript input), Dr. Todd Blute (confocal microscopy), Dr. Christopher Starr and Ricardo Pillai (field work), Andrew Hoadley (colony collection and brain illustrations), and Zach Coto and Frank Azorsa (animal husbandry and manuscript input), as well as three anonymous reviewers.
Funding
This study was supported by National Science Foundation grants IOS 1354291 and IOS 1953393 to JFAT, an award from the Boston University Undergraduate Research Opportunities Program to EMF, and the Department of Biology Brenton R. Lutz Award and the Belamarich Dissertation Writing Award to IBM.
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IBM and JFAT designed the study. IBM drafted the manuscript. IBM, EMF, and JFAT developed and edited the manuscript. IBM and EMF prepared and imaged brains. EMF measured neuropils and IBM and EMF statistically analyzed volumetric data. JFAT secured funding.
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The authors have no conflicts of interest or competing interests to declare. Colonies were collected in Trinidad in compliance with the laws of Trinidad and Tobago and imported to USA in compliance with the conditions of permit USDA APHIS PPQ526P–12–04067. All ants were housed in conditions promoting colony health with minimal disturbance and varied foraging options. The USDA inspected and approved our containment facility. We collected sufficient samples for study while minimizing impact on colony populations. This study necessitated humanely killing sterile workers by cold anaesthetization to stain and image brains.
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Dedicated to the memory of Edward O. Wilson in recognition of his inspiring work on leafcutter ants.
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Muratore, I.B., Fandozzi, E.M. & Traniello, J.F.A. Behavioral performance and division of labor influence brain mosaicism in the leafcutter ant Atta cephalotes. J Comp Physiol A 208, 325–344 (2022). https://doi.org/10.1007/s00359-021-01539-6
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DOI: https://doi.org/10.1007/s00359-021-01539-6