Maternal Corticosteroids are involved in Manipulation of Offspring Sex Ratio in the Avian System
Sex ratio theory is concerned with the ratio of male to female offspring, in sexually reproducing organisms, which will be referred to as sex ratio for through this paper. Sex ratio can be classified into four different types relative to time. The primary sex ratio is the sex ratio at fertilization; the secondary sex ratio is the ratio at birth; the tertiary sex ratio is the ratio when the organisms are sexually active or mature; and the quaternary sex ratio pertains to the ratio in organisms at the post-reproductive stage. The primary focus of this paper will be directed towards primary sex ratio. Also, Fisher's principle states that the sex ratio of most species is approximately 1:1, assuming there is an equal parental expenditure on both male and female offspring (see Maternal age and offspring sex ratio in reindeer). When the fitness benefits with respect to investment in offspring differ depending on offspring sex, it is believed that animals tend to alter their offspring sex ratio (Oddie, 1998.). This has been seen in birds, where females may manipulate the sex ratio of their clutch in an attempt to benefit from direct future fitnuess gains (Komdeur et al. 1997; see sex manipulation in zebra finches ). Mothers tend to engage in this behaviour when their condition is poor (Pike, 2005), when food is scarce (Austad and Sunquist, 1986; sex manipulation in zebra finches), or when faced with poor habitat conditions (Komdeur et al., 2002) and such conditions are associated with elevated corticosteroid levels (Bonier et al.). This association is reasonable since corticosteroids constitute a class of stress hormones that are found in all vertebrates. In this paper, the link between maternal corticosteroids and sex-specific investment will be examined. By discussing specific studies, it is my intention to explore how corticosteroid levels influence offspring sex ratio and I will attempt to incorporate findings from these studies in an evolutionary framework to highlight the rationale behind such a behavior as well. For the purpose of this paper, I will be focusing on the avian system.
Hormones involved in mediating energetic balance and condition can influence offspring sex ratio (Love et al. 2005;Pike and Petrie 2003; Cameron 2004). For example, corticosterone and cortisol govern physiological and behavioural responses during stressful situations in nonmammalian tetrapods and in mammals and fish, respectively (Love et al. 2005; Sapolsky et al. 2000). Thus, it can be inferred that such hormones are associated with body condition, shown by an increase in plasma baselind corticosterone levels in birds when their body condition decreases (Love et al. 2005; Heath and Dufty 1998; Holberton et al. 1996).
OVERVIEW OF STUDIES
In a study conducted by Bonier et al. in 2007, circulating baseline cort levels were taken from female white-crowned sparrows (Zonotrichia leucophrys). Although sex ratios can occur prior to or after egg laying, the researchers only quantified cort levels during the incubation period. The mothers were subcutaneously implanted with either a placebo or a corticosterone pellet. Their clutch of eggs were collected and were placed in an incubator to allow for tissue growth for embryo sexing. The mothers, who were banded and who should have had higher cort levels at that time (hormone assays were performed to confirm this), were released and their clutches of eggs were taken, incubated, and sexed. To investigate the effects of the cort pellet implants, the number of female embryos from the preimplant and postimplant clutches were compared.
When the preimplant clutches were compared with one another, it was noted that mothers who had higher baseline cort levels produced a significantly higher proportion of female offspring per clutch. When the postimplant clutches were compared with one another, the results showed that those with mothers who were implanted with corticosterone pellets consisted of a higher proportion of female offspring in comparison to those with mothers who were implanted with placebos. The cort-implanted mothers produced a higher proportion of female embryos than they did when they were not implanted with corticosteroid pellets. Also, when cort levels returned to baseline levels in the cort-implanted females, there was not a significant different in embryo sex ratio when compared with the pre-implanted group or the placebo-implanted females. The results from this study illustrate that moderate increases in corticosteroid levels in a female increases the chances of her producing female offspring.
Furthermore, Pike and Petrie (2006) used Salastic implants to manipulate corticosterone levels in breeding female Japanese quail (Coturnix coturnix japonica) and studied the effects this had on offspring sex ratio. This particular study involved two phases. The first phase involved females laying their eggs without any hormone manipulation, having their cort levels measured, and sexing their eggs. The second phase was a repeat of phase one using the same individuals with the exception that the breeding females' cort levels were manipulated. The sex ratios across groups in the first phase did not differ significantly from parity. In contrast, the sex ratios across groups in the second phase differed significantly from parity. The sex ratio in the second phase was more biased towards females. Maternal and paternal condition did not differ between phase one or two.
Love et al. (2005) measured and manipulated baseline levels of corticosterone in wild female European starlings (Sturnus vulgaris) that were at the laying stage to explore the effects this had on sex ratio. In this study, it was observed that baseline plasma corticosterone was negatively correlated with the energetic body condition in the female starlings. When the maternal baseline plasma corticosterone was elevated using silastic implants, yolk corticosterone increased. The elevation caused the clutch to be female-biased in terms of sex ratio, which was caused by an increase in male mortality during the embryonic stage, which consistent with the idea that maternal corticosterone can be transferred to the eggs (Hayward and Wingfield 2004). When compared to the control group, it was observed that females that was implanted with corticosterone produced more daughters. In addition to causing a sex-biased change in offspring quality that favoured the female sex via sex ratio bias, male offspring were also lighter at hatching, slower growing, and had lower immune responses (PHA) than control males.
Furthermore, Pike and Petrie (2004) examined the relationship between maternal quality, offspring sex ratio, and corticosterone, using a captive population of peafowl (Pavo cristatus). Each peacock was grouped with three peahens that differed in relative body condition. What they found was a significant correlation between maternal body condition, maternal plasma corticosterone levels, and offspring sex ratio. Superior maternal condition was correlated with low levels of plasma corticosterone and male-biased clutch and thus an increase in investment in the male eggs. In contrast, low maternal condition was correlated with high levels of plasma corticosterone and female-biased clutch.
Pike and Petrie (2004) provided evidence in this study that prelaying manipulation of sex occurred. They showed that infertile eggs likely did not explain the observed biased sex ratios. Even though the ratios used were not true primary sex ratios due to the fact that they were unable
to sex infertile eggs and eggs that failed to develop a visible embryo, the results in this study suggests that the sex ratio bias occurred before egg laying. This is because there was no evidence showing that the potential for the eggs o hatch was significantly lower in the clutches belonging to females that were producing an excess of sons or daughters.
Pike and Petrie (2004) also found that females in good condition produced male eggs that weighed significantly more than female eggs. This effect was absent in females that were in poor condition. They suggest that females that had sufficient resources were investing more to the male eggs to increase their fitness. It is unclear, however, whether the increase in egg mass is a result of a larger amount of albumin or yolk. They assumed that in peacocks, eggs are ovulated and then fertilized sequentially, and yolk size of the eggs is determined before fertilization occurs. In contrast, the albumin and shell are deposited around the egg as it makes its way down the oviduct. Because meiotic division, which determines sex, occurs shortly before the process of ovulation (Pike & Petrie 2004; Romanoff & Romanoff 1949), if an increase in egg male egg mass is a result of an increase deposition of albumin this suggests that peafowl can discriminate between male and female ova internally and thus alter the amount of albumin deposited. If the increase in male egg mass is due to an increase deposition of yolk, this would suggest that sex is predetermined..