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Perinatal Testosterone Exposure and Maternal Care Effects on the Female Rat's Development and Sexual Behaviour

Natural variations in maternal care have profound influences on offspring behaviour, brain activity and hormone release. Measuring the amount of time that a rat dam spends licking/grooming (LG) her pups during their first week of life allows for characterisation of distinctive Low, Mid and High LG phenotypes. We have previously found that female offspring of High LG mothers are less sexually receptive, less motivated to mate and show a later onset of puberty relative to Low LG offspring. Given that High LG females are exposed to greater levels of testosterone in utero, we hypothesise that differences in sexual behaviour between High and Low LG female offspring are driven in part by differences in prenatal hormone exposure. To test this hypothesis, pregnant dams pre‐characterised as Low, Mid, or High LG mothers were implanted with testosterone or placebo on gestational day (GD) 16. Offspring body weight and anogenital index were assessed at GD 21 and in adulthood. Age of vaginal opening and oestrous cyclicity were assessed to determine the timing of pubertal onset. Testosterone exposure removed the difference between LG phenotypes in pubertal onset by delaying vaginal opening and the appearance of first pro‐oestrus. In adulthood, sexual behaviour in a paced mating chamber after sham surgery or ovariectomy with steroid‐replacement was examined. Our findings show that Low, Mid and High LG female offspring are differentially affected by perinatal testosterone exposure, and that this exposure removes the precocial pubertal onset of Low LG offspring and increases the sexual proceptivity and receptivity of High LG offspring. These results suggest that maternal programming of the female reproductive system may be mediated, in part, through differences in perinatal testosterone exposure, instead of solely through maternal behaviour.