Social complexity influences brain investment and neural operation costs in ants

Abstract

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.

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

“…We statistically examined modularity and integration across worker subcastes and age groups in two phylogenetically related but socially divergent formicine ant sister clades to determine the influence of colony level complexity on brain organization [Kamhi et al, 2016[Kamhi et al, , 2017. Our analysis uncovered moderate levels of modularity and limited integration, with high correlations indicative of divergent patterns of investment between species, subcaste, and age groups, rather than developmental codependence among brain regions.…”

“…Our present results indicate that brain region volumes of F. subsericea workers show higher correlations than those of O. smaragdina, providing partial support for the above hypothesis. Additionally, covariance analyses performed on relative levels of cytochrome oxidase, a marker of metabolic activity, in brain regions of mature O. smaragdina and F. subsericea workers [original data from Kamhi et al, 2016] revealed the same trend (online suppl. Table S2), providing additional molecular support for the notion that social complexity is associated with brain modularity.…”

“…Although the significance of brain size in relation to modularity or integration is not well understood and comparative studies are limited, complexity in eusocial insects appears to correlate with either a reduction [Gronenberg and Riveros, 2009;Riveros et al, 2012] or an increase [Kamhi et al, 2016] in brain size. As brains become larger, the average connection density may decrease due to greater metabolic costs and space limitations associated with maintaining axons at the same density as in a smaller brain [Striedter, 2005;Chittka and Niven, 2009].…”

“…The elaboration of the mushroom bodies (MB), a higher-order processing region in insects, has been hypothesized to correspond to a greater dependence on visual processing rather than social complexity [Farris and Schulmeister, 2011;Farris, 2016]. Nonetheless, division of labor among polymorphic workers may result in either an increase or a decrease in brain size, and differential investment in brain regions may correspond to cognitive requirements of behaviorally specialized workers [Gronenberg and Riveros, 2009;Muscedere and Traniello, 2012;Riveros et al, 2012;Kamhi et al, 2016;Gordon et al, 2017]. The varied cognitive challenges associated with group living in insects may lead to complex relationships between social organization and neural adaptation [Lihoreau et al, 2012].…”

“…The varied cognitive challenges associated with group living in insects may lead to complex relationships between social organization and neural adaptation [Lihoreau et al, 2012]. Patterns of brain scaling in eusocial insects therefore may be driven in opposing directions by distinctive aspects of insect social organization [Gronenberg and Riveros, 2009;Riveros et al, 2012;Amador-Vargas et al, 2015;Feinerman and Traniello, 2015;O'Donnell et al, 2015;Kamhi et al, 2016].…”