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

Neeraj Kumar,Ton G G Groothuis,Martijn Van Faassen,Ido Kema,Manfred Gahr,Bonnie De Vries

doi:10.1038/s41598-018-29478-4

Abstract

Maternal hormones deposited in the egg can provide a powerful model for the study of maternal effects. The differential amount of maternal hormones in the yolk of freshly laid eggs is assumed to represent differential maternal allocation. However, some evidence suggests that these amounts do not reflect maternal allocation that in fact takes place before ovulation. We compared the amounts of a wide array of gonadal steroids and their metabolites in the yolk of pre-ovulatory follicles with those of freshly laid eggs of rock pigeons using mass spectrometry. We found that between the follicle and egg stages the levels of progesterone increase whereas androstenedione and testosterone decrease in which the strength of decrease was dependent on the laying order of the egg. For conjugated estrone the change between follicle and egg differed in direction for first and second laying position yielding a significant interaction effect. For conjugated testosterone the interaction did not reach but was close to significance. This extremely early steroid metabolism was not due to maternal enzymes in the yolk as indicated by incubation of pre-ovulatory yolks treated with proteinase-K, a protein digesting enzyme. The results have significant consequences for the functional and evolutionary interpretation as well as experimental manipulation of hormone-mediated maternal effects.

Highlights

Maternal hormone deposition in eggs of oviparous species is recognized as a maternal tool to adjust offspring phenotype to the current or future environment of the offspring[1,2,3,4]
The variation in yolk hormone levels is assumed to be due to differential maternal hormone deposition depending on some context, for instance the laying order of eggs, mate quality, social hierarchy of the female within a group, seasonal variation in predation risk, food availability, etc
If the early decrease in hormone concentrations before oviposition is due to dilution with albumen and water, the total amount of hormones deposited in the ovarian follicle should be the same as in the whole egg at oviposition, only its concentration should decrease

Summary

Introduction

Maternal hormone deposition in eggs of oviparous species is recognized as a maternal tool to adjust offspring phenotype to the current or future environment of the offspring[1,2,3,4]. The above-mentioned decline in some yolk hormone concentrations between the time of ovulation and oviposition could potentially be explained by (1) the addition of albumen and water, diluting the maternal deposited hormone concentrations, or (2) very early metabolic processes. Such metabolic processes have been found after oviposition by developing embryos upon egg incubation[8,9,10,11] but whether this occurs already before oviposition in the reproductive track of the mother has not yet been tested. We investigated the role of maternal enzymes in the yolk for the postulated early steroid metabolism by incubating follicle yolks treated with Proteinase-K that digests the maternal protein enzymes

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Conclusion