Effects of avpr1a length polymorphism on male social behavior and reproduction in semi‐natural populations of prairie voles (Microtus ochrogaster)

Abstract

Intraspecific variation in sociosexual behavior has typically been investigated in the context of its relationship with environmental factors, but neurogenetic factors can also influence sociosexual behavior. In laboratory studies of prairie voles (Microtus ochrogaster), length polymorphism of microsatellite DNA within the gene (avpr1a) encoding the vasopressin 1a receptor is correlated with variation in male sociosexual behavior. However, field studies of prairie voles have found the relationship between male avpr1a microsatellite allele length and sociosexual behavior to be more ambiguous, possibly because most males had alleles of intermediate length. We tested the hypothesis that avpr1a microsatellite allele length mediates male sociosexual behavior in field settings by releasing voles into field enclosures where every male possessed two avpr1a microsatellite alleles at least one standard error longer or shorter than the mean length in their population of origin. Voles from an Illinois and Kansas population were examined separately as social monogamy appears more prevalent in the Illinois population. Illinois males with long avpr1a microsatellite alleles had smaller home ranges and overlapped a greater proportion of the home range of the female that they overlapped the most. Kansas males showed the opposite pattern. Illinois, but not Kansas, males with long avpr1a microsatellite alleles sired offspring with more females and sired more litters. Our results support the hypothesis that genetic variation associated with the avpr1a gene plays a role in mediating male prairie vole sociosexual behavior in nature. However, the relationship between specific male behaviors and male avpr1a microsatellite allele length sometimes differed significantly between Kansas and Illinois voles, suggesting relationships between specific male sociosexual behaviors and polymorphism associated with the avpr1a locus are complex, possibly involving specific nucleotide sequences or other population‐specific genetic differences.

Stabilizing selection on microsatellite allele length at arginine vasopressin 1a receptor and oxytocin receptor loci

“…Several reasons may explain why studies can identify a different mode of selection on avpr1a and oxtr microsatellite loci. First, some analyses of prairie vole reproductive behaviour partitioned avpr1a alleles into short and long categories [ 9 , 17 , 18 ]; this categorical approach to analysis emphasizes the centre of the microsatellite allele length distribution rather than fitness associated with the longest and shortest alleles. Second, laboratory and field environments can target different components of reproductive success, for example with laboratory studies directed towards mate choice [ 8 ] while field experiments often include effects such as intraspecific competition and survival of offspring to weaning [ 17 , 19 ].…”

“…Fourth, some field experiments used animals that were bred in laboratory colonies (e.g. [ 9 , 16 , 19 ]) and thus reflect patterns after potential stabilizing selection on allele length during laboratory breeding; indeed, the pattern of reproductive success associated with avpr1a microsatellite allele length in male prairie voles differed between a field experiment using laboratory-derived animals [ 16 ] and an analysis of parentage in a wild population [ 17 ]. Finally, our finding that the difference in allele length can affect breeding success would not be apparent from previous analyses of vole reproduction that quantified the fitness of genotypes that differed in mean/summed allele length (e.g.…”

“…In the prairie vole Microtus ochrogaster genome, discovery of an association between the length of a microsatellite within the 5′ regulatory region of the vasopressin 1a receptor gene ( avpr1a ) and brain V1aR density [ 2 , 5 , 6 ] stimulated research into potential genetic control over mating behaviour. Hence, microsatellite allele length at avpr1a is associated with behaviours relevant to mate choice, such as home range size, memory use and partner preference [ 5 , 7 – 9 ]. Associations between allelic variation at a microsatellite locus in the 5′ regulatory region of avpr1a and gene expression, brain receptor density and/or social and sexual behaviour have been found also in chimpanzees and humans [ 10 – 15 ].…”

A generalization of the informational view of non-random mating: Models with variable population frequencies

“…On the other hand, laboratory studies demonstrate that length polymorphism of microsatellite DNA related with genes within the vasopressin-oxytocin pathway (e.g. arginine vasopressin receptor 1a, Avpr1a, and oxytocin receptor, Oxtr) are correlated with female social and sexual preferences (Castelli et al, 2011;Keane et al, 2017). In addition, a potential for assortative mating at the Oxtr locus has recently been suggested in the bank vole (Myodes glareolus) species (Watts et al, 2017).…”

Serotonin, behavior, and natural selection in New World monkeys

“…Differences between sexes in the modulation and regulation of aggression and dominance by both 5‐HT and arginine vasopressin (AVP) have been reported (Terranova et al ., ). Social monogamy [defined as the tendency in some social species to form sustained heterosexual pairs that cooperate in rearing offspring and stay in close spatial proximity (Kleiman, )] has been extensively studied in prairie voles ( Microtus ochrogaster ), a classical monogamous animal model, involving AVP (Mabry et al ., ; Keane et al ., ), oxytocin (OXT) (Ophir et al ., ; Johnson et al ., ) and dopamine (Aragona et al ., ) systems.…”