Social selectivity and social motivation in voles

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Abstract

Selective relationships are fundamental to humans and many other animals, but relationships between mates, family members, or peers may be mediated differently. We examined connections between social reward and social selectivity, aggression, and oxytocin receptor signaling pathways in rodents that naturally form enduring, selective relationships with mates and peers (monogamous prairie voles) or peers (group-living meadow voles). Female prairie and meadow voles worked harder to access familiar vs. unfamiliar individuals, regardless of sex, and huddled extensively with familiar subjects. Male prairie voles displayed strongly selective huddling preferences for familiar animals, but only worked harder to repeatedly access females vs. males, with no difference in effort by familiarity. This reveals a striking sex difference in pathways underlying social monogamy, and demonstrates a fundamental disconnect between motivation and social selectivity in males-a distinction not detected by the partner preference test. Meadow voles exhibited social preferences but low social motivation, consistent with tolerance rather than reward supporting social groups in this species. Natural variation in oxytocin receptor binding predicted individual variation in prosocial and aggressive behaviors. These results provide a basis for understanding species, sex, and individual differences in the mechanisms underlying the role of social reward in social preference.

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Data have been deposited in a project folder on the Open Science Framework website, available at: https://osf.io/g2jf7/

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Annaliese K Beery

UC Berkeley, Berkeley, United States

For correspondence
abeery@berkeley.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1249-9182
Sarah A Lopez

Smith College, Northampton, United States

Competing interests
The authors declare that no competing interests exist.
Katrina L Blandino

Smith College, Northampton, United States

Competing interests
The authors declare that no competing interests exist.
Nicole S Lee

University of Massachusetts Amherst, Amherst, MA, United States

Competing interests
The authors declare that no competing interests exist.
Natalie S Bourdon

Smith College, Northampton, United States

Competing interests
The authors declare that no competing interests exist.

Funding

National Institutes of Health (R15MH113085)

Annaliese K Beery

The funders had no role in study design, data collection or interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was carried out in accordance with the recommendations of the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. Animals were handed according to a research protocol (ASAF 272) approved by the Institutional Care and use committee of Smith College.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.