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Reproductive success related to uropygial gland volume varies with abundance of conspecifics in barn swallows Hirundo rustica

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Abstract

Pathogens have negative effects on the fitness of their hosts, reducing survival and/or decreasing their reproductive success. To cope with pathogen challenge, animals have developed a variety of defensive traits to evade parasite infection and minimize their detrimental effects. Uropygial gland secretion has been proposed to have antimicrobial and antifungal properties, which may potentially influence bird fitness. However, whether uropygial gland secretion may affect the breeding success of birds remains unknown. Here, we explore whether the relationship between uropygial gland volume and reproductive success could be determined by the abundance of conspecific barn swallows (Hirundo rustica), a small colonial migratory hirundine. Because a larger number of swallows nesting within the same building may boost abundance and transmission of pathogens, we predicted that the anti-pathogen properties of uropygial gland secretion may enhance bird reproductive success in environments with high density of conspecifics. We showed that barn swallows with larger uropygial glands had higher breeding success (greater total number of fledglings reared) when living in environments with higher abundance of conspecifics. In contrast, barn swallows with larger uropygial glands had lower reproductive success when breeding in environments with lower abundance of conspecifics. Furthermore, we found that the same individuals did not modify uropygial glands in response to different pathogen pressure experienced across consecutive years. These outcomes suggest that benefits of uropygial secretion are host density dependent, thus consistent with this being a heritable trait that has evolved as a consequence of divergent selection imposed by pathogens.

Significance statement

To face pathogen challenges, animals have evolved a broad range of barriers and defense mechanisms to avoid parasite infection and/or to minimize negative effects. Uropygial gland secretion has been proposed to have antimicrobial and antifungal properties, but also act as a defensive mechanism against malaria infection. However, whether uropygial gland secretions may affect the reproductive success of birds remains poorly studied. In this study, we explore, for the first time, whether the relationship between uropygial gland volume and reproductive success could be determined by the abundance of conspecifics. We found that barn swallows with larger uropygial glands had higher breeding success when living in environments with higher abundance of conspecifics. Because a larger number of swallows nesting within the same building may boost abundance and transmission of pathogens, this novel outcome is consistent with a heritable trait that has evolved as a consequence of divergent selection imposed by pathogens.

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Acknowledgments

Charles R. Brown and two anonymous reviewers provided suggestions to improve the article. We thank Juan Sangran and his family, Borja Lora and his family, Plácido, and Marzal family for allowing us to work on their properties. Thanks also to Martin, Manuel, Antonio, Fernando, Javier, Gabriel, and all the other staff that work in the farms. We also thank Marina Bollo, Celia Vinagre-Izquierdo, and all students that participated through their help during fieldwork.

Funding

This study was funded by research projects of the Spanish Ministry of Economy and Competitiveness (CGL2015-64650P), Junta de Extremadura (IB16121), and Junta of Andalucía (P12-RNM-2144). SM was supported by a PhD grant from Ministry of Economy and Competition of Spain. CLC was supported by an operating grant from the Junta of Andalucía (P12-RNM-2144).

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Author notes

  1. Sergio Magallanes and Cosme López-Calderón contributed equally to this work.

Authors and Affiliations

  1. Department of Anatomy, Cellular Biology and Zoology, University of Extremadura, E-06006, Badajoz, Spain

    Sergio Magallanes, Florentino de Lope & Alfonso Marzal

  2. Department of Zoology, Faculty of Biology, Green Building, Avenue Reina Mercedes, E-41012, Seville, Spain

    Cosme López-Calderón & Javier Balbontín

  3. Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, FR-91405, Orsay Cedex, France

    Anders P. Møller

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  1. Sergio Magallanes
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Correspondence to Alfonso Marzal.

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All the experiments comply with the current laws of Spain, where the experiments were performed. Methods were evaluated and approved by institutional Commission of Bioethics of University of Extremadura (CBUE 49/2011) and by Junta de Extremadura Local Government (72/2016).

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Magallanes, S., López-Calderón, C., Balbontín, J. et al. Reproductive success related to uropygial gland volume varies with abundance of conspecifics in barn swallows Hirundo rustica. Behav Ecol Sociobiol 72, 183 (2018). https://doi.org/10.1007/s00265-018-2598-z

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