Proceedings of the Royal Society B: Biological Sciences, 2021
Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is... more Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is context- and experience-dependent. While laboratory studies using prairie voles have identified the involvement of several neural mechanisms, efforts to translate these findings into predictable field outcomes have been inconsistent at best. Here we test the hypothesis that inhibition of oestrogen receptor alpha (ERα) in the medial amygdala of male prairie voles would significantly increase the expression of social monogamy in the field. Prairie vole populations of equal sex ratio were established in outdoor enclosures with males bred for high levels of ERα expression and low levels of prosocial behaviour associated with social monogamy. Medial amygdala ERα expression was knocked down in half the males per population. Knockdown males displayed a greater degree of social monogamy in five of the eight behavioural indices assessed. This study demonstrates the robust nature of ERα in playin...
Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2020
This is a PDF file of an article that has undergone enhancements after acceptance, such as the ad... more This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Multiple hypotheses have been proposed to explain female mate choice and some of the mechanisms u... more Multiple hypotheses have been proposed to explain female mate choice and some of the mechanisms underlying these choices. Females prairie voles display social and mating preferences for males with longer avpr1a microsatellite alleles, which provide more paternal care and exhibit less interest in novel females compared to males with shorter avpr1a microsatellite alleles. The cues females use to differentiate among males with different avpr1a genotypes are unknown, so the objective of our study was to determine if females can discriminate among males with different avpr1a genotypes using only male olfactory cues. In a laboratory choice test, females simultaneously presented with soiled bedding from a male with short versus long avpr1a microsatellite alleles showed no significant difference in the total time spent investigating each type of bedding. Nor did a greater number of females spend more time investigating soiled bedding from males with short versus long avpr1a microsatellite alleles. These findings were not influenced by female estrous status or their own avpr1a genotype. Our results suggest olfactory cues alone are insufficient to explain a female's ability to discriminate between males with different avpr1a genotypes and future research should focus on different cues or a combination of cues.
Comparative studies aid in our understanding of specific conditions favoring the initial evolutio... more Comparative studies aid in our understanding of specific conditions favoring the initial evolution of different types of social behaviors, yet there is much unexplained intraspecific variation in the expression of social behavior that comparative studies have not yet addressed. The proximate causes of this individual variation in social behavior within a species have been examined in some species but its fitness consequences have been less frequently investigated. In this study, we quantified the fitness consequences of variation in the sociality of prairie voles (Microtus ochrogaster). We characterized sociality of female and male voles in semi-natural enclosures using an automated behavioral tracking system paired with social network analyses to quantify the degree of spatial and temporal co-occurrence of different voles. We then assessed the relationship between these metrics of sociality with individual mating success (number of different conspecifics with which an individual pr...
Abstract. Habitat features associated with nest locations can affect survival and reproductive su... more Abstract. Habitat features associated with nest locations can affect survival and reproductive success of individuals living at particular nest sites. In this study we analyzed vegetation associated with nests of prairie voles (Microtus ochrogaster), living in 0.1 ha outdoor enclosures, and found they differed from plants at randomly selected locations. Although vegetation changed during the 15 wk study, vegetation at nests tended to provide cover (taller plants) or impede predators (thornier plants). Vegetation close to nests as well as in the habitat patch (enclosure) where the nest was located predicted female survival, pup survival, and female reproductive success. The number of pups produced per nest was not related to vegetation near nests but increased with increasing thorny vegetation within enclosures. Pup survival was greater when there was more woody vegetation near nests and more dicots within enclosures. Female survival was negatively associated with plant height at nests and woody vegetation within enclosures but positively related to preferred food plants within enclosures. Our results suggest fitness consequences resulting from vegetation near nests and on a larger spatial scale surrounding the nest could influence nest site selection in prairie voles.
Alternative mating tactics appear to evolve when sexual selection is strong. Because such conditi... more Alternative mating tactics appear to evolve when sexual selection is strong. Because such conditions are usually observed in species with polygynous or polyandrous mating systems, alternative mating tactics in monogamous mating systems are seldom documented and are poorly understood. In prairie voles, Microtus ochrogaster, a species widely known for forming monogamous pair-bonds, the expression of territoriality within each sex is dimorphic, and includes non-territorial "wanderers" as well as territorial "residents." To explore the variance in fitness, measured in offspring numbers, among breeding individuals expressing these alternative mating tactics, we compiled parentage data over 3 years for male and female prairie voles from natural populations in Indiana and Kansas, USA. We found that: (1) the average fitnesses of males and females within each population were identical when adjusted by the sex ratio; (2) the variance in fitness in male and female prairie voles was comparable to that of highly polygynous species; (3) The average fitnesses of male tactics, and of female tactics, were equivalent within and among years within each location; (4) consistent with negative frequency-dependent selection acting on mating phenotypes, the between-tactic variance in fitness for male and female mating tactics decreased with increasing study duration; (5) consistent with negative assortative mating, resident males, and wanderer females produced offspring primarily in monogamous partnerships, whereas wanderer males and resident females produced offspring primarily in polygamous partnerships. Our results show that the conditions necessary for the persistence of alternative mating tactics are indistinguishable from those for phenotypically less flexible alternative mating strategies, and that alternative mating tactics can evolve in both sexes in monogamous species when fitness variance within each sex is large.
Understanding population genetic structure provides insight into the evolutionary past, present, ... more Understanding population genetic structure provides insight into the evolutionary past, present, and future of a species. In this study, we examine the rangewide population genetic structure of the prairie vole, Microtus ochrogaster (n ¼ 170). Early work divided M. ochrogaster into seven subspecies using morphological characteristics. We hypothesized polymorphic microsatellite data would reveal a genetic structure roughly congruent with the current classification of subspecies based on their geographic boundaries. We predicted populations within the geographic range of one subspecies would be genetically distinguishable from populations within the geographic range of another subspecies. Microsatellite data from the seven putative subspecies suggested~90% of molecular variation was within populations. A STRUCTURE cluster analysis had a best supported k ¼ 3, but most individuals were admixed for the three genetic clusters, and only individuals of M. o. ohionensis were distinctive in being essentially represented by a single cluster. Therefore, our molecular data showed evidence of relatively high gene flow and little geographic differentiation throughout the range of the six contiguous subspecies. The subspecific classification of M. ochrogaster should be re-evaluated using a comprehensive taxonomic approach that combines molecular, morphometric, and other data.
Laboratory studies have shown that vasopressin can influence sociosexual behavior through its act... more Laboratory studies have shown that vasopressin can influence sociosexual behavior through its action on the vasopressin 1a receptor (V1aR). There is substantial evidence that the length of a microsatellite in the gene (avpr1a) encoding for the V1aR can affect social attachment to females and paternal behavior in male prairie voles under laboratory conditions. However, previous field studies of prairie voles have failed to detect a strong effect of the length of a male’s avpr1a allele on their sociosexual behavior, but these studies are typically much shorter than the average prairie vole breeding lifespan. We examined the relationship between male avpr1a microsatellite allele length and sociosexual behavior in a natural population of prairie voles for 15 weeks, closer to the lifespan of prairie voles in nature. Contrary to predictions, we found that males with the longest avpr1a microsatellite alleles were significantly more likely to sire offspring with more than one female and to sire offspring that survived until trappable age than males with the shortest avpr1a microsatellite allele lengths. This relationship was the strongest for males with the longest tenure on the study site. As in previous field studies, we did not find evidence of a relationship between a male’s avpr1a genotype and any index of social behavior including male residency status or the number of females with which males associate. This is the first study to support the hypothesis that a male’s avpr1a genotype is a factor underlying variation in the genetic mating system of prairie voles under natural conditions.
Integrative studies of genetics, neurobiology and behaviour indicate that polymorphism in specifi... more 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.
The physiological state of an animal may have a significant impact on its reproductive success be... more The physiological state of an animal may have a significant impact on its reproductive success because individuals in good body condition are generally considered to be competitively superior to individuals in poor body condition. In this study, we tested if body condition at weaning affected survival and reproduction of prairie voles ( Microtus ochrogaster (Wagner, 1842)) living under ecologically relevant conditions at two different initial population densities. We detected no evidence that better body condition at weaning was associated with either enhanced survival or reproduction. Moreover, genetic analysis of parentage found that mating between males and females was random with respect to body condition. Results of this study indicate body condition at weaning was not a reliable predictor of future survival or reproduction in prairie voles. This may be because body condition at weaning does not accurately forecast the energetic state of prairie voles at later ages, or because ...
Females are generally expected to be selective when choosing their social and sexual partners. In... more Females are generally expected to be selective when choosing their social and sexual partners. In a previous laboratory study, female prairie voles (Microtus ochrogaster) showed significant social and sexual preferences for males with longer microsatellite DNA within the avpr1a gene encoding the vasopressin 1a receptor, as predicted if females select mates whose parental behaviour should increase female reproductive success. We tested the hypothesis that males with short versus long avpr1a microsatellite alleles exhibit differences in courtship behaviour, which could act as cues for female mate preference. The only behavioural difference we detected between males with short versus long avpr1a microsatellite alleles in mate preference trials was that males with short avpr1a microsatellite alleles sniffed the anogenital region of females more frequently during the first two days of the trials. Our results did not strongly support the hypothesis that a male's avpr1a genotype predic...
Microtus ochrogaster) and meadow (M. pennsylvanicus) voles are morphologically very similar speci... more Microtus ochrogaster) and meadow (M. pennsylvanicus) voles are morphologically very similar species of rodents that are often found sympatrically. To assess the reliability of morphological characters typically used to differentiate between these two species, we compared the concordance of species identification based on morphological characteristics with identifications based on a species-specific difference within the avpr1a gene. We found that intraspecific variation in morphological characteristics resulted in erroneous or ambiguous species identification in the field (generally #5%) as well as for preserved specimens (up to ,45%). Our data suggests that genotyping putative M. ochrogaster and M. pennsylvanicus at their avpr1a locus may be warranted for some individuals to ensure accurate species identification.
The quality of the habitat patch in which individuals reside may influence demographic processes,... more The quality of the habitat patch in which individuals reside may influence demographic processes, thus affecting social organization. We manipulated the risk of predation and food availability to test the hypothesis that high patch quality decreased the propensity to disperse, increased the likelihood of social units becoming groups, and increased overall group size in prairie voles (Microtus ochrogaster). Prairie voles are socially monogamous, at least in part of their range, and they display varied social organization within a population, including groups (containing a breeding pair and at least 1 additional adult of either sex), male-female pairs, and single females. Our results indicated that the likelihood of dispersal from high-quality patches was significantly less than from lowquality patches. Dispersers also were significantly more likely to settle in similar or higher quality patches than the ones in which they were originally released. These patterns were primarily due to the dispersal of young males. Although the proportion of social units that were groups appeared to decrease with lower patch quality, the difference in social organization among patch types was not statistically significant. The total number of founding voles and founding males per social unit residing in the highest quality patches at the end of the study were significantly greater than in the lowest quality patches. Thus, under the conditions of our experiment, patch quality affected dispersal and group size but not the tendency to form groups.
Behavioral changes that reduce the risk of predation in response to predator-derived odor cues ar... more Behavioral changes that reduce the risk of predation in response to predator-derived odor cues are widespread among mammalian taxa and have received a great deal of attention. Although voles of the genus Microtus are staples in the diet of many mammalian predators, including domestic cats (Felis catus), there are no previous studies on vole space utilization and activity levels in response to odor cues from domestic cats. Therefore, the objective of our study was to investigate responses of adult prairie voles (Microtus ochrogaster) living in semi-natural habitats to odor cues from domestic cat excreta. Contrary to expectations, neither adult males or females showed significant changes in space use or willingness to enter traps in response to cat odors. One hypothesis to explain our results are that prairie voles have not co-evolved with domestic cats long enough to respond to their odors. Other possible explanations include whether levels of odors in the environment were sufficient...
Individuals of either sex may display alternative behaviors to obtain copulations, but few studie... more Individuals of either sex may display alternative behaviors to obtain copulations, but few studies have examined the breeding patterns of females and males in populations where individuals of both sexes exhibit alternative reproductive tactics (ARTs). In prairie voles (Microtus ochrogaster), most adults are territorial, residing at a single nest site either as male–female pairs or as solitary individuals. However, some adults adopt nonterritorial, wandering tactics. During two field seasons monitoring prairie vole populations maintained in seminatural enclosures, we found evidence that females exhibiting different ARTs bred differentially with resident and wandering males. Females residing at a nest with a male bred significantly more often with a paired resident male, primarily their social partner, and significantly less often with male wanderers compared to single resident females or wandering females. These patterns were not due to chance, because paired resident females produce...
Intraspecific variation in sociosexual behavior has typically been investigated in the context of... more 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.
Proceedings of the Royal Society B: Biological Sciences, 2021
Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is... more Formation of long-term pair-bonds is a complex process, involving multiple neural circuits and is context- and experience-dependent. While laboratory studies using prairie voles have identified the involvement of several neural mechanisms, efforts to translate these findings into predictable field outcomes have been inconsistent at best. Here we test the hypothesis that inhibition of oestrogen receptor alpha (ERα) in the medial amygdala of male prairie voles would significantly increase the expression of social monogamy in the field. Prairie vole populations of equal sex ratio were established in outdoor enclosures with males bred for high levels of ERα expression and low levels of prosocial behaviour associated with social monogamy. Medial amygdala ERα expression was knocked down in half the males per population. Knockdown males displayed a greater degree of social monogamy in five of the eight behavioural indices assessed. This study demonstrates the robust nature of ERα in playin...
Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 2020
This is a PDF file of an article that has undergone enhancements after acceptance, such as the ad... more This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Multiple hypotheses have been proposed to explain female mate choice and some of the mechanisms u... more Multiple hypotheses have been proposed to explain female mate choice and some of the mechanisms underlying these choices. Females prairie voles display social and mating preferences for males with longer avpr1a microsatellite alleles, which provide more paternal care and exhibit less interest in novel females compared to males with shorter avpr1a microsatellite alleles. The cues females use to differentiate among males with different avpr1a genotypes are unknown, so the objective of our study was to determine if females can discriminate among males with different avpr1a genotypes using only male olfactory cues. In a laboratory choice test, females simultaneously presented with soiled bedding from a male with short versus long avpr1a microsatellite alleles showed no significant difference in the total time spent investigating each type of bedding. Nor did a greater number of females spend more time investigating soiled bedding from males with short versus long avpr1a microsatellite alleles. These findings were not influenced by female estrous status or their own avpr1a genotype. Our results suggest olfactory cues alone are insufficient to explain a female's ability to discriminate between males with different avpr1a genotypes and future research should focus on different cues or a combination of cues.
Comparative studies aid in our understanding of specific conditions favoring the initial evolutio... more Comparative studies aid in our understanding of specific conditions favoring the initial evolution of different types of social behaviors, yet there is much unexplained intraspecific variation in the expression of social behavior that comparative studies have not yet addressed. The proximate causes of this individual variation in social behavior within a species have been examined in some species but its fitness consequences have been less frequently investigated. In this study, we quantified the fitness consequences of variation in the sociality of prairie voles (Microtus ochrogaster). We characterized sociality of female and male voles in semi-natural enclosures using an automated behavioral tracking system paired with social network analyses to quantify the degree of spatial and temporal co-occurrence of different voles. We then assessed the relationship between these metrics of sociality with individual mating success (number of different conspecifics with which an individual pr...
Abstract. Habitat features associated with nest locations can affect survival and reproductive su... more Abstract. Habitat features associated with nest locations can affect survival and reproductive success of individuals living at particular nest sites. In this study we analyzed vegetation associated with nests of prairie voles (Microtus ochrogaster), living in 0.1 ha outdoor enclosures, and found they differed from plants at randomly selected locations. Although vegetation changed during the 15 wk study, vegetation at nests tended to provide cover (taller plants) or impede predators (thornier plants). Vegetation close to nests as well as in the habitat patch (enclosure) where the nest was located predicted female survival, pup survival, and female reproductive success. The number of pups produced per nest was not related to vegetation near nests but increased with increasing thorny vegetation within enclosures. Pup survival was greater when there was more woody vegetation near nests and more dicots within enclosures. Female survival was negatively associated with plant height at nests and woody vegetation within enclosures but positively related to preferred food plants within enclosures. Our results suggest fitness consequences resulting from vegetation near nests and on a larger spatial scale surrounding the nest could influence nest site selection in prairie voles.
Alternative mating tactics appear to evolve when sexual selection is strong. Because such conditi... more Alternative mating tactics appear to evolve when sexual selection is strong. Because such conditions are usually observed in species with polygynous or polyandrous mating systems, alternative mating tactics in monogamous mating systems are seldom documented and are poorly understood. In prairie voles, Microtus ochrogaster, a species widely known for forming monogamous pair-bonds, the expression of territoriality within each sex is dimorphic, and includes non-territorial "wanderers" as well as territorial "residents." To explore the variance in fitness, measured in offspring numbers, among breeding individuals expressing these alternative mating tactics, we compiled parentage data over 3 years for male and female prairie voles from natural populations in Indiana and Kansas, USA. We found that: (1) the average fitnesses of males and females within each population were identical when adjusted by the sex ratio; (2) the variance in fitness in male and female prairie voles was comparable to that of highly polygynous species; (3) The average fitnesses of male tactics, and of female tactics, were equivalent within and among years within each location; (4) consistent with negative frequency-dependent selection acting on mating phenotypes, the between-tactic variance in fitness for male and female mating tactics decreased with increasing study duration; (5) consistent with negative assortative mating, resident males, and wanderer females produced offspring primarily in monogamous partnerships, whereas wanderer males and resident females produced offspring primarily in polygamous partnerships. Our results show that the conditions necessary for the persistence of alternative mating tactics are indistinguishable from those for phenotypically less flexible alternative mating strategies, and that alternative mating tactics can evolve in both sexes in monogamous species when fitness variance within each sex is large.
Understanding population genetic structure provides insight into the evolutionary past, present, ... more Understanding population genetic structure provides insight into the evolutionary past, present, and future of a species. In this study, we examine the rangewide population genetic structure of the prairie vole, Microtus ochrogaster (n ¼ 170). Early work divided M. ochrogaster into seven subspecies using morphological characteristics. We hypothesized polymorphic microsatellite data would reveal a genetic structure roughly congruent with the current classification of subspecies based on their geographic boundaries. We predicted populations within the geographic range of one subspecies would be genetically distinguishable from populations within the geographic range of another subspecies. Microsatellite data from the seven putative subspecies suggested~90% of molecular variation was within populations. A STRUCTURE cluster analysis had a best supported k ¼ 3, but most individuals were admixed for the three genetic clusters, and only individuals of M. o. ohionensis were distinctive in being essentially represented by a single cluster. Therefore, our molecular data showed evidence of relatively high gene flow and little geographic differentiation throughout the range of the six contiguous subspecies. The subspecific classification of M. ochrogaster should be re-evaluated using a comprehensive taxonomic approach that combines molecular, morphometric, and other data.
Laboratory studies have shown that vasopressin can influence sociosexual behavior through its act... more Laboratory studies have shown that vasopressin can influence sociosexual behavior through its action on the vasopressin 1a receptor (V1aR). There is substantial evidence that the length of a microsatellite in the gene (avpr1a) encoding for the V1aR can affect social attachment to females and paternal behavior in male prairie voles under laboratory conditions. However, previous field studies of prairie voles have failed to detect a strong effect of the length of a male’s avpr1a allele on their sociosexual behavior, but these studies are typically much shorter than the average prairie vole breeding lifespan. We examined the relationship between male avpr1a microsatellite allele length and sociosexual behavior in a natural population of prairie voles for 15 weeks, closer to the lifespan of prairie voles in nature. Contrary to predictions, we found that males with the longest avpr1a microsatellite alleles were significantly more likely to sire offspring with more than one female and to sire offspring that survived until trappable age than males with the shortest avpr1a microsatellite allele lengths. This relationship was the strongest for males with the longest tenure on the study site. As in previous field studies, we did not find evidence of a relationship between a male’s avpr1a genotype and any index of social behavior including male residency status or the number of females with which males associate. This is the first study to support the hypothesis that a male’s avpr1a genotype is a factor underlying variation in the genetic mating system of prairie voles under natural conditions.
Integrative studies of genetics, neurobiology and behaviour indicate that polymorphism in specifi... more 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.
The physiological state of an animal may have a significant impact on its reproductive success be... more The physiological state of an animal may have a significant impact on its reproductive success because individuals in good body condition are generally considered to be competitively superior to individuals in poor body condition. In this study, we tested if body condition at weaning affected survival and reproduction of prairie voles ( Microtus ochrogaster (Wagner, 1842)) living under ecologically relevant conditions at two different initial population densities. We detected no evidence that better body condition at weaning was associated with either enhanced survival or reproduction. Moreover, genetic analysis of parentage found that mating between males and females was random with respect to body condition. Results of this study indicate body condition at weaning was not a reliable predictor of future survival or reproduction in prairie voles. This may be because body condition at weaning does not accurately forecast the energetic state of prairie voles at later ages, or because ...
Females are generally expected to be selective when choosing their social and sexual partners. In... more Females are generally expected to be selective when choosing their social and sexual partners. In a previous laboratory study, female prairie voles (Microtus ochrogaster) showed significant social and sexual preferences for males with longer microsatellite DNA within the avpr1a gene encoding the vasopressin 1a receptor, as predicted if females select mates whose parental behaviour should increase female reproductive success. We tested the hypothesis that males with short versus long avpr1a microsatellite alleles exhibit differences in courtship behaviour, which could act as cues for female mate preference. The only behavioural difference we detected between males with short versus long avpr1a microsatellite alleles in mate preference trials was that males with short avpr1a microsatellite alleles sniffed the anogenital region of females more frequently during the first two days of the trials. Our results did not strongly support the hypothesis that a male's avpr1a genotype predic...
Microtus ochrogaster) and meadow (M. pennsylvanicus) voles are morphologically very similar speci... more Microtus ochrogaster) and meadow (M. pennsylvanicus) voles are morphologically very similar species of rodents that are often found sympatrically. To assess the reliability of morphological characters typically used to differentiate between these two species, we compared the concordance of species identification based on morphological characteristics with identifications based on a species-specific difference within the avpr1a gene. We found that intraspecific variation in morphological characteristics resulted in erroneous or ambiguous species identification in the field (generally #5%) as well as for preserved specimens (up to ,45%). Our data suggests that genotyping putative M. ochrogaster and M. pennsylvanicus at their avpr1a locus may be warranted for some individuals to ensure accurate species identification.
The quality of the habitat patch in which individuals reside may influence demographic processes,... more The quality of the habitat patch in which individuals reside may influence demographic processes, thus affecting social organization. We manipulated the risk of predation and food availability to test the hypothesis that high patch quality decreased the propensity to disperse, increased the likelihood of social units becoming groups, and increased overall group size in prairie voles (Microtus ochrogaster). Prairie voles are socially monogamous, at least in part of their range, and they display varied social organization within a population, including groups (containing a breeding pair and at least 1 additional adult of either sex), male-female pairs, and single females. Our results indicated that the likelihood of dispersal from high-quality patches was significantly less than from lowquality patches. Dispersers also were significantly more likely to settle in similar or higher quality patches than the ones in which they were originally released. These patterns were primarily due to the dispersal of young males. Although the proportion of social units that were groups appeared to decrease with lower patch quality, the difference in social organization among patch types was not statistically significant. The total number of founding voles and founding males per social unit residing in the highest quality patches at the end of the study were significantly greater than in the lowest quality patches. Thus, under the conditions of our experiment, patch quality affected dispersal and group size but not the tendency to form groups.
Behavioral changes that reduce the risk of predation in response to predator-derived odor cues ar... more Behavioral changes that reduce the risk of predation in response to predator-derived odor cues are widespread among mammalian taxa and have received a great deal of attention. Although voles of the genus Microtus are staples in the diet of many mammalian predators, including domestic cats (Felis catus), there are no previous studies on vole space utilization and activity levels in response to odor cues from domestic cats. Therefore, the objective of our study was to investigate responses of adult prairie voles (Microtus ochrogaster) living in semi-natural habitats to odor cues from domestic cat excreta. Contrary to expectations, neither adult males or females showed significant changes in space use or willingness to enter traps in response to cat odors. One hypothesis to explain our results are that prairie voles have not co-evolved with domestic cats long enough to respond to their odors. Other possible explanations include whether levels of odors in the environment were sufficient...
Individuals of either sex may display alternative behaviors to obtain copulations, but few studie... more Individuals of either sex may display alternative behaviors to obtain copulations, but few studies have examined the breeding patterns of females and males in populations where individuals of both sexes exhibit alternative reproductive tactics (ARTs). In prairie voles (Microtus ochrogaster), most adults are territorial, residing at a single nest site either as male–female pairs or as solitary individuals. However, some adults adopt nonterritorial, wandering tactics. During two field seasons monitoring prairie vole populations maintained in seminatural enclosures, we found evidence that females exhibiting different ARTs bred differentially with resident and wandering males. Females residing at a nest with a male bred significantly more often with a paired resident male, primarily their social partner, and significantly less often with male wanderers compared to single resident females or wandering females. These patterns were not due to chance, because paired resident females produce...
Intraspecific variation in sociosexual behavior has typically been investigated in the context of... more 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.
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Papers by Brian Keane