Comparative analysis of constraints and caste differences in brain investment among social paper wasps

Abstract

We compared species mean data on the size of functionally distinct brain regions to test the relative rates at which investment in higher-order cognitive processing (mushroom body calyces) versus peripheral sensory processing (optic and antennal lobes) increased with increasing brain size. Subjects were eusocial paper wasps from queen and worker castes of 10 species from different genera. Relative investment in central processing tissue increased with brain size at a higher rate than peripheral structure investment, demonstrating that tissue devoted to higher-order cognitive processing is more constrained by brain size. This pattern held for raw data and for phylogenetically independent contrasts. These findings suggest that there is a minimum necessary investment in peripheral sensory processing brain tissue, with little to gain from additional investment. In contrast, increased brain size provides opportunities to invest in additional higher-order cognitive processing tissue. Reproductive castes differed within species in brain tissue investment, with higher central-to-peripheral brain tissue ratios in queens than in workers. Coupled with previous findings that paper wasp queen, but not worker, brain architecture corresponds to ecological and social variation, queen brain evolution appears to be most strongly shaped by cognitive demands, such as social interactions. These evolutionary patterns of neural investment echo findings in other animal lineages and have important implications, given that a greater investment in higherorder processing has been shown to increase the prevalence of complex and flexible behaviors across the animal kingdom.Hymenoptera | mushroom bodies | social brain | Vespidae A s brains evolve, both relative expansion of specific brain regions and general increases in absolute brain size can enable changes in animal cognitive capacity (1). Of particular note is the frequent convergent evolution of central brain regions that perform higher-order cognitive processing. Larger central processing centers are associated with enhanced capacity for learning, memory, and behavioral innovation among species (1-3). In primates, increased investment in higher-order cognitive processing structures, such as the neocortex and hippocampus, has been linked to increased cognitive performance (4), and the neocortex is five times larger in primates than in insectivores after accounting for differences in whole brain size (5). Increased hippocampal size in passerine birds has been associated with improved memory and the advent of food-storing behavior (6). Increased size and complexity of the mushroom bodies (MB), the neural centers of higher-order cognitive processing in insects, are paired with an increase in the prevalence of generalist feeding ecologies across species (7) and with social dominance status within species (8-10).Molecular evidence supports a single origin of the CNS in bilaterally symmetrical animals, including insects and vertebrates, occurring before the protostome-deuterostome split (11). ...

Investment in higher order central processing regions is not constrained by brain size in social insects

“…Overall, these results indicate that brain size does not affect brain component scaling in the same way among Polistes species, suggesting that brain size is unlikely to be a general predictor of brain composition in the genus [49].…”

“…We had direct access to three of the original databases from these studies and were able to extract additional measurements not reported in the initial publications [52,57,58]. For Neotropical polistine wasp brain scaling, we used only data reported in the original publication [49]; these measurements were corrected prior to analysis owing to unit scaling errors present in the original study, as described in the electronic supplementary material. Species names and original source publications of all studied taxa are listed in the electronic supplementary material, table S2.…”

“…We used brain composition data from four published studies of worker brain scaling in ants [57], honeybees and bumblebees [52], and social wasps [49,58] in our analyses, along with counts of the number of ommatidia per eye reported for the ant species [57]. We also collected new brain volumetrics and ommatidia counts from four additional ant species, using similar methods; our detailed protocol is described in the electronic supplementary material.…”

“…Absolute brain size was recently proposed to constrain the evolution of the organization of the functional module comprising the C, AL and OL in polistine wasps [49]; interspecific comparisons suggested that small-brained wasps have lower ratios of C volume to the combined volume of the AL þ OL (C/AO hereafter) owing to positive allometry between C and brain size and negative allometry between AL þ OL and brain size. Absolute brain size has thus been argued to constrain relative neural investment in central processing (C) versus peripheral sensory neuropils (AL and OL) in this taxon and, by inference, in animals generally [49]. Here, we examine whether size-related developmental constraints have indeed significantly impacted the evolution of neuropil organization within the C/AL/OL module in a broad sample of social hymenopteran taxa (electronic supplementary material, figure S1) that vary in brain size over more than two orders of magnitude (figure 1).…”

“…Understanding how these aspects of brain composition affect worker behaviour and division of labour has been a prominent goal of social insect research, and significant interspecific variation in brain composition associated with task performance has begun to be identified in ants [21,33,47,50] and wasps [51]. Absolute brain size was recently proposed to constrain the evolution of the organization of the functional module comprising the C, AL and OL in polistine wasps [49]; interspecific comparisons suggested that small-brained wasps have lower ratios of C volume to the combined volume of the AL þ OL (C/AO hereafter) owing to positive allometry between C and brain size and negative allometry between AL þ OL and brain size. Absolute brain size has thus been argued to constrain relative neural investment in central processing (C) versus peripheral sensory neuropils (AL and OL) in this taxon and, by inference, in animals generally [49].…”