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

Abstract

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 þ 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.

Evolution of brain elaboration

“…However, cockroaches are not social and form at most loosely organized aggregates [66,67]. Large mushroom bodies are also found in Odonata (dragonflies and damselflies) [37], Isoptera (termites) [68], butterflies of the genus Heliconius (Lepidoptera) [69], feeding generalist scarab beetles (Coleoptera) [70,71], and parasitoid and parasitic wasps (Hymenoptera), all of which are solitary [61,[72][73][74] (figure 1). With the exception of termites, none of these species demonstrates true colony-based social behaviour.…”

Specialization and group size: brain and behavioural correlates of colony size in ants lacking morphological castes

“…using group-level signals), which would increase the need for increased memory and learning as society size increases [19,23]. In social insects, the effect of social life on brain size and anatomy has been tested by comparing solitary and social species [24], and by comparing facultatively social species in their solitary and social phases [25]. Monomorphic ants that are obligate plant associates allow an accurate test of the TSH and the SBH, because workers show size-independent task specialization and colony size can be more accurately quantified in the field than for soil-nesting ant species.…”

Development of site fidelity in the nocturnal amblypygid, Phrynus marginemaculatus

“…The hypothesis that odors are essential for navigation by amblypygids is also supported by the fact that they possess enormous mushroom bodies, an invertebrate brain region associated with olfactory learning, spatial memory, and sensory integration (Strausfeld et al 1998;Wolff and Strausfeld 2015). This brain region contains several million neurons, and variation in its size and complexity has been attributed to the use of olfactory maps and the intensity of navigational demands (Farris and Schulmeister 2011;Jacobs 2012;Strausfeld 2012;Wolff and Strausfeld 2015; but see; Pfeiffer and Homberg 2014; Turner-Evans and Jayaraman 2016). Additional suggestions regarding the potential role of the odor source as a learned landmark come from comparisons of inbound and outbound trajectories (Fig.…”