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Caste Differences in the Mushroom Bodies of Swarm-Founding Paper Wasps: Implications for Brain Plasticity and Brain Evolution (Vespidae, Epiponini)

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Caste Differences in the Mushroom Bodies of Swarm-Founding Paper Wasps: Implications for Brain Plasticity and Brain Evolution (Vespidae, Epiponini) Behav Ecol Sociobiol (2017) 71: 116 DOI 10.1007/s00265-017-2344-y ORIGINAL ARTICLE Caste differences in the mushroom bodies of swarm-founding paper wasps: implications for brain plasticity and brain evolution (Vespidae, Epiponini) Sean O’Donnell1 & Susan J. Bulova1 & Sara DeLeon1 & Meghan Barrett2 & Katherine Fiocca2 Received: 28 February 2017 /Revised: 20 June 2017 /Accepted: 25 June 2017 /Published online: 13 July 2017 # Springer-Verlag GmbH Germany 2017 Abstract a positive association of MB investment with social dom- Eusocial insect reproductive castes (in Hymenoptera, fe- inance is widespread. male reproductive queens and sterile workers) differ dra- matically in behavior. Castes may differ in the cognitive Significance statement demands that affect patterns of brain tissue investment. Social insect castes (reproducing queens and sterile workers) Queens and workers diverge most strongly in the ad- differ strongly in behavior, particularly in swarm-founding spe- vanced eusocial, or swarm-founding species, where cies where queens are largely nest-bound. Caste comparisons queens do not forage and rarely leave their nests. We are a powerful model for understanding brain/behavior relation- asked whether reproductive castes of swarm-founding pa- ships. We measured the relative size of a key insect brain re- per wasps in the tribe Epiponini differed in the relative gion, the mushroom bodies (MB), in 16 swarm-founding wasp sizes of their mushroom bodies (MB), a key brain region species. MB are involved in sensory integration, and in learning involved in sensory integration, and in learning and mem- and memory. Queens had relatively larger MB than workers, ory. We measured brain-size corrected volumes of the MB and the magnitude of the queen-worker differences increased dendritic-field neuropils (calyces) and the MB axonal with species average colony size. We suggest the reproductive bundles (peducles and lobes) for queens and workers from dominance and social contact of nest-bound queens promotes 16 species of 10 genera of the tribe Epiponini. The subject greater mushroom body investment. species spanned much of the epiponine phylogeny, differ- ing in colony size and degree of caste differentiation. Keywords Brain evolution . Mushroom bodies . Paper Queens had significantly higher relative MB investment wasps . Polistinae than workers, both for the MB in toto and for the MB calyces. The magnitude of queen-worker MB size differ- ences did not covary significantly with body size, but Introduction species with larger colonies had stronger caste differences in MB size. A review of caste differences in MB volume The neuroecology of caste in social insects across a wide range of social Hymenoptera taxa suggested Neuroecology theory assumes brain tissue is costly and rela- tive investment in different brain regions is therefore Communicated by W. Hughes constrained. Neuroecological models predict differences in animals’ sensory environments will lead to differences in * ’ Sean O Donnell brain structure as a result of brain plasticity (at the individual [email protected] level) or brain evolution (when comparing species) (Barton et al. 1995; Hampton and Shettleworth 1996;Nivenand 1 Department of Biodiversity Earth and Environmental Science, Laughlin 2008; but see Kamhi et al. 2016). Relative brain Drexel University, Philadelphia, PA 19104, USA region sizes are expected to correspond to the cognitive de- 2 Department of Biology, Drexel University, Philadelphia, PA, USA mands an animal confronts. Comparisons of individuals or 116 Page 2 of 9 Behav Ecol Sociobiol (2017) 71: 116 species that differ in behavior or ecology can be used to test the stalk-like MB lobes and peduncles (Strausfeld 2002), which hypotheses about the cognitive forces shaping adaptive differ- comprise the Kenyon cell axons; these regions are involved in ences in brain investment. modifying neural activity in the calyx and long-term memory The distinct behavioral roles of females from different re- formation (Pascual and Preat 2001;Giurfa2003). productive castes—mated, egg-laying queens versus unmated, sterile workers—are characteristics of eusocial Social behavior and brain investment Hymenoptera (Holldobler and Wilson 2009). Queen and worker behavior entail different ecological and social environ- Controversy exists over expected direction of queen vs. worker ments. Queen-worker differences are greatest in the complex caste differences in MB size. Based on the limited task repertoire societies of advanced eusocial, swarm-founding species of queens, reduced MB investment could be characteristic of (Jeanne 2003; Jeanne and Suryanarayanan 2011). queens (Julian and Gronenberg 2002; Gronenberg and Riveros In these species, colonies are initiated by social groups of 2009; Roat and da Cruz Landim 2010). Alternatively, the chal- many workers and one to many queens (Jeanne 1991, 2003). lenges of maintaining social and/or reproductive dominance may Swarm-founding queens are largely nest-bound (except for place strong cognitive demands on queens (O'Donnell et al. mating flights and colony emigrations). In-nest queens engage 2007;Smithetal.2010; Rehan et al. 2015). Brain development in extensive social contact but perform relatively few tasks. In is affected by social experience, both positively (social enrich- contrast, workers perform outside-nest tasks including forag- ment) and negatively (social deprivation), in many animals in- ing, but often act alone (Eberhard 1975; O'Donnell 1996; cluding insects (Heisenberg et al. 1995; Ehmer et al. 2001;Lee Richter 2000;O’Donnelletal.2014). We asked whether and Goto 2013;Saleetal.2014; Seid and Junge 2016). Social queens and workers of eusocial wasps (Vespidae) differed in insect’s perception of rewarding stimuli can be modified by so- brain structure, and whether these differences might reflect cial context, and gene expression profiles in the brain are affected behavioral differences between the castes. by social interactions (Barron et al. 2009; McNeill et al. 2016). Social dominance is associated with greater MB size or greater Mushroom bodies as key brain regions in social insect MB neuropil development in facultatively social bees (Smith neuroecology et al. 2010; Rehan et al. 2015) and in primitively social paper wasps (Molina and O’Donnell 2007, 2008; O'Donnell et al. To test for caste differences in brain structure, we focused on the 2007). Few comparisons of mature adult queen and worker mushroom bodies (MB), paired neuropils in the forebrain of brains are available for advanced eusocial species. We sampled insects and other arthropods (Strausfeld et al. 1998;Fahrbach MB investment (MB size relative to brain size and to body size) 2006). The MB function in sensory integration, and in learning in both castes from a diverse set of epiponine wasp species to test and memory (Lozano et al. 2001;Davis2005;Farris2013). for caste differences in MB size. A previous study suggested Evolutionary increases in MB size and structural complexity paper wasp queens, including some epiponines, had larger MB correspond to greater species-typical ecological complexity relative to their peripheral processing lobes than their workers (Farris 2008, 2013). At the individual level, the MB are devel- (O'Donnelletal.2011). However, this caste comparison did not opmentally plastic, varying in volume with behavioral differ- correct for overall brain size differences and may have been ences (Withers et al. 2008; Riveros and Gronenberg 2010; affected by reduced peripheral lobe size in queens due to their Muscedere and Traniello 2012). Positive associations of MB simplified in-nest environments (O’Donnell et al. 2014). size with foraging behavior occur in diverse eusocial Hymenoptera (Farris et al. 2001;O’Donnell et al. 2004; Behavioral diversity in the Epiponini: variation in social Fahrbach and Dobrin 2009; Riveros and Gronenberg 2010; complexity Muscedere and Traniello 2012). Volume increases in the MB calyces (the neuropils receiving input from the sensory lobes) We used a generic phylogeny of the Neotropical radiation of are associated with greater dendrite length and complexity and swarm-founding Epiponini to select subject taxa that spanned synaptic density of the intrinsic MB neurons (Kenyon cells), much of the evolutionary history of the lineage (Fig. 1; Wenzel suggesting greater neural connectivity (Farris et al. 2001; and Carpenter 1994). We asked whether the magnitude of queen- Ehmer and Gronenberg 2004; Jones et al. 2009; Seid et al. worker brain differences covaried with species differences in 2005; Fahrbach 2006). In most eusocial Hymenoptera, distinct social complexity. We used two indicators of variation in caste regions of the MB neuropil (calyx) receive input from visual specialization: colony size and degree of queen-worker develop- and olfactory modalities. The compound eyes input to the MB mental differentiation. Although all epiponines are swarm foun- calyx collar region (visual processing), and the antennae input ders, epiponine species vary widely in colony size: typical adult to the MB calyx lip region (olfactory processing) (Gronenberg populations in mature nests span over five orders of magnitude 2001). We tested whether caste differences in brain structure (Jeanne 1991, 2003). Strength of division of labor and caste were consistent across both calyx regions. We also quantified specialization generally increase with colony size within and Behav Ecol Sociobiol (2017) 71: 116 Page 3 of 9 116 Fig. 1 Genus-level phylogeny, subgenus-level
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