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O'donnell S., M.R. Clifford, S. Deleon, C. Papa, N. Zahedi & S.J. Bulova

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O'donnell S., M.R. Clifford, S. Deleon, C. Papa, N. Zahedi & S.J. Bulova Behav Ecol Sociobiol (2014) 68:529–536 DOI 10.1007/s00265-013-1667-6 ORIGINAL PAPER A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae) Sean O’Donnell & Marie R. Clifford & Susan J. Bulova & Sara DeLeon & Christopher Papa & Nazaneen Zahedi Received: 31 July 2013 /Revised: 25 November 2013 /Accepted: 4 December 2013 /Published online: 19 December 2013 # Springer-Verlag Berlin Heidelberg 2013 Abstract Adaptive brain architecture hypotheses predict brain architecture. Caste polymorphism was not related to brain region investment matches the cognitive and sensory the magnitude of queen-worker brain differences, and demands an individual confronts. Social hymenopteran queen independent-founder caste brain differences were greater than and worker castes differ categorically in behavior and physi- swarm-founder caste differences. Greater caste separation in ology leading to divergent sensory experiences. Queens in independent-founder brain structure suggests a role for adult mature colonies are largely nest-bound while workers depart experience in the development of caste-specific brain nests to forage. We predicted social paperwasp castes would anatomy. differ in tissue allocation among brain regions. We expected workers to invest relatively more than queens in neural tissues Keywords Antennal lobe . Brain evolution . Mushroom that process visual input. As predicted, we found workers body . Neural plasticity . Optic lobe invested more in visual relative to antennal processing than queens both in peripheral sensory lobes and in central pro- cessing brain regions (mushroom bodies). Although we did Introduction not measure individual brain development changes, our com- parative data provide a preliminary test of mechanisms of Brain tissues are compartmentalized into anatomically dis- caste differences. Paperwasp species differ in the degree of crete regions that perform distinct cognitive processes caste differentiation (monomorphic versus polymorphic (Tanaka et al. 2012; Arrenberg and Driever 2013; Brown castes) and in colony structure (independent- versus swarm- and Piscopo 2013; Mantini et al. 2013). Brain tissue is meta- founding); these differences could correspond to the magni- bolically and developmentally expensive (Laughlin 2001; tude of caste brain divergence. If caste differences resulted Niven and Laughlin 2008; Navarrete et al. 2011). Natural from divergent developmental programs (experience- selection should act on brain architecture such that the relative expectant brain growth), we predicted species with morpho- investment in each brain region matches the animal’scogni- logically distinct queens, and/or swarm-founders, would show tive demands (Chittka and Niven 2009; Gronenberg and greater caste divergence of brain architecture. Alternatively, if Riveros 2009; Shultz and Dunbar 2010). Investment in func- adult experience affected brain plasticity (experience- tionally distinct brain regions should reflect behavior and dependent brain growth), we predicted independent- ecology at the individual and species levels (Cooper et al. founding species would show greater caste divergence of 1993;Catania2005;Linseyetal.2007). Social insect castes present an excellent opportunity to test Communicated by M. Giurfa adaptive brain architecture hypotheses. Queens and workers play distinct social roles, and neuroecological theory predicts S. O’Donnell (*) : S. J. Bulova : S. DeLeon : C. Papa : N. Zahedi Department of Biodiversity, Earth & Environmental Science, Drexel their different behaviors and sensory experience will be University, 3245 Chestnut Street, Philadelphia, PA 19104, USA reflected in distinct brain architectures (Gronenberg and e-mail: [email protected] Riveros 2009). In most social insects, reproductive castes are categorically distinct phenotypes that result from develop- M. R. Clifford Department of Biology, University of Washington, Seattle, mental plasticity (West-Eberhard 1981). In female eusocial WA 98195, USA Hymenoptera, reproductive queens and sterile workers can 530 Behav Ecol Sociobiol (2014) 68:529–536 develop from similar genotypes depending on the environ- processing tissue volume as an index of the degree of reliance ment early in larval development (Hunt et al. 2007;Martins on visual versus antennal inputs, both in the peripheral lobes et al. 2010). We asked whether brain investment differed and in the mushroom bodies. Paperwasp queens are largely between reproductive castes—egg-laying queens and sterile nest-bound and experience less complex visual environments workers—in eusocial paperwasps (Vespidae, Polistinae). and lower light levels than their foraging workers. Behavioral Paperwasp queens and workers differ strongly in behavior activity under lower light conditions is associated with de- and ecology. Queens are generally nest-bound, rarely flying creases in visual processing tissue (Catania 2005;Bartonetal. from mature colonies, while workers perform diverse tasks 1995; Fujun et al. 2012). We predicted paperwasp workers including leaving the nest to forage (Herman et al. 2000; would invest relatively more than their queens in visual Bruyndonckx et al. 2006; Chavarria-Pizarro and West- processing brain regions (the optic lobes and the collar Eberhard 2010; De Souza and Prezoto 2012). However, regions of the mushroom body calyx; Gronenberg 1999; paperwasps vary widely in colony size and social complexity. O’Donnell et al. 2011). Independent-founding species have relatively small colonies, Different developmental programs could lead to caste- and adult females are relatively plastic in their reproductive specific brain architecture (experience-expectant brain roles. Dominance interactions among females affect social growth). Alternatively, brain structure could respond to indi- status and opportunities for reproduction (Molina and viduals’ caste-specific environments (experience-dependent O’Donnell 2008). Swarm-founding wasps have larger colo- brain growth; Fahrbach et al. 1998; Farris et al. 2001). We nies with less plasticity in reproductive roles (Jeanne 2003). used comparisons of paperwasp species with different social Paperwasp species further differ in the degree of female caste structures as an indirect means of assessing the relative im- differentiation. Paperwasps range from species with no detect- portance of experience-expectant and experience-dependent able caste categories (independent-founders and some swarm- brain development. We categorized our subject species as founders) to swarm-founding species with discrete queen/ independent-founders (primitively eusocial) and swarm- worker body size and shape differences (O’Donnell 1998a; founders (advanced eusocial), and we identified species with Noll et al. 2004). morphologically distinct queens (highly eusocial) (O’Donnell We used the relative volumes of brain regions that process 1998a;Jeanne2003;Nolletal.2004). We tested whether the two distinct sensory inputs—the compound eyes (vision) and magnitude of queen-worker differences in brain architecture the antennae (chemosensation and tactile)—to test whether differed between the three social structure categories (inde- caste differences correspond to environmental context. pendent-founders, caste monomorphic swarm-founders, and Distinct brain regions process visual information from the caste dimorphic swarm-founders). The degree of specializa- compound eyes and chemosensory input from the antennae tion of reproductive castes on different social roles increases in social Hymenoptera, including paperwasps (Gronenberg as larger, more complex societies evolve from independent- 1999; Ehmer and Hoy 2000;O’Donnell et al. 2011). founding ancestors with smaller colonies (Bourke 1999; Anatomically distinct peripheral lobes process visual and Anderson and McShea 2001;Jeanne2003). If experience- chemosensory inputs (optic and antennal lobes, respectively; expectant growth predominates, we expected caste differences Gronenberg 1999; Hansson and Stensmyr 2011), and these to be greater in species with morphologically distinct queen/ lobes innervate distinct regions of central processing neuropils worker castes and/or greater in swarm-founders relative to called mushroom bodies (Strausfeld et al. 1998; Fahrbach independent-founders. In contrast, reproductive caste status 2006). The optic lobes innervate the collar region of the in independent-founders is relatively plastic and influenced by mushroom body calyx, and the antennal lobes innervate the dominance interactions (Molina and O’Donnell 2008). If lip region of the mushroom body calyx (Gronenberg 1999). experience-dependent brain growth predominates, queen- Both the antennal and optic lobes show structural plasticity worker differences could be stronger in independent-founders. following changes in sensory input and experience (Barth et al. 1997;Eickhoffetal.2012;Arenasetal.2012). Differences in mushroom body calyx volume are related to Materials and methods caste and task performance in many social Hymenoptera including paperwasps (Gronenberg et al. 1996; Farris Subject species et al. 2001;O’Donnell et al. 2004, 2007; Muscedere and Traniello 2012). We analyzed the brain architecture of one species from each of Because queens and workers occupy different sensory 12 genera of Neotropical eusocial paperwasps (Polistinae). environments, and paperwasp brain regions vary in size with Our subjects spanned the 19 currently recognized experience, we predicted there would be caste differences
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