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.

Keywords: affiliation; alloparenting; natural variation; parental care; social behavior.

Figure 1

Breeder ranking data. Total pup-directed contact time (in seconds) for high-, medium-, and low-contact breeder pairs. Means and standard errors are also presented for specific parental behaviors found to be significantly different between high- and low-contact breeder pairs during early parental care observations of subject offspring (data presented in Figure 2).

Figure 2

Early parental care data. (A) High-contact offspring received more total parental care than did low-contact offspring [F_{(1, 228)} = 3.69, adjusted p = 0.05]. There was an increased amount of total maternal care directed toward high-contact compared to low-contact offspring [F_{(1, 228)} = 9.51, adjusted p = 0.002]. (B) Fathers of low-contact offspring spent more time huddling [F_{(1, 228)} = 5.47, adjusted p = 0.04] and pseudohuddling [F_{(1, 228)} = 19.87, adjusted p = 0.0004] over pups, while high-contact fathers spent more time in non-huddling contact [F_{(1, 228)} = 30.24, adjusted p = 0.0004]. Low-contact fathers also spent more time nest building [F_{(1, 228)} = 6.71, adjusted p = 0.02]. (C) Mothers of high-contact offspring spent more time in passive nursing postures [lateral nursing F_{(1, 228)} = 29.17, adjusted p = 0.0006] and neutral nursing [F_{(1, 228)} = 32.06, adjusted p = 0.0006] while low-contact offspring received more active nursing [F_{(1, 228)} = 8.45, adjusted p = 0.01]. (D) Mothers of low-contact offspring spent more time nest building [F_{(1, 228)} = 5.88, adjusted p = 0.04]. ^*p < 0.05, ^**p < 0.01, ^***p < 0.001.

Figure 3

Developmental marker data. (A) Low-contact offspring had higher weights on PND1 [F_{(1, 59)} = 36.17, p < 0.0001] and at weaning [F_{(1, 63)} = 10.07, p = 0.0023] compared to high-contact offspring. (B) Low-contact offspring were observed at younger ages with eyes open [F_{(1, 55)} = 31.85, p < 0.0001], leaving the nest [F_{(1, 55)} = 35.76, p < 0.0001], and eating solid food [F_{(1, 51)} = 43.70, p < 0.0001] than were high-contact offspring. ^*p < 0.01, ^**p < 0.0001.

Figure 4

Juvenile affiliation data. (A) High-contact offspring spent more time sniffing the novel juvenile [F_{(1, 70)} = 5.51, p = 0.02] while low-contact offspring spent more time autogrooming [F_{(1, 70)} = 4.35, p = 0.04]. (B) When split by sex, low-contact males spent more time autogrooming [F_{(1, 31)} = 5.65, p = 0.02]. High-contact females spent more time sniffing [F_{(1, 25)} = 7.46, p = 0.009] while low-contact females tended to lunge more [F_{(1, 25)} = 3.50, p = 0.06]. ^*p < 0.05, ^**p < 0.01, ⁺p = 0.06.

Figure 5

Alloparental care data. (A) High-contact offspring spent more time in non-huddling contact with pups [F_{(1, 66)} = 5.31, p = 0.02]. Low-contact offspring spent more time autogrooming [F_{(1, 66)} = 5.21, p = 0.02] and retrieved pups more [F_{(1, 66)} = 6.59, p = 0.01]. (B) High-contact males spent more time in non-huddling contact with infants [F_{(1, 29)} = 4.07, p = 0.05] while low-contact males tended to spend more time autogrooming [F_{(1, 29)} = 3.47, p = 0.07]. Low-contact females retrieved infants more often [F_{(1, 24)} = 5.01, p = 0.03]. ^*p < 0.05, ^**p = 0.01, ⁺p = 0.07.

Figure 6

Prepulse inhibition of tactile startle stimuli. (A) Low-contact offspring showed a greater potentiation of a tactile startle during tactile Trials 3 [F_{(1, 468)} = 3.85, p = 0.05] and 5 [F_{(1, 468)} = 6.45, p = 0.01] compared to high-contact offspring. (B) Low-contact males potentiated their startle response more than high-contact males during tactile Trial 5 [F_{(1, 468)} = 4.57, p = 0.03] and low-contact females potentiated their startle response more than high-contact females during tactile Trial 5 [F_{(1, 468)} = 4.05, p = 0.04]. ^*p < 0.05, ^**p = 0.01.

Figure 7

Parental care components. (A) High-contact breeders had higher scores for passive parental care [F_{(1, 228)} = 56.09, p < 0.0001] while low-contact breeders had higher scores for active parental care [F_{(1, 228)} = 5.07, p = 0.02] and paternal care [F_{(1, 228)} = 16.29, p < 0.0001]. (B) High-contact male offspring had higher scores for passive parental care compared to low-contact male offspring [F_{(1, 228)} = 33.68, p < 0.0001] and had lower scores for paternal care [F_{(1, 228)} = 7.18, p = 0.008]. The same paternal was seen in female offspring [passive parental care, F_{(1, 228)} = 22.52, p < 0.0001; paternal care, F_{(1, 228)} = 9.82, p = 0.002]. ^*p < 0.05, ^**p < 0.01, ^***p < 0.0001.