Abstract
Phenotypic differentiation is common among populations that have large geographic distributions. One proposed mechanism driving phenotype divergence is sexual selection, which predicts that trait differences among closely related populations are underlain by variation in reproductive performance. Here, we examined a population of Asian Barn Swallows (Hirundo rustica gutturalis) in northeastern China. We ask whether traits shown to be under divergent sexual selection in other Barn Swallow populations are under sexual selection in this north Asian population by determining whether two features of phenotype variation, tail streamer length and ventral plumage colouration (including both throat and belly regions), are sexually dimorphic, associated with patterns of assortative mating and predictive of reproductive success. In this population, the length of tail streamers did not correlate with ventral plumage colouration in either males or females. The length of tail streamers was sexually dimorphic, but we did not find assortative mating by tail streamer length. By contrast, we found no sexual dichromatism but we did find assortative mating by throat colouration. Our correlational results indicated that the breeding performance of male Barn Swallows was associated with differences in their ventral plumage colouration, suggesting that ventral plumage colouration is likely a target of sexual selection in this population. Our finding that tail streamer length is unlikely to be under sexual selection is consistent with studies of other H. rustica gutturalis populations. The result that ventral plumage colour is likely to be under sexual selection is partially consistent with previous studies on Japanese H. rustica gutturalis, in which male throat but not belly plumage colour is the sexually selected trait.
Zusammenfassung
Die Bauchfärbung, nicht die Länge der äu ßeren Schwanzfedern ist assoziiert mit der saisonalen Reproduktionsleistung einer chinesischen Population von Rauschwalben ( Hirundo rustica gutturalis ).
Phänotypische Differenzierung ist verbreitet zwischen Populationen mit einer weiten geografischen Verbreitung. Ein möglicher Mechanismus, der die phänotypische Divergenz antreibt, ist die sexuelle Selektion, die bestimmt, dass der Merkmalsausprägung zwischen nah verwandten Populationen die Variation der Reproduktionsleistung zugrunde liegt. In der vorliegenden Studie untersuchten wir eine Population asiatischer Rauchschwalben (Hirundo rustica gutturalis) in Nordostchina. Wir gingen der Frage nach, inwiefern Eigenschaften, die sich unter sexueller Selektion in anderen Rauchschwalbenpopulationen divergent zeigten, in dieser untersuchten nordasiatischen Population sexuell selektiert wurden. Wir bestimmten, ob zwei Eigenschaften der phänotypischen Variation, die Länge der äußeren Schwanzfedern und die Farbe des Bauchgefieders (inklusive Kehle und Bauchregionen) geschlechtsdimorph sind, im Zusammenhang mit Mustern der assortativen Verpaarung und prognostiziertem Bruterfolg. In der untersuchten Population korrelierte die Länge der äußeren Schwanzfedern weder bei Männchen noch bei Weibchen mit der Färbung des Bauchgefieders. Die Länge der äußeren Schwanzfedern war bei den Geschlechtern unterschiedlich, jedoch fanden wir keine assortative Verpaarung über die Schwanzlänge. Dagegen fanden wir keinen Geschlechtsdichromatismus, allerdings eine assortative Verpaarung über die Kehlfärbung. Unsere korrelierenden Ergebnisse zeigen, dass die Brutleistung männlicher Rauchschwalben assoziiert war mit Unterschieden in der Färbung ihres Bauchgefieders. Dies deutet darauf hin, dass die Farbe der Bauchfedern möglicherweise ein Ziel der sexuellen Selektion in dieser Population ist. Die Länge der äußeren Schwanzfedern unterliegt wahrscheinlich nicht der sexuellen Selektion. Dies ist konsistent mit Studien an anderen H. rustica gutturalis Populationen. Die wahrscheinlich der sexuellen Selektion unterliegende Bauchgefiederfärbung ist in Teilen übereinstimmend mit früheren Untersuchungen an japanischen Rauchschwalben, in denen die Kehlfärbung der Männchen, jedoch nicht die Bauchfärbung die sexuell selektierte Eigenschaft ist.
Similar content being viewed by others
References
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. 2015 67:48 https://doi.org/10.18637/jss.v067.i01
Bro-Jørgensen J (2010) Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol Evol 25:292–300
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595
Clutton-Brock T (2009) Sexual selection in females. Anim Behav 77:3–11. https://doi.org/10.1016/j.anbehav.2008.08.026
Costanzo A et al (2017) Lifetime reproductive success, selection on lifespan, and multiple sexual ornaments in male European Barn Swallows. Evolution 71:2457–2468. https://doi.org/10.1111/evo.13312
Coyne JA, Orr HA (2004) Speciation. Freeman, New York
Cuthill IC, Partridge JC, Bennett AT, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214
Dor R, Safran RJ, Sheldon FH, Winkler DW, Lovette IJ (2010) Phylogeny of the genus Hirundo and the Barn Swallow subspecies complex. Mol Phylogenet Evol 56:409–418
Eikenaar C, Whitham M, Komdeur J, Van der Velde M, Moore IT (2011) Testosterone, plumage colouration and extra-pair paternity in male North-American Barn Swallows. PLoS One 6:e23288
Evans MR (1998) Selection on swallow tail streamers. Nature 394:233–234
Hasegawa M, Arai E (2013) Differential female access to males with large throat patches in the Asian Barn Swallow Hirundo rustica gutturalis. Zool Sci 30:913–918. https://doi.org/10.2108/zsj.30.913
Hasegawa M, Arai E (2017) Negative interplay of tail and throat ornaments at pair formation in male Barn Swallows. Behaviour 154:835–851
Hasegawa M et al (2010a) Low level of extra-pair paternity in a population of the Barn Swallow Hirundo rustica gutturalis. Ornithol sci 9:161–164
Hasegawa M, Arai E, Watanabe M, Nakamura M (2010b) Mating advantage of multiple male ornaments in the Barn Swallow Hirundo rustica gutturalis. Ornithol Sci 9:141–148. https://doi.org/10.2326/osj.9.141
Hasegawa M, Arai E, Watanabe M, Nakamura M (2017) Reproductive advantages of multiple female ornaments in the Asian Barn Swallow Hirundo rustica gutturalis. J Ornithol 158:517–532. https://doi.org/10.1007/s10336-016-1401-z
Jiang Y, Bolnick DI, Kirkpatrick M (2013) Assortative mating in animals. Am Nat 181:E125–E138
Kleven O, Jacobsen F, Izadnegahdar R, Robertson RJ, Lifjeld JT (2006) Male tail streamer length predicts fertilization success in the North American Barn Swallow (Hirundo rustica erythrogaster). Behav Ecol Sociobiol 59:412–418
Kojima W, Kitamura W, Kitajima S, Ito Y, Ueda K, Fujita G, Higuchi H (2009) Female Barn Swallows gain indirect but not direct benefits through social mate choice. Ethology 115:939–947
Liu Y (2017) Sexual selection strategy of northeastern Chinese Barn Swallows (Hirundo rustica). Queen Mary University of London, London
Maan ME, Seehausen O (2011) Ecology, sexual selection and speciation. Ecol Lett 14:591–602
Møller AP (1990) Male tail length and female mate choice in the monogamous swallow Hirundo rustica. Anim Behav 39:458–465
Møller AP (1991) Sexual selection in the monogamous Barn Swallow (Hirundo rustica). I. Determinants of tail ornament size. Evolution 45:1823–1836
Møller AP (1992) Sexual selection in the monogamous Barn Swallow (Hirundo rustica). II. Mechanisms of sexual selection. J Evol Biol 5:603–624
Møller AP (1993) Sexual selection in the Barn Swallow Hirundo rustica. III. Female tail ornaments. Evolution 1:417–431
Møller AP (1994) Sexual selection and the Barn Swallow. Oxford University Press, Oxford
Neuman C, Safran R, Lovette I (2007) Male tail streamer length does not predict apparent or genetic reproductive success in North American Barn Swallows Hirundo rustica erythrogaster. J Avian Biol 38:28–36
Panhuis TM, Butlin R, Zuk M, Tregenza T (2001) Sexual selection and speciation. Trends Ecol Evol 16:364–371. https://doi.org/10.1016/S0169-5347(01)02160-7
R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ritchie MG (2007) Sexual selection and speciation. Annu Rev Ecol Evol Syst 38:79–102
Romano A, Costanzo A, Rubolini D, Saino N, Møller AP (2017) Geographical and seasonal variation in the intensity of sexual selection in the Barn Swallow Hirundo rustica: a meta-analysis. Biol Rev 92:1582–1600
Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352
Safran RJ, McGraw KJ (2004) Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American Barn Swallows. Behav Ecol 15:455–461
Safran R, Neuman C, McGraw K, Lovette I (2005) Dynamic paternity allocation as a function of male plumage color in Barn Swallows. Science 309:2210–2212
Safran RJ, McGraw KJ, Wilkins MR, Hubbard JK, Marling J (2010) Positive carotenoid balance Correlates with greater reproductive performance in a wild bird. PLoS One 5:e9420. https://doi.org/10.1371/journal.pone.0009420
Safran RJ, Scordato ESC, Symes LB, Rodríguez RL, Mendelson TC (2013) Contributions of natural and sexual selection to the evolution of premating reproductive isolation: a research agenda. Trends Ecol Evol 28:643–650. https://doi.org/10.1016/j.tree.2013.08.004
Safran RJ, Vortman Y, Jenkins BR, Hubbard JK, Wilkins MR, Bradley RJ, Lotem A (2016) The maintenance of phenotypic divergence through sexual selection: an experimental study in Barn Swallows Hirundo rustica. Evolution 70:2074–2084
Saino N, Primmer CR, Ellegren H, Møller AP (1997) An experimental study of paternity and tail ornamentation in the Barn Swallow (Hirundo rustica). Evolution 51:562–570
Scordato ES, Safran RJ (2014) Geographic variation in sexual selection and implications for speciation in the Barn Swallow. Avian Res 5:8
Servedio MR (2016) Geography, assortative mating, and the effects of sexual selection on speciation with gene flow. Evol Appl 9:91–102. https://doi.org/10.1111/eva.12296
Svensson L, Mullarney K, Zetterstrom D, Grant PJ (2011) Collins bird guide. HarperCollins, London
Tobias JA, Montgomerie R, Lyon BE (2012) The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Philos Trans R Soc B Biol Sci 367:2274–2293. https://doi.org/10.1098/rstb.2011.0280
Tomás G (2015) Hatching date vs. laying date: what should we look at to study avian optimal timing of reproduction? J Avian Biol 46:107–112. https://doi.org/10.1111/jav.00499
Turner A (2006) The Barn Swallow. Black, London
Vortman Y, Lotem A, Dor R, Lovette IJ, Safran RJ (2011a) The sexual signals of the East-Mediterranean Barn Swallow: a different swallow tale. Behav Ecol 22:1344–1352
Vortman Y, Lotem A, Dor R, Lovette IJ, Safran RJ (2011b) The sexual signals of the East-Mediterranean Barn Swallow: a different swallow tale. Behav Ecol 22:1344–1352
Vortman Y, Lotem A, Dor R, Lovette I, Safran RJ (2013) Multiple sexual signals and behavioral reproductive isolation in a diverging population. Am Nat 182:514–523
Zheng Z (1987) A synopsis of the avifauna of China. Science Press, Beijing
Zink RM, Pavlova A, Rohwer S, Drovetski SV (2006) Barn Swallows before barns: population histories and intercontinental colonization. Proc R Soc Lond B Biol Sci 273:1245–1251
Acknowledgements
We thank Prof. Zhengwang Zhang and colleagues of the Avian Research Group for generous facilities in the College of Life Sciences, Beijing Normal University. We are also grateful to Prof. Stephen Rossiter, Prof. Richard Nichols, Prof. Tim Blackburn and Dr Jon Blount for their guidance on Yu Liu’s Ph.D. project, of which this study is a part. Financial support was provided by the China Scholarship Council and Queen Mary, University of London. The experiments comply with the current laws of China, where they were performed. We are grateful to two anonymous reviewers whose comments helped improve the clarity of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by O. Krüger.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Liu, Y., Scordato, E.S.C., Safran, R. et al. Ventral colour, not tail streamer length, is associated with seasonal reproductive performance in a Chinese population of Barn Swallows (Hirundo rustica gutturalis). J Ornithol 159, 675–685 (2018). https://doi.org/10.1007/s10336-018-1555-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-018-1555-y