Behavioral performance requirements for division of labor influence adaptive brain mosaicism in a socially complex ant

Abstract

Brain evolution is hypothesized to be driven by neuroarchitectural requirements for behavioral performance. Assessments of such needs should be informed by the nature of sensory and motor processes underpinning behavior. We developed a novel metric to estimate the relative neuroanatomical investments required to perform tasks varying in sensorimotor and processing demands across polymorphic and polyethic workers of the leafcutter ant Atta cephalotes and quantified brain size and structure to examine their correspondence with our computational approximations. Investment in multi-sensory integration and motor requirements for task performance was estimated to be greatest for media workers whose leaf-harvesting repertoire involves the most diverse and demanding sensory and motor processes, including plant discrimination, leaf cutting, and fragment transportation. Volumetric analysis of confocal brain images revealed that absolute brain size increased with worker size and compartmental scaling allometries among functionally specialized brain compartments differed among polymorphic workers. The mushroom bodies, centers of sensory integration and learning, and the antennal lobes, which process olfactory inputs, were significantly larger in medias than in minim workers (fungal gardeners) and major workers ("soldiers"), which had lower estimated task-related neural demands. Minims had a proportionally larger central complex, perhaps to control navigation in subterranean fungal garden chambers. These results indicate that variation in task performance requirements has selected for adaptive variation in brain size and mosaic scaling.

When and Why Did Human Brains Decrease in Size? A New Change-Point Analysis and Insights From Brain Evolution in Ants

“…Large brains may not be required to generate complex behavior, and brain mosaicism and circuitry-rather than overall size-may be important Rowe, 2007, 2013;Chittka and Niven, 2009;Avarguès-Weber et al, 2018;Logan et al, 2018;Godfrey and Gronenberg, 2019). Computational models (e.g., Feinerman and Traniello, 2016;Reséndiz-Benhumea et al, 2021) and patterns in some ant clades (Muscedere and Traniello, 2012;Riveros et al, 2012;Muratore et al, 2021) suggest that group-level cognition may select for reduced brain size and/or adaptive brain size variation. Moreover, complex systems theory predicts that greater social complexity derives from individual simplicity (Delgado and Solé, 1997), although the neurobiological and behavioral meaning of "simplicity" is unclear.…”

“…Ants have nevertheless emerged as important models for understanding the role of sociality (Ilies et al, 2015;Kamhi et al, 2016Kamhi et al, , 2019Godfrey and Gronenberg, 2019) and behavioral performance and cognition (Muratore and Traniello, 2020;Muratore et al, 2021) in brain evolution. Analyses of sociality and brain size scaling (e.g., Godfrey and Gronenberg, 2019;Muratore and Traniello, 2020) and information processing through social interaction (e.g., Davidson et al, 2016) can contribute to broadly understanding how social biology may have influenced general aspects of human brain evolution.…”

“…Analyses of sociality and brain size scaling (e.g., Godfrey and Gronenberg, 2019;Muratore and Traniello, 2020) and information processing through social interaction (e.g., Davidson et al, 2016) can contribute to broadly understanding how social biology may have influenced general aspects of human brain evolution. The allometric scaling of functionally specialized brain centers in ants allows the adaptiveness of brain mosaics to be explored (e.g., Muratore et al, 2021) and the metabolic costs of neural tissues that are highly significant to brain evolution (Aiello and Wheeler, 1995) can be recorded in individual ant brains (Coto and Traniello, 2021). Studies of the influences of diet, which is considered significant in primate (and human) brain evolution (Wrangham, 2009;DeCasien et al, 2017), are facilitated by the diverse feeding ecologies of ants.…”

“…For example, mushroom bodies are disproportionally large in the brains of media (mid-size) workers of the fungus-growing ant Atta cephalotes. The diverse and behaviorally challenging task repertoire of these workers encompasses leaf-harvesting, and their social role and neuroanatomy differs from that of smaller and larger workers that perform other tasks (Muratore et al, 2021). Using this ant as a model to understand how agriculture has influenced brain evolution may help identify social conditions, life histories, and ecological factors favoring either an increase or decrease in brain size.…”