Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects

The social brain hypothesis posits that the cognitive demands of social behaviour have driven evolutionary expansions in brain size in some vertebrate lineages. In insects, higher brain centres called mushroom bodies are enlarged and morphologically elaborate (having doubled, invaginated and subcompartmentalized calyces that receive visual input) in social species such as the ants, bees and wasps of the aculeate Hymenoptera, suggesting that the social brain hypothesis may also apply to invertebrate animals. In a quantitative and qualitative survey of mushroom body morphology across the Hymenoptera, we demonstrate that large, elaborate mushroom bodies arose concurrent with the acquisition of a parasitoid mode of life at the base of the Euhymenopteran (Orussioidea + Apocrita) lineage, approximately 90 Myr before the evolution of sociality in the Aculeata. Thus, sociality could not have driven mushroom body elaboration in the Hymenoptera. Rather, we propose that the cognitive demands of host-finding behaviour in parasitoids, particularly the capacity for associative and spatial learning, drove the acquisition of this evolutionarily novel mushroom body architecture. These neurobehavioural modifications may have served as pre-adaptations for central place foraging, a spatial learning-intensive behaviour that is widespread across the Aculeata and may have contributed to the multiple acquisitions of sociality in this taxon

Neuronal connections and the function of the corpora pedunculata in the brain of the American cockroach, Periplaneta americana (L.) Based on portions of a dissertation submitted to the Department of Zoology, The University of Michigan, in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Weiss, '70).

The fiber constituents and connections of the calyces — the input-receiving regions — of the corpora pedunculata (“mushroom bodies”) were studied in reduced silver preparations from the American cockroach, Periplaneta americana (L.). In the outer synaptic layer of the calyces five fiber classes were distinguished, the first three of which arise outside the mushroom body. (1) Four highly similar neurons with somata near the optic lobe branch into different parts of the ipsiateral protocerebrum, including both calyces. Their fibers are highly constant in arrangement and position and contain small nucleus-like bodies. (2) The tractus olfactorio-globularis ( sensu lato ) emits fiber groups which course along the calycal walls as “calycal tracts” before ultimately dissipating into the synaptic layer. Variability within these tracts is described. (3) Fibers of undertermined origin outside the mushroom body radiate from the calycal center outwards through the synaptic layer. (4) From the inner calycal layer of neurites belonging to intrinsic mushroom-body neurons, perpendicular collaterals enter the synaptic layer. (5) Intrinsic-neuron somata near the calycal rim emit fibers which course tangentially within the synaptic layer from calycal rim to center. These fibers form a special peripheral zone in the pedunculus. The predominant presumably afferent calycal fiber class is that derived from the tractus olfactorio-globularis. No evidence was found for tracts from optic lobe to calyces. On this basis, and in light of the experimental and comparative anatomical literature, it is suggested that the corpora pedunculata of P. americana and other pterygotes are fundamentally second-order antennal sensory processing centers. Conflicting observations in earlier reports are critically discussed.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/50257/1/1051420103_ftp.pd