Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles (Microtus ochrogaster)

Abstract

Family relationships help shape species-typical social and emotional development, but our understanding of how this shaping occurs is still relatively limited. Prairie voles are a socially monogamous and biparental species that is well situated to complement traditional animal models, such as rats and mice, in investigating the effects of family experience. In this series of studies, we aimed to test hypotheses relating to how prairie vole families function under undisturbed, standard laboratory conditions. In the first study, we compared the parental behavior of primiparous biparental (BP) and single-mother (SM) prairie vole family units for 12 postnatal days and then tested for sex differences, behavioral coordination, and family structure effects. Under BP conditions, nest attendance was coordinated and shared equally by both sexes, while pup-directed and partner-directed licking and grooming (LG) were coordinated in a sex and social-context-dependent manner. Contrary to our expectations, SMs showed no evidence of strong parental compensation in response to the lack of the father, indicating a minimal effect of family structure on maternal behavior but a large effect on pup care. In the second study, we examined the effects of these BP and SM rearing conditions on family dynamics in the next generation and found that SM-reared adult parents exhibited lower rates of pup-directed LG in comparison to BP-reared counterparts. Situated in the context of human family dynamics and psychology, these results suggest that the study in prairie voles may help improve our understanding of family systems and how perturbations to these systems can affect adults and offspring.

FIGURE 1

Nest occupancy and coordination in Experiment 1. For each data set, the first 12 PNDs were grouped into 3-day bins for analysis and for graphing: PND1 –3 = PND Bin 1, PND4–6 = PND Bin 2, etc. (A) Parents attended to the nest at approximately equal rates regardless of sex or group, and all decreased nest attendance over time. In the BP-group, BP-mothers and BP-fathers huddled on the nest at a high rate and were alone with their pups at approximately equal rates. (B) BP-parents left the nest exposed less than expected, suggesting behavioral coordination, for all five PND bins (*p < .05, paired t-tests), and BP pups were left exposed significantly less than SM pups. Bars represent mean ± SEM. ***p < .001, NS, not significant. Huddling indicates the time when both male and female were huddling together on the nest.

FIGURE 2

Licking and grooming (LG). For each data set, the first 12 PNDs were grouped into 3-day bins for analysis and for graphing: PND1–3 = PND Bin 1, PND4–6 = PND Bin 2, etc. (A) BP-mothers LG pups at a higher rate than BP-fathers, but there was no difference between BP-mothers and SMs in pup-directed LG. (B) BP-fathers exhibit partner-directed LG at a higher rate than BP-mothers. (C) BP-fathers also show a greater rate of allogrooming than BP-mothers; BP-mothers and SMs show no difference in allogrooming. (D) BP-mothers LG pups at a higher rate than BP-fathers when both parents are attending to the nest; when attending to the pups alone, however, BP-mothers and BP-fathers LG pups at essentially the same rate. Both parents increase pup-directed LG in response being alone with the pups. (E) BP-mothers show little allogrooming, regardless of whether they are alone on the nest or accompanied; BP-fathers show significantly more allogrooming than BP-mothers when attending to the nest together, but little autogrooming when attending to the pups alone. Bars represent mean ± SEM. *** p < .001, NS, not significant.

FIGURE 3

Nursing, sustenance, and exploratory activities. For each data set, the first 12 PNDs were grouped into 3-day bins for analysis and for graphing: PND1–3 = PND Bin 1, PND4–6 = PND Bin 2, etc. (A) BP-mothers and SMs nurse pups at essentially equal rates. (B) There are also no differences in sustenance-related eating and drinking activities. (C) BP-fathers engage in a slightly higher frequency of exploratory activities (wandering, gnawing, digging, climbing, jumping) than BP-mothers; BP-mothers have a trend toward a higher rate than SMs (p = .051). Bars represent mean ± SEM. *p < .05, NS, not significant.

FIGURE 4

Rearing condition influences parenting of the next generation. (A) As a positive control for differences in adult social behavior between BP- and SM-reared animals, females from the BP/BP and SM/SM pairings were tested for partner preference. Similar to Ahern and Young (2009), as a group, BP-reared females exhibited a significant partner preference after 24 hr of cohabitation (p < .001), whereas SM-females did not (p = .107). (B) During the first six PNDs, BP/BP and SM/SM parents huddled at equal rates. (C) There were no differences in pup exposure and both groups showed nest coordination (observed exposure < expected, p < .05 for both). (D) SM-reared parents exhibited lower frequencies of pup-directed LG than BP-reared parents (p = .001), despite both groups showing a sex difference (BP: p = .006; SM: p < .001; Bonferroni adjusted p = .025). Bars represent mean ± SEM. ***p < .001, *p < .05, NS, not significant.