Inter-individual variation in expression of maternal behaviour in sheep

At birth, ewes rapidly form a selective attachment to their offspring and subsequently restrict maternal care to their own lambs. This attachment occurs during a period of intense maternal licking of the offspring, accompanied by frequent low pitched bleats (a specific maternal vocalisation). Maternal licking wanes over the first day of life and thereafter maternal behaviour is expressed as a close spatial association between ewe and lamb, distress behaviours when the ewe and lamb are separated, and frequent sucking interactions. The expression of maternal care is impaired in primiparous ewes. These ewes show a delay in starting to lick their lambs, have a higher rate of rejection behaviours (e.g. aggressive behaviours towards the lamb), make more distress vocalisations and are more likely to show avoidance when the lamb attempts to suck. However, the total amount of licking behaviour and the frequency of low-pitched bleats are not affected by maternal experience. Furthermore, although behaviour improves with experience, individual ewes show consistency in their maternal responsiveness from one pregnancy to the next (1). These data suggest that there are underlying differences between ewes in their expression of maternal behaviour, which persist over consecutive pregnancies. To investigate the potential mechanisms underlying variation in maternal behaviour we compared the maternal responsiveness of two breeds of ewe (Suffolk, Scottish Blackface). Blackface ewes consistently show higher levels of licking behaviour over the first two hours after birth and emit more low pitched bleats than Suffolk ewes. Suffolk ewes display more fearful and aggressive behaviours towards their lambs, have higher incidences of lamb abandonment, and are more likely to move away as the lamb attempts to suck. In tests of maternal recognition 3 days after birth, Blackface ewes were better able to recognise their own lamb from a distance, and spent more time with their lamb than Suffolk ewes. Blackface ewes maintain closer spatial associations with their own lambs from birth to weaning than Suffolk ewes. Embryo transfer between breeds demonstrated that these behavioural differences were due to maternal responsiveness and not to variation in lamb behaviour (2). In addition to consistency across different parities within ewe, ewes are also consistent in their expression of maternal behaviour throughout lactation. The onset of maternal behaviour in the sheep is primed by circulating concentrations of oestradiol and progesterone in pregnancy and triggered by the release of central oxytocin at birth. Maternal behaviour in the sheep is also potentiated by endogenous opioids. To investigate any role these factors may have on individual differences in behavioural expression, we measured oestradiol and progesterone concentration in plasma throughout gestation, and cortisol and oxytocin concentrations in plasma at parturition. A subset of ewes were administered naltrexone at the onset of labour to investigate the role of opioid modulation in mediating individual differences in behavioural expression. Blackface ewes had higher circulating oestradiol concentrations than Suffolk ewes from mid gestation onwards (P<0.001) and a greater oestradiol:progesterone ratio (P<0.001). There was no effect of previous maternal experience. Circulating oestradiol concentrations were positively correlated with maternal licking (P=0.06), the length of sucking bouts (P<0.01), and the frequency of low pitched bleats (P<0.005). The birth of the lamb was associated with a rapid and transitory peak in plasma oxytocin concentration, which did not differ between breeds. There was no relationship between plasma oxytocin concentration and maternal behaviour, nor were there any breed differences in the response to naltrexone treatment. Plasma cortisol concentrations were higher in Blackface ewes than Suffolk ewes in late gestation, but this difference disappeared on the day of parturition. Plasma cortisol concentration immediately after birth was negatively correlated with maternal licking behaviour. The data suggest that maternal oestradiol concentration may be partly responsible for inter-individual variation in maternal behaviour seen in sheep, but does not appear to mediate the effects of previous maternal experience. Recent data in the sheep suggest that parity-related differences occur in the central expression of oestradiol-receptor-α (3) although receptor density decreases at parturition. Nevertheless, our data are consistent with a hypothesis that individual differences in maternal behaviour in the sheep are mediated by the effects of oestradiol on the oxytocinergic system, and that these effects continue to influence maternal behaviour expression throughout lactation. (1) Dwyer CM & Lawrence AB (2000), Behav 137, 1391-1413