The neuroplasticity of division of labor: worker polymorphism, compound eye structure and brain organization in the leafcutter ant Atta cephalotes

Abstract

32Our understanding of how the design of peripheral sensory structures is coupled with neural 33 processing capacity to adaptively support division of labor is limited. Workers of the remarkably 34 polymorphic fungus-growing ant Atta cephalotes are behaviorally specialized by size: the 35 smallest workers (minims) tend fungi in dark subterranean chambers while larger workers 36 perform tasks mainly outside the nest. These strong differences in worksite light conditions are 37 predicted to influence sensory and processing requirements for vision. We found that eye 38 structure and visual neuropils have been be selected to maximize task performance according to 39 light availability. Minim eyes had few ommatidia, large interommatidial angles and eye 40 parameter values, suggesting selection for visual sensitivity over acuity. Large workers had 41 larger eyes with disproportionally more and larger ommatidia, and smaller interommatidial 42 angles and eye parameter values, reflecting peripheral sensory adaptation to ambient rainforest 43 light. Additionally, optic lobe and mushroom body collar volumes were disproportionately small 44 in minims, and within the optic lobe, lamina and lobula relative volumes increased with worker 45 size whereas the medulla decreased. Visual system phenotypes thus correspond to task 46 specializations in dark or light environments and reflect a functional neuroplasticity 47 underpinning division of labor in this socially complex agricultural ant. 48 49

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

“…cephalotes (Arganda et al, 2020), we assumed greater investment in neuropils such as the MBs and ALs would be required to process more diverse stimulus arrays and coordinate sensorimotor processes. For example, tasks such as leaf selection, cutting, and transport involve olfactory discrimination, proprioception and mechanosensory and muscular systems to control the mandibles, appendages, head position, and direction of movement (Currier et al, 2020;Green et al, 2019;Khalife et al, 2018), whereas other tasks differ substantially in these needs.…”

“…A. cephalotes worker OL proportional volume increases with worker size and is highest in majors, which have greater visual acuity (Arganda et al, 2020). The repertoire of Atta majors appears limited to defense (Powell & Clark, 2004a;Wilson, 1980a), mainly an extranidal task that likely involves target detection.…”

“…Worker size-related specializations include fungal care, nursing immatures, leaf selection, cutting, and transport, waste management and hygienic behavior, and colony defense. These tasks differ in requirements for multimodal sensory perception, integrative processing, and motor functions associated with monitoring the growth of fungus and brood development, decoding plant chemistry, leaf harvesting, navigation, recognizing infectious agents, detecting environmental hazards, and combating predators and parasites (Arenas & Roces, 2016a, 2016bArganda et al, 2020;Goes et al, 2020;Green & Kooij, 2018;Groh et al, 2014;Howard et al, 1996;Saverschek & Roces, 2011). This pattern of division of labor characterizes Atta cephalotes, whose workers range in size from 0.5 to more than 4.5mm in head width and are divisible into groups according to task repertoires (Table 1).…”