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Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae).

ABSTRACT: The social brain hypothesis assumes the evolution of social behaviour changes animals' ecological environments, and predicts evolutionary shifts in social structure will be associated with changes in brain investment. Most social brain models to date assume social behaviour imposes additional cognitive challenges to animals, favouring the evolution of increased brain investment. Here, we present a modification of social brain models, which we term the distributed cognition hypothesis. Distributed cognition models assume group members can rely on social communication instead of individual cognition; these models predict reduced brain investment in social species. To test this hypothesis, we compared brain investment among 29 species of wasps (Vespidae family), including solitary species and social species with a wide range of social attributes (i.e. differences in colony size, mode of colony founding and degree of queen/worker caste differentiation). We compared species means of relative size of mushroom body (MB) calyces and the antennal to optic lobe ratio, as measures of brain investment in central processing and peripheral sensory processing, respectively. In support of distributed cognition predictions, and in contrast to patterns seen among vertebrates, MB investment decreased from solitary to social species. Among social species, differences in colony founding, colony size and caste differentiation were not associated with brain investment differences. Peripheral lobe investment did not covary with social structure. These patterns suggest the strongest changes in brain investment--a reduction in central processing brain regions--accompanied the evolutionary origins of eusociality in Vespidae.

SUBMITTER: O'Donnell S

PROVIDER: S-EPMC4590486 | biostudies-literature | 2015 Jul

REPOSITORIES: biostudies-literature

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Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae).

O'Donnell Sean S Bulova Susan J SJ DeLeon Sara S Khodak Paulina P Miller Skye S Sulger Elisabeth E

Proceedings. Biological sciences 20150701 1810

The social brain hypothesis assumes the evolution of social behaviour changes animals' ecological environments, and predicts evolutionary shifts in social structure will be associated with changes in brain investment. Most social brain models to date assume social behaviour imposes additional cognitive challenges to animals, favouring the evolution of increased brain investment. Here, we present a modification of social brain models, which we term the distributed cognition hypothesis. Distribute ...[more]

PMID: 26085587

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Project description:Theoretically intelligence should evolve to help animals solve specific types of problems posed by the environment, but it remains unclear how environmental complexity or novelty facilitates the evolutionary enhancement of cognitive abilities, or whether domain-general intelligence can evolve in response to domain-specific selection pressures. The social complexity hypothesis, which posits that intelligence evolved to cope with the labile behaviour of conspecific group-mates, has been strongly supported by work on the sociocognitive abilities of primates and other animals. Here we review the remarkable convergence in social complexity between cercopithecine primates and spotted hyaenas, and describe our tests of predictions of the social complexity hypothesis in regard to both cognition and brain size in hyaenas. Behavioural data indicate that there has been remarkable convergence between primates and hyaenas with respect to their abilities in the domain of social cognition. Furthermore, within the family Hyaenidae, our data suggest that social complexity might have contributed to enlargement of the frontal cortex. However, social complexity failed to predict either brain volume or frontal cortex volume in a larger array of mammalian carnivores. To address the question of whether or not social complexity might be able to explain the evolution of domain-general intelligence as well as social cognition in particular, we presented simple puzzle boxes, baited with food and scaled to accommodate body size, to members of 39 carnivore species housed in zoos and found that species with larger brains relative to their body mass were more innovative and more successful at opening the boxes. However, social complexity failed to predict success in solving this problem. Overall our work suggests that, although social complexity enhances social cognition, there are no unambiguous causal links between social complexity and either brain size or performance in problem-solving tasks outside the social domain in mammalian carnivores.

Project description:BackgroundThe success of herbivorous insects has been shaped largely by their association with microbes. Seed parasitism is an insect feeding strategy involving intimate contact and manipulation of a plant host. Little is known about the microbial associates of seed-parasitic insects. We characterized the bacterial symbionts of Megastigmus (Hymenoptera: Torymidae), a lineage of seed-parasitic chalcid wasps, with the goal of identifying microbes that might play an important role in aiding development within seeds, including supplementing insect nutrition or manipulating host trees. We screened multiple populations of seven species for common facultative inherited symbionts. We also performed culture independent surveys of larvae, pupae, and adults of M. spermotrophus using 454 pyrosequencing. This major pest of Douglas-fir is the best-studied Megastigmus, and was previously shown to manipulate its tree host into redirecting resources towards unfertilized ovules. Douglas-fir ovules and the parasitoid Eurytoma sp. were also surveyed using pyrosequencing to help elucidate possible transmission mechanisms of the microbial associates of M. spermotrophus.ResultsThree wasp species harboured Rickettsia; two of these also harboured Wolbachia. Males and females were infected at similar frequencies, suggesting that these bacteria do not distort sex ratios. The M. spermotrophus microbiome is dominated by five bacterial OTUs, including lineages commonly found in other insect microbiomes and in environmental samples. The bacterial community associated with M. spermotrophus remained constant throughout wasp development and was dominated by a single OTU - a strain of Ralstonia, in the Betaproteobacteria, comprising over 55% of all bacterial OTUs from Megastigmus samples. This strain was also present in unparasitized ovules.ConclusionsThis is the first report of Ralstonia being an abundant and potentially important member of an insect microbiome, although other closely-related Betaproteobacteria, such as Burkholderia, are important insect symbionts. We speculate that Ralstonia might play a role in nutrient recycling, perhaps by redirecting nitrogen. The developing wasp larva feeds on megagametophyte tissue, which contains the seed storage reserves and is especially rich in nitrogen. Future studies using Ralstonia-specific markers will determine its distribution in other Megastigmus species, its mode of transmission, and its role in wasp nutrition.

Dataset Information

Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae).

Publications

Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae).

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