Gonadal steroid levels in rock pigeon eggs do not represent adequately maternal allocation

Kumar, Neeraj; Faassen, Martijn van; Vries, Bonnie de; Gahr, Manfred; Groothuis, Ton G. G.

doi:10.1038/s41598-018-29478-4

Cited by 11 publications

(5 citation statements)

References 24 publications

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“…Alternatively, the embryonic activity could have been responsible for activating maternal enzymes in the yolk. However, in another study on rock pigeon we did not find any evidence for presence of maternal enzymes in the yolk (Kumar et al, 2018).…”

Section: Discussioncontrasting

confidence: 67%

Early embryonic modification of maternal hormones differs systematically among embryos of different laying order: A study in birds

Kumar

Faassen

Gahr

et al. 2018

General and Comparative Endocrinology

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Vertebrate embryos are exposed to maternal hormones that can profoundly affect their later phenotype. Although it is known that the embryo can metabolize these maternal hormones, the metabolic outcomes, their quantitative dynamics and timing are poorly understood. Moreover, it is unknown whether embryos can adjust their metabolic activity to, for example, hormones or other maternal signals. We studied the dynamics of maternal steroids in fertilized and unfertilized rock pigeon eggs during early incubation. Embryos of this species are naturally exposed to different amounts of maternal steroids in the egg according to their laying position, which provides a natural context to study differential embryonic regulation of the maternal signals. We used mass spectrometric analyses to map changes in the androgen and estrogen pathways of conversion. We show that the active hormones are heavily metabolized only in fertilized eggs, with a corresponding increase in supposedly less potent metabolites already within one-fourth of total incubation period. Interestingly, the rate of androgen metabolism was different between embryos in different laying positions. The results also warrant a re-interpretation of the timing of hormone mediated maternal effects and the role of the supposedly biologically inactive metabolites. Furthermore, the results also provide a potential solution as to how the embryo can prevent maternal steroids in the egg from interfering with its sexual differentiation processes as we show that the embryo can metabolize most of the maternal steroids before sexual differentiation starts.

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Section: Discussioncontrasting

confidence: 67%

Early embryonic modification of maternal hormones differs systematically among embryos of different laying order: A study in birds

Kumar

Faassen

Gahr

et al. 2018

General and Comparative Endocrinology

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“…In brief, nests were located by visually searching for the bulky nest structure of robins; when located, the contents were examined using a telescopic mirror. Because maternal investment into egg yolks, including yolk hormones, can vary with laying order (e.g., Schwabl 1993 , but see Kumar et al. 2018 ), we aimed to standardize our study by only using nests where the identity of the first laid egg was known for collection and yolk analyses (see below); therefore, we monitored several mid-construction and completed but empty nests prior to the first egg appearing.…”

Section: Methodsmentioning

confidence: 99%

Inter-Individual Variation in Anti-Parasitic Egg Rejection Behavior: A Test of the Maternal Investment Hypothesis

Hauber

Āboliņš-Ābols

Kim

et al. 2020

Integrative Organismal Biology

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Synopsis Hosts of avian brood parasites may reduce or forego the costs of caring for foreign young by rejecting parasitic eggs from the nest. Yet, many host species accept parasitic eggs and, even among rejecter species, some individuals go on to incubate and hatch them. The factors explaining the variation in egg rejection between species have received much theoretical and empirical attention, but the causes of intraspecific variation in different individuals’ propensity for accepting parasitic eggs are less well understood. Here we tested the maternal investment hypothesis, which predicts that hosts with costlier clutches will be more likely to reject parasitic eggs from their nest. We studied variation in the egg rejection responses of American robins (Turdus migratorius), a robust egg-rejecter host of the brood parasitic brown-headed cowbird (Molothrus ater), to 3D-printed cowbird-sized eggs which were painted dark blue, a color known to induce variable and repeatable egg rejection responses in individual robins. Costlier clutch investment was estimated by earlier laying date, larger clutch size, heavier unincubated yolk mass, and variable yolk steroid hormone concentrations. There was no statistical support for most of our predictions. However, we detected more concentrated and greater overall amount of deoxycorticosterone deposited in egg yolks of rejecters relative to acceptors, although this accounted for no more than 14% of variance in the data. Future work should test experimentally the potential physiological linkage between maternal egg yolk steroid investment and egg rejection propensity in this and other host species of avian brood parasites.

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“…as used in [38,62 -64]). Finally, a recent study revealed that maternal hormones are already partly metabolized in the oviduct after ovulation [59]. This provides another hurdle for the interpretation and experimentation with maternal hormones, as levels measured at oviposition may not adequately reflect what the mother initially deposited in the egg.…”

Section: (C) What Is In An Egg? Challenges and Advances In The Measurement Of Yolk Hormonesmentioning

confidence: 99%

Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model

Groothuis

Hsu

Kumar

et al. 2019

Phil. Trans. R. Soc. B

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105

129

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Maternal effects can adaptively modulate offspring developmental trajectories in variable but predictable environments. Hormone synthesis is sensitive to environmental factors, and maternal hormones are thus a powerful mechanism to transfer environmental cues to the next generation. Birds have become a key model for the study of hormone-mediated maternal effects because the embryo develops outside the mother's body, facilitating the measurement and manipulation of prenatal hormone exposure. At the same time, birds are excellent models for the integration of both proximate and ultimate approaches, which is key to a better understanding of the evolution of hormone-mediated maternal effects. Over the past two decades, a surge of studies on hormone-mediated maternal effects has revealed an increasing number of discrepancies. In this review, we discuss the role of the environment, genetic factors and social interactions in causing these discrepancies and provide a framework to resolve them. We also explore the largely neglected role of the embryo in modulating the maternal signal, as well as costs and benefits of hormone transfer and expression for the different family members. We conclude by highlighting fruitful avenues for future research that have opened up thanks to new theoretical insights and technical advances in the field. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine’.

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Gonadal steroid levels in rock pigeon eggs do not represent adequately maternal allocation

Cited by 11 publications

References 24 publications

Early embryonic modification of maternal hormones differs systematically among embryos of different laying order: A study in birds

Early embryonic modification of maternal hormones differs systematically among embryos of different laying order: A study in birds

Inter-Individual Variation in Anti-Parasitic Egg Rejection Behavior: A Test of the Maternal Investment Hypothesis

Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model

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