Multi-Level Effects Driving Cognitive and Behavioral Variability among Prairie Voles: Insights into Reproductive Decision-Making from Biological Levels of Organization

Abstract

Behavioral phenotypes play an active role in maximizing fitness and shaping the evolutionary trajectory of species by offsetting the ecological and social environmental factors individuals experience. How these phenotypes evolve and how they are expressed is still a major question in ethology today. In recent years, an increased focus on the mechanisms that regulate the interactions between an individual and its environment has offered novel insights into the expression of alternative phenotypes. In this review, we explore the proximate mechanisms driving the expression of alternative reproductive phenotypes in the male prairie vole (Microtus ochrogaster) as one example of how the interaction of an individual's social context and internal milieu has the potential to alter behavior, cognition, and reproductive decision-making. Ultimately, integrating the physiological and psychological mechanisms of behavior advances understanding into how variation in behavior arises. We take a "levels of biological organization" approach, with prime focus placed on the level of the organism to discuss how cognitive processes emerge as traits, and how they can be studied as important mechanisms driving the expression of behavior.

Keywords: Alternative mating tactics; Animal cognition; Proximate and ultimate mechanisms; Social behavior; Social brain.

Figure 1:

Levels of biological organization spanning the population to the molecular levels. Center and right columns provide examples of level specific mechanisms and corresponding traits discussed in the article that operate at each level. These mechanisms and traits both influence and are influenced by each other at adjacent levels. Darker grey lines represent descending influences; lighter grey lines represent ascending influences.

Figure 2:

Schematic of brain structures central to the prairie vole pair bonding neural circuit, the social decision-making network, and the socio-spatial memory neural circuit. The prairie vole pair bonding neural circuit (PBNC) is drawn in blue. Dark blue represents areas exclusively part of the PBNC; light blue represents areas that are part of both the PBNC and the social decision-making network (SDMN). The socio-spatial memory neural circuit (SSMC) is drawn in green. Dark green represents areas exclusively part of the SSMC; light green represents areas that are part of both the SSMC and the SDMN. Beige areas represent nuclei that are exclusively part of the SDMN. One area, the lateral septum (red), is considered part of all three networks. Abbreviations: AH: anterior hypothalamus; ATh: anterior thalamus; BLA: basolateral amygdala; BST: bed nucleus of the stria terminalis; HPC: hippocampus; LS: lateral septum; MeA: medial amygdala; NAc: nucleus accumbens; PAG: periaqueductal grey; PFC: prefrontal cortex; POA: preoptic area of the hypothalamus; RSC: retrosplenial cortex; SHi: septohippocampal nucleus; Str: striatum; VPall: ventral pallidum; VMH: ventromedial hypothalamus; VTA: ventral tegmental area.