Individual variation in social behavior seems ubiquitous, but we know little about how it relates to brain diversity. Among monogamous prairie voles, levels of vasopressin receptor (encoded by the gene avpr1a) in brain regions related to spatial memory predict male space use and sexual fidelity in the field. We find that trade-offs between the benefits of male fidelity and infidelity are reflected in patterns of territorial intrusion, offspring paternity, avpr1a expression, and the evolutionary fitness of alternative avpr1a alleles. DNA variation at the avpr1a locus includes polymorphisms that reliably predict the epigenetic status and neural expression of avpr1a, and patterns of DNA diversity demonstrate that avpr1a regulatory variation has been favored by selection. In prairie voles, trade-offs in the fitness consequences of social behaviors seem to promote neuronal and molecular diversity.

Although prairie voles (Microtus ochrogaster) are socially monogamous, males vary in both sexual and spatial fidelity. Most males form pairbonds, cohabit with one female, and defend territories. Wandering males, in contrast, have expansive home ranges that overlap many males and females. In the laboratory, pairing is regulated by arginine vasopressin and its predominant CNS receptor, vasopressin 1a receptor (V1aR). We investigated individual differences in forebrain V1aR expression of male prairie voles in mixed-sex seminatural enclosures. Individual differences in V1aR were compared with space use measured by radio telemetry and paternity determined with microsatellite markers. Animals engaging in extra-pair fertilizations (EPFs) as either wanderers or paired residents overlapped significantly more in same-and opposite-sex home ranges. Surprisingly, neither social fidelity measured by space use nor sexual fidelity measured by paternity was associated with V1aR expression in the ventral pallidum (VPall) or lateral septum, areas causally related to pairbond formation. In contrast, V1aR expression in the posterior cingulate/retrosplenial cortex (PCing) and laterodorsal thalamus (LDThal), areas implicated in spatial memory, strongly covaried with space use and paternity. Animals engaging in EPFs either as wanderers or paired residents exhibited low levels of LDThal and PCing V1aR expression. Individual differences in brain and behavior parallel differences between prairie voles and promiscuous congeners. The concordance among space use, paternity, and V1aR in spatial circuits suggests a common link between the mechanisms of spatial behaviors and success at EPF. The combined data demonstrate how organismal biology can inform our understanding of individual and species differences in behavioral mechanisms.posterior cingulate cortex ͉ retrosplenial cortex ͉ extra-pair fertilization ͉ monogamy ͉ neurobiology

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Despite its well-described role in female affiliation, the influence of oxytocin on male pairbonding is largely unknown. However, recent human studies indicate that this nonapeptide has a potent influence on male behaviors commonly associated with monogamy. Here we investigated the distribution of oxytocin receptors (OTR) throughout the forebrain of the socially monogamous male prairie vole (Microtus ochrogaster). Because males vary in both sexual and spatial fidelity, we explored the extent to which OTR predicted monogamous or non-monogamous patterns of space use, mating success and sexual fidelity in free-living males. We found that monogamous males expressed higher OTR density in the nucleus accumbens than non-monogamous males, a result that mirrors species differences in voles with different mating systems. OTR density in the posterior portion of the insula predicted mating success. Finally, OTR in the hippocampus and septohippocampal nucleus, which are nuclei associated with spatial memory, predicted patterns of space use and reproductive success within mating tactics. Our data highlight the importance of oxytocin receptor in neural structures associated with pairbonding and socio-spatial memory in male mating tactics. The role of memory in mating systems is often neglected, despite the fact that mating tactics impose an inherently spatial challenge for animals. Identifying mechanisms responsible for relating information about the social world with mechanisms mediating pairbonding and mating tactics is crucial to fully appreciate the suite of factors driving mating systems.

Like many adaptive behaviors, acoustic communication often requires rapid modification of motor output in response to sensory cues. However, little is known about the sensorimotor transformations that underlie such complex natural behaviors. In this study, we examine vocal exchanges in Alston’s singing mouse (Scotinomys teguina). We find that males modify singing behavior during social interactions on a subsecond time course that resembles both traditional sensorimotor tasks and conversational speech. We identify an orofacial motor cortical region and, via a series of perturbation experiments, demonstrate a hierarchical control of vocal production, with the motor cortex influencing the pacing of singing behavior on a moment-by-moment basis, enabling precise vocal interactions. These results suggest a systems-level framework for understanding the sensorimotor transformations that underlie natural social interactions.

Patterns of geographic variation in communication systems can provide insight into the processes that drive phenotypic evolution.Although work in birds, anurans, and insects demonstrates that acoustic signals are sensitive to diverse selective and stochastic forces, processes that shape variation in mammalian vocalizations are poorly understood. We quantified geographic variation in the advertisement songs of sister species of singing mice, montane rodents with a unique mode of vocal communication. We tested three hypotheses to explain spatial variation in the song of the lower altitude species, Scotinomys teguina: selection for species recognition in sympatry with congener, S. xerampelinus, acoustic adaptation to different environments, and stochastic divergence. Mice were sampled at seven sites in Costa Rica and Panamá; genetic distances were estimated from mitochondrial control region sequences, between-site differences in acoustic environment were estimated from climatic data. Acoustic, genetic and geographic distances were all highly correlated in S. teguina, suggesting that population differentiation in song is largely shaped by genetic drift. Contrasts between interspecific genetic-acoustic distances were significantly greater than expectations derived from intraspecific contrasts, indicating accelerated evolution of species-specific song. We propose that, although much intraspecific acoustic variation is effectively neutral, selection has been important in shaping species differences in song. K E Y W O R D S :Acoustic adaptation, bird song, character displacement, ecological selection, mammal, speciation.Understanding the origins of phenotypic diversity is a fundamental goal of evolutionary biology; few phenotypes are as diverse as signals used in intraspecific communication (Endler 1992;Bradbury and Vehrencamp 1998). Acoustic signals make particularly good models for signal evolution because variation is readily quantifiable, and population and species differences can accrue over short evolutionary timescales with significant impact

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Social interactions are central to most animals and have a fundamental impact upon the phenotype of an individual. Social behavior (social interactions among conspecifics) represents a central challenge to the integration of the functional and mechanistic bases of complex behavior. Traditionally, studies of proximate and ultimate elements of social behavior have been conducted by distinct groups of researchers, with little communication across perceived disciplinary boundaries. However, recent technological advances, coupled with increased recognition of the substantial variation in mechanisms underlying social interactions, should compel investigators from divergent disciplines to pursue more integrative analyses of social behavior. We propose an integrative conceptual framework intended to guide researchers towards a comprehensive understanding of the evolution and maintenance of mechanisms governing variation in sociality.The study of social behavior in the 21st century All animals interact with conspecifics at some point in their lives. Members of the same species tend to be each other's fiercest competitors and strongest allies, as evidenced by the intense cooperation and conflict that characterize many intraspecific interactions [1]. These interactions are the products of genetic, epigenetic, endocrine, and neural mechanisms that -in conjunction with environmental conditions -affect Darwinian fitness and evolve via natural selection. Building upon Aristotle's four questions, Tinbergen [2] posited that understanding behavior requires the integration of studies of mechanism and function. Only by asking questions both from a proximate perspective (i.e., focusing on causation and development) and an ultimate perspective (i.e., focusing on adaptive value and evolutionary descent) can behavior be fully understood. Social behavior in particular lends itself to such an integrative approach not only because it commands the attention of many disciplines [3] but also because even many behaviors commonly considered nonsocial often occur in a social context (e.g., mating, fighting, parental care). Social behavior is also special because the selective agents are other members of the same species, and this results in intriguing evolutionary dynamics. Nevertheless, in the intervening decades since Tinbergen's