Potential mechanisms of avian sex manipulation

Abstract

The aim of this review is to consider the potential mechanisms birds may use to manipulate the sex of their progeny, and the possible role played by maternal hormones. Over the past few years there has been a surge of reports documenting the ability of birds to overcome the rigid process of chromosomal sex determination. However, while many of these studies leave us in little doubt that mechanisms allowing birds to achieve this feat do exist, we are only left with tantalizing suggestions as to what the precise mechanism or mechanisms may be. The quest to elucidate them is made no easier by the fact that a variety of environmental conditions have been invoked in relation to sex manipulation, and there is no reason to assume that any particular mechanism is conserved among the vast diversity of species that can achieve it. In fact, a number of intriguing proposals have been put forward. We begin by briefly reviewing some of the most recent examples of this phenomenon before highlighting some of the more plausible mechanisms, drawing on recent work from a variety of taxa. In birds, females are the heterogametic sex and so non-Mendelian segregation of the sex chromosomes could conceivably be under maternal control. Another suggestion is that follicles that ultimately give rise to males and females grow at different rates. Alternatively, the female might selectively abort embryos or 'dump lay' eggs of a particular sex, deny certain ova a chance of ovulation, fertilization or zygote formation, or selectively provision eggs so that there is sex-specific embryonic mortality. The ideas outlined in this review provide good starting points for testing the hypotheses both experimentally (behaviourally and physiologically) and theoretically.

Differential allocation in relation to mate song quality in the Bengalese finch

“…However, evidence regarding the ability of birds to adaptively adjust primary sex ratio is still controversial, because of inconsistencies among studies and an incomplete understanding of the underlying mechanisms (Cockburn et al, 2002;West & Sheldon, 2002;Pike & Petrie, 2003;Ewen et al, 2004;Cassey et al, 2006). Because we did not determine the sex of unhatched eggs in the current study, our results could not provide firm evidence that the primary sex ratio was affected.…”

“…Because we did not determine the sex of unhatched eggs in the current study, our results could not provide firm evidence that the primary sex ratio was affected. Observed moderate biases in hatchling sex ratio could be caused either by biases in egg sex ratio, or by sex-specific embryo mortality (Pike & Petrie, 2003). Considering that male chicks are more vulnerable than females in this species (Soma et al, 2006), it is possible that male embryos are also subject to sex-specific mortality under particular reproductive conditions (cf., Love et al, 2005).…”

The evolution of sex ratios and sex-determining systems

“…There are four main categories of genes that can be the focus of selection on sex determination ( Figure 1): (i) sexdetermining genes expressed within the offspring, affecting the probability of developing into male or female, such as the sex-determining region Y (SRY) present on the mammalian Y chromosome [12]; (ii) genes acting in the parents and biasing the distribution of genetic sex-determining factors among the offspring; for example, genes controlling sex chromosome segregation [13]; (iii) parental effects genes, that is, genes expressed in the parents but where the gene product (e.g. mRNA or yolk hormones) acts as a sex-determining factor in the offspring, [11,14]; and (iv) genes acting in the parents and biasing the distribution of external environmental sex-determining factors among the offspring; for example, via choice of oviposition sites in species with ESD [15,16].…”

“…via antagonistic pleiotropy) and, therefore, might be initially selected against [4]. An alternative evolutionary response to selection for biased sex ratios would therefore be maternal control over offspring sex, for example, by female control over sex chromosome segregation [13,18]. However, as first identified by Trivers [19], parents and offspring can have different 'optima' for sex ratios, with the parental genome usually favoring a more biased sex ratio than does the offspring genome ( [19] but see Ref.…”

“…However, some species of birds and mammals show non-random sex ratios at conception (e.g. Refs [39][40][41]), suggesting maternal control over chromosome segregation or maternal or offspring production of a sex-determining factor that override chromosomal sex in the developing fetus [13,18]. Nevertheless, the most promising model systems for investigating the relationships between sex ratio selection and sex determination will be those in which different sex-determining systems occur within or between closely related populations or species.…”