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Evolution of short tails and breakdown of honest signaling system during a severe winter in the Pacific swallow Hirundo tahitica

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Abstract

In dynamic selection regimes, an honest signal that indicates high quality in favorable environments might be negatively related to quality in unfavorable environments, though empirical evidence is scarce. Here, we studied the relationship between plumage ornaments and physiological state in the Pacific swallow Hirundo tahitica on Amami Oshima Island in 2 years with contrasting weather conditions: a once-in-a-century severe winter and a mild winter in the following year. Previous studies have shown that, during the severe winter, many Pacific swallows, particularly those with long tails, died whereas no carcasses were found in the next year, indicating relaxed selection during mild years. Here we showed that after the severe winter, the offspring generation had shorter tails than the parental generation, which could not be explained by age or yearly difference in tail length, indicating the evolution of short tails. Moreover, the relationship between tail length and body condition differed between years: longer-tailed swallows had a better body condition in the mild winter, whereas the reverse tendency was found in the severe winter. A similar relationship was found between plasma corticosterone level, an indicator of physiological stress, and tail length (i.e., swallows with longer tails tended to have lower corticosterone levels during the mild winter while the reverse pattern was found during the severe winter). In contrast, another plumage ornament, pheomelanin pigmentation, was positively linked to body condition during the two study years and had no detectable relationship with the plasma corticosterone levels. Differences in the relationship between specific plumage traits and physiology may help to explain the diversity of tail length and plumage coloration in hirundines.

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Acknowledgements

We greatly appreciate all house owners who allowed us to study Pacific swallows in their houses. We also thank Dr. Taku Mizuta for managing our field study. We appreciate Dr. Nobuyuki Kutsukake and lab members of the Laboratory of Evolutionary Studies of Biosystems, Sokendai. We thank Drs. Yohei Terai, Takahiro Kato, and Mrs. Yukiko Nakanishi for their technical support on laboratory experiments. MH was supported by a Research Fellowship of the Japan Society for the Promotion of Science (JSPS, 15J10000).

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MH conceived the research and wrote the draft, EA and MH collected field data and did the ELISA assays; SI and KW helped EA to do pigment analysis. All co-authors contributed to manuscript writing.

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Correspondence to Masaru Hasegawa.

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Data will be archiving to Dryad.

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The permits for the current study including capturing, measurements, blooding and feather collection were provided by Kagoshima Prefecture in Japan (#163 and #143 in 2016 and 2017, respectively), following the Wildlife Protection and Hunting Management Law.

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Hasegawa, M., Arai, E., Ito, S. et al. Evolution of short tails and breakdown of honest signaling system during a severe winter in the Pacific swallow Hirundo tahitica. Evol Ecol 33, 403–416 (2019). https://doi.org/10.1007/s10682-019-09978-z

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