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.

Lateral septum DREADD activation alters male prairie vole prosocial and antisocial behaviors, not partner preferences

“…The transition from being a single (un-bonded) male to a pair bonded socially monogamous male is accompanied by a suite of characteristic changes in behavior. Single males (referred to as “wanderers” in nature) are non-territorial and typically inhabit expansive home ranges that intrude into the home ranges of many other conspecifics 31 , 32 . The high rates of home range overlap appear to be indicative of indiscriminate prosocial attraction to others.…”

Re‐wiring of the bonded brain: Gene expression among pair bonded female prairie voles changes as they transition to motherhood

“…A deeper understanding of the mechanistic regulation of behavior across environmental heterogeneity can be achieved by considering how the brain responds to physical and social energetic trade‐offs, such as those associated with motherhood. 12 …”

“…A deeper understanding of the mechanistic regulation of behavior across environmental heterogeneity can be achieved by considering how the brain responds to physical and social energetic trade-offs, such as those associated with motherhood. 12 Mammalian maternal care is ubiquitous and typically consists of nursing, nurturing, and defensive behaviors driven by an underlying social bond established shortly after the birth of offspring. 13,14 Considering that mammalian offspring care is highly demanding, it can be assumed that energetic trade-offs associated with the major lifehistory transition from being nulligravid (i.e., never pregnant) to becoming a first-time mother are probably significantparticularly for species that form multiple types of social bonds.…”

“…Although this neuroplasticity necessary for the successful expression of maternal care has been relatively well outlined, 5,11 it remains unclear how such neural shifts disrupt the regulation of social behaviors that precede them. A deeper understanding of the mechanistic regulation of behavior across environmental heterogeneity can be achieved by considering how the brain responds to physical and social energetic trade‐offs, such as those associated with motherhood 12 …”

The neural circuits of monogamous behavior

“…Concerning prairie vole mating tactics, individuals that display promiscuous behavior are often labeled as “wanderers,” which generally exhibit better spatial and navigational memory and overlap several home ranges, increasing the probability of opportunistic mating. In opposition, voles labeled as “residents,” have a more monogamous strategy, often displaying territorial behavior and mate guarding for mating success ( Getz et al, 2005 ; Ophir et al, 2008b ; Phelps et al, 2017 ; Madrid et al, 2020 ; Forero and Ophir, 2022 ). Nonetheless, some individuals may not necessarily fit into these categories and, as later explained in more detail, socio-sexual circuits are subjected to modulation by several genetic and external factors that enable behavioral adaptation and, more broadly, adaptation to ecological pressures in the environment.…”