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Extrapair mating opportunity explains the evolutionary transition between the presence and absence of tail ornamentation in swallows

Abstract

Evolutionary drivers of the gain and loss of ornamentation are often unclear even for classic ornamentation such as swallows’ tails, because macroevolutionary analysis, which is needed to clarify the factors responsible for the transition, is rarely conducted. Some behavioural experiments support the hypothesis that sexual selection is responsible for the evolution of “forked” tails, while others support the hypothesis that foraging on large prey favours the evolution of forked tails. However, empirical tests of these hypotheses used already-ornamented species and macroevolutionary studies of forked/forkless tails, which is critical for inferring the evolutionary forces driving the transition between the presence and absence of ornamentation, are still lacking. Here, using a clade of swallows and martins (Aves: Hirundininae), we examined the evolutionary transition between forkless and forked tails in relation to measures of foraging mode and sexual selection. We found replicated evolution of forkless tails from forked tails, all in clades with sexually monomorphic plumage. Furthermore, we detected correlated evolution of tail shape (i.e., forkless/forked) and extrapair mating opportunity, measured as incubation type which is tightly linked to extrapair paternity both within and among species. A transition from forked to forkless tails was less likely to occur than the reverse transition when extrapair mating opportunities were readily available, but not when extrapair mating opportunities were limited. In contrast, the tail shape was more likely to evolve independently with prey size (i.e., small/large) and social foraging behaviour (i.e., social/solitary foraging). These findings indicate that the intensity of sexual selection, rather than foraging mode, explains the evolutionary transition between the presence and absence of tail ornamentation, questioning the widespread perspective that capturing large prey is an evolutionary force driving and maintaining forked tails.

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Data availability

The data sets supporting this article have been uploaded as part of electronic supplementary material, table S1.

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Acknowledgements

We thank Dr Shumpei Kitamura and his lab members at Ishikawa Prefectural University for their kindest advices. We are grateful to Dr Angela Turner for her kindly support on the valuable information on swallows. We also thank Drs Sari Raja-aho, Petri Suorsa, Jari Lehto for their kind support when taking a picture of the sand martin. We thank Dr Christopher Clark and anonymous reviewers for critical comments.

Funding

MH was supported by the Research Fellowship of the Japan Society for the Promotion of Science (JSPS, 15J10000) and KAKENHI grant (JSPS, 19K06850).

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MH performed data analysis and wrote the manuscript. EA collected data and modified the manuscript.

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Correspondence to Masaru Hasegawa.

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This comparative study does not include any treatments of animals, as all the information was gathered from literatures.

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Hasegawa, M., Arai, E. Extrapair mating opportunity explains the evolutionary transition between the presence and absence of tail ornamentation in swallows. Evol Ecol (2022). https://doi.org/10.1007/s10682-022-10196-3

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Keywords

  • Evolutionary transition analysis
  • Plumage ornamentation
  • Prey size
  • Sexually selected traits
  • Social foraging