TL;DR: Differential regulation of neuropeptide receptor expression may explain species differences in the ability to form pair bonds and have intriguing implications for the neurobiology of social attachment in the authors' own species.
Abstract: A neurobiological model for pair-bond formation has emerged from studies in monogamous rodents. The neuropeptides oxytocin and vasopressin contribute to the processing of social cues necessary for individual recognition. Mesolimbic dopamine is involved in reinforcement and reward learning. Concurrent activation of neuropeptide and dopamine receptors in the reward centers of the brain during mating results in a conditioned partner preference, observed as a pair bond. Differential regulation of neuropeptide receptor expression may explain species differences in the ability to form pair bonds. These and other studies discussed here have intriguing implications for the neurobiology of social attachment in our own species.
TL;DR: This review considers the behavioral, ecological, and reproductive characteristics of mammals exhibiting monogamy, i.e., mating exclusivity, from a discussion of the life histories of selected species of monogamous primates, carnivores, rodents and ungulates.
Abstract: This review considers the behavioral, ecological, and reproductive characteristics of mammals exhibiting monogamy, i.e., mating exclusivity. From a discussion of the life histories of selected species of monogamous primates, carnivores, rodents and ungulates, several trends emerge. Two forms of monogamy occur, Type I, facultative, and Type II, obligate. The selective pressures leading to these two forms of monogamy may have been different. Facultative monogamy may result when a species exists at very low densities, with males and females being so spaced that only a single member of the opposite sex is available for mating. Obligate monogamy appears to occur when a solitary female cannot rear a litter without aid from conspecifics, but the carrying capacity of the habitat is insufficient to allow more than one female to breed simultaneously within the same home range. Within both types of monogamy, the following traits are typically seen: (1) adults show little sexual dimorphism either physically or behaviorally: (2) the adult male and female exhibit infrequent socio-sexual interactions except during the early stages of pair bond formation. Additional trends specific to mammals exhibiting obligate monogamy are: (1) the young exhibit delayed sexual maturation in the presence of the parents, and thus only the adult pair breeds; (2) the older juveniles aid in rearing young siblings; and (3) the adult male (father) aids in the rearing of young by any or all of the following: carrying, feeding, defending, and socializing offspring.
TL;DR: It is demonstrated that central AVP is both necessary and sufficient for selective aggression and partner preference formation, two critical features of pair bonding in the monogamous prairie vole.
Abstract: Monogamous social organization is characterized by selective affiliation with a partner, high levels of paternal behaviour and, in many species, intense aggression towards strangers for defence of territory, nest and mate. Although much has been written about the evolutionary causes of monogamy, little is known about the proximate mechanisms for pair bonding in monogamous mammals. The prairie vole, Microtus ochrogaster, is a monogamous, biparental rodent which exhibits long-term pair bonds characterized by selective affiliation (partner preference) and aggression. Here we describe the rapid development of both selective aggression and partner preferences following mating in the male of this species. We hypothesized that either arginine-vasopressin (AVP) or oxytocin (OT), two nine-amino-acid neuropeptides with diverse forebrain projections, could mediate the development of selective aggression and affiliation. This hypothesis was based on the following observations: (1) monogamous and polygamous voles differ specifically in the distribution of forebrain AVP and OT receptors; (2) AVP innervation in the prairie vole brain is sexually dimorphic and important for paternal behaviour; (3) central AVP pathways have been previously implicated in territorial displays and social memory; and (4) central OT pathways have been previously implicated in affiliative behaviours. We now demonstrate that central AVP is both necessary and sufficient for selective aggression and partner preference formation, two critical features of pair bonding in the monogamous prairie vole.
TL;DR: It is shown that a change in the expression of a single gene in the larger context of pre-existing genetic and neural circuits can profoundly alter social behaviour, providing a potential molecular mechanism for the rapid evolution of complex social behaviour.
Abstract: The molecular mechanisms underlying the evolution of complex behaviour are poorly understood. The mammalian genus Microtus provides an excellent model for investigating the evolution of social behaviour. Prairie voles (Microtus ochrogaster) exhibit a monogamous social structure in nature, whereas closely related meadow voles (Microtus pennsylvanicus) are solitary and polygamous. In male prairie voles, both vasopressin and dopamine act in the ventral forebrain to regulate selective affiliation between adult mates, known as pair bond formation, as assessed by partner preference in the laboratory. The vasopressin V1a receptor (V1aR) is expressed at higher levels in the ventral forebrain of monogamous than in promiscuous vole species, whereas dopamine receptor distribution is relatively conserved between species. Here we substantially increase partner preference formation in the socially promiscuous meadow vole by using viral vector V1aR gene transfer into the ventral forebrain. We show that a change in the expression of a single gene in the larger context of pre-existing genetic and neural circuits can profoundly alter social behaviour, providing a potential molecular mechanism for the rapid evolution of complex social behaviour.
TL;DR: The convergence of evidence from these animal studies makes oxytocin and vasopressin attractive candidates for the neural modulation of human social relationships as well as potential therapeutic targets for the treatment of psychiatric disorders associated with disruptions in social behavior, including autism.