Differential investment in visual and olfactory brain regions is linked to the sensory needs of a wasp social parasite and its host

Abstract

Obligate insect social parasites evolve traits to effectively locate and then exploit their hosts, whereas hosts have complex social behavioral repertoires, which include sensory recognition to reject potential conspecific intruders and heterospecific parasites.While social parasites and host behaviors have been studied extensively, less is known about how their sensory systems function to meet their specific selective pressures.Here, we compare investment in visual and olfactory brain regions in the paper wasp Polistes dominula, and its obligate social parasite P. sulcifer, to explore the links among sensory systems,brain and behavior. Our results show significant relative volumetric differences between these two closely related species, consistent with their very different life histories. Social parasites show proportionally larger optic lobes and central complex to likely navigate long-distance migrations and unfamiliar landscapes to locate the specific species of hosts they usurp. Contrastingly, hosts have larger antennal lobes and calyces of the mushroom bodies compared with social parasites, as predicted by their sensory means to maintain social cohesion via olfactory signals, allocate colony tasks, forage, and recognize conspecific and heterospecific intruders. Our work suggests how this tradeoff between visual and olfactory brain regions may facilitate different sensory adaptations needed to perform social and foraging tasks by the host, including recognition of parasites, or to fly long distances and successful host localizing by the social parasite.

Caste, Sex, and Parasitism Influence Brain Plasticity in a Social Wasp

“…We first dehydrated each head capsule with a series of increasing ethanol and acetone concentrations. We then used the established concentrations for the Embed 812 resin kit (Electron Microscopy Sciences, Hatfield, United States) to embed the head capsule while maintaining their brain dimensions, following the histology protocol for Polistes wasps (O 'Donnell et al, 2015;Rozanski et al, 2021). The samples were moved repeatedly between an open-air rocking shaker (Thermo Fisher Scientific, Waltham, United States) and a vacuum to improve infiltration of the solvent.…”

“…We also traced the two calyx substructures process olfactory and visual stimuli: lip and collar, respectively, and the central complex. The remaining structures in the protocerebrum were grouped as the central brain (Figure 1A), following the established method for this species (Rozanski et al, 2021) and ants (Sheehan et al, 2019). Outlining of brain regions was done blind to the category for each sample.…”

“…While brain plasticity within and across social insects has been extensively studied (Godfrey and Gronenberg, 2019), no studies have explored plasticity within a species that has morphologically similar individuals, various colony tasks, and a parasite that potentially alters brain morphology. We predicted that the relative volume of selected brain regions reflects specific sensory needs for each caste and sex (reproductive females, female workers, and males) (Rozanski et al, 2021). We also predicted higher volume of visual regions in males to detect and identify potential mates or rival males in a lek, compared to females.…”

“…For instance, neuroplasticity has evolved across many lineages as a result of variable selective pressures acting on the cognitive demands of sensory and perceptual systems (Barton et al, 1995;Barton and Harvey, 2000;Catania, 2005). Since brain tissue is energetically expensive, plasticity in specific brain structures may be linked to the sensory and processing needs of adaptive behaviors (Isler and Van Schaik, 2006;Niven and Laughlin, 2008;Riveros and Gronenberg, 2010;Pyza, 2013;Montgomery et al, 2016;Dunbar and Shultz, 2017;Rozanski et al, 2021). Investment in neural tissue may be mediated by experience (Jones et al, 2009;Riveros and Gronenberg, 2010;Cabirol et al, 2018), diet (Murphy et al, 2014;DeCasien et al, 2017), environmental stimuli (Burns et al, 2009;Axelrod et al, 2018), tradeoffs with reproduction (Pitnick et al, 2006), and/or endocrine factors (Ball et al, 2002;Lendvai et al, 2013).…”

“…Here, we take advantage of the primitively eusocial paper wasp Polistes dominula to test how brain plasticity is associated with behavioral flexibility (Pardi, 1996;O'Donnell et al, 2014O'Donnell et al, , 2018O'Donnell and Bulova, 2017;Rozanski et al, 2021). In this temperate wasp species, the recognition of nestmates, caste, and sex relies on both chemical and visual cues (Dani et al, 2001;Cappa et al, 2016Cappa et al, , 2020Beani et al, 2019;Cini et al, 2019).…”