Available online at www.sciencedirect.com ScienceDirect Development and evolution of brain allometry in wasps (Vespidae): size, ecology and sociality Sean O’Donnell and Susan Bulova We review research on brain development and brain evolution for variation in brain investment. We review the in the wasp family Vespidae. Basic vespid neuroanatomy and neuroecology of the wasp family Vespidae, a phylogenet- some aspects of functional neural circuitry are well- ically well-characterized clade with diverse behavior and characterized, and genomic tools for exploring brain plasticity ecology [1,2]. Vespidae provide excellent opportunities are being developed. Although relatively modest in terms of for exploring the interface between behavior, ecology, species richness, the Vespidae include species spanning much and neuroscience. We discuss species differences in of the known range of animal social complexity, from solitary behavior and ecology, and how these differences shape nesters to highly eusocial species with some of the largest the wasps’ cognitive environments. We survey evidence known colonies and multiple reproductives. Eusocial species for adaptive brain structure variation in Vespidae, differ in behavior and ecology including variation in queen/ pointing out some areas where gaps in our knowledge worker caste differentiation and in diurnal/nocturnal activity. exist, and suggest targets for additional sampling of either Species differences in overall brain size are strongly associated taxa or wasp ecological variation that may yield exciting with brain allometry; relative sizes of visual processing tissues discoveries. increase at faster rates than antennal processing tissues. The lower relative size of the central-processing mushroom bodies Neuroecologists often use comparative approaches, (MB) in eusocial species compared to solitary relatives asking whether species differences in neuroanatomy or suggests sociality may relax demands on individual cognitive neural circuit function correspond to particular ecological abilities. However, queens have greater relative MB volumes niches. Brain investment is under strong individual than their workers, and MB development is positively and evolutionary constraints because neural tissue is associated with social dominance status in some species. relatively expensive, both in terms of developmental Fruitful areas for future investigations of adaptive brain production and of metabolic maintenance [3,4]; for flying investment in the clade include sampling of key overlooked animals, brains may impose additional biomechanical taxa with diverse social structures, and the analysis of neural challenges [5]. Brain structure variation that is correlations with ecological divergence in foraging resources better predicted by ecology than by species relatedness and diel activity patterns. (i.e., phylogeny) may have been shaped by adaptation to ecological conditions or particular cognitive challenges [6]. Address Department of Biodiversity Earth & Environmental Science, Drexel University, Philadelphia, PA, USA Eusocial paper wasps and their relatives Corresponding author: O’Donnell, Sean ([email protected]) (Vespidae) as models for neuroecology Vespid wasp brain structure and function Current Opinion in Insect Science 2017, 22:54–61 As in other social Hymenoptera, vespid wasp brains are This review comes from a themed issue on Social insects compartmentalized into anatomically discrete regions Edited by Amy Toth and Adam Dolezal that perform distinct cognitive functions (Figure 1). Some brain regions primarily or exclusively process visual input For a complete overview see the Issue and the Editorial from the compound eyes; others process chemosensory Available online 22nd May 2017 input from the antenna [7]. Furthermore, vespid brains http://dx.doi.org/10.1016/j.cois.2017.05.014 include both peripheral sensory processing regions (the 2214-5745/ã 2017 Elsevier Inc. All rights reserved. sensory lobes) and central processing regions including the mushroom bodies (MB) (Figure 1). Work on insect model systems suggests the MB are involved in higher-order cognitive processing such as learning and memory, spatial orientation and navigation, and sensory modality integration [8,9].[81_TD$IF] Recent genomic research has Neuroecology: the analysis of adaptive brain generated powerful tools for analyzing the role of gene plasticity and brain evolution expression in the development and function of vespid Neuroecology is the study of adaptive neural system brains [10,11]. Comparative genetic approaches to social development and evolution. The cognitive challenges insect brain function analysis are in the early stages of imposed by animal’s environments are expected to select development [12 ,13]. Current Opinion in Insect Science 2017, 22:54–61 www.sciencedirect.com Neuroecology of Vespidae O’Donnell and Bulova 55 Figure 1 MB Vespa ducalis OL 1.46 mm3 AL Leipomeles 1 mm dorsata 0.08 mm3 ∼18.3-fold brain volume difference Polybia dimidiata (queen) Mushroom bodies Chemosensory (antennal) Visual (optic) lobe lobe Current Opinion in Insect Science (Top) Representative stained thin-sections along the frontal plane through worker head capsules of a small-bodied species (Leipomeles dorsata) and a large-bodied species (Vespa ducalis) of eusocial vespid wasp. Boxed labels indicate key brain regions: MB—mushroom bodies, OL—optic lobes, AL—antennal lobes. Scale bar applies to both images; approximate total brain volume is given for each wasp. (Bottom) 3-D reconstruction of a paper wasp brain in frontal view from serial thin sections, with some major brain regions indicated. Light blue—optic lobes, dark green— antennal lobes, purple—protocerbral mass and subesophageal ganglion, orange—mushroom body lobes and peduncle, dark blue—mushroom body calyx collar region, light green—mushroom body calyx lip region. Developmental brain plasticity and individual differences and unmated sterile workers. Since the pioneering work in behavior of Pardi [14], eusocial Vespidae, particularly paper wasps Eusocial Vespidae colonies are characterized by repro- (Polistinae), have been important models for understand- ductive division of labor with mated, egg-laying queens ing reproductive competition and division of labor in www.sciencedirect.com Current Opinion in Insect Science 2017, 22:54–61 56 Social insects animal societies. The colonies of primitively eusocial or species, queens perform many worker-like tasks, such independent-founding paperwaps in the genera Polistes, as foraging for nest-building materials and food, up to the Mischocyttarus, Ropalidia, Parapolybia and Belonogaster are point of worker adult emergence. Queen and worker empirically tractable societies: all build open nest-combs behavior then typically diverge strongly [38]: queens allowing observations of behavior, have moderate colony remain largely nest-bound, while most workers spend sizes with large-bodied adults that can be individually time (and energy) on foraging flights. In swarm-founding marked, and engage in social dominance related to species, queens apparently never perform worker-like reproductive competition [15–20]. Size and shape duties such as foraging. Workers thus experience more polyphenic worker subcastes are not known in wasps. complex and variable light levels and spatial challenges. However, eusocial Vespidae exhibit a wide range of Workers invest significantly more than their queens in female caste differentiation [21,22]. Distinct female visual processing brain tissues, particularly in the castes result from developmental plasticity in response peripheral optic lobes [35]. Queen-worker behavior to larval environment, rather than genetic differences differences are diminished in marginal habitats with short [23–25]. In honey bees, queen vs. worker brain colony growth seasons [38]; paper wasp populations or architecture differences arise in part during the pre-pupal species in such harsh ecological settings are good targets and pupal stages of development [26] (Farris & for future neuroecological analyses. O’Donnell, unpublished data for paper wasps). Paper wasp brains exhibit substantial structural dynamism dur- Species differences in brain architecture: size-allometry ing the adult stage. Age-related changes in MB neurons In addition to their advantages for studies of (Kenyon cells) occurred after adult emergence in neuro-physiology, neuro-genetics, and brain plasticity, Mischocyttarus wasps: cell bodies shrank, while associated Vespidae are excellent subjects for comparative analyses. neuropil expanded [27]. MB development corresponds Paper wasp species vary over a wide range of body sizes, with task performance in swarm-founding Polybia and brain size corresponds to body size (Figure 2)[39]. workers [28] and with social dominance status in However, eusocial vespid brain volume and body size independent-founding Polistes and Mischocyttarus females (head capsule volume) do not covary isometrically: [29,30]. Increases in Polybia MB neuropil (calyx) volume smaller-bodied species have relatively larger brains, an were associated with increases in dendritic field size and example of Haller’s rule (Figure 2). Minimum brain size synaptic connectivity of the Kenyon cell neurons, sug- requirements may constrain the allometry of brain/body gesting MB volume increases are related to functional size relationships: as body size reaches lower limits, changes in neural processing ability [31]. absolute brain size cannot continue to decrease further due