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

No abstract

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.

Animals produce a tremendous diversity of sounds for communication to perform life's basic functions, from courtship and parental care to defence and foraging. Explaining this diversity in sound production is important for understanding the ecology, evolution and behaviour of species. Here, we present a theory of acoustic communication that shows that much of the heterogeneity in animal vocal signals can be explained based on the energetic constraints of sound production. The models presented here yield quantitative predictions on key features of acoustic signals, including the frequency, power and duration of signals. Predictions are supported with data from nearly 500 diverse species (e.g. insects, fishes, reptiles, amphibians, birds and mammals). These results indicate that, for all species, acoustic communication is primarily controlled by individual metabolism such that call features vary predictably with body size and temperature. These results also provide insights regarding the common energetic and neuromuscular constraints on sound production, and the ecological and evolutionary consequences of producing these sounds.