The Molecular and Evolutionary Genetic Implications of Being Truly Social for the Social Insects

Abstract

Abstract The social complexity that characterizes the eusocial insects strongly affects all aspects of social insect life, including the molecular and evolutionary genetic basis of social insect traits. Quantitative genetic theory and empirical approaches have been developed over the past 60 years specifically to study the genetic implications of social interactions. Surprisingly, given the obvious biological importance of social interactions in social insects, this research tradition has been and continues to be widely overlooked throughout the social insect literature, including in recent sociogenomic studies focused on understanding the molecular underpinnings of social life. Instead, the overwhelming majority of social insect genetic research has relied on conventional genetic approaches developed for solitary organisms focused on the one-to-one association of an individual's genes to its own traits. I survey social insect studies that conclusively demonstrate the importance of indirect genetic effects (IGEs), which arise from social interactions, for social insect trait expression and evolution. I explain why these genetically based social effects are expected to be ubiquitous in social insects and I explain the relevance of the IGE framework, originally developed within quantitative genetics, for molecular genetic studies of social insect traits such as behaviour and caste. I discuss the problems of ignoring IGEs and relying solely on conventional direct genetic effect approaches. Finally, I discuss the strong potential of using the IGE approach and other more systems-level-focused approaches to complement conventional reductionist approaches in elucidating the genetic basis of social insect trait expression and evolution.