Social Complexity and Brain Evolution: Comparative Analysis of Modularity and Integration in Ant Brain Organization

2019 ◽  
Vol 93 (1) ◽  
pp. 4-18 ◽  
Author(s):  
J. Frances Kamhi ◽  
Iulian Ilieş ◽  
James F.A. Traniello
Keyword(s):  
Social Organization ◽  
Social Information Processing ◽  
Brain Region ◽  
Life Histories ◽  
Social Complexity ◽  
Brain Size ◽  
Brain Evolution ◽  
Oecophylla Smaragdina ◽  
Brain Organization ◽  
Eusocial Insects

The behavioral demands of living in social groups have been linked to the evolution of brain size and structure, but how social organization shapes investment and connectivity within and among functionally specialized brain regions remains unclear. To understand the influence of sociality on brain evolution in ants, a premier clade of eusocial insects, we statistically analyzed patterns of brain region size covariation as a proxy for brain region connectivity. We investigated brain structure covariance in young and old workers of two formicine ants, the Australasian weaver ant Oecophylla smaragdina, a pinnacle of social complexity in insects, and its socially basic sister clade Formica subsericea. As previously identified in other ant species, we predicted that our analysis would recognize in both species an olfaction-related brain module underpinning social information processing in the brain, and a second neuroanatomical cluster involved in nonolfactory sensorimotor processes, thus reflecting conservation of compartmental connectivity. Furthermore, we hypothesized that covariance patterns would reflect divergence in social organization and life histories either within this species pair or compared to other ant species. Contrary to our predictions, our covariance analyses revealed a weakly defined visual, rather than olfactory, sensory processing cluster in both species. This pattern may be linked to the reliance on vision for worker behavioral performance outside of the nest and the correlated expansion of the optic lobes to meet navigational demands in both species. Additionally, we found that colony size and social organization, key measures of social complexity, were only weakly correlated with brain modularity in these formicine ants. Worker age also contributed to variance in brain organization, though in different ways in each species. These findings suggest that brain organization may be shaped by the divergent life histories of the two study species. We compare our findings with patterns of brain organization of other eusocial insects.

scholarly journals Social complexity influences brain investment and neural operation costs in ants

2016 ◽  
Vol 283 (1841) ◽  
pp. 20161949 ◽  
Author(s):  
J. Frances Kamhi ◽  
Wulfila Gronenberg ◽  
Simon K. A. Robson ◽  
James F. A. Traniello
Keyword(s):  
Group Size ◽  
Social Complexity ◽  
Brain Size ◽  
Collective Intelligence ◽  
Brain Evolution ◽  
Division Of Labour ◽  
Adaptive Behaviour ◽  
Oecophylla Smaragdina ◽  
Energetic Costs ◽  
Cognitive Demands

The metabolic expense of producing and operating neural tissue required for adaptive behaviour is considered a significant selective force in brain evolution. In primates, brain size correlates positively with group size, presumably owing to the greater cognitive demands of complex social relationships in large societies. Social complexity in eusocial insects is also associated with large groups, as well as collective intelligence and division of labour among sterile workers. However, superorganism phenotypes may lower cognitive demands on behaviourally specialized workers resulting in selection for decreased brain size and/or energetic costs of brain metabolism. To test this hypothesis, we compared brain investment patterns and cytochrome oxidase (COX) activity, a proxy for ATP usage, in two ant species contrasting in social organization. Socially complex Oecophylla smaragdina workers had larger brain size and relative investment in the mushroom bodies (MBs)—higher order sensory processing compartments—than the more socially basic Formica subsericea workers . Oecophylla smaragdina workers, however, had reduced COX activity in the MBs. Our results suggest that as in primates, ant group size is associated with large brain size. The elevated costs of investment in metabolically expensive brain tissue in the socially complex O. smaragdina , however, appear to be offset by decreased energetic costs.

scholarly journals Convergent mosaic brain evolution is associated with the evolution of novel electrosensory systems in teleost fishes

2021 ◽  
Author(s):  
Erika L. Schumacher ◽  
Bruce A. Carlson
Keyword(s):  
Brain Region ◽  
Brain Size ◽  
Brain Evolution ◽  
Brain Regions ◽  
Torus Semicircularis ◽  
Micro Computed Tomography ◽  
Electrosensory System ◽  
Electric Fishes ◽  
Weakly Electric ◽  
Region Size

AbstractBrain region size generally scales allometrically with total brain size, but mosaic shifts in brain region size independent of brain size have been found in several lineages and may be related to the evolution of behavioral novelty. African weakly electric fishes (Mormyroidea) evolved a mosaically enlarged cerebellum and hindbrain, yet the relationship to their behaviorally novel electrosensory system remains unclear. We addressed this by studying South American weakly electric fishes (Gymnotiformes) and weakly electric catfishes (Synodontis spp.), which evolved varying aspects of electrosensory systems, independent of mormyroids. If the mormyroid mosaic increases are related to evolving an electrosensory system, we should find similar mosaic shifts in gymnotiforms and Synodontis. Using micro-computed tomography scans, we quantified brain region scaling for multiple electrogenic, electroreceptive, and non-electrosensing species. We found mosaic increases in cerebellum in all three electrogenic lineages relative to non-electric lineages and mosaic increases in torus semicircularis and hindbrain associated with the evolution of electrogenesis and electroreceptor type. These results show that evolving novel electrosensory systems is repeatedly and independently associated with changes in the sizes of individual brain regions independent of brain size, which suggests that selection can impact structural brain composition to favor specific regions involved in novel behaviors.

scholarly journals Maternal investment, life histories and the evolution of brain structure in primates

2019 ◽  
Vol 286 (1911) ◽  
pp. 20191608 ◽  
Author(s):  
Lauren E. Powell ◽  
Robert A. Barton ◽  
Sally E. Street
Keyword(s):  
Life History ◽  
Life Histories ◽  
Brain Size ◽  
Developmental Trajectories ◽  
Adult Life ◽  
Maternal Investment ◽  
Brain Evolution ◽  
Brain Structures ◽  
Juvenile Period ◽  
Adult Lifespan

Life history is a robust correlate of relative brain size: larger-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. The cognitive buffer hypothesis (CBH) proposes an adaptive explanation for this relationship: large brains may permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing for reduced mortality and increased lifespan. By contrast, the developmental costs hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains, predicting correlations with pre-adult life-history phases. Here, we test novel predictions of the hypotheses in primates applied to the neocortex and cerebellum, two major brain structures with distinct developmental trajectories. While neocortical growth is allocated primarily to pre-natal development, the cerebellum exhibits relatively substantial post-natal growth. Consistent with the DCH, neocortical expansion is related primarily to extended gestation while cerebellar expansion to extended post-natal development, particularly the juvenile period. Contrary to the CBH, adult lifespan explains relatively little variance in the whole brain or neocortex volume once pre-adult life-history phases are accounted for. Only the cerebellum shows a relationship with lifespan after accounting for developmental periods. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental phases, and imply that environmental input during post-natal maturation may be particularly crucial for the development of cerebellar function. They also suggest that relatively extended post-natal maturation times provide a developmental mechanism for the marked expansion of the cerebellum in the apes.

Neuroanatomical and Morphological Trait Clusters in the Ant Genus Pheidole: Evidence for Modularity and Integration in Brain Structure

2015 ◽  
Vol 85 (1) ◽  
pp. 63-76 ◽  
Author(s):  
Iulian Ilieş ◽  
Mario L. Muscedere ◽  
James F.A. Traniello
Keyword(s):  
Social Information Processing ◽  
Brain Structure ◽  
Developmental Trajectories ◽  
Size Variation ◽  
Brain Evolution ◽  
Brain Structures ◽  
Interspecific Variation ◽  
Distinct Species ◽  
Brain Regions ◽  
Brain Organization

A central question in brain evolution concerns how selection has structured neuromorphological variation to generate adaptive behavior. In social insects, brain structures differ between reproductive and sterile castes, and worker behavioral specializations related to morphology, age, and ecology are associated with intra- and interspecific variation in investment in functionally different brain compartments. Workers in the hyperdiverse ant genus Pheidole are morphologically and behaviorally differentiated into minor and major subcastes that exhibit distinct species-typical patterns of brain compartment size variation. We examined integration and modularity in brain organization and its developmental patterning in three ecotypical Pheidole species by analyzing intra- and interspecific morphological and neuroanatomical covariation. Our results identified two trait clusters, the first involving olfaction and social information processing and the second composed of brain regions regulating nonolfactory sensorimotor functions. Patterns of size covariation between brain compartments within subcastes were consistent with levels of behavioral differentiation between minor and major workers. Globally, brains of mature workers were more heterogeneous than brains of newly eclosed workers, suggesting diversified developmental trajectories underscore species- and subcaste-typical brain organization. Variation in brain structure associated with the striking worker polyphenism in our sample of Pheidole appears to originate from initially differentiated brain templates that further diverge through species- and subcaste-specific processes of maturation and behavioral development.

scholarly journals Maternal investment, life histories, and the evolution of brain structure in primates

2019 ◽  
Author(s):  
Lauren E Powell ◽  
Sally E Street ◽  
Robert A Barton
Keyword(s):  
Life History ◽  
Life Histories ◽  
Brain Size ◽  
Developmental Trajectories ◽  
Maternal Investment ◽  
Brain Evolution ◽  
Juvenile Period ◽  
Adult Lifespan ◽  
Cerebellar Function

AbstractLife history is a robust correlate of relative brain size: large-brained mammals and birds have slower life histories and longer lifespans than smaller-brained species. One influential adaptive hypothesis to account for this finding is the Cognitive Buffer Hypothesis (CBH). The CBH proposes that large brains permit greater behavioural flexibility and thereby buffer the animal from unpredictable environmental challenges, allowing reduced mortality and increased lifespan. In contrast, the Developmental Costs Hypothesis (DCH) suggests that life-history correlates of brain size reflect the extension of maturational processes needed to accommodate the evolution of large brains. The hypotheses are not mutually exclusive but do make different predictions. Here we test novel predictions of the hypotheses in primates: examining how the volume of brain components with different developmental trajectories correlate with relevant phases of maternal investment, juvenile period and post-maturational lifespan. Consistent with the DCH, structures with different allocations of growth to pre-natal versus post-natal development exhibit predictably divergent correlations with the associated periods of maternal investment and pre-maturational lifespan. Contrary to the CBH, adult lifespan is uncorrelated with either whole brain size or the size of individual brain components once duration of maternal investment is accounted for. Our results substantiate and elaborate on the role of maternal investment and offspring development in brain evolution, suggest that brain components can evolve partly independently through modifications of distinct developmental mechanisms, and imply that postnatal maturational processes involving interaction with the environment may be particularly crucial for the development of cerebellar function. They also provide an explanation for why apes have relatively extended maturation times, which relate to the relative expansion of the cerebellum in this clade.

New research frameworks in the study of chimpanzee and gorilla sociality and communication

2019 ◽  
Author(s):  
Sam G. B. Roberts ◽  
Anna Roberts
Keyword(s):  
Social Evolution ◽  
Social Complexity ◽  
Brain Size ◽  
Social Systems ◽  
Strongly Correlated ◽  
The Social ◽  
Human Social Evolution ◽  
Research Frameworks ◽  
New Research ◽  
Large Groups

Group size in primates is strongly correlated with brain size, but exactly what makes larger groups more ‘socially complex’ than smaller groups is still poorly understood. Chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla) are among our closest living relatives and are excellent model species to investigate patterns of sociality and social complexity in primates, and to inform models of human social evolution. The aim of this paper is to propose new research frameworks, particularly the use of social network analysis, to examine how social structure differs in small, medium and large groups of chimpanzees and gorillas, to explore what makes larger groups more socially complex than smaller groups. Given a fission-fusion system is likely to have characterised hominins, a comparison of the social complexity involved in fission-fusion and more stable social systems is likely to provide important new insights into human social evolution

scholarly journals Polymorphism and division of labour in a socially complex ant: neuromodulation of aggression in the Australian weaver ant, Oecophylla smaragdina

2015 ◽  
Vol 282 (1811) ◽  
pp. 20150704 ◽  
Author(s):  
J. Frances Kamhi ◽  
Kelley Nunn ◽  
Simon K. A. Robson ◽  
James F. A. Traniello
Keyword(s):  
Social Systems ◽  
Division Of Labour ◽  
Oecophylla Smaragdina ◽  
Minor Worker ◽  
Task Specialization ◽  
Territorial Defence ◽  
Weaver Ant ◽  
Eusocial Insects ◽  
Worker Size ◽  
Pharmacological Manipulations

Complex social structure in eusocial insects can involve worker morphological and behavioural differentiation. Neuroanatomical variation may underscore worker division of labour, but the regulatory mechanisms of size-based task specialization in polymorphic species are unknown. The Australian weaver ant, Oecophylla smaragdina , exhibits worker polyphenism: larger major workers aggressively defend arboreal territories, whereas smaller minors nurse brood. Here, we demonstrate that octopamine (OA) modulates worker size-related aggression in O. smaragdina . We found that the brains of majors had significantly higher titres of OA than those of minors and that OA was positively and specifically correlated with the frequency of aggressive responses to non-nestmates, a key component of territorial defence. Pharmacological manipulations that effectively switched OA action in major and minor worker brains reversed levels of aggression characteristic of each worker size class. Results suggest that altering OA action is sufficient to produce differences in aggression characteristic of size-related social roles. Neuromodulators therefore may generate variation in responsiveness to task-related stimuli associated with worker size differentiation and collateral behavioural specializations, a significant component of division of labour in complex social systems.

STUDIES ON THE APOIDEA OF WESTERN NOVA SCOTIA WITH SPECIAL REFERENCE TO VISITORS TO APPLE BLOOM

1933 ◽  
Vol 9 (5) ◽  
pp. 443-457 ◽  
Author(s):  
C. E. Atwood
Keyword(s):  
Nova Scotia ◽  
Special Reference ◽  
Social Organization ◽  
Life Histories ◽  
Pupal Stage ◽  
Simple Type ◽  
Nest Construction ◽  
Wild Bees ◽  
Males And Females ◽  
Nova Scotian

This paper describes the results of studies on the wild bees of Nova Scotia, which were carried out in connection with apple pollination investigations in the Annapolis-Cornwallis Valley, Nova Scotia.The biology of the Apoidea in general is reviewed from the literature, and a list of bees taken on apple bloom is given. As the members of the genera Halictus and Andrena were found to be the most important native pollinators, the greater part of the paper is devoted to accounts of the habits and life histories of representative species.The members of the genus Andrena were found to have a simple type, such as is generally found among solitary bees. The females provision the nest and then die; the larvae develop to the pupal stage in their underground cells, then emerge as adults the following season. All Nova Scotian species studied were one-generation forms.The bees of the genus Halictus show a primitive social organization, more complex in some species than in others. The first brood consists of females only, which are apparently sterile and work at nest construction, the gathering of pollen, etc. They are followed later in the season by a brood of males and females; these females, after being fertilized, hibernate for the winter, while the males die in the fall. The hibernating habits of different species are described, and notes are given on some parasites and inquilines of the two genera.

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