Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster)

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.

Intergenerational transmission of sociality: the role of parents in shaping social behavior in monogamous and non-monogamous species

“…This may cause them to actively maintain social contact with conspecifics, an idea that is supported by their decreased rates of dispersal from the natal nest discussed previously. These high contact offspring display decreased anxiety-like behavior in an elevated plus maze as adolescents (Perkeybile et al, 2013;Arias del Razo and Bales, 2016), and adult male offspring also initiate aggression with a novel animal less often than their low contact counterparts (Perkeybile and Bales, 2015b). This again indicates that increased early parental care programs the offspring to engage in more pro-social behavior later in life.…”

“…This variation results in offspring which experience differences not only in the amount but also in the type of parental care. Distribution of offspring care between the mother and father differs between high contact and low contact pairs, where fathers of low contact pairs spend a greater amount of time caring for offspring than do fathers of high contact pairs, even while total combined care time from both the mother and father is still decreased in low contact pairs (Perkeybile et al, 2013). Our lab has been working to understand the consequences these natural differences in parental care have on a number of offspring outcomes such as social behavior, stress responsiveness, neuropeptide systems and sensory system organization.…”

“…Cross-fostering indicates that alloparenting in voles is transmitted non-genomically, with the parental behavior experienced by the offspring predicting the alloparental behavior shown (Perkeybile et al, 2015). There are additional group differences in other social behaviors, including an increase in affiliative behavior toward a novel juvenile in high contact offspring during the early adolescent period (Perkeybile et al, 2013). While alloparenting of unrelated offspring is sensitive to the early rearing environment, it is not yet known how parental care of own offspring is impacted.…”

“…Prairie voles show significant amounts of variation in several social behaviors in laboratory and field studies, including alloparenting De Vries, 2000, 2001;Roberts et al, 1998), mating strategies Ophir et al, 2008) and parental care (Perkeybile et al, 2013;Wang and Novak, 1992). In the field, dispersal from the natal nest is also variable, with up to 70-75% of offspring remaining in the natal nest and serving as non-reproductive alloparents to future offspring of the breeding pair (Getz and McGuire, 1997;McGuire et al, 1993).…”

“…In many regards, variation in early parenting has very similar consequences for offspring behavior as does early handling or early neuropeptide exposure, and these outcomes are often sex-dependent. High contact male offspring engage in a greater amount of alloparental care of infants (Perkeybile et al, 2013;Arias del Razo and Bales, 2016). Cross-fostering indicates that alloparenting in voles is transmitted non-genomically, with the parental behavior experienced by the offspring predicting the alloparental behavior shown (Perkeybile et al, 2015).…”