Toward an integrative understanding of social behavior: new models and new opportunities

Abstract

Social interactions among conspecifics are a fundamental and adaptively significant component of the biology of numerous species. Such interactions give rise to group living as well as many of the complex forms of cooperation and conflict that occur within animal groups. Although previous conceptual models have focused on the ecological causes and fitness consequences of variation in social interactions, recent developments in endocrinology, neuroscience, and molecular genetics offer exciting opportunities to develop more integrated research programs that will facilitate new insights into the physiological causes and consequences of social variation. Here, we propose an integrative framework of social behavior that emphasizes relationships between ultimate-level function and proximate-level mechanism, thereby providing a foundation for exploring the full diversity of factors that underlie variation in social interactions, and ultimately sociality. In addition to identifying new model systems for the study of human psychopathologies, this framework provides a mechanistic basis for predicting how social behavior will change in response to environmental variation. We argue that the study of non-model organisms is essential for implementing this integrative model of social behavior because such species can be studied simultaneously in the lab and field, thereby allowing integration of rigorously controlled experimental manipulations with detailed observations of the ecological contexts in which interactions among conspecifics occur.

Keywords: behavioral genetics; behavioral neuroendocrinology; integrative models of social behavior; model systems; psychopathology.

Figure 1

An integrative framework for studying social behavior. This framework is consistent with the recursive evolutionary paradigm (Feder et al., 2000) wherein the genotype of an individual works in concert with the environment to produce a given phenotype (Box A). This has adaptive and non-adaptive consequences that determine the genotypes in the next generation (Box B). Social phenotypes may influence the environment in multiple ways, indicating a dynamic bi-directional relationship that can affect processes in both boxes. Since the environment in turn influences both proximate mechanisms and ultimate processes, it is important to study both to gain an integrative understanding of social behavior. For example, if a social behavior decreases predation threat, behavioral biologists should examine how that decrease affects the neuroendocrine mechanisms underlying that behavior in addition to how it affects the selective landscape. Moreover, because proximate mechanisms (Box A) are themselves subject to evolutionary dynamics (Box B), there is a need for research measuring selection on and heritability of that neuroendocrine mechanism rather than simply the direct effect on the social behavior. This model, while not exhaustive, provides a framework and guidance for synthetic research of sociality.