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

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.

Mothers, Fathers, and Others: Neural Substrates of Parental Care.

Parental care is essential for the survival of offspring in altricial mammalian species. However, in most mammals, virgin females tend to avoid or attack infants. Moreover, most males demonstrate avoidance and aggression toward infants, and have little to no involvement in parental care. What mechanisms suppress avoidance, and support approach towards pups, to promote maternal care? In biparental and cooperatively breeding species, what mechanisms allow nonmothers (i.e., fathers and alloparents) to demonstrate parental care? In this review we consider the mechanisms that subserve parental care in mothers, fathers, and others (i.e., alloparents). We emphasize recent discoveries and research trends with particular emphasis on neuroendocrinology, neuroplasticity, transcriptomics, and epigenetics. Finally, we consider outstanding questions and outline opportunities for future research.

Intergenerational transmission of the behavioral consequences of early experience in prairie voles.

We examined intergenerational and epigenetic effects of early handling manipulations on the social behavior of the prairie vole (Microtus ochrogaster), a monogamous rodent. Laboratory-born parents and their newborn pups were assigned to either a MAN0 "zero handling" manipulation (transfer with a cup during weekly cage changes) or a MAN1 "gloved handling" manipulation (transfer with a gloved hand). Previous studies from our laboratory (Bales et al., 2007) showed that MAN0 juvenile males that received this manipulation as pups are less alloparental and that MAN0 adult females that received this manipulation as pups display impaired pair-bonding. In the present study, when MAN0 and MAN1 pups reached adulthood, they were mated in three combinations (MAN1 female x MAN1 male; MAN0 female x MAN1 male; MAN1 female and MAN0 male). Once the pairs produced offspring, we examined their parental behavior towards their own pups. The offspring of these pairings (F2 generation) also were tested as juveniles for alloparental behavior. MAN1 females paired with a MAN0 male displayed higher levels of parenting behaviors. In the F2 generation, juvenile offspring with a MAN0 parent were less alloparental than were offspring from other pairs. These results suggest that early experiences can be transmitted intergenerationally.

Alloparenting experience affects future parental behavior and reproductive success in prairie voles (Microtus ochrogaster).

Various hypotheses have been proposed to explain the function of alloparental behavior in cooperatively breeding species. We examined whether alloparental experience as juveniles enhanced later parental care and reproductive success in the prairie vole (Microtus ochrogaster), a cooperatively breeding rodent. Juveniles cared for one litter of siblings (1EX), two litters of siblings (2EX) or no siblings (0EX). As adults, these individuals were mated to other 0EX, 1EX or 2EX voles, yielding seven different pair combinations, and we recorded measures of parental behaviors, reproductive success, and pup development. As juveniles, individuals caring for siblings for the first time were more alloparental; and as adults, 0EX females paired with 0EX males spent more time in the nest with their pups. Taken together, these results suggest that inexperienced animals spend more time in infant care. As parents, 1EX males spent more time licking their pups than 2EX and 0EX males. Pups with either a 1EX or 2EX parent gained weight faster than pups with 0EX parents during certain developmental periods. While inexperienced animals may spend more time in pup care, long-term benefits of alloparenting may become apparent in the display of certain, particularly important parental behaviors such as licking pups, and in faster weight gain of offspring.