Emergent intra-pair sex differences and behavioral coordination in pair bonded prairie voles

Abstract

In pair bonding animals, coordinated behavior between partners is required for the pair to accomplish shared goals such as raising young. Despite this, experimental designs rarely assess the behavior of both partners within a bonded pair. Thus, we lack an understanding of the interdependent behavioral dynamics between partners that likely facilitate relationship success. To identify intra-pair behavioral correlates of pair bonding, we used socially monogamous prairie voles, a species in which females and males exhibit both overlapping and distinct pair bond behaviors. We tested both partners using social choice and non-choice tests at short- and long-term pairing timepoints. Females developed a preference for their partner more rapidly than males, with preference driven by different behaviors in each sex. Further, as bonds matured, intra-pair behavioral sex differences and coordinated behavior emerged — females consistently huddled more with their partner than males did, and partner huddle time became correlated between partners. When animals were allowed to freely interact with a partner or a novel in sequential free interaction tests, pairs spent more time interacting together than either animal did with a novel. Pair interaction was correlated with female, but not male, behavior. Via a social operant paradigm, we found that pair-bonded females, but not males, are more motivated to access and huddle with their partner than a novel vole. Together, our data indicate that as pair bonds mature, sex differences and coordinated behavior emerge, and that these intra-pair behavioral changes are likely organized and driven by the female animal.

Prolonged partner separation erodes nucleus accumbens transcriptional signatures of pair bonding in male prairie voles

“…1A). We began by pairing all study animals for 2 weeks, a duration that reliably produces mature pair bonds ( 25, 26 ). For the separation timepoints, the ability to form a new bond after loss serves as a behavioral metric of loss adaptation.…”

“…Finally, we employed tubal ligation, an approach that sterilizes females while leaving them hormonally intact. There is conflicting work suggesting that pregnancy can affect pair bonding behaviors while other studies find no difference in male partner preference between intact and ovariectomized females ( 12, 26, 76, 77 ). Regardless, our results suggest that male voles have the capacity to remember and potentially resume an affiliative relationship – pair bonded or not - despite prolonged separation and isolation.…”

“…Both opposite-sex and same-sex pairs cohabitated for 2 weeks prior to baseline partner preference tests. While mating was not confirmed, this duration of cohabitation results in pregnancy in at least 90% of intact pairs, and the pair bonds in intact animals assessed in a separate study in our lab were behaviorally indistinguishable from those in the current study (t-tests: partner preference score t (28.7) = 0.39, p = 0.70; partner huddle duration t (28.6) = -0.29, p = 0.78; novel huddle duration t (24.5) = -0.81, p = 0.42; total distance traveled t (26.3) = -1.86, p = 0.075) ( 25, 26 ). Interestingly, the presence of young at the nest also does not influence the amount of time a male remains after losing his partner in the wild ( 24 ).…”

“…For transcriptomic analysis, reads were aligned to the Ensembl prairie vole genome 1.0 and only genes with >10 reads were retained. Pairwise differential expression comparisons were done using DESeq (v1.30.1) (26) using a threshold of log2FoldChange +/- 0.30 and p-value < 0.05. Threshold-free analysis of directional regulation was accomplished using RRHO2 (v1.0) (27, 28).…”

“…We instead paired animals for two weeks prior to separation. Pair bonds strengthen and mature over this extended cohabitation period, which may contribute to the observed perseverance of partner preference for weeks after separation (25,26). In addition, our longitudinal study design resulted in re-exposure to the partner in the partner preference test performed 48 hours post-separation.…”