Alexander G. Ophir

Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings

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.

Social but not genetic monogamy is associated with greater breeding success in prairie voles

Much attention has focused on distinguishing between social and genetic monogamy in avian taxa. However, surprisingly few studies have directly investigated this distinction among mammals. We investigated the genetic mating system of the prairie vole, Microtus ochrogaster, a popular model for mammalian monogamy and human attachment. We used space use patterns to define paired and single animals and assessed paternity using microsatellite loci. Prairie voles in this study engaged in significantly more extrapair fertilizations than predicted under genetic monogamy but fewer than predicted under random mating, demonstrating social but not genetic monogamy. Furthermore, we found that paired individuals were more likely to produce offspring than were unpaired individuals of either sex. This finding was true for both sexes and was attributable to differences in fertilization rates rather than litter sizes. Among mated individuals, however, faithful animals were no more successful than those that mated outside a pair. Taken together, our data demonstrate that paired prairie voles have greater breeding success than single voles, but such success is not contingent on mating exclusively with a social partner. If this species is to serve as a model for human love, our findings emphasize the need to distinguish between mammalian social attachment and sexual fidelity.

Central Vasopressin and Oxytocin Receptor Distributions in Two Species of Singing Mice

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. J. Comp. Neurol. 516:321–333, 2009.

Conservation and diversity of Foxp2 expression in muroid rodents: Functional implications

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. J. Comp. Neurol. 512:84–100, 2009.

Field tests of cis-regulatory variation at the prairie vole avpr1a locus: Association with V1aR abundance but not sexual or social fidelity

The neuropeptide vasopressin and its receptor V1aR are broadly implicated in social behavior and play a central role in several key aspects of male mating tactics in voles. In the prairie vole, a microsatellite in the cis-regulatory region of the gene encoding V1aR (avpr1a) provides a potential genetic basis for individual variation in neural phenotype and behavior; recent studies found that allele length predicts V1aR expression and male social attachment in the laboratory. Here, we explore the relationship between avpr1a microsatellite length, V1aR neural phenotype, and field measures of monogamy and fitness in male prairie voles. We found significant effects of allele length on V1aR expression in structures integral to pairbond formation. These effects did not, however, translate to differences in mating tactics or reproductive success. Together, these data suggest that, while length polymorphism in the avpr1a microsatellite influences neuronal phenotype, this variation does not contribute significantly to male reproductive success and field behavior. We propose that previously reported behavioral effects may be mediated primarily by sequence variation at this locus, for which allele length is an imperfect proxy. By combining genetic, neuronal and ecological approaches, these data provide novel insights into the contribution of genotype to natural diversity in brain and behavior.

MORPHOLOGICAL, GENETIC, AND BEHAVIORAL COMPARISONS OF TWO PRAIRIE VOLE POPULATIONS IN THE FIELD AND LABORATORY

Abstract Reports of geographic variation in behavior and morphology among prairie voles (Microtus ochrogaster) from Illinois, Kansas, and Tennessee have led to the belief that these animals vary in their mating strategies and the degree to which they are monogamous. Despite this, few studies have directly compared behavior between populations. Because the prairie vole is commonly discussed as a model for mammalian monogamy, understanding how aspects of social attachment and the mating system vary could provide further insight into the evolution of monogamy. We therefore conducted a series of experiments in the laboratory and field to assess morphological, behavioral, or genetic differences between 2 populations of this species. Voles from Illinois were morphologically similar to voles from Tennessee and exhibited comparable social and mating behavior under both laboratory and field conditions. Although genetically distinct, the 2 populations demonstrated similar levels of heterozygosity and allelic richness. Sexual dimorphism, a common indicator of mating strategy, was absent in voles from 7 widely distributed regions from across their geographic range. In the context of these results, we question the degree to which the previously described population differences are ecologically meaningful. If differences between prairie voles from Kansas and Illinois do indeed exist, examination of our data suggests that those from Kansas are atypical of prairie voles overall.

Monogamous and Promiscuous Rodent Species Exhibit Discrete Variation in the Size of the Medial Prefrontal Cortex

Limbic-associated cortical areas, such as the medial prefrontal and retrosplenial cortex (mPFC and RS, respectively), are involved in the processing of emotion, motivation, and various aspects of working memory and have been implicated in mating behavior. To determine whether the independent evolution of mating systems is associated with a convergence in cortical mechanisms, we compared the size of mPFC and RS between the monogamous prairie vole (Microtus ochrogaster) and the promiscuous meadow vole (Microtus pennsylvanicus), and between the monogamous California mouse (Peromyscus californicus) and the promiscuous white-footed mouse (Peromyscus leucopus). For both promiscuous mice and voles, the mPFC occupied a significantly larger percentage of total cortex than in the monogamous species. No significant differences were observed for the RS or overall cortex size with respect to mating system, supporting the convergent evolution of mPFC size, specifically. Individual differences in the mating behavior of male prairie voles (wandering versus pair-bonding), presumably facultative tactics, were not reflected in the relative size of the mPFC, which is likely a heritable trait. Given the importance of the mPFC for complex working memory, particularly object-place and temporal order memory, we hypothesize that the relatively greater size of the mPFC in promiscuous species reflects a greater need to remember multiple individuals and the times and locations in which they have been encountered in the home range.

Female-directed aggression predicts paternal behavior, but female prairie voles prefer affiliative males to paternal males.

In the socially monogamous prairie vole, Microtus ochrogaster, male affiliation and parental care are influenced by the neuropeptide arginine vasopressin and expression of its receptor V1aR. If parental care and adult affiliation can be considered a behavioral syndrome, females might use male affiliative behavior as a cue to choose a good father. We investigated three questions: (1) do females prefer affiliative males; (2) do males that are affiliative with females demonstrate paternal behavior with pups; and (3) is male V1aR expression related to male behavior or female preference? We evaluated paternal behavior of individual males, then offered sexually receptive females a choice between paternal and non-paternal males and measured the proportion of time each male spent engaging in affiliative behavior with the choosing female. Females showed a preference for more affiliative males, but affiliation was not predictive of paternal care. Thus females did not discriminate between paternal and non-paternal males. Perhaps surprisingly, paternal behavior was correlated with the relative amount of aggression males directed toward females. Finally, females did not discriminate between males with high or low V1aR expression and V1aR expression did not predict male affiliative behavior or parental care. These data suggest that male affiliative behavior, but not paternal care, is associated with female mate choice.