Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird

Abstract

Maternal modification of offspring sex in birds has strong fitness consequences, however the mechanisms by which female birds can bias sex of their progeny in close concordance with the environment of breeding are not known. In recently established populations of house finches (Carpodacus mexicanus), breeding females lay a sex-biased sequence of eggs when ambient temperature causes early onset of incubation. We studied the mechanisms behind close association of incubation and sex-determination strategies in this species and discovered that pre-ovulation oocytes that produce males and females differed strongly in the temporal patterns of proliferation and growth. In turn, sex-specific exposure of oocytes to maternal secretion of prolactin and androgens produced distinct accumulation of maternal steroids in oocyte yolks in relation to oocyte proliferation order. These findings suggest that sex difference in oocyte growth and egg-laying sequence is an adaptive outcome of hormonal constraints imposed by the overlap of early incubation and oogenesis in this population, and that the close integration of maternal incubation, oocytes' sex-determination and growth might be under control of the same hormonal mechanism. We further document that population establishment and the evolution of these maternal strategies is facilitated by their strong effects on female and offspring fitness in a recently established part of the species range.

Heritability of dispersal rate and other life history traits in the Glanville fritillary butterfly

“…Recent studies on birds have shown that maternal effects can be strongly sex-specific and apparently play an important role in the evolution of sexual dimorphism (Badyaev, 2005;Badyaev et al, 2005Badyaev et al, , 2006. Sex-specific maternal effects can arise by for example, mothers allocating variable amounts of nutrients or hormones to sons and daughters in relation to their own condition (Badyaev et al, , 2006.…”

Hormone-mediated maternal effects in birds:mechanismsmatter but what do we know of them?

“…Unfortunately, most of the information on oocyte proliferation and maturation and follicular steroid production comes from poultry, selected for maximal egg production; therefore, we cannot necessarily assume that the processes are exactly the same in wild birds, and some evidence exists that this is not the case (Young & Badyaev 2004;Badyaev et al 2005). Nevertheless, these studies reveal general principles of how ovarian steroids might accumulate in oocytes and how to study these processes.…”

“…Finally, some studies measured hormone concentrations after completion of laying (onset of incubation), which is inappropriate since gonadal androgens and oestrogen rapidly decline during that phase (e.g. Schwabl 1996a; Sockman & Schwabl 1999;Badyaev et al 2005).…”

“…Even if one, based on the above considerations, only takes those studies into account that most likely would detect correlations (the first three studies in table 1 and those by Williams et al (2005), Navara et al (2006) and Groothuis et al (submitted)), there is still no consistent picture. Even the two studies that took yolk layers into account produced different results (Badyaev et al 2005;Egbert 2006). In sum, these data are inconclusive and do not allow us to reject any of the three hypotheses.…”

“…However, hormone accumulation occurs before sex determination by meiosis. Therefore, it is more likely that the sex of the egg is a consequence of hormone concentrations rather than yolk hormone concentrations being adjusted to the sex of the egg (see Badyaev et al 2005).…”