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Leg coloration is associated with habitat type and social environment in swallows and martins

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Abstract

Plumage ornaments, such as colourful feathers and deeply forked tails, are classic examples of sexually selected ornaments, and are shown to be related to ecological factors on an evolutionary time scale. In contrast, although colourful bare skin could also be a visual ornament, few studies have examined the evolutionary relationship between colourful bare skin and ecological factors and its interrelationship with plumage ornaments. Using a phylogenetic comparative approach, we studied leg (and foot) coloration in relation to ecological factors, particularly in habitat type (montane or not), and to well-known sexually selected traits, deeply forked tails and reddish plumage coloration, in the subfamily Hirundininae. We showed that mountain species had redder legs than others. Although we also found that social breeders had redder legs than others, the relationship between habitat type and leg coloration remained significant even after controlling for this relationship. In contrast, tail fork depth and reddish plumage coloration were not significantly related to habitat type. Because leg coloration and these plumage ornaments were not significantly interrelated, they likely evolved partially independently. We also found that mountain species had longer nestling periods than others, indicating higher parental investment in montane area in these monogamous birds. Because bare skin coloration is a dynamic honest signal of the current body condition and parental care ability, birds might utilise this information for successful breeding, particularly in environments where extensive parental care is required.

Zusammenfassung

Die Färbung der Beine hängt mit dem Habitattyp und dem sozialen Umfeld von Schwalben zusammen.

Gefiederschmuck wie z.B. bunte Federn und tief gegabelte Schwänze sind klassische Beispiele für sexuell selektierte Schmuckelemente und hängen auf einer evolutionären Zeitskala bekanntermaßen mit ökologischen Faktoren zusammen. Obwohl farbige nackte Haut auch ein optischer Schmuck sein könnte, gibt es nur wenige Studien zu einem evolutionären Zusammenhang zwischen farbiger nackter Haut und ökologischen Faktoren sowie einer Wechselbeziehung mit dem Gefiederschmuck. Anhand eines phylogenetischen Vergleichs untersuchten wir bei der Unterfamilie Hirudininae die Färbung von Beinen (und Füßen) in Abhängigkeit von ökologischen Faktoren, insbesondere vom Habitattyp (bergig oder nicht), und von bekannten sexuell selektierten Merkmalen wie tief gegabelten Schwänzen und rötlicher Gefiederfärbung. Dabei haben wir gezeigt, dass Arten aus bergigen Habitaten rötere Beine haben als andere. Obwohl wir auch feststellen konnten, dass gemeinschaftlich brütende Arten rötere Beine als andere hatten, blieb die Beziehung zwischen Habitattyp und Beinfärbung auch bei Berücksichtigung dieses Zusammenhangs signifikant. Die Tiefe der Schwanzgabel sowie die rötliche Färbung des Gefieders standen dagegen in keinem signifikanten Zusammenhang mit dem Habitattyp. Da die Beinfarbe und die Schmuckelemente des Gefieders nicht signifikant zusamenhingen, haben sie sich wahrscheinlich teilweise unabhängig voneinander entwickelt. Außerdem stellten wir fest, dass die Nestlingszeiten bei Bergvögeln länger waren als bei anderen Arten, was bei diesen monogamen Vögeln in bergigen Gebieten auf höhere elterliche Investitionen hinweist. Da die Färbung der nackten Haut ein klarer, zuverlässiger Indikator der aktuellen physischen Verfassung und der Fähigkeit zur Brutpflege ist, könnten Vögel diese Information für eine erfolgreiche Fortpflanzung nutzen, insbesondere in Umgebungen, in denen eine intensive Pflege durch die Eltern erforderlich ist.

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References

  • Andersson M (1982) Female choice selects for extreme tail length in a widowbird. Nature 299:818–820

    Article  Google Scholar 

  • Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Book  Google Scholar 

  • Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KJ (eds) Bird coloration I. Harvard University Press, Oxford, pp 41–89

    Google Scholar 

  • Arai E, Hasegawa M, Sato M, Sakai H, Ito S, Wakamatsu K (2019) Eumelanin levels in rufous feathers explain plasma testosterone levels and survival in swallows. Ecol Evol 9:2755–2764

    Article  PubMed  PubMed Central  Google Scholar 

  • Badyaev AV (1997a) Altitudinal variation in sexual dimorphism: a new pattern and alternative hypotheses. Behav Ecol 80:128–138

    Google Scholar 

  • Badyaev AV (1997b) Avian life history variation along altitudinal gradients: an example with Cardueline finches. Oecologia 111:357–364

    Article  Google Scholar 

  • Badyaev AV, Ghalambor CK (1998) Does a trade-off exist between sexual ornamentation and ecological plasticity? sexual dichromatism and occupied elevational range in finches. Oikos 82:319–326

    Article  Google Scholar 

  • Badyaev AV, Ghalambor CK (2001) Evolution of life hisotries along elevational gradients: trade-off between parental care and fecundity. Ecology 82:2948–2960

    Article  Google Scholar 

  • Bortolotti GR (2006) Natural selection and coloration: protection, concealment, advertisement, or deception? In: Hill GE, McGraw KJ (eds) Bird coloration II. Harvard University Press, Oxford, pp 3–35

    Chapter  Google Scholar 

  • Boyle WA, Sandercock BK, Martin K (2016) Patterns and drivers of intraspecific variation in avian life history along elevational gradients: a meta-analysis. Biol Rev 91:469–482

    Article  Google Scholar 

  • Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Amer Natl 127:415–445

    Article  Google Scholar 

  • Burley N, Coopersmith CB (1987) Bill colour preferences of zebra finches. Ethology 76:133–151

    Article  Google Scholar 

  • Changizi MA, Zhang Q, Shimojo S (2006) Bare skin, blood and the evolution of primate colour vision. Biol Lett 2:217–221

    Article  PubMed  PubMed Central  Google Scholar 

  • Christy JH (1995) Mimicry, mate choice, and the sensory trap hypothesis. Amer Natl 146:171–181

    Article  Google Scholar 

  • Clotfelter ED, Schubert KA, Nolan V Jr, Ketterson ED (2003) Mouth color signals thermal state of nestling Dark-Eyed Juncos (Junco hyemalis). Ethology 109:171–182

    Article  Google Scholar 

  • Dale J, Dey CJ, Delhey K, Kempenaers B, Valcu M (2015) The effects of life history and sexual selection on male and female plumage colouration. Nature 527:367–370

    Article  CAS  PubMed  Google Scholar 

  • de Villemereuil P, Nakagawa S (2014) General quantitative genetic methods for comparative biology. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology: concepts and practice. Springer, New York, pp 287–301

    Chapter  Google Scholar 

  • de Villemereuil P, Gimenez O, Doligez B (2013) Comparing parent offspring regression with frequentist and Bayesian animal models to estimate heritability in wild populations: a simulation study for Gaussian and binary traits. Methods Ecol Evol 4:260–275

    Article  Google Scholar 

  • De Zwaan DR, Greenwood JL, Martin K (2017) Feather melanin and microstructure variation in dark-eyed junco Junco hyemalis across an elevational gradient in the Selkirk Mountains. J Avian Biol 48:552–562

    Article  Google Scholar 

  • Dey CJ, Valcu M, Kempenaers E, Dale J (2015) Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes). J Evol Biol 28:250–258

    Article  CAS  PubMed  Google Scholar 

  • Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510

    Article  PubMed  Google Scholar 

  • Dugas MB, Border S (2022a) Effects of a novel ectoparasite on condition and mouth coloration of nestling barn swallows. Biol J Linn Soc 135:52–61

    Article  Google Scholar 

  • Dugas MB, Border S (2022b) Experimental reduction of a nest ectoparasite affects mouth coloration of nestling Cliff Swallows Petrochelidon pyrrhonota. J Ornithol 163:553–563

    Article  Google Scholar 

  • Dugas MB, McGraw KJ, Strickler SA (2018) Mouth coloration in nestling Cave Swallows (Petrochelidon fulva) differs from that of adults, is carotenoid based and correlated with body mass. J Ornithol 159:581–586

    Article  Google Scholar 

  • Elkins N (2004) Weather and bird behaviour, 3rd edn. T & AD Poyser, London

    Google Scholar 

  • Fitzpatrick JW (1985) Form, foraging behavior, and adaptive radiation in the Tyrannidae. Ornithol Monogr 36:447–470

    Article  Google Scholar 

  • Galván I, Nielsen JT, Møller AP (2014) Intensity of melanin-based color and risk of predation in the Barn Swallow Hirundo rustica. Acta Ornithol 49:47–56

    Article  Google Scholar 

  • Garamszegi LZ, Mundry R (2014) Multimodel-inference in comparative analyses. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology: concepts and practice. Springer, NY, pp 305–331

    Chapter  Google Scholar 

  • Gomes ACR, Funghi C, Soma M, Sorenson MD, Cardoso GC (2017) Multimodal signalling in estrildid finches: song, dance and colour are associated with different ecological and life-history traits. J Evol Biol 30:1336–1346

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M (2021) Male barn swallows tolerate nestling-like courtship calls of rival males. Front Ecol Evol 9:759438

    Article  Google Scholar 

  • Hasegawa M, Arai E (2017) Egg size decreases with increasing female fork tail depth in family Hirundinidae. Evol Ecol 31:559–569

    Article  Google Scholar 

  • Hasegawa M, Arai E (2018a) Differential visual ornamentation between brood parasitic and parental cuckoos. J Evol Biol 31:446–456

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M, Arai E (2018b) Convergent evolution of the tradeoff between egg size and tail fork depth in swallows and swifts. J Avian Biol 49:e01684

    Article  Google Scholar 

  • Hasegawa M, Arai E (2020) Fork tails evolved differently in swallows and swifts. J Evol Biol 33:911–919

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M, Arai E (2021) Opposing population trends of fork-tailed swallows and reddish-coloured swallows in our changing world. J Evol Biol 34:331–338

    Article  PubMed  Google Scholar 

  • Hasegawa M, Arai E, Watanabe M, Nakamura M (2013) Male nestling-like courtship calls attract female barn swallows Hirundo rustica gutturalis. Anim Behav 86:949–953

    Article  Google Scholar 

  • Hasegawa M, Arai E, Kutsukake N (2016) Evolution of tail fork depth in genus Hirundo. Ecol Evol 6:851–858

    Article  PubMed  PubMed Central  Google Scholar 

  • Hill GE (1994) Trait elaboration via adaptive mate choice: sexual conflict in the evolution of signals of male quality. Ethol Ecol Evol 6:351–370

    Article  Google Scholar 

  • Hill GE, McGraw KJ (2006) Bird coloration II: function and evolution. Harvard University Press, Oxford

    Book  Google Scholar 

  • Hille S, Cooper CB (2015) Elevational trends in life histories: revising the pace-of-life framework. Biol Rev 90:204–213

    Article  PubMed  Google Scholar 

  • Iverson ENK, Karubian J (2017) The role of bare parts in avian signaling. Auk 134:587–611

    Article  Google Scholar 

  • Ives AR, Garland TJ (2014) Phylogenetic regression for binary dependent variables. In: Garamszegi LZ (ed) Modern phylogenetic comparative methods and their application in evolutionary biology: concepts and practice. Springer, New York, pp 231–262

    Chapter  Google Scholar 

  • Jawor JM, Breitwisch R (2003) A unique ornament display in female Northern Cardinals. Wilson Bull 115:464–467

    Article  Google Scholar 

  • Johnson AE, Mitchell JS, Brown MB (2016) Convergent evolution in social Swallows (Aves: Hirundinidae). Ecol Evol 7:550–560

    Article  PubMed  PubMed Central  Google Scholar 

  • Keith S, Urban EK, Fry CH (1992) The birds of Africa, Vol 4: broadbills to chats. Academic Press, London, pp p125-197

    Google Scholar 

  • Kilner RM (2006) Function and evolution of color in young birds. In: Hill GE, McGraw KJ (eds) Bird coloration II. Harvard University Press, Oxford, pp 201–232

    Google Scholar 

  • Körner K (2007) The use of ‘altitude’ in ecological research. Trends Ecol Evol 22:569–574

    Article  PubMed  Google Scholar 

  • Ligon RA, Diaz CD, Morano JL, Troscianko J, Stevens M, Moskeland A et al (2018) Evolution of correlated complexity in the radically different courtship signals of birds-of-paradise. PLoS Biol 16:e2006962

    Article  PubMed  PubMed Central  Google Scholar 

  • Marcias Garcia C, Ramirez E (2005) Evidence that sensory traps can evolve into honest signals. Nature 434:501–505

    Article  Google Scholar 

  • Møller AP (1994) Sexual selection and the Barn Swallow. Oxford University Press

    Google Scholar 

  • Montoya B, Torres R (2015) Male skin color signals direct and indirect benefits in a species with biparental care. Behav Ecol 26:425–434

    Article  Google Scholar 

  • Morales J, Cuervo JJ, Moreno J, Soler JJ (2019) Juvenile plumage whiteness is associated with the evolution of clutch size in passerines. Behav Ecol 30:1106–1112

    Article  Google Scholar 

  • Nicolaï MPJ, Shawkey MD, Porchetta S, Claus R, D’Alba L (2020) Exposure to UV radiance predicts repeated evolution of concealed black skin in birds. Nat Comm 11:2414

    Article  Google Scholar 

  • Norberg RÅ (1994) Swallow tail streamer is a mechanical device for self deflection of tail leading edge, enhancing aerodynamic efficiency and flight manoeuvrability. Proc R Soc Lond B 257:227–233

    Article  Google Scholar 

  • O’Kane PM, Connerton IF, White KL (2016) Pilot study of long-term anaesthesia in broiler chickens. Vet Anaesth Analg 43:72–75

    Article  PubMed  Google Scholar 

  • Owens IPF (2006) Ecological explanations for interspecific variability in coloration. In: Hill GE, McGraw KJ (eds) Bird coloration II. Harvard University Press, Oxford, pp 380–416

    Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D (2015) Package ‘nlme’ http://cran.r-project.org/web/packages/nlme/nlme.pdf (accessed on 21 Dec, 2015)

  • Quintero I, Jetz W (2018) Global elevational diversity and diversification of birds. Nature 555:246–250

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rubolini D, Liker A, Garamszegi LZ, Møller AP, Saino N (2015) Using the BirdTree.org website to obtain robust phylogenies for avian comparative studies: a primer. Curr Zool 61:959–965

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  Google Scholar 

  • Saino N, Calza S, Martinelli R, De Bernardi F, Ninni P, Møller AP (2000) Better red than dead: carotenoid based mouth coloration reveals infection in barn swallow nestlings. Proc R Soc Lond B 267:57–61

    Article  CAS  Google Scholar 

  • Saino N, Ambrosini R, Martinelli R, Ninni P, Møller AP (2003) Gape coloration reliably reflects immunocompetence of barn swallow (Hirundo rustica) nestlings. Behav Ecol 14:16–22

    Article  Google Scholar 

  • Simons MJP, Verhulst S (2011) Zebra finch females prefer males with redder bills independent of song rate—a meta-analysis. Behav Ecol 22:755–762

    Article  Google Scholar 

  • Snell-Rood EC, Badyaev AV (2008) Ecological gradient of sexual selection: elevation and song elaboration in finches. Oecologia 157:545–551

    Article  PubMed  Google Scholar 

  • Soma M, Garamszegi LZ (2015) Evolution of courtship display in Estrildid finches: dance in relation to female song and plumage ornamentation. Front Ecol Evol 3:4

    Article  Google Scholar 

  • Terrill RS, Schultz AJ (2022) Feather function and the evolution of birds. Biol Rev (in Press). https://doi.org/10.1111/brv.12918

    Article  Google Scholar 

  • Thomas ALR (1993) On the aerodynamics of birds’ tails. Phil Trans R Soc Lond B 340:361–380

    Article  Google Scholar 

  • Thomson DL, Furness RW, Monaghan P (1998) The analysis of ordinal response data in the behavioural sciences. Anim Behav 56:1041–1043

    Article  CAS  PubMed  Google Scholar 

  • Tietze DR, Martens J, Fischer BS, Sun Y-H, Klussmann-Kolb A, Packert M (2015) Evolution of leaf warbler songs (Aves: Phylloscopidae). Ecol Evol 5:781–798

    Article  PubMed  PubMed Central  Google Scholar 

  • Tobias JA, Seddon N (2009) Sexual selection and ecological generalism are correlated in antbirds. J Evol Biol 22:623–636

    Article  CAS  PubMed  Google Scholar 

  • Torres R, Velando A (2005) Male preference for female foot colour in the socially monogamous blue-footed booby, Sula nebouxii. Anim Behav 69:59–65

    Article  Google Scholar 

  • Turner AK (2006) The barn swallow. T & A D Poyser, London

    Google Scholar 

  • Turner AK, Rose C (1994) A handbook to the swallows and martins of the world. Helm, London

    Google Scholar 

  • van Doorn GS, Weissing FJ (2004) The evolution of female preferences for multiple indicators of quality. Amer Natl 164:173–186

    Article  Google Scholar 

  • van Doorn GS, Weissing FJ (2006) Sexual conflict and the evolution of female preferences for indicators of male quality. Amer Natl 168:742–757

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Nobuyuki Kutsukake and his lab members at Sokendai (The Graduate University for Advanced Studies) and 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. MH was supported by the Research Fellowship of the Japan Society for the Promotion of Science (JSPS, 15J10000 and 19K06850). We thank anonymous reviewers for critical comments.

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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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The authors declare that they have no conflicts of interests.

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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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This study is a phylogenetic comparative study and thus we did not handle live (or dead) birds.

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Communicated by F. Bairlein.

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Hasegawa, M., Arai, E. Leg coloration is associated with habitat type and social environment in swallows and martins. J Ornithol 164, 931–942 (2023). https://doi.org/10.1007/s10336-023-02074-8

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