Quantitative genetics of plumage color: Lifetime effects of early nest environment on a colorful sexual signal

Ecology and Evolution

Volumn 5, Issue 16, 2015, Pages 3436-3449

  Hubbard, Joanna K ^a   Jenkins, Brittany R ^a,b   Safran, Rebecca J ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

Animal model; Barn swallow; Developmental plasticity; Heritability; Melanin plumage color

Indexed keywords

ANIMALIA; HIRUNDO; HIRUNDO RUSTICA ERYTHROGASTER;

EID: 84939471449     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.1602     Document Type: Article

References (85)

1. Andersson, M. B. 1994. Sexual selection. Princeton University Press, Princeton.
2. Beamonte-Barrientos, R., A. Velando, H. Drummond, and R. Torres . 2010. Senescence of maternal effects: aging influences egg quality and rearing capacities of a long-lived bird. Am. Nat. 175:469-480.
3. Bensch, S., T. Price, and J. Kohn . 1997. Isolation and characterization of microsatellite loci in a Phylloscopus warbler. Mol. Ecol. 6:91-92.
4. Bolund, E., H. Schielzeth, and W. Forstmeier . 2011. Correlates of male fitness in captive zebra finches - a comparison of methods to disentangle genetic and environmental effects. BMC Evol. Biol. 11:327.
5. Bonduriansky, R. 2007. Sexual selection and allometry: a critical reappraisal of the evidence and ideas. Evolution 61:838-849.
6. Bradley, R. J., J. K. Hubbard, B. R. Jenkins, and R. J. Safran . 2014. Patterns and ecological predictors of age-related performance in female North American barn swallows, Hirundo rustica erythrogaster. Behav. Ecol. Sociobiol., 68:1883-1892.
7. Buchanan, K. L., K. A. Spencer, A. R. Goldsmith, and C. K. Catchpole . 2003. Song as an honest signal of past developmental stress in the European starling (Sturnus vulgaris). Proc. Biol. Sci. 270:1149-1156.
8. D'Alba, L., C. Van Hemert, K. A. Spencer, B. J. Heidinger, L. Gill, N. P. Evans, et al. 2014. Melanin-based color of plumage: role of condition and of feathers' microstructure. Integr. Comp. Biol., 54:1-12.
9. Danchin, E. 2013. Avatars of information: towards an inclusive evolutionary synthesis. Trends Ecol. Evol. 28:351-358.
10. De Villemereuil, P. 2012. Tutorial Estimation of a biological trait heritability using the animal model How to use the MCMCglmm R package.
11. Duckworth, R. A., V. Belloni, and S. R. Anderson . 2015. Cycles of species replacement emerge from locally induced maternal effects on offspring behavior in a passerine bird. Science 347:875-877.
12. Emlen, D. J. 1994. Environmental control of horn length dimorphism in the beetle onthophagus acuminatus (Coleoptera: Scarabaeidae). Proc. Biol. Sci. 256:131-136.
13. Evans, S. R., and B. C. Sheldon . 2012. Quantitative genetics of a carotenoid-based color: heritability and persistent natal environmental effects in the great tit. Am. Nat. 179:79-94.
14. Evans, S. R., and B. C. Sheldon . 2013. Pigments versus structure: examining the mechanism of age-dependent change in a carotenoid-based colour. J. Anim. Ecol. 82:418-428.
15. Falconer, D. S., and T. F. C. Mackay . 1996. Introduction to quantitative genetics. Longman, Essex.
16. Garant, D., B. C. Sheldon, and L. Gustafsson . 2004. Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components. Evolution 58:634-644.
17. Grant, B. R. 1990. The significance of subadult plumage in Darwin's finches, Geospiza fortis. Behav. Ecol. 1:161-170.
18. Griffith, S. C., I. P. F. Owens, and T. Burke . 1999. Environmental determination of a sexually selected trait. Nature 400:358-360.
19. Griffith, S. C., T. H. Parker, and V. A. Olson . 2006. Melanin- versus carotenoid-based sexual signals: is the difference really so black and red? Anim. Behav. 71:749-763.
20. Groothuis, T. G. G., and N. von Engelhardt . 2005. Investigating maternal hormones in avian eggs: measurement, manipulation, and interpretation. Ann. N. Y. Acad. Sci. 1046:168-180.
21. Hadfield, J. D. 2010. MCMC methods for multi-respoinse generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33:1-22.
22. Hadfield, J. D., and I. P. F. Owens . 2006. Strong environmental determination of a carotenoid-based plumage trait is not mediated by carotenoid availability. J. Evol. Biol. 19:1104-1114.
23. Hadfield, J. D., A. Nutall, D. Osorio, and I. P. F. Owens . 2007. Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour. J. Evol. Biol. 20:549-557.
24. Hanotte, O., C. Zanon, A. Pugh, C. Greig, A. Dixon, and T. Burke . 1994. Isolation and characterization of microsatellite loci in a passerine bird: the reed bunting Emberiza schoeniclus. Mol. Ecol. 3:529-530.
25. Haywood, S., and C. M. Perrins . 1992. Is clutch size in birds affected by environmental conditions during growth? Proc. Biol. Sci. 249:195-197.
26. Hoekstra, H. E., K. E. Drumm, and M. W. Nachman . 2004. Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes. Evolution 58:1329-1341.
27. Hubbard, J. K., J. A. C. Uy, M. E. Hauber, H. E. Hoekstra, and R. J. Safran . 2010. Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet. 26:231-239.
28. Ingleby, F. C., J. Hunt, and D. J. Hosken . 2010. The role of genotype-by-environment interactions in sexual selection. J. Evol. Biol. 23:2031-2045.
29. Jensen, H., T. Svorkmo-Lundberg, T. H. Ringsby, and B.-E. Saether . 2006. Environmental influence and cohort effects in a sexual ornament in the house sparrow, Passer domesticus. Oikos 114:212-224.
30. Johnson, J. A., and K. K. Burnham . 2013. Timing of breeding and offspring number covary with plumage colour among Gyrfalcons Falco rusticolus. The Ibis 155:177-188.
31. Kleven, O., F. Jacobsen, R. Izadnegahdar, R. J. Robertson, and J. T. Lifjeld . 2006. Male tail streamer length predicts fertilization success in the North American barn swallow (Hirundo rustica erythrogaster). Behav. Ecol. Sociobiol. 59:412-418.
32. Kruuk, L. E. B. 2004. Estimating genetic parameters in natural populations using the 'animal model'. Philos. Trans. R. Soc. Lond. B Biol. Sci. 359:873-890.
33. Lande, R., and S. J. Arnold . 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
34. Lindström, J. 1999. Early development and fitness in birds and mammals. Trends Ecol. Evol. 14:343-348.
35. Lynch, M., and B. Walsh . 1998. Genetics and analysis of quantitative traits. Sinauer, Sunderland.
36. MacDonald, I. F., B. Kempster, L. Zanette, and S. A. MacDougall-Shackleton . 2006. Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning. Proc. Biol. Sci. 273:2559-2564.
37. Maia, R., C. Eliason, P.-P. Bitton, S. M. Doucet, and M. D. Shawkey . 2013. Pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol. Evol. 4:906-913.
38. McDonald, D. B., and W. K. Potts . 1994. Cooperative display and relatedness among males in a lek-mating bird. Science 266:1030-1032.
39. McGraw, K. J. 2006. Mechanics of melanin-based coloration. Pp. 243-294 in G. E. Hill and K. J. McGraw, eds. Bird coloration: mechanisms and measurement. Harvard University Press, Cambridge.
40. McGraw, K. J., R. J. Safran, M. R. Evans, and K. Wakamatsu . 2004. European barn swallows use melanin pigments to color their feathers brown. Behav. Ecol. 15:889-891.
41. McGraw, K. J., R. J. Safran, and K. Wakamatsu . 2005. How feather colour reflects its melanin content. Funct. Ecol. 19:816-821.
42. Merilä, J., and E. Svensson . 1997. Are fat reserves in migratory birds affected by condition in early life? J. Avian Biol. 28:279-286.
43. Miller, C. W., and A. J. Moore . 2007. A potential resolution to the lek paradox through indirect genetic effects. Proc. Biol. Sci. 274:1279-1286.
44. Moczek, A. P., and D. J. Emlen . 1999. Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae). J. Evol. Biol. 12:27-37.
45. Møller, A. P. 1994. Sexual selection and the barn swallow. Oxford University Press, New York.
46. Montgomerie, R. 2006. Analyzing colors. Pp. 90-147 in G. E. Hill and K. J. McGraw, eds. Bird Coloration: mechanisms and measurement. Harvard University Press, Cambridge.
47. Mousseau, T. A., and C. W. Fox . 1998. The adaptive significance of maternal effects. Trends Ecol. Evol. 13:403-407.
48. Müller, W., V. C. Goerlich, J. Vergauwen, T. G. G. Groothuis, and M. Eens . 2012. Sources of variation in yolk hormone deposition: consistency, inheritance and developmental effects. Gen. Comp. Endocrinol. 175:337-343.
49. Mundy, N. I. 2005. A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc. Biol. Sci. 272:1633-1640.
50. Mundy, N. I. 2006. Genetic basis of color variation in wild birds. Pp. 469-506 in G. E. Hill and K. J. McGraw, eds. Bird coloration: mechanisms and measurement. Harvard University Press, Cambridge.
51. Neuman, C. R., R. J. Safran, and I. J. Lovette . 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.
52. Nowicki, S., S. Peters, and J. Podos . 1998. Song learning, early nutrition and sexual selection in songbirds. Am. Zool. 38:179-190.
53. Nowicki, S., W. A. Searcy, and S. Peters . 2002. Brain development, song learning and mate choice in birds: a review and experimental test of the 'nutritional stress hypothesis'. Journal of Comparative Physiology. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 188:1003-1014.
54. Ohlsson, T., H. G. Smith, L. Råberg, and D. Hasselquist . 2002. Pheasant sexual ornaments reflect nutritional conditions during early growth. Proc. Biol. Sci. 269:21-27.
55. Potti, J., and S. Montalvo . 2008. Male colour variation in Spanish Pied Flycatchers Ficedula hypoleuca. The Ibis 133:293-299.
56. Primmer, C. R., A. P. Møller, and H. Ellegren . 1995. Resolving genetic relationships with microsatellite markers: a parentage testing system for the swallow Hirundo rustica. Mol. Ecol. 4:493-498.
57. Punzalan, D., M. Cooray, F. Helen Rodd, and L. Rowe . 2008. Condition dependence of sexually dimorphic colouration and longevity in the ambush bug Phymata americana. J. Evol. Biol. 21:1297-1306.
58. Räsänen, K., and L. E. B. Kruuk . 2007. Maternal effects and evolution at ecological time-scales. Funct. Ecol. 21:408-421.
59. R Core Team 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/.
60. Rooney, K., and S. E. Ozanne . 2011. Maternal over-nutrition and offspring obesity predisposition: targets for preventative interventions. Int. J. Obes. 35:883-890.
61. Roulin, A., and C. Dijkstra . 2003. Genetic and environmental components of variation in eumelanin and phaeomelanin sex-traits in the barn owl. Heredity 90:359-364.
62. Safran, R. J., and K. J. McGraw . 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.
63. Safran, R. J., C. R. Neuman, K. J. McGraw, and I. J. Lovette . 2005. Dynamic paternity allocation as a function of male plumage color in barn swallows. Science 309:2210-2212.
64. Safran, R. J., K. M. Pilz, K. J. McGraw, S. M. Correa, and H. Schwabl . 2008. Are yolk androgens and carotenoids in barn swallow eggs related to parental quality? Behav. Ecol. Sociobiol. 62:427-438.
65. Safran, R. J., K. J. McGraw, M. R. Wilkins, J. K. Hubbard, and J. Marling . 2010. Positive carotenoid balance correlates with greater reproductive performance in a wild bird. PLoS ONE 5:e9420.
66. Safran, R. J., Y. Vortman, B. R. Jenkins, J. K. Hubbard, M. R. Wilkins, R. J. Bradley, and A. Lotem . 2010. Phenotypic evolution through divergent sexual selection in closely related population of barn swallows Hirundo rustica.
67. Saino, N., C. R. Primmer, H. Ellegren, and A. P. Møller . 1997. An experimental study of paternity and tail ornamentation in the barn swallow (Hirundo rustica). Evolution 51:562-570.
68. Saino, N., M. Romano, D. Rubolini, C. Teplitsky, R. Ambrosini, M. Caprioli, et al. 2013. Sexual dimorphism in melanin pigmentation, feather coloration and Its heritability in the barn swallow (Hirundo rustica). PLoS ONE 8:e58024.
69. Scordato, E. S., and R. J. Safran . 2014. Geographic variation in sexual selection and implications for speciation in the Barn Swallow. Avian Res. 5:1-13.
70. Scordato, E. S. C., A. L. Bontrager, and T. D. Price . 2012. Cross-generational effects of climate change on expression of a sexually selected trait. Curr. Biol. 22:78-82.
71. Siefferman, L., G. E. Hill, and F. S. Dobson . 2005. Ornamental plumage coloration and condition are dependent on age in eastern bluebirds Sialia sialis. J. Avian Biol. 36:428-435.
72. Spencer, K. A., K. L. Buchanan, A. R. Goldsmith, and C. K. Catchpole . 2003. Song as an honest signal of developmental stress in the zebra finch (Taeniopygia guttata). Horm. Behav. 44:132-139.
73. Stoddard, M. C., and R. O. Prum . 2008. Evolution of avian plumage color in a tetrahedral color space: a phylogenetic analysis of new world buntings. Am. Nat. 171:755-776.
74. Tilgar, V., R. Mänd, P. Kilgas, and M. Mägi . 2009. Long-term consequences of early ontogeny in free-living Great Tits Parus major. J. Ornithol. 151:61-68.
75. Tschirren, B., E. Postma, A. N. Rutstein, and S. C. Griffith . 2012. When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring. Proc. Biol. Sci. 279:1233-1240.
76. Tsyusko, O. V., M. B. Peters, C. Hagen, T. D. Tuberville, T. A. Mousseau, A. P. Møller, et al. 2007. Microsatellite markers isolated from barn swallows (Hirundo rustica). Mol. Ecol. Notes, 7:833-835.
77. Turner, A. 2006. The barn swallow. T & A D Poyser, London.
78. Uy, J. A. C., R. G. Moyle, C. E. Filardi, and Z. A. Cheviron . 2009. Difference in plumage color used in species recognition between incipient species is linked to a single amino acid substitution in the melanocortin-1 receptor. Am. Nat. 174:244-254.
79. Verhulst, S., C. M. Perrins, and R. Riddington . 1997. Natal dispersal of great tits in a patchy environment. Ecology 78:864-872.
80. Vortman, Y., A. Lotem, R. Dor, I. J. Lovette, and R. J. Safran . 2011. The sexual signals of the East-Mediterranean barn swallow: a different swallow tale. Behav. Ecol. 22:1344-1352.
81. Vortman, Y., A. Lotem, R. Dor, I. Lovette, and R. J. Safran . 2013. Multiple sexual signals and behavioral reproductive isolation in a diverging population. Am. Nat. 182:514-523.
82. Walker, L. K., M. Stevens, F. Karadaş, R. M. Kilner, and J. G. Ewen . 2013. A window on the past: male ornamental plumage reveals the quality of their early-life environment. Proc. Biol. Sci. R. Soc. 280:20122852.
83. White, J. M., J. E. Legates, and E. J. Eisen . 1968. Maternal effects among lines of mice selected for body weight. Genetics 60:395-408.
84. Wilson, A. J., D. Réale, M. N. Clements, M. M. Morrissey, E. Postma, C. A. Walling, et al. 2010. An ecologist's guide to the animal model. J. Anim. Ecol. 79:13-26.
85. Wolak, M., D. J. Fairbairn, and Y. R. Paulsen . 2012. Guidelines for estimating repeatability. Methods Ecol. Evol. 3:129-137.