Prenatal manipulation of yolk androgen levels affects egg size but not egg colour in a songbird

Abstract

Maternal allocation of androgens to the egg yolk allows mothers to adaptively manipulate offspring phenotype. Increases of egg androgen levels have often been shown to induce sex-specific effects. Some previous studies suggest that females specifically may suffer a fitness reduction after early exposure to high androgen levels. In this study, we explored whether female birds that developed exposed to high yolk androgen concentrations would reduce their maternal investment later in life. We explored two different aspects of female reproduction in spotless starlings (Sturnus unicolor): egg coloration (a post mating sexual signal in this species) and egg size. We manipulated androgen yolk levels in a large sample of clutches of this species. We monitored the reproduction of the females that hatched from these eggs, measuring the size and colour of the eggs they laid throughout their life (from 1 to 7 years of age). We found no overall difference in egg colour in relation to treatment, clutch number or age. However, females exposed to high egg androgen levels showed a steeper decrease in egg size along the laying order than controls. This pattern likely results in a more unbalanced distribution of resources within the clutch, possibly favouring brood size reductions in experimental females. In addition, control and experimental females differed in how egg volume changed with age. These results show that some egg characteristics may be affected by the female’s exposure to yolk androgens during her own embryonic development. Our research calls for further long-term research on the influence of prenatal androgens on the fitness mechanisms regulating reproductive investment and its potential signalling role in a perspective of sexual selection.

Significance statement

In birds, mothers prepare the offspring to the environment they will encounter at hatching by depositing a mixture of compounds into the eggs. Androgens specifically exert a variety of effects during embryo development and chick growth, but some of these may be negative in adult life. In particular, early androgen may be detrimental for females in the long term, decreasing maternal investment and fitness. Using the spotless starling as study species, we tested whether an experimental increase in yolk androgens negatively affects breeding investment, measured by egg colour (a sexual signal) and egg size. We found no effects of the treatment on egg colour. However, females exposed to high androgen levels during their development reduced egg size along the laying order more strongly than controls. This may affect nestling survival, and indicates that prenatal yolk androgens may influence some egg characteristics with known relevance for offspring viability.

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Data availability

The datasets generated and/or analysed during the current study are available in the Figshare repository, at the permanent link: https://doi.org/10.6084/m9.figshare.13574312.v1.

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Acknowledgments

We would like to thank two anonymous reviewers for their valuable comments that have substantially improved the manuscript. We are very grateful to all the people that have contributed to collating the data presented in this study, including field technicians: Oscar Magaña, Hector Bintanel and Lara Moreno; MSc students: Blanca Jimeno, Louise Froud, Elodie Faux, Irene García Celada, Thomas Crouchet and Pablo Salmón; and volunteers: Lucia Manzanares, Robyn Womack, Cristiano Gala, Evan Burnett, Hannah van Noordt, Benoit Vallas, Joao Heriberto de Oliveira, Angelica Camacho, Jorge Garcia Campa, Lara de la Cita, Aida Rodrigues and Simon Degrise. This study is a contribution to the research developed at “El Ventorrillo” field station.

Funding

This paper is the result of a long-term study financed by a series of research grants by the Spanish Ministerio de Ciencia, Innovación y Universidades to DG (refs.: CGL2008-03501/BOS, CGL2011-26318 and CGL2017-83843-C2-1-P) and LP-R (ref.: PGC2018-099596-B-I00, co-financed by the European Regional Development Fund -ERDF-). From 2009 to 2013, JM was supported by a FPI grant (BES-2009-021383) from the ICINN and currently by a postdoctoral grant from the Juan De La Cierva Subprogram (FJCI-2017-34109), with the financial sponsorship of the MICINN. RM was funded by a Marie Skłodowska Curie Action within the Horizon 2020 Initiative from the European Commission.

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Correspondence to Stefania R. D’Arpa.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed (RD 53/2013). Capture and manipulation of birds were authorised by the Consejería de Medio Ambiente (Comunidad de Madrid, Spain) under licence from the Spanish institutional authorities (Consejería de Medio Ambiente and Centro de Migración de Aves de SEO/BirdLife). The androgen manipulation experiment complies with the animal laws in Spain in 2011 (Real Decreto 1201/2005, 10-10-2005). Permission to work in the area was granted by both the Parque Regional de la Cuenca Alta del Manzanares (Consejería de Medio Ambiente de la Comunidad Autónoma de Madrid: Ref. 10/129049.9/11) and the Ayuntamiento de Soto del Real, Spain.

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Communicated by M. Leonard

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D’Arpa, S.R., Muriel, J., Monclús, R. et al. Prenatal manipulation of yolk androgen levels affects egg size but not egg colour in a songbird. Behav Ecol Sociobiol 75, 52 (2021). https://doi.org/10.1007/s00265-021-02991-9

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Keywords

  • Maternal effects
  • Androgens
  • Biliverdin
  • Egg coloration
  • Post mating sexual selection