Chronic social isolation enhances reproduction in the monogamous prairie vole (Microtus ochrogaster)

Abstract

Chronic stressors are generally considered to disrupt reproduction and inhibit mating. Here we test the hypothesis that a chronic stressor, specifically social isolation, can facilitate adaptive changes that enhance/accelerate reproductive effort. In general, monogamous species display high levels of prosociality, delayed sexual maturation, and greater parental investment in fewer, higher quality offspring compared with closely related polygynous species. We predicted that chronic social isolation would promote behavioral and neurochemical patterns in prairie voles associated with polygyny. Male and female prairie voles were isolated for four weeks and changes in mating behavior, alloparental care, estrogen receptor (ER) α expression and tyrosine hydroxylase (TH) expression in brain regions regulating sociosexual behavior were examined. In males, isolation accelerated copulation, increased ERα in the medial amygdala (MEApd) and bed nucleus of the stria terminalis (BSTpm), and reduced TH expression in the MEApd and BSTpm, but had no effect on alloparental behavior. In females, isolation resulted in more rapid estrus induction and reduced TH expression in the MEApd and BSTpm, but had no effect on estradiol sensitivity or ERα expression. The results support the hypothesis that ERα expression in the MEApd and BSTpm is a critical determinant of male copulatory behavior and/or mating system. The lack of change in alloparental behavior suggests that changes in prosocial behavior are selective and regulated by different mechanisms. The results also suggest that TH in the MEApd and BSTpm may play a critical role in determining mating behavior in both sexes.

Keywords: Estrogen receptor alpha; Isolation; Prairie vole; Prosocial behavior; Reproduction; Tyrosine hydroxylase.

Figure 1. Isolation accelerated copulatory behavior in male prairie voles

A. Pair-housed and isolated males showed a similar reduction in intromission latency (IL) with experience. B. Isolated males required fewer intromissions per ejaculation (I/E) than pair-housed males and this feature was stable across all three tests. C. Isolated males displayed a reduced ejaculation latency (EL); however, pair-housed males achieved similar reductions with experience. D. Isolated males displayed a shorter post-ejaculation interval (PEI); however, pair-housed males achieved similar reductions with experience. *, p < 0.05 compared to pair-housed males on the same test day. #, p < 0.05 compared to test day 1 in the same housing condition. ^, p < 0.05 compared to test day 2 in the same housing condition. For all measures N = 9 per group, except for PEI in which N = 4 (pair-housed males) and N = 7 (isolated males). Vertical lines represent SEM.

Figure 2. Isolation accelerated estrus induction following exposure to a novel male without affecting sensitivity to exogenous estradiol

A. Following pairing with a novel male, isolated females displayed sexual receptivity with a shorter latency than pair-housed females. B. There were no significant differences in sexual receptivity between groups following exogenous estradiol benzoate (EB) administration. After cessation of EB treatments, all females displayed sexual receptivity following a 72-hour cohabitation (cohab) with a male irrespective of housing condition, confirming that they were all capable of displaying sexual receptivity. *, p < 0.05 compared to pair-housed females. #, p < 0.05 compared to 2 days of EB treatment. N = 10 per group. Vertical lines represent SEM.

Figure 3. Isolation increased ERα Expression in the MEApd and BNST of males

Representative estrogen receptor α (ERα) expression in the posterodorsal medial amydala (MEApd) of pair-housed females (A), isolated females (B), pair-housed males (C) and isolated males (D). Mean ERα expression in the MEApd (E) and bed nucleus of the stria terminalis (BNST) (F) for each group. *, p < 0.05 compared to pair-housed individuals of the same sex. #, p < 0.05 compared to females in the same housing condition. N = 8 per group. Vertical lines represent SEM, ot = optic tract.

Figure 4. Isolation reduced TH expression in both males and females

Representative tyrosine hydroxylase (TH) expression in the posterodorsal medial amygdala (MEApd) of pair-housed females (A), isolated females (B), pair-housed males (C) and isolated males (D). Mean TH expression in the MEApd (E) and bed nucleus of the stria terminalis (BNST) (F) for each group. *, p < 0.05 compared to pair-housed individuals of the same sex. #, p < 0.05 compared to females in the same housing condition. N = 8 per group. Vertical lines represent SEM, ot = optic tract.