Specificity in Sociality: Mice and Prairie Voles Exhibit Different Patterns of Peer Affiliation

Abstract

Social behavior is often described as a unified concept, but highly social (group-living) species exhibit distinct social structures and may make different social decisions. Prairie voles (Microtus ochrogaster) are socially monogamous rodents that often reside in extended family groups, and exhibit robust preferences for familiar social partners (same- and opposite-sex) during extended choice tests, although short-term preferences are not known. Mice (Mus musculus) are gregarious and colonial, but in brief laboratory tests of social preference they typically prefer social novelty. This preference for novel vs. familiar peers may represent a species-specific difference in social decision-making between mice and prairie voles. However, the tests used to measure preferences in each species differ markedly in duration and degree of contact, such that the behaviors cannot be directly compared. We assessed whether social preferences for novelty or familiarity differed between mice and prairie voles of both sexes when assessed with matching protocols: the sociability/social preference test (SPT) typically used in mice (short, no direct contact), and the partner preference test (PPT) used in voles (long, direct contact). A subset of voles also underwent a PPT using barriers (long, no direct contact). In the short SPT, behavior did not differ between species. In the longer test, pronounced partner preferences emerged in prairie voles, but mice exhibited no social preferences and rarely huddled. No sex differences were evident in either test. Direct physical contact was required for partner preferences in huddling time in voles, but preference for the partner chamber was evident with or without contact. Both prairie voles and mice are social, but they exhibit important differences in the specificity and extent of their social behavior. While mice are often used to study social approach and other behaviors, voles are a more suitable species for the study of selective social relationships. Consideration of these differences will be important for studies examining the neural mechanisms supporting different kinds of peer social behavior.

Keywords: affiliation; mouse; partner preference; prairie vole; selective; sociability; social approach; social behavior.

Figure 1

Social behavior differences between mice and prairie voles across test types. (A) Schematic version of the 10 min social preference test (SPT), and (B) schematic of the 3 h partner preference test (PPT). Both tests were run with both species. (C,D) Time spent in the chamber occupied by the familiar partner, no subject, or a stranger in the SPT (C) and PPT (D). (E,F) Time spent adjacent to the cup (investigation time) or the tethered subject (huddling time) across tests. Different letters above the bars indicate groups significantly different in post hoc tests corrected for multiple comparisons.

Figure 2

Comparison of a standard PPT involving a tethered partner and stranger to a modified test using wire pencil cups over the stimulus voles. Both versions of the test lasted 3 h. (A) Time adjacent to the tethered stimulus subject or pencil cup containing the subject. (B) Time in each chamber. Chamber times were equivalent with and without direct contact, but partner preferences in time spent adjacent to the partner were only found in the test that allowed full contact. Letters indicate groups with significantly different means. (C) Species comparisons of activity, defined as the number of entries to the center chamber. Mice were significantly more active over the 3-h PPT (***p < 0.0001, t-test).