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Development and evolution of brain allometry in wasps (): 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 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 , 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 Science 2017, 22:54–61 As in other social , vespid wasp brains are This review comes from a themed issue on Social 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].

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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

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(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- (), have been important models for understand- ductive division of labor with mated, egg-laying queens ing reproductive competition and division of labor in

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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 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 to minimal brain investment constraints. Conversely, Social interactions and brain structure as body size increases, further increases in brain Several lines of evidence suggest social interactions affect investment may be disfavored by the high costs of neural adult paper wasp brain development. Some species of tissue [40,41]. Furthermore, brain regions evolve with Polistes can recognize individual nestmate’s faces during brain size at different rates. Investment in visual social interactions [32]; brain architecture differed processing regions (lobes and MB calyx) increase with between species that did and did not use face recognition brain size faster than chemosensory processing regions [33]. Polistes dominulus females in social nest-founding (Figure 3)[42]. The developmental basis of these groups had larger antennal lobes and MB calyx collars changes in brain allometry is unknown. than solitary females, suggesting sociality affected adult brain development [34]. Similarly, in a comparative Species differences in brain architecture: social analysis, paper wasp queens had significantly larger structure MB calyces than their workers; the high rate of social Vespid social structures are diverse. Examples of most of interactions for nest-bound queens may be related to MB the known range of animal sociality levels or grades can be development [35]. Eusocial vespid males typically found in this one family [2]. All species of Euparagiinae, engage only in mating behavior, but male Mischocyttarus Masarinae (pollen wasps), and Eumeninae (potter wasps) mastigophporus are unusual by being dominant over are solitary nesters; Stenogastinae (hover wasps) range female nest mates [36]. Male M. mastigophporus MB size from solitary nesting to relatively simple societies; and all correlated positively with their rate of dominating female Vespinae ( and yellowjackets) and Polistinae nestmates [37]. (paper wasps) are eusocial. Two important grade-shifts in social complexity occurred in the Vespidae family. The reproductive castes of eusocial Vespidae provide The transition from solitary-nesting to primitive or excellent opportunities for exploring how brain architec- independent-founding occurred twice, in ture develops in response to variation in sensory environ- the Paleotropical hover-wasps (Stenogastrinae) and in ments. Queens and workers often differ dramatically in the (Polistinae + Vespinae) clade [43,44]. A significant behavior, leading to distinct environmental experiences decrease in relative MB investment accompanied the during adulthood [35]. In independent-founding origin of sociality in the Polistinae, and further changes

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Figure 2

3 1.6

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0.6 Linear regression r2 = 0.98, p<0.0001 0.4

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0.0 Species mean total brain volume, mm

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0.08 Inverse 3rd-order regression r2 = 0.89, p<0.0001 0.06

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0.02 Volume ratio, brain:head capsule Volume 0.00 0204060 80 Species mean head capsule volume, mm3

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(Top) Eusocial Vespidae species-mean total brain volume increases with head capsule volume. (Bottom) Plotting head-volume relative brain volume against head-volume shows the brain/body size relationship is allometric, and illustrates Haller’s rule: body-size relative brain size increases at the lower limits of body size within a clade. This pattern is presumably caused by clade-specific limits on minimum absolute brain size. Dashed lines show best-fit regression relationships, all regression model parameters were significant ( p < 0.05) in all regression models. Volumes were obtained from serial thin sections of vespid wasp head capsules using methods described in O’Donnell et al. [35,42,45]. in social structure (colony size, swarm-founding, and caste The transition from independent- to swarm-founding polyphenism) did not predict MB investment variation occurred four times among the eusocial Polistinae [48]. [45]. These patterns suggest cooperative information There are independent radiations of swarm-founding sharing or ‘distributed cognition’ was an adaptive paper wasps in the Paleotropics, where both African advantage to even simple grades of eusociality. Given Polybioides and some species of Australasian Ropalidia their range of social structures and colony sizes [46], and have separately achieved this grade [49,50], and in the their distinctive patterns of colony development [47], Neotropics, where a radiation of 19 currently-recognized Stenogastrinae are important subjects for future genera of the paper wasp tribe Epiponini occurred [22]. neurological research. There was also a convergent origin of swarming in the www.sciencedirect.com Current Opinion in Insect Science 2017, 22:54–61 58 Social insects

Figure 3 3 0.4

Visual (optic lobes) 0.3

0.2 Chemosensory (antennal lobes) Apoica 0.1 Peripheral lobe volume, mm

0.0

3 0.16 Visual (MB collar)

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Chemosensory 0.04 (MB lip) MB calyx region volume, mm

0.00 0.0 0.1 0.2 0.3 0.4 0.5 0.6 Protocerebral mass volume, mm3

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Species-mean volumes of visual processing brain regions (solid triangles) and chemosensory processing regions (open circles) plotted against an index of overall brain size (the volume of the protocerebral mass: Figure 1) for 19 species of eusocial Vespidae, ranging from the smallest-bodied species sampled (Leipolemeles dorsata) to the largest (Vespa ducalis). The dashed lines show the best-fit linear regression relationships for each structure. (Top) Peripheral lobes, data point for the nocturnal Apoica is indicated. Slopes differ significantly (ANCOVA, F1,36 = 258.9, p < 0.001). (Bottom) Mushroom body calyx regions. Slopes differ significantly (ANCOVA, F1,36 = 66.3, p < 0.001). Volumes were obtained from serial thin sections of vespid wasp head capsules using methods described in O’Donnell et al. [35,42,45].

Vespinae subfamily: colonies of the Paleotropical genus little evidence for significant neurological variation Provespa are swarm-initiated [51]. In general, the origins related to species-level social structure differences. Mean of swarming are associated with increases in mature mature colony size, mode of founding (independent vs. colony size and may also enable increased division of swarm), and degree of queen-worker differentiation all labor and behavioral specialization of queens and workers failed to predict brain-size relative mushroom body [21,22,52,53]. However, among eusocial Vespidae, volume and sensory lobe volumes [42,45]. Studies of comparative analyses of brain architecture have provided swarm-founders have focused on Neotropical Epiponini;

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brain investment patterns of the Old-world taxa not supported for wasps in a comparative analysis [45]. Polybioides, the swarming Ropalidia, and Provespa await Sociality in family-based, colony-selected systems may investigation. permit evolutionary decreases in brain investment at the individual level. However, within colonies, social inter- Species differences in ecology: potential for action differences often correspond with individual’s neuroecological analyses brain structure, suggesting social demands may drive In some ways, vespid wasps are relatively ecologically increased brain development [27,29,33,34,37]. Ecological homogeneous. Most species are predaceous, foraging for differences, such as light levels during activity, are protein to feed their larvae by attacking and dismember- reflected in both species [42] and individual [35] dif- ing relatively small, soft-bodied insects as prey. ferences in brain structure. Little is known about how Caterpillars (lepidopteran larvae) are frequently neural substrates affect foraging resource shifts, and inter- well-represented in vespid diets [54,55]. A fascinating actions such as nesting associations. Neuroecological divergent wasp feeding ecology is found in the vespid approaches applied to under-sampled wasp taxa, such subfamily Masarinae, the pollen wasps: like most bees, as pollen wasps [56], nocturnal Vespinae [51], and hover these insects collect pollen as a protein source instead of wasps [46], are needed to test the generality of the insect prey [56]. A few species of Vespinae and of patterns we summarized, and will provide novel insights swarm-founding Epiponinae are necropagous, collecting into the ecology and sociobiology of insect brain plasticity flesh from vertebrate and large invertebrate carcasses and brain evolution. [57,58]. Some eusocial vespids at least occasionally engage in group foraging when attacking large-bodied prey [59]. Adult wasps obtain much of their nutrition from Acknowledgements sugary solutions [60]. Wasps visit a wide array of relatively Funding was provided by NSF grant IOS-1209072 and Drexel University startup funds. Thanks to Katherine Fiocca, Meghan Barrett, Skye Miller, generalized flowers and collect floral nectar, and some Paulina Khodak, and Elisabeth Sulger for assistance with neuroanatomy plants have flowers specially adapted for wasp visitation data collection. and wasp pollination; chemical attractants in nectar may promote wasp visitation [61,62]. Vespid wasps frequently References and recommended reading visit plant extrafloral nectaries and plant-sucking insects Papers of particular interest, published within the period of review, to obtain honeydew [63]. The sensory and cognitive have been highlighted as: mechanisms that underlie the diversity of vespid wasp  of special interest feeding ecologies are largely unexplored.  of outstanding interest

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