In many species, including humans, there is evidence for parental effects on within-sex variations in reproductive behavior. In the present studies we found that variations in postnatal maternal care were associated with individual differences in female sexual behavior in the rat. Females born to and reared by dams that showed enhanced pup licking/grooming (i.e., High LG mothers) over the first week postpartum showed significantly reduced sexual receptivity and alterations in the pacing of male mounting (i.e., longer inter-intromission intervals) observed in a paced mating test. There were minimal effects on the sexual behavior of the male offspring. The female offspring of High LG mothers showed a reduced lordosis rating, a decreased mount:intromission ratio, received fewer ejaculations and were less likely to achieve pregnancy following mating in the paced mating context. The data suggest maternal influences on the sexual development of the female rat that are functionally relevant for reproductive success. Together with previous studies these findings imply that maternal care can ‘program’ reproductive strategies in the female rat.
Early life experience influences adult sexual behavior in the rat. Prolonged maternal separation during the early postnatal period leads to altered reproductive behavior in males (Rhees et al., 2001). Experimental manipulations that decrease maternal anogenital licking (AGL) reduce penile reflexes in adult males by altering the morphology of motoneurons in the spinal nucleus of the bulbocavernosus (Lenz and Sengelaub, 2006 and Moore, 1992b). Reduced pup AGL impairs male sexual behavior, increasing the latency to ejaculate and decreasing mounting efficiency. Neonatal handling, which increases pup licking in the dam (Lee and Williams, 1975 and Liu et al., 1997), increases the frequency of anovulatory estrous cycles in adult females (Gomes et al., 2005) and decreases sexual receptivity (Gomes et al., 2006). These findings suggest maternal effects on sexual development in the rat.
Natural variations in maternal care in the rat are an important source of individual differences in neuroendocrine development (Cameron et al., 2005 and Meaney, 2001). Such variations in pup licking/grooming LG stably influence estrogen receptor α (ERα) expression in the female offspring in brain regions that regulate reproductive behaviors (Cameron et al., submitted for publication, Champagne et al., 2003b and Champagne et al., 2006). Thus, females reared by Low LG mothers are more sexually receptive to males than are the female offspring of High LG mothers (Cameron et al., 2005 and Cameron et al., 2006). The results of cross-fostering studies reveal evidence for direct effects of postnatal maternal care on both ERα expression (Champagne et al., 2003b) as well as reproductive behaviors, including both maternal behavior (Francis et al., 1999) and sexual receptivity (Cameron et al., submitted for publication). Indeed, such effects include even rudimentary features of sexual development such as the timing of puberty, which occurs at a significantly younger age in the female offspring of Low compared to High LG mothers.
We (Cameron et al., submitted for publication) have reported that the female offspring of High and Low LG dams differed in sexual receptivity, measured using a lordosis rating (Hardy and DeBold, 1972), as well as in the pacing of sexual activity. Female rats tested for sexual behavior in a context (e.g., a pacing chamber, (Erskine et al., 2004)) that permits withdrawal from the male show active pacing of male mounting. Females show a preference for conditions that permit such pacing and the resultant timing of male mounting is functionally important for successful mating (Edwards and Pfeifle, 1983). When tested in the pacing chamber, the female offspring of High LG mothers showed both a reduced lordosis rating and a significantly longer intromission interval (Cameron et al., submitted). In the current study, we examined the functional importance of such differences in sexual behavior using the pacing chamber in which the female was provided the opportunity to mate with two sexually active males; one the offspring of a High LG mother, the other from a Low LG dam. The results of both field studies (Calhoun, 1962) and those in semi-natural environments (McClintock and Adler, 1978 and McClintock and Anisko, 1982) suggest that sexually receptive female rats normally copulate with multiple males. Thus, we considered the testing condition that involves multiple males as the most relevant context in which to examine the functional importance of the maternal effect on sexual behavior in the female offspring. Moreover, this testing condition also provided the opportunity to examine possible partner-preferences. Interestingly, group mating under laboratory conditions reveals individual differences in partner-preference (McClintock and Anisko, 1982). While little is known about the factors that determine partner-preference in the female rat, apart from influences such as strain (Austin and Dewsbury, 1986, Coria-Avila et al., 2006 and Coria-Avila et al., 2004), the female pacing of copulation is associated with partner-preferences (Coria-Avila et al., 2006, Paredes and Alonso, 1997 and Paredes and Vazquez, 1999). Partner preference experiments that allow females to simultaneously mate with two males (Lovell et al., 2006) or four males (Ferreira-Nuno et al., 2005) provide evidence for a preferred mate, defined as the male with which the female spent the most time during testing. Such preferences appear stable over the testing period (French et al., 1972).
In the studies reported here we investigate the functional significance of maternal effects on sexual behavior in the female offspring and on female partner preference. Effects of natural variations in maternal care on the male's behavior were first observed during training with a stimulus female. The behaviors of receptive females and experienced male offspring from High and Low LG dams were then observed during mating using the pacing chamber. The results further reveal maternal effects on the sexual behavior of female offspring and suggest that these effects are potentially important for reproductive success.
