The metabolic cost of avian egg formation: possible impact of yolk precursor production?

Abstract

Physiological mechanisms underlying one of the major assumptions of life history theory, namely that an increased effort in current reproduction may have a negative impact on future reproductive success, are not well understood (Stearns, 1992). One reason for this lack of knowledge is that, in avian systems, most of the research attention has been focused on manipulations of reproductive effort at the incubation or chickprovisioning stages (Monaghan and Nager, 1997) and, thus, the potential physiological costs incurred earlier in breeding, i.e. during follicle development and egg production, have received very little attention. Recent research, however, has shown that the energy cost of egg production in birds may be significant Vézina and Williams, 2002). We recently showed that the physiological process of egg formation in female European starlings (Sturnus vulgaris) is responsible for a 22% increase in resting metabolic rate (RMR) in laying individuals (Vézina and Williams, 2002). We further demonstrated that 18% of the variation in elevated laying RMR was explained by the maintenance and activity cost of the working oviduct (Vézina and Williams, 2003) and emphasized that this organ is probably costly enough that selection has led to a very tight size-function relationship, explaining its rapid pattern of recrudescence and regression. However, 82% of the variation in laying RMR remains unexplained, suggesting that other energy-consuming physiological mechanisms must be responsible, at least in part, for the metabolic cost of egg production (Vézina and Williams, 2003).Another component of egg production that is likely to be energetically costly is the increased liver activity involved in protein and lipid production for oogenesis. During the process of egg formation, the hypothalamus initiates a hormonal cascade by releasing gonadotropin-releasing hormone (GnRH), which induces the release of follicle-stimulating hormone (FSH) and luteinizing hormone (LH) from the pituitary gland (Williams, 1998;Scanes, 2000). These hormones stimulate the ovary to produce estrogens (Williams, 1998), which then trigger the production of the egg-yolk precursors, vitellogenin (VTG) and yolk-targeted very-lowdensity lipoprotein (VLDLy), by the liver (Bergink et al., 1974;Deeley et al., 1975;Wallace, 1985;Walzem, 1996;Williams, 1998), which are then secreted into the blood. During rapid yolk development, plasma VTG and VLDLy are taken up by the ovary and are processed within the follicles into yolk, the nutrient and energy source for the developing avian embryo Little is known about the energy costs of egg production in birds. We showed in previous papers that, during egg production, European starlings (Sturnus vulgaris) undergo a 22% increase in resting metabolic rate (RMR) and that the maintenance and activity costs of the oviduct are responsible for 18% of the variation in elevated laying RMR. Therefore, other energy-consuming physiological mechanisms must be responsible for the remaining unexplained variation in elevated laying ...

Widespread patterns of sexually dimorphic gene expression in an avian hypothalamic–pituitary–gonadal (HPG) axis

“…Females, unlike males, must grow and maintain follicles and the oviduct, which is energetically costly58. In a passerine species, females increased their resting metabolic rate by 22% during egg laying, of which 18% was attributed to maintenance of the oviduct58. While birds in our study were not actively nesting, we could not control for reproductive stage of the gonads.…”

“…This may be due to their varying stages of follicular development. Females, unlike males, must grow and maintain follicles and the oviduct, which is energetically costly58. In a passerine species, females increased their resting metabolic rate by 22% during egg laying, of which 18% was attributed to maintenance of the oviduct58.…”

Hematological changes associated with egg production: estrogen dependence and repeatability

“…hepatic synthesis and release of yolk precursors (Williams, 1999). Alternatively, homeostatic mechanisms (hemoconcentration or hemodilution) may act to maintain hematocrit within an optimum range that best meets the increased metabolic demands during egg production (Vezina et al, 2003;Vezina et al, 2006); therefore, any inhibitory effects of exogenous estradiol on erythropoiesis may be masked as a result. Given that hematocrit is a critical determinant of blood viscosity (Gaudard et al, 2003), it may not be advantageous for females to deviate from a set range because this would compromise blood flow dynamics and influence efficiency of oxygen and/or nutrient delivery to tissues (Nikinmaa, 1990;Hebert et al, 1997) during key reproductive stages.…”

Temperature-induced elevation of basal metabolic rate does not affect testis growth in great tits

“…However, the exact metabolic costs of testis enlargement and maintenance are notoriously hard to determine (Greenman et al, 2005). As an example, the cost of gonadal growth may be met through reallocation of resources among different physiological systems, rather than in an additive manner (Vézina et al, 2003). In this respect, testis growth rate in our cold temperature treatment group may have been maintained thanks to a reallocation of energy originally dedicated to e.g.…”