Paternal line effects of early experiences persist across three generations in rhesus macaques

The effects of early stress may not be limited to the exposed generation, but are sometimes passed on to subsequent generations. Such non-genetic transgenerational inheritance is a potentially important developmental and evolutionary force. We compared the transgenerational effects of maternal and paternal line early stress on anxiety- and health-related traits in three non-exposed generations (F1, F2 and F3) of semi-naturalistically raised rhesus macaques. As infants, F0 macaques were exposed to nursery rearing (NR) or semi-naturalistic social conditions (CONTROL). Three hundred forty non-exposed F1-F3 descendants were CONTROL reared and physiological and behavioral measures were collected during standardized assessment at 3-4 months of age. Paternal line NR was significantly associated with greater nervousness in F1-F3 and lower immune cell counts in F1-F2. Maternal-line NR effects were not observed. This study suggests that acquired stress-related traits may be inherited across generations in primates, through complex social or germ-line mechanisms.