Steven M. Phelps

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.

Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): Patterns of variation and covariation

The vasopressin V1a receptor is a gene known to be central to species differences in social behavior, including differences between the monogamous prairie vole and its promiscuous congeners. To examine how individual differences compare with species differences, we characterize variability in the expression of the vasopressin V1a receptor (V1aR) in a large sample of wild prairie voles. We find a surprising degree of intraspecific variation in V1aR binding that does not seem attributable to experimental sources. Most brain regions exhibit differences between upper and lower quartiles that are comparable to differences between species in this genus. Regions that are less variable have been implicated previously in regulating monogamous behaviors, suggesting that the lack of variation at these sites could reflect natural selection on mating system. Many brain regions covary strongly. The overall pattern of covariation reflects the developmental origins of brain regions. This finding suggests that shared mechanisms of transcriptional regulation may limit the patterns of gene expression. Such biases may shape both the efficacy of selection and the pattern of individual and species differences. Overall, our data indicate that the prairie vole would be a useful model for exploring how individual differences in gene expression influence complex social behaviors. J. Comp. Neurol. 466:564–576, 2003.

Regulation of male sexual behavior by progesterone receptor, sexual experience, and androgen

Recent studies have demonstrated that physiological doses of progesterone may facilitate the androgen-dependent display of male sexual behavior in laboratory rats and three species of lizard. We used mice with a targeted disruption of the progesterone receptor to investigate whether such interactions exist in male mice and whether they may be modified by sexual experience. We found that naive intact male progesterone receptor knockout (PRKO) mice exhibit reduced mount frequencies compared to wild-type (WT) mice. Also unlike WT mice, sexually experienced PRKO males show profound losses in many measures of sexual behavior following castration. In a second experiment, we tested whether male mice heterozygous for a null mutation at the progesterone receptor locus were responsive to testosterone and progesterone treatment. We found that heterozygous males showed a reduced response to testosterone. The data are consistent with experiments indicating that the progesterone receptor is able to facilitate male-typical sex behaviors in other species and suggest novel mechanisms underlying the interaction of androgens and experience.

An evolutionary framework for studying mechanisms of social behavior

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.

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.

Oxytocin receptor density is associated with male mating tactics and social monogamy

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. This article is part of a Special Issue entitled Oxytocin, Vasopressin, and Social Behavior.

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.

GEOGRAPHIC VARIATION IN THE SONGS OF NEOTROPICAL SINGING MICE: TESTING THE RELATIVE IMPORTANCE OF DRIFT AND LOCAL ADAPTATION

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.

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.

A Cognitive Framework for Mate Choice and Species Recognition

Mating decisions contribute to both the fitness of individuals and the emergence of evolutionary diversity, yet little is known about their cognitive architecture. We propose a simple model that describes how preferences are translated into decisions and how seemingly disparate patterns of preference can emerge from a single perceptual process. The model proposes that females use error‐prone estimates of attractiveness to select mates based on a simple decision rule: choose the most attractive available male that exceeds some minimal criterion. We test the model in the túngara frog, a well‐characterized species with an apparent dissociation between mechanisms of mate choice and species recognition. As suggested by our model results, we find that a mate attraction feature alters assessments of species status. Next, we compare female preferences in one‐choice and two‐choice tests, contexts thought to emphasize species recognition and mate choice, respectively. To do so, we use the model to generate maximum‐likelihood estimators of preference strengths from empirical data. We find that a single representation of preferences is sufficient to explain response probabilities in both contexts across a wide range of stimuli. In this species, mate choice and species recognition are accurately and simply summarized by our model. While the findings resolve long‐standing anomalies, they also illustrate how models of choice can bridge theoretical and empirical treatments of animal decisions. The data demonstrate a remarkable congruity of perceptual processes across contexts, tasks, and taxa.