Developmental and dominance‐associated differences in mushroom body structure in the paper wasp <i>Mischocyttarus mastigophorus</i>

O’Donnell, Sean; Donlan, Nicole A.; Jones, Theresa A.

doi:10.1002/dneu.20324

Cited by 36 publications

(57 citation statements)

References 43 publications

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“…The gross developmental pattern of M. genalis MB is strikingly similar to both small-and large-colony obligately eusocial bees, wasps and ants in displaying large decreases in Kenyon cell body volume early in adult life and modest increases in neuropil volume with age and experience (Fahrbach 2006;O'Donnell et al 2006). In fact, regardless of any functional interpretation, the N : K ratios of newly emerged and mature (both solitary and social) M. genalis are nearly identical to those of honeybees, despite the massive differences in colony size, social organization and phyletic distance between the two species ( §3 and Withers et al 1993).…”

Section: Discussionmentioning

confidence: 92%

“…Arneson & Wcislo 2003;Bhadra & Gadagkar 2008). Recent studies have shown a social component to MB plasticity in two species of obligately social paper wasps (Vespidae) with small colonies, which are the only two species studied to date in which dominance is maintained by individual aggressive interactions rather than by pheromones (O'Donnell et al 2006;Molina & O'Donnell 2007Molina et al 2009). Ehmer et al (2001), in contrast, did not find a difference in MB volume between dominant and subordinate wasps of Polistes dominulus wasps, but they did not measure MB subregions.…”

Section: Introductionmentioning

confidence: 99%

“…First, if sociality is more cognitively demanding than solitary living, social females should have higher N : K ratios, or larger absolute MB neuropil volume, than solitary reproductives. Second, being part of a group in itself may not influence brain plasticity so much as the demands of achieving and maintaining high dominance status, as suggested by the studies of small-colony paper wasps (O'Donnell et al 2006;Molina & O'Donnell 2007Molina et al 2009). If so, only social queens should have a larger N : K ratio and/or MB neuropil volume than solitary reproductives, while that of social workers should be comparable to solitary bees.…”

Section: Introductionmentioning

confidence: 99%

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Socially induced brain development in a facultatively eusocial sweat beeMegalopta genalis(Halictidae)

et al. 2010

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Changes in the relative size of brain regions are often dependent on experience and environmental stimulation, which includes an animal's social environment. Some studies suggest that social interactions are cognitively demanding, and have examined predictions that the evolution of sociality led to the evolution of larger brains. Previous studies have compared species with different social organizations or different groups within obligately social species. Here, we report the first intraspecific study to examine how social experience shapes brain volume using a species with facultatively eusocial or solitary behaviour, the sweat bee Megalopta genalis. Serial histological sections were used to reconstruct and measure the volume of brain areas of bees behaving as social reproductives, social workers, solitary reproductives or 1-day-old bees that are undifferentiated with respect to the social phenotype. Social reproductives showed increased development of the mushroom body (an area of the insect brain associated with sensory integration and learning) relative to social workers and solitary reproductives. The gross neuroanatomy of young bees is developmentally similar to the advanced eusocial species previously studied, despite vast differences in colony size and social organization. Our results suggest that the transition from solitary to social behaviour is associated with modified brain development, and that maintaining dominance, rather than sociality per se, leads to increased mushroom body development, even in the smallest social groups possible (i.e. groups with two bees). Such results suggest that capabilities to navigate the complexities of social life may be a factor shaping brain evolution in some social insects, as for some vertebrates.

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Section: Discussionmentioning

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Socially induced brain development in a facultatively eusocial sweat beeMegalopta genalis(Halictidae)

et al. 2010

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“…These behavioral differences result from changes in the nervous system induced by social experience. Social status affects neurogenesis in rodents (Kozorovitskiy and Gould, 2004) and crayfish (Song et al, 2007), neuronal size in fish (White et al, 2002), brain morphology in wasps (O'Donnell et al, 2007) and naked mole rats (Holmes et al, 2007), and cell receptor populations in crayfish (Spitzer et al, 2005) and fish (Burmeister et al, 2007). Social status also affects the serotonergic neuromodulation of synaptic responses in both crayfish (Yeh et al, 1996(Yeh et al, , 1997 and fish (Whitaker et al, 2011), and the excitability of neural circuits that produce different behaviors (Krasne et al, 1997;Herberholz et al, 2001;Neumeister et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Neural Circuit Reconfiguration by Social Status

Issa¹,

Drummond²,

Cattaert³

et al. 2012

J. Neurosci.

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The social rank of an animal is distinguished by its behavior relative to others in its community. Although social-status-dependent differences in behavior must arise because of differences in neural function, status-dependent differences in the underlying neural circuitry have only begun to be described. We report that dominant and subordinate crayfish differ in their behavioral orienting response to an unexpected unilateral touch, and that these differences correlate with functional differences in local neural circuits that mediate the responses. The behavioral differences correlate with simultaneously recorded differences in leg depressor muscle EMGs and with differences in the responses of depressor motor neurons recorded in reduced, in vitro preparations from the same animals. The responses of local serotonergic interneurons to unilateral stimuli displayed the same status-dependent differences as the depressor motor neurons. These results indicate that the circuits and their intrinsic serotonergic modulatory components are configured differently according to social status, and that these differences do not depend on a continuous descending signal from higher centers.

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“…(Fig. 1) Like other eusocial Hymenoptera, paper wasps show behavior-related individual variation in adult brain structure (23)(24)(25). Paper wasp species also differ in the relative amounts of tissue invested in brain regions that process input from different sensory modalities (26).…”

mentioning

confidence: 99%

Comparative analysis of constraints and caste differences in brain investment among social paper wasps

O’Donnell

Clifford

Molina³

2011

Proc. Natl. Acad. Sci. U.S.A.

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We compared species mean data on the size of functionally distinct brain regions to test the relative rates at which investment in higher-order cognitive processing (mushroom body calyces) versus peripheral sensory processing (optic and antennal lobes) increased with increasing brain size. Subjects were eusocial paper wasps from queen and worker castes of 10 species from different genera. Relative investment in central processing tissue increased with brain size at a higher rate than peripheral structure investment, demonstrating that tissue devoted to higher-order cognitive processing is more constrained by brain size. This pattern held for raw data and for phylogenetically independent contrasts. These findings suggest that there is a minimum necessary investment in peripheral sensory processing brain tissue, with little to gain from additional investment. In contrast, increased brain size provides opportunities to invest in additional higher-order cognitive processing tissue. Reproductive castes differed within species in brain tissue investment, with higher central-to-peripheral brain tissue ratios in queens than in workers. Coupled with previous findings that paper wasp queen, but not worker, brain architecture corresponds to ecological and social variation, queen brain evolution appears to be most strongly shaped by cognitive demands, such as social interactions. These evolutionary patterns of neural investment echo findings in other animal lineages and have important implications, given that a greater investment in higherorder processing has been shown to increase the prevalence of complex and flexible behaviors across the animal kingdom.Hymenoptera | mushroom bodies | social brain | Vespidae A s brains evolve, both relative expansion of specific brain regions and general increases in absolute brain size can enable changes in animal cognitive capacity (1). Of particular note is the frequent convergent evolution of central brain regions that perform higher-order cognitive processing. Larger central processing centers are associated with enhanced capacity for learning, memory, and behavioral innovation among species (1-3). In primates, increased investment in higher-order cognitive processing structures, such as the neocortex and hippocampus, has been linked to increased cognitive performance (4), and the neocortex is five times larger in primates than in insectivores after accounting for differences in whole brain size (5). Increased hippocampal size in passerine birds has been associated with improved memory and the advent of food-storing behavior (6). Increased size and complexity of the mushroom bodies (MB), the neural centers of higher-order cognitive processing in insects, are paired with an increase in the prevalence of generalist feeding ecologies across species (7) and with social dominance status within species (8-10).Molecular evidence supports a single origin of the CNS in bilaterally symmetrical animals, including insects and vertebrates, occurring before the protostome-deuterostome split (11). ...

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Developmental and dominance‐associated differences in mushroom body structure in the paper wasp Mischocyttarus mastigophorus

Cited by 36 publications

References 43 publications

Socially induced brain development in a facultatively eusocial sweat beeMegalopta genalis(Halictidae)

Socially induced brain development in a facultatively eusocial sweat beeMegalopta genalis(Halictidae)

Neural Circuit Reconfiguration by Social Status

Comparative analysis of constraints and caste differences in brain investment among social paper wasps

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