Synthesis of Tinbergen’s four questions and the future of sociogenomics

Abstract

It has been 55 years since Nikolaas Tinbergen formalized the field of ethology by identifying four types of inquiry that address the “how” and “why” of animal behavior from both a contemporary and historical perspective. This framework has been particularly useful in exploring eusocial behavior among insects, due to integration across levels of analysis and timescales of influence. Although the former has proceeded quite deliberately, the latter has received less attention. Here, I synthesize recent findings regarding the mechanisms, ontogeny, evolution, and function of eusociality in ants, bees, and wasps. This synthesis reveals that there has been rapid gain of knowledge regarding the genetic underpinnings of eusocial behavior, but an understanding of the fitness consequences of these molecular mechanisms lags behind. Similarly, it has become clear that maternal or sibling effects on development are major drivers of caste-related behavior, but the mechanisms that produce these effects are largely unknown. Developmental caste determination and caste-biasing require sensitivities to social cues, but how this plasticity evolved from solitary ancestors is unknown. Understanding the origins of developmental plasticity is necessary to understand how plasticity shapes the evolutionary trajectory of social traits. Likewise, the influence of social function on molecular evolution has been studied within a robust theoretical framework; however, these studies will benefit from an understanding of how ancestral conditions promote the acquisition of social function in the first place. Future studies that span both levels of analysis and timescales of influence will further advance the integrative field of ethology that Tinbergen envisioned.