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A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae)

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Abstract

Adaptive brain architecture hypotheses predict brain region investment matches the cognitive and sensory demands an individual confronts. Social hymenopteran queen and worker castes differ categorically in behavior and physiology leading to divergent sensory experiences. Queens in mature colonies are largely nest-bound while workers depart nests to forage. We predicted social paperwasp castes would differ in tissue allocation among brain regions. We expected workers to invest relatively more than queens in neural tissues that process visual input. As predicted, we found workers invested more in visual relative to antennal processing than queens both in peripheral sensory lobes and in central processing brain regions (mushroom bodies). Although we did not measure individual brain development changes, our comparative data provide a preliminary test of mechanisms of caste differences. Paperwasp species differ in the degree of caste differentiation (monomorphic versus polymorphic castes) and in colony structure (independent- versus swarm-founding); these differences could correspond to the magnitude of caste brain divergence. If caste differences resulted from divergent developmental programs (experience-expectant brain growth), we predicted species with morphologically distinct queens, and/or swarm-founders, would show greater caste divergence of brain architecture. Alternatively, if adult experience affected brain plasticity (experience-dependent brain growth), we predicted independent-founding species would show greater caste divergence of brain architecture. Caste polymorphism was not related to the magnitude of queen-worker brain differences, and independent-founder caste brain differences were greater than swarm-founder caste differences. Greater caste separation in independent-founder brain structure suggests a role for adult experience in the development of caste-specific brain anatomy.

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Acknowledgments

Thanks to two anonymous reviewers for thoughtful and helpful comments on earlier versions of the paper. Emily Johnson, Joshua Matlock, Yamile Molina, Abigal Mudd, Jason Stafstrom, Eve Swearingen, and Ceri Weber assisted with histology and neuroanatomy. Specimens were collected under research permits from the Republics of Ecuador and Costa Rica and in accordance with their laws. M.R.C. was supported by an NSF Graduate Research Fellowship under Grant No. DGE-0718124; S.O’D. was supported by NSF grant IOS-1209072.

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Authors and Affiliations

  1. Department of Biodiversity, Earth & Environmental Science, Drexel University, 3245 Chestnut Street, Philadelphia, PA, 19104, USA

    Sean O’Donnell, Susan J. Bulova, Sara DeLeon, Christopher Papa & Nazaneen Zahedi

  2. Department of Biology, University of Washington, Seattle, WA, 98195, USA

    Marie R. Clifford

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  1. Sean O’Donnell
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  2. Marie R. Clifford
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  3. Susan J. Bulova
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  4. Sara DeLeon
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Correspondence to Sean O’Donnell.

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Communicated by M. Giurfa

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O’Donnell, S., Clifford, M.R., Bulova, S.J. et al. A test of neuroecological predictions using paperwasp caste differences in brain structure (Hymenoptera: Vespidae). Behav Ecol Sociobiol 68, 529–536 (2014). https://doi.org/10.1007/s00265-013-1667-6

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