Developmental sexual dimorphism and the evolution of mechanisms for adjustment of sex ratios in mammals.

Sex allocation theory predicts biased offspring sex ratios in relation to local conditions if they would maximize parental lifetime reproductive return. In mammals, the extent of the birth sex bias is often unpredictable and inconsistent, leading some to question its evolutionary significance. For facultative adjustment of sex ratios to occur, males and females would need to be detectably different from an early developmental stage, but classic sexual dimorphism arises from hormonal influences after gonadal development. Recent advances in our understanding of early, pregonadal sexual dimorphism, however, indicate high levels of dimorphism in gene expression, caused by chromosomal rather than hormonal differences. Here, we discuss how such dimorphism would interact with and link previously hypothesized mechanisms for sex-ratio adjustment. These differences between males and females are sufficient for offspring sex both to be detectable to parents and to provide selectable cues for biasing sex ratios from the earliest stages. We suggest ways in which future research could use the advances in our understanding of sexually dimorphic developmental physiology to test the evolutionary significance of sex allocation in mammals. Such an approach would advance our understanding of sex allocation and could be applied to other taxa.

In utero exposure to the oestrogen mimic diethylstilbestrol disrupts gonadal development in a viviparous reptile.

The ubiquitous presence of endocrine-disrupting chemicals (EDCs) in the environment is of major concern. Studies on oviparous reptiles have significantly advanced knowledge in this field; however, 30% of reptilian species are viviparous (live-bearing), a parity mode in which both yolk and a placenta support embryonic development, thus exposure to EDCs may occur via multiple routes. In this first study of endocrine disruption in a viviparous lizard (Niveoscincus metallicus), we aimed to identify effects of the oestrogen mimic diethylstilbestrol (DES) on gonadal development. At the initiation of sexual differentiation, pregnant N. metallicus were treated with a single dose of DES at 100 or 10µgkg(--1), a vehicle solvent or received no treatment. There was no dose-response effect, but the testes of male neonates born to DES-exposed mothers showed reduced organisation of seminiferous tubules and a lack of germ cells compared with those from control groups. The ovaries of female neonates born to DES-exposed mothers exhibited phenotypic abnormalities of ovarian structure, oocytes and follicles compared with controls. The results indicate that, in viviparous lizards, maternal exposure to oestrogenic EDCs during gestation may have profound consequences for offspring reproductive fitness.

Placental and embryonic tissues exhibit aromatase activity in the viviparous lizard Niveoscincus metallicus.

Aromatase is a key regulator of circulating testosterone (T) and 17-ß-oestradiol (E2), two steroids which are critical to the development, maintenance and function of reproductive tissues. The role of aromatase in sexual differentiation in oviparous (egg-laying) reptiles is well understood, yet has never been explored in viviparous (live-bearing) reptiles. As a first step towards understanding the functions of aromatase during gestation in viviparous reptiles, we measured aromatase activity in maternal and embryonic tissues at three stages of gestation in the viviparous skink, Niveoscincus metallicus. Maternal ovaries and adrenals maintained high aromatase activity throughout gestation. During the early phases of embryonic development, placental aromatase activity was comparable to that in maternal ovaries, but declined significantly at progressive stages of gestation. Aromatase activity in the developing brains and gonads of embryos was comparable with measurements in oviparous reptiles. Aromatase activity in the developing brains peaked mid development, and declined to low levels in late stage embryos. Aromatase activity in the embryonic gonads was low at embryonic stage 29-34, but increased significantly at mid-development and then remained high in late stage embryos. We conclude that ovarian estrogen synthesis is supplemented by placental aromatase activity and that maternal adrenals provide an auxiliary source of sex steroid. The pattern of change in aromatase activity in embryonic brains and gonads suggests that brain aromatase is important during sexual differentiation, and that embryonic gonads are increasingly steroidogenic as development progresses. Our data indicate vital roles of aromatase in gestation and development in viviparous lizards.

Yolk contributes steroid to the multidimensional endocrine environment of embryos of Niveoscincus metallicus, a viviparous skink with a moderately complex placenta.

Maternally-derived testosterone (T) and 17-ß-oestradiol (E2) provide epigenetic mechanisms by which mothers can actively influence offspring phenotype. In amniotes, maternal steroids may be derived from yolk or transferred across the placenta according to parity mode. Viviparous reptiles utilise both a yolk and a placenta to support their developing embryos, but it has not yet been confirmed whether yolk is a source of maternal T and E2 in such species. We investigated this question using the viviparous lizard Niveoscincus metallicus as our model species. We measured T and E2 in the yolks during vitellogenesis, immediately post-ovulation and at progressive stages of gestation. Our results confirm that yolk is a substantial source of T and E2 in N. metallicus. Contrary to the pattern seen in many oviparous species, we did not observe a marked decline in yolk concentrations of either T or E2 after the initiation of sexual differentiation in the embryos. Rather, we found no statistically significant decline in yolk concentrations of both T and E2 post-ovulation. In viviparous reptiles that utilise both yolk and placenta to nourish their embryos, yolk likely plays an important role in these dynamics but that role is not yet clear. Further research is warranted to understand the importance of yolk steroids in the endocrine environment of the developing viviparous reptile.