Social selectivity and social motivation in voles

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar vs. unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females vs. males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy, and demonstrates a fundamental disconnect between motivation and social selectivity in males-a distinction not detected by the partner preference test. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

Meadow voles differentiate between scents of different sources

Scent marks are an important means of transmitting information between rodents, and they can be produced from several body sources. Previous studies have shown that scents from multiple sources can convey the same information; female meadow voles, for example, have three scent sources that communicate sex. However, possessing three separate sources that convey the same information is likely costly due to the metabolic energy required to produce these signals and the increased chance that eavesdropping individuals may intercept information present in these signals. In this study, we investigated if these scent sources could communicate other information, in addition to scent donor sex, by determining if male meadow voles could distinguish scent marks taken from different sources of a single female scent donor. This was accomplished with a habituation-test method, that allowed us to compare how male meadow voles differently investigate scent from a familiar and novel source of a female scent donor. Male meadow voles could distinguish between faeces and urine scent marks of a female, but could only distinguish mouth from urine and faeces scent marks when first familiarized with mouth scent marks. Our findings suggest that mouth, urine, and faeces scent marks of female meadow voles produce both redundant and distinct information. The overlap in information between scent marks produced from separate sources may be needed to provide social context, which allows receiving individuals to accurately weigh the tradeoffs associated with responding to an olfactory cue. While this overlap in information remains costly, this cost may be minimized by the different fade-out times of scent marks from distinct body sources, which may limit the amount of time information in a scent mark is available to a time period where this information is socially relevant.

Social selectivity and social motivation in voles

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (prairie voles) or peers (meadow voles). Female prairie and meadow voles worked harder to access familiar vs. unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles also displayed strongly selective huddling preferences for familiar animals, but worked hardest to repeatedly access females vs. males, with no difference in effort by familiarity. This demonstrates a fundamental disconnect between motivation and social selectivity in males, and reveals a striking sex difference in pathways underlying social monogamy. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor genotype was associated with oxytocin receptor density, and both genotype and receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

Comparative neurotranscriptomics reveal widespread species differences associated with bonding

Background Pair bonding with a reproductive partner is rare among mammals but is an important feature of human social behavior. Decades of research on monogamous prairie voles (Microtus ochrogaster), along with comparative studies using the related non-bonding meadow vole (M. pennsylvanicus), have revealed many of the neural and molecular mechanisms necessary for pair-bond formation in that species. However, these studies have largely focused on just a few neuromodulatory systems. To test the hypothesis that neural gene expression differences underlie differential capacities to bond, we performed RNA-sequencing on tissue from three brain regions important for bonding and other social behaviors across bond-forming prairie voles and non-bonding meadow voles. We examined gene expression in the amygdala, hypothalamus, and combined ventral pallidum/nucleus accumbens in virgins and at three time points after mating to understand species differences in gene expression at baseline, in response to mating, and during bond formation. Results We first identified species and brain region as the factors most strongly associated with gene expression in our samples. Next, we found gene categories related to cell structure, translation, and metabolism that differed in expression across species in virgins, as well as categories associated with cell structure, synaptic and neuroendocrine signaling, and transcription and translation that varied among the focal regions in our study. Additionally, we identified genes that were differentially expressed across species after mating in each of our regions of interest. These include genes involved in regulating transcription, neuron structure, and synaptic plasticity. Finally, we identified modules of co-regulated genes that were strongly correlated with brain region in both species, and modules that were correlated with post-mating time points in prairie voles but not meadow voles. Conclusions These results reinforce the importance of pre-mating differences that confer the ability to form pair bonds in prairie voles but not promiscuous species such as meadow voles. Gene ontology analysis supports the hypothesis that pair-bond formation involves transcriptional regulation, and changes in neuronal structure. Together, our results expand knowledge of the genes involved in the pair bonding process and open new avenues of research in the molecular mechanisms of bond formation.

Comparative Assessment of Familiarity/Novelty Preferences in Rodents

Sociality—i.e., life in social groups—has evolved many times in rodents, and there is considerable variation in the nature of these groups. While many species-typical behaviors have been described in field settings, the use of consistent behavioral assays in the laboratory provides key data for comparisons across species. The preference for interaction with familiar or novel individuals is an important dimension of social behavior. Familiarity preference, in particular, may be associated with more closed, less flexible social groups. The dimension from selectivity to gregariousness has been used as a factor in classification of social group types. Laboratory tests of social choice range from brief (10 minutes) to extended (e.g., 3 hours). As familiarity preferences typically need long testing intervals to manifest, we used 3-hour peer partner preference tests to test for the presence of familiarity preferences in same-sex cage-mates and strangers in rats. We then conducted an aggregated analysis of familiarity preferences across multiple rodent species (adult male and female rats, mice, prairie voles, meadow voles, and female degus) tested with the same protocol. We found a high degree of consistency within species across data sets, supporting the existence of strong, species-typical familiarity preferences in prairie voles and meadow voles, and a lack of familiarity preferences in other species tested. Sociability, or total time spent near conspecifics, was unrelated to selectivity in social preference. These findings provide important background for interpreting the neurobiological mechanisms involved in social behavior in these species.

Comparative neurotranscriptomics reveal widespread species differences associated with bonding

BackgroundPair bonding with a reproductive partner is rare among mammals but is an important feature of human social behavior. Decades of research on monogamous prairie voles (Microtus ochrogaster), along with comparative studies using the related non-bonding meadow vole (M. pennsylvanicus), have revealed many of the neural and molecular mechanisms necessary for pair-bond formation in that species. However, these studies have largely focused on just a few neuromodulatory systems. To test the hypothesis that neural gene expression differences underlie differential capacities to bond, we performed RNA-sequencing on tissue from three brain regions important for bonding and other social behaviors across bond-forming prairie voles and non-bonding meadow voles. We examined gene expression in the amygdala, hypothalamus, and combined ventral pallidum/nucleus accumbens in virgins and at three time points after mating to understand species differences in gene expression at baseline, in response to mating, and during bond formation.ResultsWe first identified species and brain region as the factors most strongly associated with gene expression in our samples. Next, we found gene categories related to cell structure, translation and metabolism that differed in expression across species in virgins, as well as categories associated with cell structure, synaptic and neuroendocrine signaling, and transcription and translation that varied among the focal regions in our study. Additionally, we identified genes that were differentially expressed across species after mating in each of our regions of interest. These include genes involved in regulating transcription, neuron structure, and synaptic plasticity. Finally, we identified modules of co-regulated genes that were strongly correlated with brain region in both species, and modules that were correlated with post-mating time points in prairie voles but not meadow voles.ConclusionsThese results reinforce the importance of pre-mating differences that confer the ability to form pair bonds in prairie voles but not promiscuous species such as meadow voles. Gene ontology analysis supports the hypothesis that pair-bond formation involves transcriptional regulation, and changes in neuronal structure. Together, our results expand knowledge of the genes involved in the pair bonding process and open new avenues of research in the molecular mechanisms of bond formation.

The effect of social odour context on the amount of time male meadow voles, Microtus pennsylvanicus, self-groom

Communicational behaviours by individuals provide information for not only the intended target(s) of the signal but any non-target individual(s) that may be nearby. For terrestrial mammals a major form of communication and social information is through odours via scent marking and self-grooming. Self-grooming is a ubiquitous behaviour in mammals with the function thought to primarily be centred on personal care. But it has been found in rodents that self-grooming will occur in the presence of social odours thus potentially serving a communicative role. For example, male meadow voles (Microtus pennsylvanicus) self-groom in the presence of a female conspecific odour but not a male conspecific odour. Most studies examining self-grooming as a form of olfactory communication have used single odour donors but in a natural environment individuals will come across complex social odour situations. Therefore, we examined how male meadow voles respond to complex social odours with regards to their self-grooming behaviour. We tested the hypothesis that self-grooming can act as a form of olfactory communication and that male meadow voles will control this behaviour measured by differences in self-grooming rates based on social contexts. Male meadow voles did not show differences in the amount of time spent self-grooming to social odours that contained a female and varying number of rival males (0, 1, 3, or 5) or if the social odour contained an acquainted or novel male. Male meadow voles did self-groom more to a social odour that contained a female and a younger male compared to when the social odour contained a female and older male. Male meadow voles appear to adjust their self-grooming behaviour based on the context of the social information. This may be a strategy that can maximize that individual’s fitness by adjusting how much information is provided to potential rivals and mates.