Brain Size and Visual Environment Predict Species Differences in Paper Wasp Sensory Processing Brain Regions (Hymenoptera: Vespidae, Polistinae)

Abstract

The mosaic brain evolution hypothesis predicts that the relative volumes of functionally distinct brain regions will vary independently and correlate with species' ecology. Paper wasp species (Hymenoptera: Vespidae, Polistinae) differ in light exposure: they construct open versus enclosed nests and one genus (Apoica) is nocturnal. We asked whether light environments were related to species differences in the size of antennal and optic processing brain tissues. Paper wasp brains have anatomically distinct peripheral and central regions that process antennal and optic sensory inputs. We measured the volumes of 4 sensory processing brain regions in paper wasp species from 13 Neotropical genera including open and enclosed nesters, and diurnal and nocturnal species. Species differed in sensory region volumes, but there was no evidence for trade-offs among sensory modalities. All sensory region volumes correlated with brain size. However, peripheral optic processing investment increased with brain size at a higher rate than peripheral antennal processing investment. Our data suggest that mosaic and concerted (size-constrained) brain evolution are not exclusive alternatives. When brain regions increase with brain size at different rates, these distinct allometries can allow for differential investment among sensory modalities. As predicted by mosaic evolution, species ecology was associated with some aspects of brain region investment. Nest architecture variation was not associated with brain investment differences, but the nocturnal genus Apoica had the largest antennal:optic volume ratio in its peripheral sensory lobes. Investment in central processing tissues was not related to nocturnality, a pattern also noted in mammals. The plasticity of neural connections in central regions may accommodate evolutionary shifts in input from the periphery with relatively minor changes in volume.

Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae)

“…The nocturnal paper wasp Apoica appeared to have an exceptionally high antennal/optic volume ratio, possible reflecting adaptation to activity in low-light conditions [42].…”

Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca)

“…Studies tracking brain architecture changes with worker age and experience could be used to distinguish between evolved and plastic mechanisms of brain structure development. The slave‐maker/slave species differences in mushroom body calyx investment were not explained by brain or body size differences, and therefore were not a result of differential brain region allometry (O'Donnell et al ., ).…”

“…This pattern holds for changes in sensory ecology. The evolution of activity under lower light conditions is associated with decreases in visual processing tissue (Barton, Purvis & Harvey, ; Catania, ; Fujun et al ., ; O'Donnell et al ., ). We hypothesize that the evolution of parasitism will lead to reduced brain investment when parasites exploit host sensory and cognitive systems.…”

Nasonia Parasitic Wasps Escape from Haller's Rule by Diphasic, Partially Isometric Brain-Body Size Scaling and Selective Neuropil Adaptations

“…Examples of absolute brain size influencing neuropil composition include Drosophila melanogaster, for which the optic lobe size is relatively smaller in smaller individuals [Lanet et al, 2013]. A decrease in relative optic lobe volume in smaller brains is also observed in a comparison of 13 paper wasp species [O'Donnell et al, 2013]. In T. evanescens, the relative volume of antennal lobe glomeruli is smaller in the smallest wasps, although their number is constant [van der Woude and Smid, 2016], whereas relative antennal lobe volume is not influenced by brain or body size in much larger species like bumblebees and honeybees [Mares et al, 2005;Gronenberg and Couvillon, 2010].…”