Extra-pair paternity patterns in European barn swallows Hirundo rustica are best explained by male and female age rather than male ornamentation
Adaptive explanations for the evolution of extra-pair paternity (EPP) in birds often assume cuckolding males to be better-ornamented than cuckolded males. Several studies have confirmed that either male sexual ornamentation is associated with EPP or that phenotypes of cuckolded and cuckolding males differ. Expression of male ornamentation may change with age; however, a recent meta-analysis has identified age itself as an important factor that differed in cuckolding and cuckolded males. The age of social female partner may also affect EPP, though this has received little attention. Here, by using detailed data on age of individual barn swallows (Hirundo rustica rustica), we identified age as the major predictor of male and female promiscuity. Our results revealed that, whereas a male’s ability to obtain an extra-pair mate increased linearly with age, the only predictor of the probability of a male being cuckolded was the age of his social partner, with older females engaging more frequently in EPP. In contrast, male ornamentation was not significantly related to EPP pattern. Tarsus length was the sole significant phenotypic trait in comparison between cuckolding and cuckolded males. Our data provide little support for the hypothesis that extra-pair mate choice in our barn swallow population was ornament driven. This may indicate either a non-adaptive scenario for EPP, for example with older males better able to coerce females into copulation, or EPP mating based on other than absolute mate-choice criteria associated with the expression of male ornamentation.
We analysed patterns of extra-pair paternity (EPP) in barn swallows. Derived from observation of 160 nests, our results appear to differ from the findings of some previous studies that identified ornamental traits as being associated with extra-pair and within-pair paternity (WPP) in this iconic model taxon of sexual selection. In particular, tail streamer length had no detectable association with WPP or a male’s ability to obtain an extra-pair partner. Pairwise comparisons of cuckolded and cuckolding males, involving 76 mixed paternity nests, also supported the hypothesis that male ornamentation does not play a role in determining EPP patterns in the focal barn swallow population. When statistically controlled for clutch initiation date, the probability of obtaining an extra-pair partner only increased with increasing age of males, while WPP was only associated with the age of their female social partners. Our data provide little support for the hypothesis that extra-pair mate choice in our barn swallow population is ornament driven and indicated that age, rather than ornaments, would be a better predictor of paternity.
KeywordsExtra-pair fertilisations Within-pair paternity EPP Sexual ornamentation Sexual selection Tail streamer length
We would like to thank J. Cepák, A. Hund, J. Hubbard, P. Munclinger and A. Petrželková for help in the field. Kevin Roche provided valuable comments on the manuscript and proofread the final text. This study would not have been possible without the collaboration of the Kotrba family at Hamr farm, the Kraus family at Šaloun farm and the Pulec family. We would also like to thank the Associate Editor and anonymous reviewers for their insightful comments on the paper.
TA conceived and designed the study; MA and OT undertook ornament analysis; RM, TA, OT, MA and JK performed the fieldwork; RM and JK conducted paternity analysis. TA and RM carried out the statistical analysis; RM and TA wrote the manuscript. All co-authors contributed to the final version of the manuscript and gave approval for its publication.
This research was funded through Project GA15-11782S and 19-22538S of the Czech Science Foundation.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflicts of interest.
This study complied with all applicable international, national and/or institutional guidelines on the use of animals. All protocols were non-invasive and adhered to the laws and guidelines of the Czech Republic (Czech Research Permit Numbers 6628/2008-10001). All protocols were approved by the Animal Care and Use Committees at the Czech Academy of Sciences (041/2011) and Charles University in Prague (4789/2008-30).
- Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9:855–868Google Scholar
- Bartoń K (2016) MuMIn: multi-model inference. R package version 1.15.6, https://CRAN.R-project.org/package=MuMIn
- Costanzo A, Ambrosini R, Caprioli M, Gatti E, Parolini M, Canova L, Rubolini D, Romano A, Gianfranceschi L, Saino N (2017b) Lifetime reproductive success, selection on lifespan, and multiple sexual ornaments in male European barn swallows. Evolution 71:2457–2468PubMedCrossRefPubMedCentralGoogle Scholar
- Maia R, Eliason CM, Bitton PP, Doucet SM, Shawkey MD (2013) pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol 4:906–913Google Scholar
- Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, OxfordGoogle Scholar
- Ninni P (2003) Carotenoid signals in barn swallows. PhD thesis, Université Pierrre et Marie Curie, Paris, FranceGoogle Scholar
- Turner A (2006) The barn swallow. T & AD Poyser, LondonGoogle Scholar