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Age-related patterns of yolk androgen deposition are consistent with adaptive brood reduction in spotless starlings

  • Jaime MurielEmail author
  • Lorenzo Pérez-Rodríguez
  • Diego Gil
Original Article

Abstract

Female birds can influence offspring development by adjusting egg size or by a differential allocation of egg resources. Such maternal effects can be expected to be shaped by natural selection, given the costs connected to the allocation of maternal resources. Among egg components, yolk androgens play an important role in affecting offspring life-history traits. Despite their relevance for nestling development, factors accounting for the observed within- and between-clutch variation are still poorly known. By using a cross-sectional sampling approach, we tested the effect of female age, laying order and laying date on the deposition of yolk androstenedione (A4) and testosterone (T), since young and older females could maximize their fitness differently according to breeding conditions. We found a remarkable lack of differences in overall yolk androgen levels across different ages. However, comparing first-year with older females, our results showed that age did not influence yolk T levels at the beginning of the breeding season, whereas at the end, first-year females transferred lower hormone levels than older females. Within clutches, both androgens increased across the laying sequence, suggesting that late nestlings benefit from an increased allocation that could compensate hatching asynchrony. However, when considering A4, we found that, whereas older females always increased A4 levels across the laying sequence, first-year females did not increase it at the end of the breeding season, thus increasing the likelihood of brood reduction when environmental conditions became hardest. These findings suggest that yolk A4 variation may be particularly important at the within-clutch scale, by providing females with a tool to modify nestling hierarchies.

Significance statement

The study of maternal effects shows that avian mothers can adjust offspring development to environmental conditions by altering egg composition. The effects of maternal age on such egg allocation process depend on the balance of benefits and costs that affects each age class. We examine if young and older mothers differ in terms of yolk androgen deposition and egg quality, since age may influence offspring fitness, and could represent a costly maternal investment. We found an absence of overall age-dependent patterns in yolk androgen deposition, except when we considered laying order and laying date. In late clutches, when breeding conditions are harsher, 1-year-old females carried out a lower deposition of both resources (yolk mass) and modifiers (androgens) than older mothers did. We suggest that such a pattern would reinforce the effects of hatching asynchrony, favouring brood reduction at the end of the breeding season by first-year females.

Keywords

Yolk androstenedione Yolk testosterone Age-specific pattern Prenatal investment Maternal effects Sturnus unicolor 

Notes

Acknowledgements

We are very grateful to all the volunteers who helped to collect data over the completely breeding season. We also thank the two anonymous journal reviewers and Associate Editor for their invaluable comments on earlier drafts of the article. This study is a contribution to the research developed at the ‘El Ventorrillo’ field station.

Funding information

The project was funded by projects CGL2011-26318 to DG (Ministerio de Economía y Competitividad) and PGC2018-099596-B-I00 to LP-R (Ministerio de Ciencia, Innovación y Universidades, co-financed by the European Regional Development Fund -ERDF). JM was supported by a postdoctoral contract from the University of Extremadura (Junta de Extremadura—IB16121) and a postdoctoral grant from the Juan de la Cierva Subprogram (FJCI-2017-34109), with the financial sponsorship of the MICINN. LP-R was supported by a postdoctoral contract for accessing the Spanish System of Science, Technology and Innovation (SECTI) from the University of Castilla-La Mancha.

Compliance with ethical standards

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. Our study was in accordance with ethical approval from the Spanish ethics committee since eggs were removed before the incubation and the corresponding embryonic development began (RD 53/2013). Capture and manipulation of birds were authorized 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). Permission to work in the area was granted by both the Parque Regional de la Cuenca Alta del Manzanares and the Ayuntamiento de Soto del Real, Spain.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2019_2770_MOESM1_ESM.docx (282 kb)
ESM 1 (DOCX 281 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Anatomía, Biología Celular y ZoologíaUniversidad de ExtremaduraBadajozSpain
  2. 2.Instituto Pirenaico de Ecología—IPE (CSIC)JacaSpain
  3. 3.Instituto de Investigación en Recursos Cinegéticos—IREC (CSIC, UCLM, JCCM)Ciudad RealSpain
  4. 4.Departamento de Ecología EvolutivaMuseo Nacional de Ciencias Naturales (MNCN-CSIC)MadridSpain

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