Researchers have begun to identify specific genes that appear to influence social behavior in animals. While these studies have made a substantial contribution towards understanding the link between genes and behavior, they have been conducted almost exclusively on captive animals in the laboratory. Since laboratory settings can be highly artificial, these studies may not reflect what happens in the real world. Therefore, the next logical step in studying the relationship between genes and social behavior is to investigate how genetic differences among individuals effect social behavior in a species' natural environment. Prairie voles (Microtus ochrogaster) are rodents that typically form behavioral attachments to one opposite-sex partner during their lifetime (social monogamy). Although the prairie vole is a popular laboratory model for studying monogamy, in nature this species varies in the degree of social monogamy exhibited among populations as well as within populations. A recent study suggests that variation in social bonding among prairie voles in nature might be due in part to genetic differences in a single gene that codes for a receptor localized in the brain that binds a specific chemical messenger called vasopressin. In laboratory tests, males with longer versions of this gene spent significantly more time in contact with their female partner compared to an unfamiliar female, relative to males with shorter forms of this gene. These data are intriguing because they suggest that size differences in the gene coding for the vasopressin receptor causally affect social attachment and possibly mate fidelity among male prairie voles. This study will be the first to examine the real world consequences on social attachment of genetic variation in the gene coding for the vasopressin receptor in male prairie voles. Detecting a significant relationship between size differences in the gene coding for the vasopressin receptor and social/genetic indices of monogamy would be strong evidence that this gene influences social behavior in male prairie voles under ecologically relevant conditions. Vasopressin is known to be involved in the regulation of complex social behaviors in mammals such as social recognition, aggression and affiliation. Thus, prairie voles may be an excellent animal model for studying social attachment among other mammals, including humans. In particular, prairie voles can provide a tractable model to investigate how genetic changes may influence the activity of specific areas in the brain, which may impact the display of social behaviors, such as the formation of social attachments or bonds. The proposed research will also require extensive contributions from undergraduate and graduate students, providing opportunities for them to gain first-hand experience conducting scientific research.

Project Report

In many animal species, individuals exhibit variation in social behavior. This variation in behavior has generally been attributed to varying environmental conditions, but researchers have begun to identify and investigate specific genes that appear to influence social behavior as well. While studies of behavioral genetics have made a substantial contribution towards understanding the link between genes and behavior, they have been conducted almost exclusively on captive animals in the laboratory. Laboratory settings typically lack many of the factors present in the animal’s natural environment. Therefore, it is crucial to study behavior in more realistic surroundings to understand the extent to which environmental factors versus genetic differences among individuals explain the variation in social behavior observed in a species’ natural environment. Prairie voles (Microtus ochrogaster) are rodents that typically form behavioral attachments to an opposite-sex partner (social monogamy) and are an excellent animal model for studying the basis of social attachment in mammals, including humans. Recent research suggests that variation in social bonding among prairie voles might be due in part to genetic differences in a single gene (avpr1a) that codes for a receptor (V1aR) in the brain. This receptor binds a specific chemical messenger called vasopressin. Vasopressin is involved in the regulation of complex social behaviors in mammals such as social recognition, aggression and affiliation. In laboratory tests, males with longer versions of the avpr1a gene show more V1aR receptors in specific brain regions and greater social preference for their female partner compared to an unfamiliar female, relative to males with shorter forms of this gene. These data are intriguing because they suggest that size differences in the gene coding for the vasopressin receptor may be contributing to variation in social monogamy observed among prairie voles in nature. Our results from laboratory preference trials showed that female prairie voles displayed significant social and sexual preferences for males that possessed longer avpr1a alleles. In a two year study of prairie vole populations living in semi-natural 0.1 ha outdoor enclosures, we detected considerable variation among individuals in social monogamy as well in their tendency to mate with only their social partner (genetic monogamy). We found no evidence that the avpr1a genotype of males influenced variation in social monogamy in these populations but some indices of social monogamy were correlated with population density. On the other hand, genetic parentage data indicated that a male’s avpr1a genotype significantly influenced the number of females with which he sired offspring and the total number of offspring sired. These findings are consistent with the hypothesis that a male’s avpr1a genotype may be contributing to variation in genetic monogamy in natural populations. Our research also was to first to investigate if male avpr1a genotypes were correlated with measures of social or genetic monogamy in natural populations of prairie voles. Data collected over three breeding seasons indicated that prairie voles from a natural population in Kansas exhibited greater social and genetic monogamy than individuals from a natural population in Indiana. However, we found no evidence of a relationship between the size of the avpr1a gene in a male and any of our correlates of either social (e.g., home range overlap between a male and female) or genetic monogamy in either population. Variation in social and genetic monogamy was correlated with population density and the distribution of vegetation. These results suggest that factors other than male avpr1a genotype appear to be more important determinants of social and genetic monogamy in nature and illustrate the importance of investigating if findings from studies of captive animals are biologically important in natural populations. In addition to the scientific goals of our research, we also endeavored to train students in an integrated approach to studying animal behavior through the incorporation of genetics and neurobiology into our research on prairie vole social behavior. Funding from this grant supported, at least in part, three graduate students, one high school teacher, and 45 undergraduate students that participated in some component of this research project. For most of these undergraduate students, this was their first experience conducting scientific research outside a classroom setting. Students learned methods of conducting ecological field research (e.g., live-trapping; radio-tracking), molecular research (e.g., DNA extraction and amplification), and data analysis. Some of the undergraduate students that were more deeply involved in the project have had the opportunity to present the results of their research at local, regional or national meetings (10 students) and have been co-authors on publications in peer-reviewed journals (6 students). We think that their experiences while participating in our research will prove to be valuable assets for those undergraduate students pursuing careers in science.

Agency
National Science Foundation (NSF)
Institute
Division of Integrative Organismal Systems (IOS)
Application #
0614015
Program Officer
Michelle M. Elekonich
Project Start
Project End
Budget Start
2007-03-15
Budget End
2012-02-29
Support Year
Fiscal Year
2006
Total Cost
$413,873
Indirect Cost
Name
Miami University Oxford
Department
Type
DUNS #
City
Oxford
State
OH
Country
United States
Zip Code
45056