Sequence variation in melanocortin-1-receptor and tyrosinase-related protein 1 genes and their relationship with melanin-based plumage trait expression in Lesser Kestrel (Falco naumanni) males

  • Margherita Corti
  • Stefano Podofillini
  • Matteo Griggio
  • Luca Gianfranceschi
  • Anne-Lyse Ducrest
  • Alexandre Roulin
  • Jacopo G. Cecere
  • Nicola Saino
  • Diego Rubolini
Short Communication
  • 35 Downloads

Abstract

Lesser kestrel males display inter-individual variation in melanin-based plumage traits, like ventral plumage colouration and breast/underwing spottiness. We explored whether such plumage variability was associated with single-nucleotide genetic polymorphisms of melanocortin-1-receptor (MC1R) and tyrosinase-related protein 1 (TYRP1), two genes involved in the melanogenesis pathway. No statistically significant associations between single-nucleotide mutations and male plumage traits emerged, though in some cases very rare (< 2%) homozygous mutated individuals displayed extreme plumage phenotypes. Hence, large inter-individual male Lesser Kestrel plumage variation, which is consistent between years and partly age related, was only marginally related to untranslated region and coding sequence variation of MC1R and TYRP1.

Keywords

Falconidae Genotype–phenotype associations Melanogenesis pathway Plumage melanisation Single nucleotide polymorphism Rare variants 

Zusammenfassung

Variation in MC1R- und TYRP1-Gensequenzen in Relation zur Expression melaninbasierter Gefiedermerkmale bei Rötelfalkenmänchen (Falco naumanni) Rötelfalkenmännchen zeigen interindividuelle Variation in melaninbasierten Gefiedermerkmalen, wie z.B. der Bauchgefiederfärbung und der Brust- und Unterflügeltüpfelung. Wir untersuchten, ob eine solche Gefiedervariation mit einer Sequenzvariation von MC1R und TYRP1 zusammenhängt, zwei Genen, die an der Melaninsynthese beteiligt sind, Es fand sich kein statistisch signifikanter Zusammenhang zwischen Einzelnukleotidmutationen und den Gefiedermerkmalen der Männchen, aber in einigen Fällen zeigten Individuen mit sehr seltener (< 2%) homozygoter Mutation extreme Phänotypen in der Gefiederfärbung. Die große interindividuelle Variationsbreite in der Gefiederfärbung männlicher Rötelfalken, die von Jahr zu Jahr konsistent bleibt und teilweise altersabhängig ist, steht also lediglich geringfügig mit der Variation in der nicht-kodierenden Region und den kodierenden Sequenzen des MC1R und TYRP1 Gens in Zusammenhang.

Notes

Acknowledgements

We thank the Provincia di Matera (E. De Capua), the Provveditorato Interregionale per le Opere Pubbliche, and the Comune di Matera for authorizing our work on the breeding colonies, as well as for constant support during field activities. We also wish to thank A. Curcio, E. Fulco and M. Visceglia for assistance with fieldwork, C. Simon for assistance with laboratory work, L. M. San-Jose and two anonymous reviewers for useful suggestions. Study of the Naumanni76 team (paper no. 2).

Supplementary material

10336_2018_1537_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)
10336_2018_1537_MOESM2_ESM.docx (19 kb)
Supplementary material 2 (DOCX 18 kb)

References

  1. Bergman TJ, Beehner JC (2008) A simple method for measuring colour in wild animals: validation and use on chest patch colour in Geladas (Theropithecus gelada). Biol J Linn Soc 94:231–240.  https://doi.org/10.1111/j.1095-8312.2008.00981.x CrossRefGoogle Scholar
  2. Bourgeois YX, Bertrand JA, Delahaie B, Cornuault J, Duval T, Milá B, Thébaud C (2016) Candidate gene analysis suggests untapped genetic complexity in melanin-based pigmentation in birds. J Hered 107:327–335.  https://doi.org/10.1093/jhered/esw017 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bourgeois YX, Delahaie B, Gautier M, Lhuillier E, Malé PJG, Bertrand JA, Cornuault J, Wakamatsu K, Bouchez O, Mould C, Bruxaux J, Holota H, Milá B, Thébaud C (2017) A novel locus on chromosome 1 underlies the evolution of a melanic plumage polymorphism in a wild songbird. R Soc Open Sci 4:160805.  https://doi.org/10.1098/rsos.160805 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cortimiglia C, Castiglioni B, Pizzi F, Stella A, Capra E (2017) Involvement of tyrosinase-related protein 1 gene in the light brown plumage phenotype of Falco cherrug. Anim Genet 48:125–126.  https://doi.org/10.1111/age.12506 CrossRefPubMedGoogle Scholar
  5. Dreiss AN, Roulin A (2010) Age-related change in melanin-based coloration of Barn Owls (Tyto alba): females that become more female-like and males that become more male-like perform better. Biol J Linn Soc 101:689–704.  https://doi.org/10.1111/j.1095-8312.2010.01503.x CrossRefGoogle Scholar
  6. Ducrest AL, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, colouration and behavioural syndromes. Trends Ecol Evol 23:502–510.  https://doi.org/10.1016/j.tree.2008.06.001 CrossRefPubMedGoogle Scholar
  7. Galeotti P, Rubolini D, Dunn PO, Fasola M (2003) Colour polymorphism in birds: causes and functions. J Evol Biol 16:635–646.  https://doi.org/10.1046/j.1420-9101.2003.00569.x CrossRefPubMedGoogle Scholar
  8. González JR, Armengol L, Sole X, Guino E, Mercader JM, Estivill X, Moreno J (2007) SNPassoc: an R package to perform whole genome association studies. Bioinformatics 23:654–655.  https://doi.org/10.1093/bioinformatics/btm025 CrossRefGoogle Scholar
  9. Hoi H, Griggio M (2008) Dual utility of a melanin-based ornament in bearded tits. Ethology 114:1094–1100.  https://doi.org/10.1111/j.1439-0310.2008.01566.x CrossRefGoogle Scholar
  10. Johnson JA, Ambers AD, Burnham KK (2012) Genetics of plumage color in the Gyrfalcon (Falco rusticolus): analysis of the melanocortin-1 receptor gene. J Hered 103:315–321.  https://doi.org/10.1093/jhered/ess023 CrossRefPubMedGoogle Scholar
  11. Lopez-Idiaquez D, Vergara P, Fargallo JA, Martinez-Padilla J (2016) Old males reduce melanin-pigmented traits and increase reproductive outcome under worse environmental conditions in Common Kestrels. Ecol Evol 6:1224–1235.  https://doi.org/10.1002/ece3.1910 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Nadeau NJ, Mundy NI, Gourichon D, Minvielle F (2007) Association of a single-nucleotide substitution in TYRP1 with roux in Japanese Quail (Coturnix japonica). Anim Genet 38:609–613.  https://doi.org/10.1111/j.1365-2052.2007.01667.x CrossRefPubMedGoogle Scholar
  13. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142.  https://doi.org/10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  14. Podofillini S, Cecere JG, Griggio M, Curcio A, De Capua EL, Fulco E, Pirrello S, Saino N, Serra L, Visceglia M, Rubolini D (2018) Home, dirty home: effect of old nest material on nest-site selection and breeding performance in a cavity-nesting raptor. Curr Zool.  https://doi.org/10.1093/cz/zoy012 Google Scholar
  15. San-Jose LM, Roulin A (2017) Genomics of coloration in natural animal populations. Philos Trans R Soc B 372:20160337.  https://doi.org/10.1098/rstb.2016.0337 CrossRefGoogle Scholar
  16. San-Jose LM, Ducrest AL, Ducret V, Béziers P, Simon C, Wakamatsu K, Roulin A (2015) Effect of the MC1R gene on sexual dimorphism in melanin-based colorations. Mol Ecol 24:2794–2808.  https://doi.org/10.1111/mec.13193 CrossRefPubMedGoogle Scholar
  17. Senar JC, Camerino M (1998) Status signalling and the ability to recognize dominants: an experiment with Siskins (Carduelis spinus). Proc R Soc B 265:1515–1520.  https://doi.org/10.1098/rspb.1998.0466 CrossRefPubMedCentralGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2018

Authors and Affiliations

  • Margherita Corti
    • 1
  • Stefano Podofillini
    • 1
  • Matteo Griggio
    • 2
  • Luca Gianfranceschi
    • 3
  • Anne-Lyse Ducrest
    • 4
  • Alexandre Roulin
    • 4
  • Jacopo G. Cecere
    • 5
  • Nicola Saino
    • 1
  • Diego Rubolini
    • 1
  1. 1.Department of Environmental Science and PolicyUniversity of MilanMilanItaly
  2. 2.Department of BiologyUniversity of PadovaPadovaItaly
  3. 3.Department of BiosciencesUniversity of MilanMilanItaly
  4. 4.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland
  5. 5.Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA)Ozzano dell’EmiliaItaly

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