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.

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.

FOXP2, the first gene causally linked to a human language disorder, is implicated in song acquisition, production and perception in oscine songbirds, the evolution of speech and language in hominids and the evolution of echolocation in bats. Despite the evident relevance of Foxp2 to vertebrate acoustic communication, a comprehensive description of neural expression patterns is currently lacking in mammals. Here we use immunocytochemistry to systematically describe the neural distribution of Foxp2 protein in four species of muroid rodents: Scotinomys teguina and S. xerampelinus (‘singing mice’), the deer mouse, Peromyscus maniculatus, and the lab mouse, Mus musculus. While expression patterns were generally highly conserved across brain regions, we identified subtle but consistent interspecific differences in Foxp2 distribution, most notably in the medial amygdala and nucleus accumbens, and in layer V cortex throughout the brain. Throughout the brain, Foxp2 was highly enriched in areas involved in modulation of fine motor output (striatum, mesolimbic dopamine circuit, olivocerebellar system), and in multimodal sensory processing and sensorimotor integration (thalamus, cortex). We propose a generalized model for Foxp2-modulated pathways in the adult brain including, but not limited to, fine motor production and auditory perception.

The neuropeptides arginine vasopressin (AVP) and oxytocin (OT) are key modulators of vertebrate sociality. Although some general behavioral functions of AVP and OT are broadly conserved, the detailed consequences of peptide release seem to be regulated by species-specific patterns of receptor distribution. We used autoradiography to characterize central vasopressin 1a receptor (V1aR) and OT receptor (OTR) distributions in two species of singing mice, ecologically specialized Central American rodents with a highly developed form of vocal communication. While both species exhibited high V1aR binding in the auditory thalamus (medial geniculate), binding in structures involved in vocal production (periaqueductal gray and anterior hypothalamus) was significantly higher in the more vocal species, Scotinomys teguina. In S. xerampelinus, receptor binding was significantly higher in a suite of interconnected structures implicated in social and spatial memory, including OTR in the hippocampus and medial amygdala, and V1aR in the anterior and laterodorsal thalamus. This pattern is concordant with species differences in population density and social spacing, which should favor enhanced sociospatial memory in S. xerampelinus. We propose that V1aR and OTR distributions in singing mice support an integral role for the AVP/OT system in several aspects of sociality, including vocal communication and sociospatial memory.

Aging is often perceived as a degenerative process caused by random accrual of cellular damage over time. In spite of this, age can be accurately estimated by epigenetic clocks based on DNA methylation profiles from almost any tissue of the body. Since such pan-tissue epigenetic clocks have been successfully developed for several different species, it is difficult to ignore the likelihood that a defined and shared mechanism instead, underlies the aging process. To address this, we generated 10,000 methylation arrays, each profiling up to 37,000 cytosines in highly-conserved stretches of DNA, from over 59 tissue-types derived from 128 mammalian species. From these, we identified and characterized specific cytosines, whose methylation levels change with age across mammalian species. Genes associated with these cytosines are greatly enriched in mammalian developmental processes and implicated in age-associated diseases. From the methylation profiles of these age-related cytosines, we successfully constructed three highly accurate universal mammalian clocks for eutherians, and one universal clock for marsupials. The universal clocks for eutherians are similarly accurate for estimating ages (r>0.96) of any mammalian species and tissue with a single mathematical formula. Collectively, these new observations support the notion that aging is indeed evolutionarily conserved and coupled to developmental processes across all mammalian species - a notion that was long-debated without the benefit of this new and compelling evidence.