Evidence that Maternal Diet Alters Steroid Levels and Primary Offspring Sex Ratio in the Zebra Finch

Abstract

The growing interest in the reproductive benefits of biasing offspring sex ratios in avian species has generated curiosity and provided much insight into the potential factors and mechanisms controlling sex-ratio adjustment. Differing offspring sex ratios often occur in response to changes in the environment. Of particular interest, but less understood, are the mechanisms regulating primary (pre-ovulatory) sex-ratio adjustment. Recently, a number of bird studies have suggested that females (the heterogametic sex) are capable of using primary mechanisms to adjust offspring sex ratios; however the mechanism responsible for this is unknown.

Sex of offspring is determined in the first meiotic division when one sex chromosome is retained in the oocyte while the other segregates to the polar body. During this time, follicular steroid production is limited primarily to progesterone (P4) and so it has been suggested that maternal steroids, which are sensitive to environmental perturbations, could also influence sex chromosome segregation. Additionally, primary offspring sex ratios have been shown to be affected by some of the same environmental factors that are known for inducing changes in an individual’s hormonal milieu. Researchers studying the effects of elevated levels of maternal steroids on primary sex ratio have mainly done so by administering pharmacological doses of exogenous hormones to mothers, but none have examined endogenous hormones at meiosis I (critical time in sex determination). We manipulated both diet quality and perceived availability in breeding female zebra finches (Taeniopygia guttata) so that we could examine the effect this changing factor would have on natural levels of P4, corticosterone (CORT), and testosterone (T) in circulation during meiosis I and throughout the day. We found that females fed the high quality diet produced significantly more male offspring (81%) and exhibited moderately low to very low levels of these steroids. Females fed the low quality diet produced 38% males and had the highest P4 levels, but relatively low levels of CORT. When the high quality diet was perceived to be restricted females produced 46% males and had the highest CORT levels, while P4 remained relatively low. All three steroids reached their peak during the period of meiosis I; however T levels were very low (below 1ng/ml) in all diet treatments throughout the day. Our results suggest that no one hormone is responsible for primary sex ratio adjustment in this species. It appears that natural levels of maternal steroids, particularly P4 and CORT, in circulation during meiosis I play an integral yet complex role in the mechanism.