Abstract
Natural variation in early parental care may contribute to long-term changes in behavior in the offspring. Here we investigate the role of variable early care in biparental prairie voles (Microtus ochrogaster). Total amounts of parental care were initially quantified for 24 breeder pairs and pairs were ranked in relation to one another based on total contact. Consistency in key components of care suggested a trait-like quality to parental care. Based on this ranking, breeder pairs from the top (high-contact) and bottom (low-contact) quartiles were selected to produce high- and low-contact offspring to investigate adolescent behavior after varying early care. Parental care of subject offspring was again observed postnatally. Offspring of high-contact parents spent more time passively nursing and received more paternal non-huddling contact while low-contact offspring spent more time actively nursing and received more paternal huddling and pseudohuddling in the first postnatal days (PNDs). Low-contact offspring also displayed faster rates of development on a number of physical markers. Post-weaning, offspring were evaluated on anxiety-like behavior, social behavior and pre-pulse inhibition (PPI) to a tactile and an acoustic startle. High-contact offspring spent more time sniffing a juvenile and less time autogrooming. With an infant, high-contact offspring spent more time in non-huddling contact and less time autogrooming and retrieving than did low-contact offspring. Considering sexes separately, high-contact females spent more time sniffing a novel juvenile than low-contact females. High-contact males spent more time in non-huddling contact with an infant than low-contact males; while low-contact females retrieved infants more than high-contact females. In both measures of social behavior, high-contact males spent less time autogrooming than low-contact males. These results suggest a relationship between early-life care and differences in social behavior in adolescence.
Highlights
There is a large literature in rodents investigating the effects of early manipulations, such as “handling” or “maternal separation,” on offspring development (Levine, 1957; Levine and Lewis, 1959; Denenberg et al, 1962)
EARLY PARENTAL CARE OF SUBJECT OFFSPRING Based on results from the ranking of total parental care presented in Figure 1, the breeder pairs in the high- and low-contact groups were selected to produce subject offspring for use in examining behavior post-weaning
With this study we were able to demonstrate that prairie voles in established breeder pairs vary measurably in the amount and type of care delivered to offspring in the first few days postnatally and that these differences were trait-like, as they were shown to persist from one litter to the
Summary
There is a large literature in rodents investigating the effects of early manipulations, such as “handling” or “maternal separation,” on offspring development (Levine, 1957; Levine and Lewis, 1959; Denenberg et al, 1962). Handling is often considered to be an enriching experience in that it results in changes in the animal that are typically seen as adaptive (Levine et al, 1967; Fernandez-Teruel et al, 1991; Costela et al, 1993)—they may show more moderate behavioral and physiological responses to stimuli, and greater flexibility in these responses When compared to this brief early handling, repeated long-term maternal separation during the first few weeks postpartum results in adult offspring that display an increased HPA response to stressors (Plotsky and Meaney, 1993; Ladd et al, 1996, 2004; Liu et al, 2000; Veenema et al, 2006), increased anxiety-like behavior (Ogawa et al, 1994; Boccia and Pederson, 2001; Veenema et al, 2007), increased depression-like behavior (Veenema et al, 2006), and decreased maternal care of offspring (Boccia and Pederson, 2001)
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