Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev

Department of Behavioural Biology, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands.
Neuroscience & Biobehavioral Reviews (Impact Factor: 8.8). 05/2005; 29(2):329-52. DOI: 10.1016/j.neubiorev.2004.12.002
Source: PubMed


Avian eggs contain substantial amounts of maternal hormones and so provide an excellent model to study hormone-mediated maternal effects. We review this new and rapidly evolving field, taking an ecological and evolutionary approach and focusing on effects and function of maternal androgens in offspring development. Manipulation of yolk levels of androgens within the physiological range indicates that maternal androgens affect behaviour, growth, morphology, immune function and survival of the offspring, in some cases even long after fledging. Descriptive and experimental studies show systematic variation in maternal androgen deposition both within and among clutches, as well as in relation to the sex of the embryo. We discuss the potential adaptive value of maternal androgen transfer at all these three levels. We conclude that maternal androgen deposition in avian eggs provides a flexible mechanism of non-genetic inheritance, by which the mother can favour some offspring over others, and adjust their developmental trajectories to prevailing environmental conditions, producing different phenotypes. However, the literature is less consistent than often assumed and at all three levels, the functional explanations need further experimental testing. The field would greatly benefit from an analysis of the underlying physiological mechanisms.

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    • "In addition to between-clutch variation, most studies report within-clutch patterns in yolk androgens across the laying sequence that are suggested to facilitate either brood survival or brood reduction in asynchronous broods (Schwabl 1993, 1996; Schwabl et al. 1997b; reviewed iby Groothuis et al., 2005). Flycatchers show hatching asynchrony (Lundberg and Alatalo, 1992), and within-clutch patterns have also been found: In the Hungarian population, A4 showed increasing within-clutch patterns while T did not (Hegyi et al., 2011; Michl et al., 2005); in the Swedish population, both androgens showed similar variation, increasing in the first broods and decreasing in the second (Tobler et al., 2007b). "
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    ABSTRACT: Maternal effects are a crucial mechanism in many taxa in generating phenotypic variation, affecting offspring development and fitness and thereby potentially adapting them to their expected environments. Androgen hormones in bird eggs have attracted considerable interest in past years, and it is frequently assumed that their concentrations in eggs are shaped by Darwinian selection. Currently, however, the data is scattered over species with very different life-history strategies, environments and selection pressures, making it difficult to draw any firm conclusions as to their functional significance for a given system. I review the evidence available as to the function, variation and potential adaptive value of yolk androgens (testosterone, T and androstenedione, A4) using one well-studied wild bird model system, the European flycatchers Ficedula hypoleuca and F. albicollis. These species both show genetic and environmental variation in yolk androgen levels, along with fitness correlations for the female, suggesting the potential for selection. However, variation in yolk T and A4 seem to be differentially affected, suggesting that maternal constraints/costs shape the transfer of the yolk steroids differently. Most of the environmental variation is consistent with the idea of high yolk androgen levels under poor rearing conditions, although the effect sizes in relation to environmental variation are rather small in relation to genetic among-female variation. Importantly, within-clutch patterns too vary in relation to environmental conditions. Yolk androgens seem to have multiple short- and long-term effects on phenotype and behavior; importantly, they are also correlated with the fitness of offspring and mothers. However, the effects are often sex-dependent, and not universally beneficial for the offspring. Unfortunately, conclusive data as to the adaptive benefits of clutch mean androgen levels or within clutch-patterns in different environmental conditions is still lacking.
    General and Comparative Endocrinology 09/2015; 224. DOI:10.1016/j.ygcen.2015.09.016 · 2.47 Impact Factor
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    • "Furthermore, growth in hatchling turtles is influenced by yolk composition (the proportion of protein and polar vs. nonpolar lipids, as well as steroid hormonal concentrations; Congdon and Gibbons 1985; Packard and Packard 1988; Nagle et al. 2003). Maternally produced steroid hormones (estrogens and androgens) deposited in the yolk can influence the sex ratio of the clutch or the growth rate, performance, and survivorship of the embryo (Elf 2004; Groothuis et al. 2005). Thus, even though embryos of oviparous species develop during a prolonged period outside of their mothers, endocrine studies have experimentally established that maternal plasma steroids are transferred to the yolk, affecting the phenotype of the offspring (Arcos 1972; Adkins-Regan et al. 1995). "
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    ABSTRACT: In oviparous species, preovulatory maternal effects such as investment in yolk quantity and composition or levels of yolk steroid hormones might potentially affect hatchling body sizes, growth rates, performance, and sex in species with temperature-dependent sex determination. We investigated the effects of egg mass and levels of testosterone and 17β-estradiol in the yolk on the phenotypes of hatchling Magdalena River Turtles (Podocnemis lewyana) in three populations in the Magdalena River drainage of northern Colombia. We hypothesized that, under homogeneous incubation conditions, the differences documented among clutches would be attributable to familial effects, caused by either heritable genetic factors or preovulatory maternal effects. Eggs were incubated artificially at the pivotal temperature for the species (33.4°C) and hatchlings were reared in the laboratory for 2 mo. Two eggs from each clutch were tested for testosterone and 17β-estradiol levels. Sex ratios, hatchling size, mass, and righting times varied both between clutches within a site and between populations. Egg mass was positively related to hatchling body size and mass, both at hatching and at 2 mo of age. Levels of 17β-estradiol concentrations influenced hatching success rates and incubation periods. Sex ratios were marginally related to 17β-estradiol levels, with clutches and sites with higher levels tending to produce fewer males. Our results provide evidence that preovulatory maternal effects play a role in influencing phenotypic attributes related to hatchling survivorship such as size, growth rate, and performance, and also seem to interact with incubation temperature to determine the sex of each individual and the sex ratio of the clutch, which has implications for both parental and offspring fitness.
    Herpetologica 08/2015; 71(3):196-202. DOI:10.1655/HERPETOLOGICA-D-14-00036 · 1.14 Impact Factor
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    • "This hormonal 'pleiotropy' could induce a number of life-history trade-offs (reviewed in Williams, 2012), and studies that manipulate androgen levels are helpful to identify the mechanisms underlying these processes (Andersson et al., 2004; Groothuis et al., 2005b). Androgen injection studies have shown that small changes in yolk hormone levels induce a wide range of effects (reviewed in Groothuis et al., 2005a; Gil, 2008). Some of these effects, such as accelerated embryonic development (Eising et al., 2001; Eising & Groothuis, 2003; Muriel et al., in press), increased growth rate (Eising et al., 2001; Pilz et al., 2004; Muriel et al., in press), improved competitive behaviour in nestlings (M€ uller et al., 2009, 2012) or intensified begging behaviour (Schwabl, 1996a; Eising & Groothuis, 2003), suggest that maternal yolk androgens are generally beneficial to offspring. "
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    ABSTRACT: Female birds may adjust their offspring phenotype to the specific requirements of the environment by differential allocation of physiologically active substances into yolks, such as androgens. Yolk androgens have been shown to boost embryonic development, growth rate and competitive ability of nestlings, but they can also entail immunological costs. The balance between costs and benefits of androgen allocation is expected to depend on nestling environment. We tested this hypothesis in a multi-brooded passerine, the spotless starling, Sturnus unicolor. We experimentally manipulated yolk androgen levels using a between-brood design, and evaluated its effects on nestling development, survival and immune function. Both in first and replacement broods, the embryonic development period was shorter for androgen-treated chicks than controls, but there were no differences in second broods. In replacement broods, androgen-treated chicks were heavier and larger than those hatched from control eggs, but this effect was not observed in the other breeding attempts. Androgen exposure reduced survival with respect to controls only in second broods. Regarding immune function, we detected non-significant trends for androgen treatment to activate two important components of innate and adaptive immunity (IL-6 and Ig-A levels, respectively). Similarly, androgen-treated chicks showed greater lymphocyte proliferation than controls in the first brood and an opposite trend in the second brood. Our results indicate that yolk androgen effects on nestling development and immunity depend on the environmental conditions of each breeding attempt. Variation in maternal androgen allocation to eggs could be explained as the result of context-dependent optimal strategies to maximize offspring fitness. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
    Journal of Evolutionary Biology 06/2015; 28(8). DOI:10.1111/jeb.12668 · 3.23 Impact Factor
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