Social Structure, Body Size, and Sensory Ecology in Hymenoptera Brain Evolution

Abstract

Sociality, like the evolution of multicellularity, is considered a major transition in the evolution of biological complexity. While there is strong foundational knowledge about traits that preceed the evolution of cooperative behaviors and complex forms of social structure, relatively little is known about the role of sociality or social life in individual trait evolution, particularly as it relates to the brain. Hymenoptera (sawflies, wasps, bees, and ants) range from solitary to advanced social species, providing ample comparisons for studying sociality and neural trait evolution. However, hypotheses about sociality and brain evolution have developed separate from studies of trait evolution in insects, and the first chapter of this work suggests unification of trait evolution methods with brain evolution theory. We suggest that recent advances in counting cells and synapses, and quantifying neuron phenotypes and circuit identity be used in trait-based studies of brain evolution in social insects. In the fourth chapter we test a method for quantifying total brain cell number and show this may serve as a meaningful trait for comparisons across Hymenopteran clades. While sociality is generally cited as a major evolutionary transition, superorganisms specifically represent a unique level of biological organization because there exists developmental division of reproductive labor; In superorganisms the colony, not the individual, serves as the reproductive unit upon which natural selection acts. This means the expression of traits at the individual level are selected upon at the collective level of the colony. This form of social organization evolved independently in bees, wasps, and the ancestor to all ants. Thus, all ants are superorganisms and ants show the greatest diversity in colony structure, making them a natural experiment to test how social structure drives individual trait evolution. In the second and third chapter of this work we provide evidence that colony size, a measure of social complexity, is associated with behavioral and neural trait evolution in ants. Specifically, we show that colony size scales inversely with measures of exploratory drive and relative investment in the antennal lobes, a sensory region of the brain responsibly for processing olfactory information. Furthermore, we find that closely related Sonoran Desert species that vary in colony size show differences in sensory systems related to social cue processing, particularly those involved in assessing nestmate identity. We find the large-colony species, Dorymyrmex bicolor has a greater density and number of sensilla basiconica and more glomeruli in the T6 cluster of the antennal lobe, sensory structures and regions responsible in part for processing nestmate cuticular hydrocarbons, than the small-colony Dorymyrmex insanus. Our data suggest habitat structure is also an important drivers in brain evolution in ants, as we find that species living in deserts show less investment in visual processing regions than those living in swamp environments of temperate forests.