Stud males and dud males: intra-uterine position effects on the reproductive success of male gerbils

Sexually mature male Mongolian gerbils, Meriones unguiculatus, from known intra-uterine positions were each paired with a succession of nulliparous females. Those males that had matured in intra-uterine positions adjacent to two males (2M males) sired an average of 28% more young than did those males that had matured in intra-uterine positions between two females (2F males). In a second experiment, female gerbils chose between pairs consisting of one adult 2F male gerbil and one adult 2M male gerbil. When in induced oestrus (but not when in other hormonal states), the females spent significantly more time near 2M than near 2F males. Female gerbils in oestrus thus tended to affiliate with the more reproductively capable male in their vicinity. Natural selection acts only on heritable traits (Lewontin 1978; Enders 1986). However, environmentally induced phenotypic variability correlated with reproductive success is also important to the student of evolutionary process. Such nonheritable variance in fitness can reduce the probability that those individuals carrying more fit genes will, in fact, achieve greater reproductive success than will those individuals carrying less fit genes. Consequently, non-heritable variance in individual fitness will affect the rate at which evolution can proceed. Given the potential importance to evolutionary process of non-heritable variation in reproductive success, there has been surprisingly little study of its sources in animal populations. Results of previous studies in our laboratory have revealed dramatic effects of intra-uterine position, a non-heritable characteristic, on the reproductive life histories of female Mongolian gerbils, Meriones unguiculatus. Ninety-five per cent of female gerbils that mature in intra-uterine positions between two female fetuses (2F females) exhibit vaginal introitus before reaching 25 days of age; only 41% of female gerbils from intra-uterine positions between two male fetuses (2M females) exhibit such early maturation (Clark et al. 1986; Clark & Galef 1989). Female gerbils exhibiting vaginal introitus before reaching 25 days of age have a lifetime fecundity more than twice as great as that of their late-maturing sisters (Clark et al. 1986). It is easily calculated that, on average, 2F 0003-3472/92/020215+07 $03.00/0 female gerbils wean 1.4 times as many young as do 2M female gerbils. It has also been found that the intra-uterine positions that male rodents occupy as fetuses affects their exposure to androgens during the perinatal period (vom Saal 1989; Clark et al. 1990, 1991). There is evidence consistent with the view that adult male gerbils that matured in 2M intra-uterine positions ha ve higher plasma levels oftestosterone than adult male gerbils that matured in 2F intra-uterine positions. Adult 2M male gerbils (I) scent mark more frequently, (2) have greater anogenital distances and (3) have larger ventral glands than 2F male gerbils (Clark et al. 1990); each ofthesecharacteristics is correlated with high circulating levels of testosterone (Thiessen et al. 1968; Blum & Thiessen 1971). Furthermore, recent radioimmunoassays of plasma testosterone concentrations in adult male gerbils have consistently revealed significantly higher circulating levels of testosterone in 2M than in 2F males (Clark et aI., unpublished data). The intra-uterine positions that male rodent fetuses occupy can also affect the copulatory pattern that they exhibit when adult. Both 2M male gerbils and 2M male house mice, Mus domesticus, mount oestrus females more rapidly and ejaculate after fewer intromissions and with shorter mean latencies than do 2F con specifics (vom Saal et al. 1983; vom Saa11989; Clark et al. 1990). In sum, behavioural and morphological correlates of intra-uterine position are well established in @ 1992 The Association for the Study of Animal Behaviour