Sociobiological theory proposed that similarities between human and animal societies reflect similar evolutionary origins. We used comparative genomics to test this controversial idea by determining whether superficial behavioral similarities between humans and honey bees reflect shared molecular mechanisms. We found unique and significant enrichment for autism spectrum disorder-related genes in the neurogenomic signatures of a high-level integration center of the insect brain in bees unresponsive to two different salient social stimuli. These results demonstrate deep conservation for genes implicated in autism spectrum disorder in humans and genes associated with social responsiveness in honey bees. Comparative genomics thus provides a means to test theory on the biology of social behavior.

Abstract

E. O. Wilson proposed in Sociobiology that similarities between human and animal societies reflect common mechanistic and evolutionary roots. When introduced in 1975, this controversial hypothesis was beyond science’s ability to test. We used genomic analyses to determine whether superficial behavioral similarities in humans and the highly social honey bee reflect common molecular mechanisms. Here, we report that gene expression signatures for individual bees unresponsive to various salient social stimuli are significantly enriched for autism spectrum disorder-related genes. These signatures occur in the mushroom bodies, a high-level integration center of the insect brain. Furthermore, our finding of enrichment was unique to autism spectrum disorders; brain gene expression signatures from other honey bee behaviors do not show this enrichment, nor do datasets from other human behavioral and health conditions. These results demonstrate deep conservation for genes associated with a human social pathology and individual differences in insect social behavior, thus providing an example of how comparative genomics can be used to test sociobiological theory.