Revisiting paternal absence: Female alloparental replacement of fathers recovers partner preference formation in female, but not male prairie voles (Microtus ochrogaster)

Abstract

In prairie voles (Microtus ochrogaster), biparental care of offspring is typical, and paternal absence in the pre‐weaning development of offspring alters biobehavioral development. We sought to determine whether this altered development is due to the absence of specific paternal qualities or a general reduction in pup‐directed care. We compared the biobehavioral development of pups reared under conditions of biparental (BPC), maternal‐plus‐alloparental (MPA; i.e., mother and older sister), and maternal only (MON) care. Older sisters provided a quantity of care equal to or greater than that of fathers. Growth rate and developmental milestones were unaffected by family composition, with the exception of earlier fur growth in MON conditions. In adulthood, we tested behaviors on an elevated plus maze, spontaneous alloparental care, and partner preference formation. We found no significant differences on the elevated plus maze and only marginal differences in alloparental care. While both female and male MON individuals showed deficits in partner preference formation, MPA females showed typical partner preference formation. However, the alloparental substitution of fathers was not sufficient for the typical development of partner preference formation in males. We conclude that paternal care plays a differentially important role in the social development of female and male prairie vole offspring.

Compositional variation in early‐life parenting structures alters oxytocin and vasopressin 1a receptor development in prairie voles (Microtus ochrogaster)

“…We hypothesise that OXTR and AVPR1a binding in regions associated with pair bonding will differ significantly according to early‐life experience. Because male prairie vole offspring reared under conditions of paternal absence (with or without alloparental substitution) did not show partner preference, 20 we predict that male MPA and MON offspring will demonstrate corresponding changes in the densities of OXTR and AVPR1a receptor distributions, which will themselves be distinct from receptor densities in BPC offspring. Because female prairie vole offspring reared under paternal absence with alloparental substitution do demonstrate partner preferences, whereas those reared without alloparental substitution do not, we predict that female prairie vole offspring will show similar patterns of OXTR and AVPR1a binding between MPA and BPC females, with a distinctly different pattern in the brains of MON females.…”

“…As more thoroughly outlined in Rogers and Bales, 20 all subjects were recruited from the third litter of multiparous prairie vole breeding pairs and reared from birth to weaning (PND20) under three social conditions (ie, family unit configurations): biparental care (BPC); maternal‐plus‐alloparental care (MPA; ie, mother and older sister); and maternal care only (MON). Developmental rearing conditions were established prior to birth on PND20 of each pair's second litter, thus between 0.5 and 2.5 days before expected parturition.…”

“…An initial study by Ahern and Young 18 demonstrated that both male and female prairie vole offspring reared under conditions of paternal absence demonstrated inhibited partner preference formation. In a subsequent study, it was found that prairie vole mothers left to rear offspring without supplemental care from a mate did not compensate for the reduction of care resultant of the father's absence, 19 a finding that has been replicated 20 (but see also the study by Kelly et al 21 in which mothers compensate for paternal absence when additional environmental challenges are applied). Accordingly, offspring reared under conditions of paternal absence also experienced a general decline in parental investment throughout their pre‐weaning development.…”

“…In a preceding study, 20 we aimed to address these apparently confounding variables (ie, quantity of care vs a particular paternal quality) by capitalising on a natural behaviour of the prairie vole: alloparental care. Quantity of care is represented as frequency and/or duration of pup‐directed care, whereas quality of care consists of the manner in which care is provided along with accompanying behavioural and physiological characteristics of the caregiver.…”

“…In the present study, we investigate the neuroendocrine consequences of variation in the parental composition in early‐life experience. Using brain tissue and blood collected from prairie voles reared in BPC, MON and MPA conditions, we aimed to determine whether the behavioural effects described by Rogers and Bales 20 are reflected in distributions of OXTR and AVPR1a in regions of interest tied to pair bonding. Furthemore, we correlate OXTR and AVPR1a distributions with our previously reported partner preference behaviours.…”