Hematological changes associated with egg production: estrogen dependence and repeatability

Abstract

SUMMARYThe ʻcost of reproductionʼ (i.e. the trade-off between current reproduction and future fecundity and/or survival) is a central concept in life history theory, yet we still know very little about the physiological mechanisms underlying such costs. Recently it has been recognized that reproduction itself or the regulatory (hormonal) mechanisms underlying reproduction might result in ʻcostsʼ (cf. resource-allocation based mechanisms). As one example, it has been suggested that the decrease in hematocrit observed during egg production in birds might be due to antagonistic pleiotropic effects of estrogens. This could generate costs of reproduction by reducing oxygen-carrying capacity during subsequent aerobically demanding stages such as chickprovisioning. Here we show that the reduction in hematocrit during egg-laying is dependent on receptor-mediated actions of endogenous estrogens: blocking estrogen receptors using the anti-estrogen tamoxifen reduces the decrease in hematocrit during egg production in female zebra finches (Taeniopygia guttata) such that hematocrit at the 1-egg stage is not significantly different than pre-breeding, baseline values. We also show that both pre-breeding hematocrit and the decrease in hematocrit associated with egg production are repeatable, and that females with the highest pre-breeding hematocrit values tend to show the largest decreases in hematocrit during egg production. We suggest that hematological changes during egg production are a good candidate mechanism for a regulatory-network based trade-off involving antagonistic pleiotropic effects of estrogens, which otherwise have essential reproductive functions.

Hematological changes associated with egg production: direct evidence for changes in erythropoiesis but a lack of resource dependence?

“…Inconsistencies between the two analyses can be attributed to differences in sample size (i.e. not all individuals were included in the diet quality experiment) as well as the significant degree of intraindividual variation in hematological traits typical of this population (see Wagner et al, 2008).…”

“…A reduction in hematocrit during egg production has been reported in numerous avian species (reviewed by Williams et al, 2004a;Wagner et al, 2008), ranging from -1.5% in the great tit (Horak et al, 1998a) to -10% in the red-billed quelea (Jones, 1983) relative to pre-breeding levels. Furthermore, Kalmbach et al (Kalmbach et al, 2004) concluded that the extent of anemia was proportional to egg laying effort.…”

“…Anemia -a reduction in hematocrit, hemoglobin and red blood cell number (Campbell and Ellis, 2007) -during egg production has been documented in numerous studies [(e.g. deGraw et al, 1979;Jones, 1983;Morton, 1994;Gayathri and Hegde, 2006;Wagner et al, 2008) and references therein], and may persist into later stages of incubation and chick rearing in some cases (Williams et al, 2004a). In addition, Kalmbach et al (Kalmbach et al, 2004) showed that experimentally increasing egg production in female great skuas (Stercorarius skua) increased anemia, in terms of a greater reduction in hematocrit and red blood cell number compared with control females.…”

“…Estrogens inhibit the differentiation, proliferation and survival of white and red blood cell precursors in the bone marrow (Blobel and Orkin, 1996;Medina et al, 2000;Perry et al, 2000). Blocking estrogen receptors using the anti-estrogen tamoxifen inhibits the development of anemia in egg-laying birds supporting a role for estrogen-dependent suppression of erythropoiesis in anemia (Wagner et al, 2008). The candidate mechanisms that have been proposed involve very different predictions about (1) the time-course of development and recovery from anemia, (2) whether specific changes would occur among a subset or all hematological variables (hematocrit, hemoglobin concentration, red blood cell size and number, proportion of immature red blood cells or reticulocytes; see Table 1), and (3) the extent to which development of anemia should be influenced by resource availability or diet quality.…”

Alteration of immune function endpoints and differential expression of estrogen receptor isoforms in leukocytes from 17β-estradiol exposed rainbow trout (Oncorhynchus mykiss)

“…While there is no information on the effects of E2 on erythropoiesis in fish, estradiol benzoate slowed the maturation of new red blood cells in channel catfish [21]. Elevated E2 in birds caused hemodilution by increasing plasma osmolality due to production of yolk precursors in the liver and their release to the blood, resulting in water movement into the blood to compensate [67]. Plasma vitellogenin levels are often increased in fish following E2 exposure [65], suggesting that, as in birds, hemodilution may also occur in fish.…”