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Morphology, neuroanatomy, brain gene expression, and the evolution of division of labor in the leafcutter ant Atta cephalotes

What selective forces and molecular mechanisms govern the integration of worker body size and morphology, brain architecture, and behavior in insect societies? Workers of the remarkably polyphenic and socially complex fungus-growing leafcutter ant Atta cephalotes exhibit a striking agricultural division of labor. The number of morphologically distinct and behaviorally differentiated worker groups, adaptive mosaic neural phenotypes, and brain transcriptomes have not been examined and the influences of socioecological challenges on behavioral performance, cognition, and brain evolution are unclear. We quantified worker morphological and behavioral variation to assess the number of worker size classes and characterized their social roles. We discriminated multiple worker size groups using a Gaussian mixture model: mid-sized workers (“medias”) had the most diverse task repertories and serve dominant roles in leaf harvesting, whereas workers of other size classes performed fewer, more specialized behaviors. We used variation among tasks in sensorimotor functions and task performance frequencies to create an estimate of sensory integration and processing demands across worker size groups. This metric predicted that medias require the greatest neural investment due to the high diversity of sensory inputs and motor functions associated with their task set. We quantified the volumes of key neuropils in brains of workers of different sizes and determined their allometries, finding that our estimate corresponded to proportional investment in the mushroom bodies, a brain compartment responsible for learning, memory, and sensory integration, and identifying allometric scaling patterns in other brain centers. Additionally, we measured whole-brain gene expression and identified significant differences in expression levels for numerous genes likely to underpin behavior. Differences were most pronounced between the smallest (fungal gardener “minims”) and largest (defensive “majors”), although not all expression differences were driven by worker size. Overrepresented gene functional categories included those related to sensory processing (enriched in genes upregulated in medias and minims) and metabolism (enriched in genes upregulated in majors). These results identify the nature of selective forces favoring differentiation along morphological, neuroanatomical, behavioral, and molecular axes among A. cephalotes workers and the impact of advanced division of labor on brain evolution. / 2023-03-01T00:00:00Z

Identiferoai:union.ndltd.org:bu.edu/oai:open.bu.edu:2144/43949
Date02 March 2022
CreatorsMuratore, Isabella Benter
ContributorsTraniello, James F. A., Mullen, Sean P.
Source SetsBoston University
Languageen_US
Detected LanguageEnglish
TypeThesis/Dissertation
RightsAttribution 4.0 International, http://creativecommons.org/licenses/by/4.0/

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