Susan J. Bulova

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

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.

Into the black and back: the ecology of brain investment in Neotropical army ants (Formicidae: Dorylinae)

Shifts to new ecological settings can drive evolutionary changes in animal sensory systems and in the brain structures that process sensory information. We took advantage of the diverse habitat ecology of Neotropical army ants to test whether evolutionary transitions from below- to above-ground activity were associated with changes in brain structure. Our estimates of genus-typical frequencies of above-ground activity suggested a high degree of evolutionary plasticity in habitat use among Neotropical army ants. Brain structure consistently corresponded to degree of above-ground activity among genera and among species within genera. The most above-ground genera (and species) invested relatively more in visual processing brain tissues; the most subterranean species invested relatively less in central processing higher-brain centers (mushroom body calyces). These patterns suggest a strong role of sensory ecology (e.g., light levels) in selecting for army ant brain investment evolution and further suggest that the subterranean environment poses reduced cognitive challenges to workers. The highly above-ground active genus Eciton was exceptional in having relatively large brains and particularly large and structurally complex optic lobes. These patterns suggest that the transition to above-ground activity from ancestors that were largely subterranean for approximately 60 million years was followed by re-emergence of enhanced visual function in workers.

Development and evolution of brain allometry in wasps (Vespidae): size, ecology and sociality

We review research on brain development and brain evolution in the wasp family Vespidae. Basic vespid neuroanatomy and some aspects of functional neural circuitry are well-characterized, and genomic tools for exploring brain plasticity are being developed. Although relatively modest in terms of species richness, the Vespidae include species spanning much of the known range of animal social complexity, from solitary nesters to highly eusocial species with some of the largest known colonies and multiple reproductives. Eusocial species differ in behavior and ecology including variation in queen/worker caste differentiation and in diurnal/nocturnal activity. Species differences in overall brain size are strongly associated with brain allometry; relative sizes of visual processing tissues increase at faster rates than antennal processing tissues. The lower relative size of the central-processing mushroom bodies (MB) in eusocial species compared to solitary relatives suggests sociality may relax demands on individual cognitive abilities. However, queens have greater relative MB volumes than their workers, and MB development is positively associated with social dominance status in some species. Fruitful areas for future investigations of adaptive brain investment in the clade include sampling of key overlooked taxa with diverse social structures, and the analysis of neural correlations with ecological divergence in foraging resources and diel activity patterns.

Cumulative Effects of Foraging Behavior and Social Dominance on Brain Development in a Facultatively Social Bee (Ceratina australensis)

In social insects, both task performance (foraging) and dominance are associated with increased brain investment, particularly in the mushroom bodies. Whether and how these factors interact is unknown. Here we present data on a system where task performance and social behavior can be analyzed simultaneously: the small carpenter bee Ceratina australensis. We show that foraging and dominance have separate and combined cumulative effects on mushroom body calyx investment. Female C. australensis nest solitarily and socially in the same populations at the same time. Social colonies comprise two sisters: the social primary, which monopolizes foraging and reproduction, and the social secondary, which is neither a forager nor reproductive but rather remains at the nest as a guard. We compare the brains of solitary females that forage and reproduce but do not engage in social interactions with those of social individuals while controlling for age, reproductive status, and foraging experience. Mushroom body calyx volume was positively correlated with wing wear, a proxy for foraging experience. We also found that, although total brain volume did not vary among reproductive strategies (solitary vs. social nesters), socially dominant primaries had larger mushroom body calyx volumes (corrected for both brain and body size variation) than solitary females; socially subordinate secondaries (that are neither dominant nor foragers) had the least-developed mushroom body calyces. These data demonstrate that sociality itself does not explain mushroom body volume; however, achieving and maintaining dominance status in a group was associated with mushroom body calyx enlargement. Dominance and foraging effects were cumulative; dominant social primary foragers had larger mushroom body volumes than solitary foragers, and solitary foragers had larger mushroom body volumes than nonforaging social secondary guards. This is the first evidence for cumulative effects on brain development by dominance and task performance.

Caste differences in the mushroom bodies of swarm-founding paper wasps: implications for brain plasticity and brain evolution (Vespidae, Epiponini)

Eusocial insect reproductive castes (in Hymenoptera, female reproductive queens and sterile workers) differ dramatically in behavior. Castes may differ in the cognitive demands that affect patterns of brain tissue investment. Queens and workers diverge most strongly in the advanced eusocial, or swarm-founding species, where queens do not forage and rarely leave their nests. We asked whether reproductive castes of swarm-founding paper wasps in the tribe Epiponini differed in the relative sizes of their mushroom bodies (MB), a key brain region involved in sensory integration, and in learning and memory. We measured brain-size corrected volumes of the MB dendritic-field neuropils (calyces) and the MB axonal bundles (peducles and lobes) for queens and workers from 16 species of 10 genera of the tribe Epiponini. The subject species spanned much of the epiponine phylogeny, differing in colony size and degree of caste differentiation. Queens had significantly higher relative MB investment than workers, both for the MB in toto and for the MB calyces. The magnitude of queen-worker MB size differences did not covary significantly with body size, but species with larger colonies had stronger caste differences in MB size. A review of caste differences in MB volume across a wide range of social Hymenoptera taxa suggested a positive association of MB investment with social dominance is widespread.Significance statementSocial insect castes (reproducing queens and sterile workers) differ strongly in behavior, particularly in swarm-founding species where queens are largely nest-bound. Caste comparisons are a powerful model for understanding brain/behavior relationships. We measured the relative size of a key insect brain region, the mushroom bodies (MB), in 16 swarm-founding wasp species. MB are involved in sensory integration, and in learning and memory. Queens had relatively larger MB than workers, and the magnitude of the queen-worker differences increased with species average colony size. We suggest the reproductive dominance and social contact of nest-bound queens promotes greater mushroom body investment.

Adult nutrition and reproductive physiology: a stable isotope analysis in a eusocial paper wasp (Mischocyttarus mastigophorus, Hymenoptera: Vespidae)

Division of labor in social groups can be influenced by differential nutrition. Consumption of more food or higher-quality food often affects individuals’ capacities for reproduction. In social insects, nutrients consumed during immature (e.g., larval) stages often affect adult reproductive capacity, but adult nutrition may also impact reproductive status. This study tested whether ovary development, an indicator of reproductive status, corresponded to higher trophic-level feeding for adults in the primitively eusocial paper wasp Mischocyttarus mastigophorus. Our main prediction was that females’ ovary development would correlate positively with evidence of feeding at higher trophic levels, as indicated by stable isotope ratios of nitrogen (δ15N) and carbon (δ13C). We first asked whether isotope ratios of mature females co-varied with ovary development. δ15N values were higher for mature females with better-developed ovaries, as expected if they fed on a diet richer in animal tissue. There was a negative relationship of δ13C with ovary development in mature females, as would be expected if females with developed ovaries had higher body lipid stores. To test for evidence of nutritional biasing of caste during immature development, we measured changes in isotope ratios across pupal development leading up to early adulthood (i.e., immediately before and after adult eclosion). The δ15N and δ13C values for mature pupae were similar to those of newly emerged adults and to those of mature adults lacking developed ovaries. In contrast, mature females with developed ovaries showed N-isotope signatures of a more prey-based diet and C-isotope signatures of elevated lipid content. We conclude the N and C isotopic signatures of ovary-developed mature females diverged from their levels at the end of immature development. The findings suggest reproductive caste status was associated with differences in nutrient acquisition and reflects differences in consumption of animal-derived versus plant-based foods during adulthood.Significance statementPre-adult nutrition is known to affect caste development, and thereby influence division of labor, in diverse insect societies. In temperate independent-founding (IF) paper wasps, the effects of larval nutrition on adult caste may reflect adaptations for overwintering and diapause by reproductive females. We asked whether adult nutritional content showed caste-related trophic differences in the Neotropical IF paper wasp Mischocyttarus mastigophorus. Previous studies suggested interactions among adult nest-mates affected food sharing and caused biased nutrient flow within colonies. Our data suggest adult nutrition affected reproductive physiology. We propose this pattern may be widespread in tropical IF paper wasps, where opportunities for adult reproductive plasticity are favored by long colony cycles and relatively aseasonal nest founding.