Article

Sexual versus individual differentiation: the controversial role of avian maternal hormones

Section of Behavioural Neurosciences, Department of Cell Biology and Neuroscience, Istituto Superiore di Sanità, Rome, Italy.
Trends in Endocrinology and Metabolism (Impact Factor: 8.87). 04/2007; 18(2):73-80. DOI: 10.1016/j.tem.2007.01.003
Source: PubMed

ABSTRACT Avian embryos are exposed not only to endogenous sex steroids, which are produced by their gonads and have a key role in sexual differentiation, but also to maternal steroids transferred into the egg yolk, which can modulate the development of individual differences in behavior. Studies of maternal hormones have primarily focused on ultimate questions (evolutionary trade-offs, functional significance), whereas proximate mechanistic questions have been largely ignored. A central problem that must be addressed is how exposure to maternal hormones affects the individual phenotype without interfering with sexual differentiation. Separate effects could result from the action of different hormones, at different doses or at different times, on different targets.

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    • "Many questions regarding the adaptive significance of maternal hormones in the yolk still remain unanswered. Important new insights may come from studies focusing on the physiological mechanisms through which these hormones may affect the offspring (Carere and Balthazart, 2007; Pfannkuche et al., 2011; von Engelhardt and Groothuis, 2011). A total of 28% of the females showed a significant preference the first time they were tested and 76% of the females were successful during their second preference test. "
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    ABSTRACT: It is well established that in many avian species, prenatal maternal resource allocation varies both between and within clutches and may affect offspring fitness. Differential allocation of maternal resources, in terms of egg weight and yolk composition, may therefore allow the female to adjust brood reduction and to fine-tune reproductive investment in accordance with the expected fitness returns. The adaptive value of such maternal resource allocation is thought to be context-dependent as well as species-specific. We investigated the effects of female preference for her mate on the allocation of prenatal maternal resources in the budgerigar, Melopsittacus undulatus, a monogamous species of parrot that shows an extreme hatching asynchrony. We assessed mate preferences in a two-way preference test and allowed females two breeding rounds: one with the preferred and one with the non-preferred partner. We found no effect of preference on either latency to lay or clutch size, but females mated with the preferred partner laid eggs that contained significantly more yolk. Their eggs also contained significantly more androstenedione but not testosterone. Our results suggest that in this species, female preference may influence maternal resource allocation, and that the functional roles of each androgen in the yolk should be considered separately. In addition, we found a significant effect of laying order on egg and yolk weight as well as on yolk testosterone and androstenedione levels. These measures, however, did not change linearly with the laying order and render it unlikely that female budgerigars compensate for the extreme hatching asynchrony by adjusting within-clutch allocation of prenatal maternal resources. Copyright © 2015. Published by Elsevier Inc.
    Hormones and Behavior 04/2015; 71. DOI:10.1016/j.yhbeh.2015.03.009 · 4.51 Impact Factor
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    • "In contrast, under favourable circumstances (sufficient food resources, mild climate etc.), young animals should be able to compensate additional demands by an increased food intake (Brzęk and Konarzewski, 2007). Maternal testosterone can induce phenotypic variability of offspring (Carere and Balthazart, 2007; Groothuis and Schwabl, 2008), but the final outcome can vary according to the environmental conditions experienced by developing animals (Müller et al., 2010). Most previous studies have been performed under optimal conditions, while our study is one of the few exploring effects of suboptimal conditions on growth and immune system of young chicks. "
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    ABSTRACT: Yolk testosterone concentrations vary in response to environmental conditions and different testosterone contents can subsequently modify the phenotypic traits of offspring. Apart from effects on growth, proactive behaviour and secondary sexual characteristics, possible negative impacts of maternal testosterone on the immune system are often considered a limitation for its deposition. Effects of maternal testosterone can be modulated by postnatal environmental conditions, such as the availability of food resources. However, the majority of studies considering the effects of maternal testosterone on the immune system have been conducted under optimum conditions. In our study we evaluated the influence of genetic selection for high (HET) and low (LET) egg testosterone content in Japanese quail on immune responsiveness of offspring to phytohaemagglutinin (PHA) and lipopolysaccharide (LPS) stimulation under severe protein restriction. Protein restriction negatively influenced body weight and performance in the PHA-test. We observed an increase in Cort (corticosterone) and He/Ly (heterophil/lymphocyte ratio) after LPS, while no changes occurred in total IgY levels in the protein-restricted group. HET quails showed higher body mass and total IgY levels and lower He/Ly ratio than LET quails, while the PHA index and Cort concentration did not differ between lines. No interactions were found between protein restriction and genetic line. In conclusion, the immune response was not compromised under conditions of severe protein restriction in the faster growing HET line compared with the LET line. We hypothesise that the immune responsiveness of birds with higher yolk testosterone may be linked with other maternally-derived substances in a context-dependent manner.
    Comparative Biochemistry and Physiology - Part A Molecular & Integrative Physiology 11/2014; 177. DOI:10.1016/j.cbpa.2014.07.020 · 2.37 Impact Factor
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    • "Once in the egg, androgens injected in the yolk and albumen may differ in the timing of embryonic uptake or metabolism by the developing embryos (von Engelhardt et al. 2009). Therefore, yolk and albumen steroids may differently interact with the processes of gonadal, HPG axis or brain formation, leading to variable short-and long-term effects according to experimental injection procedure (Carere & Balthazart 2007). "
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    ABSTRACT: Studies of avian species have shown that maternal effects mediated by the transfer of egg hormones can profoundly affect offspring phenotype and fitness. We previously demonstrated that the injection of a physiological amount of testosterone (T) in the eggs of ring-necked pheasants (Phasianus colchicus) disrupted the covariation among male morphological traits at sexual maturity and positively affected male mating success. Here, we investigate whether egg T exposure affected adult male circulating T levels at the onset of the breeding season (reflecting gonadal maturation), and the relationship between circulating T and male traits. Egg T exposure did not affect pre-mating plasma T. T levels were not associated with the expression of secondary sexual and non-sexual traits or socio-sexual behaviour (social rank, overall fighting ability and mating success). However, wattle brightness decreased with increasing circulating T in males hatched from T-eggs (T-males) but not among control males. In dyadic encounters during the peak mating period, control males with higher pre-mating T levels had higher chances of being dominant over other control males. However, higher pre-mating T levels did not predict success in male-male competition in encounters involving T-males. We suggest that the long-term effects of egg T on male phenotype do not originate from differential gonadal maturation according to egg T treatment. Rather, prenatal androgens may have priming effects on functioning of target tissues, translating into differential phenotypic effects according to androgen exposure during embryonic development.
    Ethology 01/2014; 120(1). DOI:10.1111/eth.12179 · 1.56 Impact Factor
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