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The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (microtus ochrogaster).

ABSTRACT: Early social attachments lie at the heart of emotional and social development in many mammals, including humans. In nature, monogamous prairie voles (Microtus ochrogaster) experience considerable natural variation in early social attachment opportunities due to differences in family structure [e.g., single-mothers (SM), solitary breeding pairs, and communal groups]. We exploited some of this natural variation in family structure to examine the influence of early social environment on the development of adult social behavior. First, we characterized the parental care received by pups reared biparentally (BP) or by SM in the laboratory. Second, we examined whether BP- and SM-reared offspring differed in adult nurturing, bonding, and emotional behaviors. Finally, we investigated the effects of rearing condition on neuropeptide systems that regulate adult social behavior [oxytocin (OT), vasopressin, and corticotropin-releasing factor, (CRF)]. Observations revealed that SM-reared pups were exposed more frequently (P < 0.01), licked and groomed less (P < 0.01), and matured more slowly (P < 0.01) than BP-reared pups. In adulthood, there were striking socio-behavioral differences: SM-reared females showed low spontaneous, pup-directed alloparental behavior (P < 0.01) and both males and females from the SM-reared condition showed delayed partner preference formation. While rearing did not impact neuropeptide receptor densities in the ventral forebrain as we predicted, SM-reared animals, particularly females, had increased OT content (P < 0.01) and greater dorsal raphe CRF2 densities (P < 0.05) and both measures correlated with licking and grooming experienced during the first 10 days of life. These results suggest that naturalistic variation in social rearing conditions can introduce diversity into adult nurturing and attachment behaviors.

SUBMITTER: Ahern TH

PROVIDER: S-EPMC2742665 | biostudies-literature | 2009

REPOSITORIES: biostudies-literature

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The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (microtus ochrogaster).

Ahern Todd H TH Young Larry J LJ

Frontiers in behavioral neuroscience 20090827

Early social attachments lie at the heart of emotional and social development in many mammals, including humans. In nature, monogamous prairie voles (Microtus ochrogaster) experience considerable natural variation in early social attachment opportunities due to differences in family structure [e.g., single-mothers (SM), solitary breeding pairs, and communal groups]. We exploited some of this natural variation in family structure to examine the influence of early social environment on the develop ...[more]

PMID: 19753327

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Project description:In many socially monogamous species, individuals form long-term pair bonds and males mate guard females. Such behavior is thought to help secure intra-pair fertilizations, the result of intra-pair copulations (IPCs), and ensure paternity. However, socially monogamous males are also often opportunistic and seek additional mating opportunities with other females, leaving their partner unguarded. The success associated with a male's decision to seek more mates over guarding his partner might be impacted by the activity of other males, specifically the proportion of other males leaving their territories to seek extra-pair copulations (EPCs). The amount of EPC-seeking males can impact the likelihood of a given male encountering an unguarded paired female, but also of being cuckolded (losing IPCs). It remains unclear under which conditions it is optimal to stay and guard or seek EPCs. Using field data from socially monogamous prairie voles (Microtus ochrogaster) to generate parameters, we used optimal performance modeling (Monte Carlo simulations) to ask when is it most reproductively advantageous for a bonded male to seek EPCs, despite the risk of losing IPCs. We defined three types of males: exclusive mating bonded males (true residents), non-exclusive mating bonded residents (roving residents), and unpaired males (wanderers). We first modeled the success of an individual male living in a context that incorporated only true and roving residents. We next added wandering males to this model. Finally, we considered the effects of including wandering males and unpaired females in our model. For all contexts, we found that as EPC-seeking in the population increases, the potential reproductive benefit for seeking EPCs increasingly outpaces the rate of cuckolding. In other words, we observe a shift in optimal strategy from true residents to rovers among paired males. Our models also demonstrate that reproductive fitness is likely to remain constant, despite the shift toward obtaining success via EPCs over IPCs. Our results show the dynamic nature of reproductive decision-making, and demonstrate that alternative reproductive decisions yield subtle but important differences despite appearing as balanced strategies.

Project description:The prairie vole (Microtus ochrogaster) is a premier animal model for understanding the genetic and neurological basis of social behaviors. Unlike other biomedical models, prairie voles display a rich repertoire of social behaviors including the formation of long-term pair bonds and biparental care. However, due to a lack of genomic resources for this species, studies have been limited to a handful of candidate genes. To provide a substrate for future development of genomic resources for this unique model organism, we report the construction and characterization of a bacterial artificial chromosome (BAC) library from a single male prairie vole and a prairie vole-mouse (Mus musculus) comparative cytogenetic map.We constructed a prairie vole BAC library (CHORI-232) consisting of 194,267 recombinant clones with an average insert size of 139 kb. Hybridization-based screening of the gridded library at 19 loci established that the library has an average depth of coverage of approximately 10x. To obtain a small-scale sampling of the prairie vole genome, we generated 3884 BAC end-sequences totaling approximately 2.8 Mb. One-third of these BAC-end sequences could be mapped to unique locations in the mouse genome, thereby anchoring 1003 prairie vole BAC clones to an orthologous position in the mouse genome. Fluorescence in situ hybridization (FISH) mapping of 62 prairie vole clones with BAC-end sequences mapping to orthologous positions in the mouse genome was used to develop a first-generation genome-wide prairie vole-mouse comparative cytogenetic map. While conserved synteny was observed between this pair of rodent genomes, rearrangements between the prairie vole and mouse genomes were detected, including a minimum of five inversions and 16 inter-chromosomal rearrangements.The construction of the prairie vole BAC library and the vole-mouse comparative cytogenetic map represent the first genome-wide modern genomic resources developed for this species. The BAC library will support future genomic, genetic and molecular characterization of this genome and species, and the isolation of clones of high interest to the vole research community will allow for immediate characterization of the regulatory and coding sequences of genes known to play important roles in social behaviors. In addition, these resources provide an excellent platform for future higher resolution cytogenetic mapping and full genome sequencing.

Dataset Information

The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (microtus ochrogaster).

Publications

The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (microtus ochrogaster).

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