Female prairie voles show social and sexual preferences for males with longer avpr1a microsatellite alleles
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Prairie vole
Paternal care
Pair bond
Animal sexual behaviour
Social Behavior
Pair bond formation has been investigated much less than many other social behaviors, perhaps in part because traditional laboratory mice and rats do not exhibit this behavior. However, pair bonding is common among monogamous animals such as the prairie vole (Microtus ochrogaster). In this review, we discuss how the prairie vole has been used as a model system to investigate the neurobiology of pair bonding. Descriptions include neuroanatomical differences between monogamous and non-monogamous voles, as well as how manipulations of vasopressin, oxytocin, dopamine, and corticosterone systems affect pair bond formation. Also summarized are potential interactions among these systems that regulate pair bonding, and the extent of sexual dimorphism in underlying mechanisms. Pair bonding in prairie voles is an excellent model system for studying central processing of social information. Understanding the mechanisms underlying this behavior may provide important insights into human disorders associated with impaired social functioning.
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Sex differences in temporal parameters of partner preference in prairie voles (Microtus ochrogaster)
Prairie voles (Microtus ochrogaster) are monogamous rodents in which both sexes form social preferences for a familiar partner. This species exhibits many of the characteristics of monogamy, including long-term social bonds, mate guarding, and biparental care. Although the behaviors associated with the development of partner preferences are superficially similar in males and females, the present study documents sex differences in the temporal parameters of partner preferences in prairie voles. Following nonsexual cohabitation, female prairie voles formed partner preferences more quickly and these preferences lasted longer than in males. These data indicate that sex differences exist in the development and maintenance of social preferences and may reflect differences in the reproductive strategies of male and female prairie voles.
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The physiological mechanisms influencing group cohesion and social preferences are largely unstudied in prairie voles (Microtus ochrogaster). In nature, prairie vole family groups usually consist of an adult male and female breeding pair, one or more litters of their offspring, and occasionally unrelated adults. Pair bonds, defined by heterosexual preferences, develop in male and female prairie voles following cohabitation or mating. However, social preferences between members of the same sex also may be important to the maintenance of communal groups. In the present study we compared the development of social preferences for conspecific strangers of the same sex versus preferences for the opposite sex, and examined the effect of the gonadal status of the stimulus animal on initial social preference. The present study revealed that reproductively naive males, but not females, showed initial preferences for partners of the opposite sex. In both sexes preferences for the opposite sex were not influenced by the presence or absence of gonadal hormones. Heterosexual and same-sex preferences for a familiar individual formed following 24 h of nonsexual cohabitation in both males and females. Male and female same-sex preferences, however, were no longer stable when the stranger in the preference test was of the opposite sex to the experimental animal. The development of same-sex preferences may help to maintain group cohesion, but same-sex preferences formed by cohabitation do not withstand the challenge of an opposite-sex stranger.
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Arvicolinae
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Glucocorticoid levels in animals may respond to and influence the development of social attachments. This hypothesis was tested in prairie voles (Microtus ochrogaster), monogamous rodents that form long-term heterosexual pair bonds. In socially naive female prairie voles, cohabitation with an unfamiliar male resulted in a dramatic decline in serum corticosterone levels. When corticosterone levels were reduced via adrenalectomy, females developed partner preferences after 1 h of cohabitation, while sham-operated and untreated females required 3 h or more of nonsexual cohabitation to establish a partner preference. In adrenalectomized and intact females, exogenous injections of corticosterone, given prior to social exposure, prevented the development of preferences for the cohabitating male. Although corticosterone inhibited the development of partner preferences, it did not interfere with the expression of previously established social preferences. These results suggest that social stimuli can modulate adrenal activity and that adrenal activity, in turn, is capable of influencing the formation of adult social preferences in female prairie voles. The involvement of the adrenal axis in the formation of partner preferences and the subsequent development of pair bonds provides a mechanism through which environmental and social factors may influence social organization in this species.
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Prairie voles are a socially monogamous species that, after cohabitation with mating, form enduring pair bonds. The plastic mechanisms involved in this social behavior are not well-understood. Neurogenesis in adult rodents is a plastic neural process induced in specific brain areas like the olfactory bulbs (OB) and dentate gyrus (DG) of the hippocampus. However, it is unknown how cell survival is modulated by social or sexual experience in prairie voles. This study aimed to evaluate if cohabitation with mating and/or social exposure to a vole of the opposite sex increased the survival of the new cells in the main and accessory OB and DG. To identify the new cells and evaluate their survival, voles were injected with the DNA synthesis marker 5-bromo-2'-deoxyuridine (BrdU) and were randomly distributed into one of the following groups: (A) Control (C), voles that did not receive any sexual stimulation and were placed alone during the behavioral test. (B) Social exposure (SE), voles were individually placed in a cage equally divided into two compartments by an acrylic screen with small holes. One male and one female were placed in opposite compartments. (C) Social cohabitation with mating (SCM), animals mated freely. Our findings demonstrated that SCM females had increases in the number of new cells (BrdU-positive cells) in the main olfactory bulb and new mature neurons (BrdU/NeuN-positive cells) in the glomerular layer (GlL). In contrast, these new cells decrease in males in the SE and SCM conditions. In the granular cell layer (GrL), SCM females had more new cells and neurons than the SE group. In the accessory olfactory bulb, in the anterior GlL, SCM decreased the number of new cells and neurons in females. On the other hand, in the DG, SCM and SE increase the number of new cells in the suprapyramidal blade in female voles. Males from SCM express more new cells and neurons in the infrapyramidal blade compared with SE group. Comparison between male and females showed that new cells/neurons survival was sex dependent. These results suggest that social interaction and sexual behavior modulate cell survival and influence the neuronal fate in a sex-dependent manner, in the OB and DG. This study will contribute to understand neural mechanisms of complex social and pair bond behaviors in the prairie voles; supporting adult neurogenesis as a plastic mechanism potentially involved in social monogamous strategy.
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The vole genus Microtus shows extraordinary diversity in the range of social behaviors among closely related species. A few species,such as Microtus ochrogaster and pinetorum (prairie and pine vole), show monogamous social organization, while other species such as Microtus montanus and pennsylvanicus (montane and meadow vole) are solitary and promiscuous. Monogamous prairie and pine voles display selective and long-lasting pair bond formation between adult mates and biparental care of the offspring both in nature as well as in the laboratory. The neuropeptide vasopressin is involved in the neural regulation of monogamous behavior in vole species. Here, we review the past and current findings related to the vasopressin system and pair bond formation in voles. First, we review vole species differences in the distribution of vasopressin VI a receptors (ViaR) in the brain as a means to identify the role of specific brain regions in pair bond for mation. Next, we discuss pharmacological manipulations with VIaR antagonist administered into specific brain regions to determine which regions are necessary for pair bond formation. We also describe vole species differences in V1aR gene structure and function and potential contribution to species differences in VIaR brain distribution and behavior. Lastly, we discuss novel findings in which gene manipulation of brain VIaR in a promiscuous vole species confers monogamous behavior. Thoroughly understanding the genetic and neural mechanisms underlying a complex social behavior can have significant implications for understanding the evolution of diverse behavior between and within pecies.
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Abstract Over‐marking occurs when one individual deposits its scent mark on the scent mark of a conspecific. Previous studies have shown that meadow voles ( Microtus pennsylvanicus ) and prairie voles ( M. ochrogaster ) that were exposed to an over‐mark of two same‐sex conspecifics, later responded similarly to the top‐scent mark but differed in their response to the bottom‐scent mark. In the present study, we examined the responses of meadow voles and prairie voles to same‐sex and mixed‐sex over‐marks to ascertain whether their responses reflect the different tactics which males and females in promiscuous (meadow voles) and monogamous (prairie voles) species use to attract opposite‐sex conspecifics and to compete with same‐sex conspecifics. Males and females of both species spent more time investigating the mark of the top‐scent donor than that of the bottom‐scent donor of an over‐mark. Meadow voles exposed to a mixed‐sex over‐mark spent more time investigating the mark of the opposite‐sex conspecific independently of whether it was from the top‐ or bottom‐scent donor. In contrast, prairie voles spent more time investigating the mark of the opposite‐sex donor if it was from the top‐scent donor. These results suggest that: (i) over‐marking serves a competitive function; (ii) the scent marks of individuals attract multiple mates in promiscuous species such as the meadow vole; and (iii) the scent marks of individuals establish and maintain pair bonds between familiar opposite‐sex conspecifics in monogamous species such as the prairie vole.
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Prairie voles (Microtus ochrogaster (Wagner, 1842)) exhibit behavioral, morphological, and neuroendocrinological traits associated with monogamy and are considered a model system to examine the biological foundations of monogamy in mammals. We examined allelic polymorphism at microsatellite loci to assess mating exclusivity in wild prairie voles sampled in east-central Illinois and found evidence of multiple paternity in five of nine litters (56%) analyzed. Thus, a female in this socially monogamous mammal with extensive mechanisms for pair bonding does not always mate solely with its partner and raises the paradox of why some pair-bonded females mate multiply.
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Event Abstract Back to Event Uncovering the neurogenetic basis of male pair bonding behavior in the prairie vole (Microtus ochrogaster) Lisa A. McGraw1, 2* and Larry J. Young1, 2 1 Emory University, Center for Behavioral Neuroscience, United States 2 Middle East Technical University, Electrical and Electronics Engineering Department, Brain Research Laboratory, Türkiye The prairie vole (Microtus ochrogaster) is a socially monogamous rodent that unlike the majority of mammalian species, forms long-term relationships between sexual partners, or pair bonds. While the roles of the neurotransmitters arginine vasopressin (AVP) and dopamine (DA), as well as their respective receptors, in mediating and modulating male pair bonding have been demonstrated, little is known about other genes and pathways affecting this behavior. To begin to expand our understanding of the genetic architecture of male pair bonding behavior, we have begun a selective breeding regime to generate two lines of prairie voles where males display either a high propensity to form pair bonds or do not form pair bonds at all. After five generations of experimental evolution, we have already observed divergence in behaviors between lines. In parallel with the selective breeding regime, we have also begun to develop a number of genomic resources for the prairie vole including a 10x coverage BAC library, a vole-mouse cytogenetic map, a comprehensive gene catalogue and a panel of ~750 single nucleotide polymorphisms (SNPs) which are being employed to generate a first generation genetic linkage map. These genomic resources will be used to perform quantitative trait loci (QTL) mapping and comparative transcriptome profiling to identify genetic loci and gene expression patterns that contribute to differences in the selectively bred lines. Conference: 2010 South East Nerve Net (SENN) and Georgia/South Carolina Neuroscience Consortium (GASCNC) conferences, Atlanta , United States, 5 Mar - 7 Mar, 2010. Presentation Type: Poster Presentation Topic: Posters Citation: McGraw LA and Young LJ (2010). Uncovering the neurogenetic basis of male pair bonding behavior in the prairie vole (Microtus ochrogaster). Front. Neurosci. Conference Abstract: 2010 South East Nerve Net (SENN) and Georgia/South Carolina Neuroscience Consortium (GASCNC) conferences. doi: 10.3389/conf.fnins.2010.04.00063 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 17 Mar 2010; Published Online: 17 Mar 2010. * Correspondence: Lisa A McGraw, Emory University, Center for Behavioral Neuroscience, Atlanta, United States, lamcgraw@gmail.com Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Lisa A McGraw Larry J Young Google Lisa A McGraw Larry J Young Google Scholar Lisa A McGraw Larry J Young PubMed Lisa A McGraw Larry J Young Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.
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