Polymorphism at the avpr1a locus in male prairie voles correlated with genetic but not social monogamy in field populations

Abstract

Integrative studies of genetics, neurobiology and behaviour indicate that polymorphism in specific genes contributes to variation observed in some complex social behaviours. The neuropeptide arginine vasopressin plays an important role in the regulation of a variety of social behaviours, including social attachment of males to females, through its action on the vasopressin 1a receptor (V1aR). In socially monogamous prairie voles (Microtus ochrogaster), polymorphism in the length of microsatellite DNA within the regulatory region of the gene (avpr1a) encoding the V1aR predicts differences among males in neural expression of V1aRs and partner preference under laboratory conditions. However, understanding the extent to which V1aR mediates variation in prairie vole social and reproductive behaviour observed in nature requires investigating the consequences of avpr1a polymorphism and environmental influences under ecologically relevant conditions. We examined the relationship between avpr1a length polymorphism and monogamy among male prairie voles living in 0.1 ha enclosures during a time similar to their natural lifespan. We found no evidence that avpr1a genotype of males predicts variation in social monogamy measured in the field but some indices of social monogamy were affected by population density. 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. Total brain concentrations of V1aR mRNA were not associated with either male behaviour or avpr1a genotype. These data show that melding ecological field studies with neurogenetics can substantially augment our understanding of the effects of genes and environment on social behaviours.

Balancing selection maintains polymorphisms at neurogenetic loci in field experiments

“…Our field experiments show how RRAM genotypes at both Avpr1a and Oxtr affect reproductive success, in agreement with some work on the Avpr1a RRAM in the prairie vole (33,34), and provide insight into the dynamics of the Oxtr locus. The major advance in understanding the eco-evolutionary dynamics of the arginine vasopressin-oxytocin pathway is that both loci have sexand population density-specific fitness optima.…”

“…Okhovat et al (5) suggested that population density could dictate the strength and direction of selection acting on divergent Avpr1a genotypes, with population density cycles thus maintaining genetic diversity. Therefore it is relevant that we observed an interaction between population density and Avpr1a RRAM allele length in bank voles, in contrast to a field study on prairie voles in which males with shorter Avpr1a RRAM alleles enjoyed greater reproductive success irrespective of density treatment (33), likely a response to the greater competition at high population density. More generally, high population density selects for longer alleles at both loci and in both sexes of the bank vole (Fig.…”

“…That sex and population density interact to vary the fitness optima for alleles at Avpr1a and Oxtr RRAM loci provides plausible mechanisms for the maintenance of genetic diversity at these loci (33,34). Apparent functional divergence between sexes can maintain polymorphisms by generating different optimal trait values between the sexes via sexual antagonism (8,9).…”

“…Polymorphisms at the Avpr1a RRAM are associated with the reproductive success of rodents in the laboratory (32) and in some (5,33,34), but not all (17), field experiments. There have been few attempts to quantify the fitness consequences of polymorphisms at the Oxtr regulatory region, or indeed the natural levels of genetic diversity, at this locus.…”

“…Directional selection is expected to erode fitness-associated genetic diversity toward an optimum value (35), but wild rodent populations contain extensive standing genetic variation, at least at Avpr1a. For example, wild prairie vole populations have more than 15 alleles at the Avpr1a RRAM locus (15,17,33,34), and Okhovat et al (5) identified an excess of intermediate-frequency alleles at nucleotide sites within Avpr1a as compared with putative neutral loci. A combination of putative fitness effects and extensive genetic and phenotypic diversity at Avpr1a and Oxtr are compelling evidence for the action of balancing selection.…”