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.

19 Reads
  • Source
    • "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). "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    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
  • Source
    • "As expected from a trait directly involved in sibling competition for parental feedings (Gil et al., 2008), we also found that nestlings from larger broods, where sibling competition is more intense, developed wider gapes. These results support previous evidence showing that birds can use adaptive developmental plasticity responses derived from maternal androgens (Gil, 2008; Groothuis et al., 2005). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Avian egg yolks contain various amounts of maternally derived androgens that can modify offspring phenotype and adjust their development to posthatching environment. Seemingly adaptive variation in yolk androgen levels with respect to breeding density conditions or male attractiveness has been found in numerous studies. One important consideration that has been overlooked in previous research is the likely non-linear nature of hormone effects. To examine possible complex dose-response effects of maternal androgens on chick development, we experimentally administered three different androgen doses of the naturally-occurring mixture of yolk testosterone and androstenedione to spotless starling eggs (Sturnus unicolor). We found that yolk androgens show a non-linear dose-response pattern for several traits. Thus, androgens had a stimulatory effect on hatching body mass and nestling skeletal growth, but maximum values were found at intermediate doses, whereas our highest dose resulted in a decrease. However, the opposite U-shaped effect was found on nestling body mass. We also detected linear negative and positive effects on embryonic development period and nestling gape width, respectively. Our results suggest differential tissue responsiveness to yolk androgens, which may result in compromises in maternal allocation to produce adapted phenotypes. Due to the non-linear dose-response pattern, future investigations should carefully consider a wide range of concentrations, since the balance of costs and benefits may strongly differ depending on concentration. © 2015. Published by The Company of Biologists Ltd.
    Journal of Experimental Biology 05/2015; 218(Pt 14). DOI:10.1242/jeb.118257 · 2.90 Impact Factor
Show more