Evolution of carotenoid pigmentation in caciques and meadowlarks (Icteridae): Repeated gains of red plumage coloration by carotenoid C4-oxygenation

Evolution

Volumn 68, Issue 3, 2014, Pages 791-801

  Friedman, Nicholas R ^a,b   McGraw, Kevin J ^c   Omland, Kevin E ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^b PALACKÝ UNIVERSITY   (Czech Republic)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Ancestral state reconstruction; Bird coloration; Carotenoids; Homoplasy; HPLC

Indexed keywords

BIOCHEMICAL COMPOSITION; CAROTENOID; COLOR; CONVERGENT EVOLUTION; FEATHER; LIQUID CHROMATOGRAPHY; OXYGEN; PHYLOGENY; RECONSTRUCTION; RESEARCH WORK; SONGBIRD;

ANIMALIA; AVES; ICTERIDAE; STURNELLA; TURDUS MERULA;

CAROTENOID;

ANCESTRAL STATE RECONSTRUCTION; ANIMAL; ARTICLE; BIRD COLORATION; CLASSIFICATION; FEATHER; GENETICS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTOLOGY; HOMOPLASY; METABOLISM; MOLECULAR EVOLUTION; OXIDATION REDUCTION REACTION; PHYLOGENY; PIGMENTATION; SONGBIRD;

ANCESTRAL STATE RECONSTRUCTION; BIRD COLORATION; CAROTENOIDS; HOMOPLASY; HPLC;

ANIMALS; CAROTENOIDS; EVOLUTION, MOLECULAR; FEATHERS; OXIDATION-REDUCTION; PHYLOGENY; PIGMENTATION; SONGBIRDS;

EID: 84896726049     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12304     Document Type: Article

References (76)

1. Aidala, Z., L. Huynen, P. L. R. Brennan, J. Musser, A. Fidler, N. Chong, G. E. Machovsky Capuska, M. G. Anderson, A. Talaba, D. Lambert et al. 2012. Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines. J. Comp. Physiol. A 198:495-510.
2. Andersson, S., M. Prager, and E. I. Anette Johansson. 2007. Carotenoid content and reflectance of yellow and red nuptial plumages in widowbirds (Euplectes spp.). Funct. Ecol. 21:272-281.
3. Arendt, J., and D. Reznick. 2007. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23:26-32.
4. Arthur, W. 2001. Developmental drive: an important determinant of the direction of phenotypic evolution. Evol. Dev. 3:271-278.
5. Barker, F. K., A. J. Vandergon, and S. M. Lanyon. 2008. Assessment of species limits among yellow-breasted meadowlarks (Sturnella spp.) using mitochondrial and sex-linked markers. Auk 125:869-879.
6. Bates, H. W. 1862. Contributions to an insect fauna of the Amazon Valley: Lepidoptera: Heliconidae. Trans. Linn. Soc. Lond. 23:495-566.
7. Beason, R. C., and E. R. Loew. 2008. Visual pigment and oil droplet characteristics of the bobolink (Dolichonyx oryzivorus), a new world migratory bird. Vision Res. 48:1-8.
8. Britton, G. 1995. UV/visible spectroscopy. Pp. 13-62 in G. Britton, S. Liaaen-Jensen, and H. Pfander, eds. Carotenoids, Vol. 1B, Spectroscopy. Birkhäuser Verlag, Basel, Switzerland.
9. Britton, G., S. Liaaen-Jensen, and H. Pfander. 2004. Carotenoids: handbook. Birkhäuser Verlag, Basel, Switzerland.
10. Brush, A. H. 1967. Pigmentation in the Scarlet Tanager, Piranga olivacea. Condor 69:549-559.
11. Brush, A. H., and D. M. Power. 1976. House finch pigmentation: carotenoid metabolism and the effect of diet. Auk 93:725-739.
12. Butler, M. A., and A. A. King. 2004. Phylogenetic comparative analysis: a modeling approach for adaptive evolution. Am. Nat. 164:683-695.
13. Cronk, Q., and I. Ojeda. 2008. Bird-pollinated flowers in an evolutionary and molecular context. J. Exp. Bot. 59:715-727.
14. Dale, J. 2006. Intraspecific variation in coloration. Pp. 36-86 in G. E. Hill and K. J. McGraw, eds. Bird coloration, Vol. 2, Function and evolution. Harvard Univ. Press, Cambridge, MA.
15. Des Marais, D. L., and M. D. Rausher. 2010. Parallel evolution at multiple levels in the origin of hummingbird pollinated flowers in Ipomoea. Evolution 64:2044-2054.
16. Friedman, N. R. 2013. The evolution of carotenoid coloration and pigmentation in the New World blackbirds. Ph.D. dissertation, University of Maryland Baltimore County.
17. Friedman, N. R., L. M. Kiere, and K. E. Omland. 2011. Convergent gains of red carotenoid-based coloration in the New World blackbirds. Auk 128:678-687.
18. Futuyma, D. J. 2005. Evolution. Sinauer Associates, Inc., Sunderland, MA.
19. Gould, S. J. 2002. The structure of evolutionary theory. Harvard Univ. Press, Cambridge, MA.
20. Grafen, A. 1989. The phylogenetic regression. Philos. Trans. R. Soc. Lond. B 326:119-157.
21. Hall, B. K. 2003. Descent with modification: the unity underlying homology and homoplasy as seen through an analysis of development and evolution. Biol. Rev. 78:409-433.
22. Hill, G. E. 1991. Plumage coloration is a sexually selected indicator of male quality. Nature 350:337-339.
23. Hill, G. E. 1992. Proximate basis of variation in carotenoid pigmentation in male house finches. Auk 109:1-12.
24. Hill, G. E. 1996. Redness as a measure of the production cost of ornamental coloration. Ethol. Ecol. Evol. 8:157-175.
25. Hill, G. E. 2006. Environmental regulation of ornamental coloration. Pp. 507-560 in G. E. Hill and K. J. McGraw, eds. Bird coloration, Vol. 1, Mechanisms and measurements. Harvard Univ. Press, Cambridge, MA.
26. Hill, G. E., and J. D. Johnson. 2012. The vitamin A-redox hypothesis: a biochemical basis for honest signaling via carotenoid pigmentation. Am. Nat. 180:E127-E150.
27. Hill, G. E., and R. Montgomerie. 1994. Plumage colour signals nutritional condition in the House Finch. Proc. R. Soc. Lond. B 258:47-52.
28. Hill, G. E., and K. J. McGraw. 2004. Correlated changes in male plumage coloration and female mate choice in cardueline finches. Anim. Behav. 67:27-35.
29. Hofmann, C. M., T. W. Cronin, and K. E. Omland. 2006. Using spectral data to reconstruct evolutionary changes in coloration: carotenoid color evolution in new world orioles. Evolution 60:1680-1691.
30. Hofmann, C. M., K. J. McGraw, T. W. Cronin, and K. E. Omland. 2007. Melanin coloration in New World orioles I: carotenoid masking and pigment dichromatism in the Orchard Oriole complex. J. Avian Biol. 38:163-171.
31. Hudon, J. 1991. Unusual carotenoid use by the Western Tanager (Piranga ludoviciana) and its evolutionary implications. Can. J. Zool. 69:2311-2320.
32. Hugall, A. F., and D. Stuart-Fox. 2012. Accelerated speciation in colour-polymorphic birds. Nature 485:631-634.
33. Inouye, C. Y., G. E. Hill, R. D. Stradi, and R. Montgomerie. 2001. Carotenoid pigments in male house finch plumage in relation to age, subspecies, and ornamental coloration. Auk 118:900-915.
34. Jaramillo A., and P. Burke. 1999. New World Blackbirds: the Icterids. Princeton Univ. Press, Princeton, NJ.
35. Johnson, K. P., and S. M. Lanyon. 2000. Evolutionary changes in color patches of blackbirds are associated with marsh nesting. Behav. Ecol. 11:515-519.
36. Kiere, L. M., C. M. Hofmann, J. J. Price, T. W. Cronin, and K. E. Omland. 2009. Discrete evolutionary color changes in caciques suggest different modes of carotenoid evolution between closely related taxa. J Avian Biol. 40:605-613.
37. Kodric-Brown, A. 1989. Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav. Ecol. Sociobiol. 25:393-401.
38. Lanyon, S. M., and K. E. Omland. 1999. A molecular phylogeny of the blackbirds (Icteridae): five lineages revealed by cytochrome-b sequence data. Auk 116:629-639.
39. Maddison, W. P., and D. R. Maddison. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. Available at http://mesquiteproject.org.
40. Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., and Hornik, K. 2012. cluster: cluster analysis basics and extensions. R package version 1.14.2.
41. Mays, H. L., K. J. McGraw, G. Ritchison, S. Cooper, V. Rush, and R. S. Parker. 2004. Sexual dichromatism in the yellow-breasted chat Icteria virens: spectrophotometric analysis and biochemical basis. J. Avian Biol. 35:125-134.
42. McGraw, K. J. 2006. Mechanics of carotenoid-based coloration. Pp. 177-242 in G. E. Hill and K. J. McGraw, eds. Bird coloration, Vol. 1, Mechanisms and measurements. Harvard Univ. Press, Cambridge, MA.
43. McGraw, K. J., M. D. Beebee, G. E. Hill, and R. S. Parker. 2003. Lutein-based plumage coloration in songbirds is a consequence of selective pigment incorporation into feathers. Comp. Biochem. Physiol. B 135:689-696.
44. McGraw, K. J., and A. J. Gregory. 2004. Carotenoid pigments in male American Goldfinches: what is the optimal biochemical strategy for becoming colourful. Biol. J. Linn. Soc. 83:273-280.
45. McGraw, K. J., J. Hudon, and G. E. Hill. 2005. A simple and inexpensive chemical test for behavioral ecologists to determine the presence of carotenoid pigments in animal tissues. Behav. Ecol. Sociobiol. 57:391-397.
46. McGraw, K. J., P. M. Nolan, and O. L. Crino. 2006. Carotenoid accumulation strategies for becoming a colorful House Finch: analyses of plasma and liver pigments in wild moulting birds. Funct. Ecol. 20:678-688.
47. McGraw, K. J., and J. G. Schuetz. 2004. The evolution of carotenoid coloration in estrildid finches: a biochemical analysis. Comp. Biochem. Physiol. B 139:45-51.
48. McGraw, K. J., A. M. Stoehr, P. M. Nolan, and G. E. Hill. 2001. Plumage redness predicts breeding onset and reproductive success in the House Finch: a validation of Darwin's theory. J. Avian Biol. 32:90-94.
49. McGraw, K. J., K. Wakamatsu, A. B. Clark, and K. Yasukawa. 2004. Red-winged blackbirds Agelaius pheoniceus use carotenoid and melanin pigments to color their epaulets. J. Avian Biol. 35:543-550.
50. McLennan, D. A., and D. R. Brooks. 1993. The phylogenetic component of cooperative breeding in perching birds: a commentary. Am. Nat. 141:790-795.
51. Mendes-Pinto, M. M., A. M. LaFountain, M. C. Stoddard, R. O. Prum, H. A. Frank, and B. Robert. 2012. Variation in carotenoid-protein interaction in bird feathers produces novel plumage coloration. J. R. Soc. Interface 9:3338-3350.
52. Montgomerie, R. 2006. Analyzing colors. Pp. 90-147 in G. E. Hill and K. J. McGraw, eds. Bird coloration, Vol. 1, Mechanisms and measurements. Harvard Univ. Press, Cambridge, MA.
53. Newbrey, J. L., and W. L. Reed. 2011. Yolk and feather carotenoids in relation to female condition and reproduction in the yellow-headed blackbird. Auk 128:382-392.
54. Olson, V. A., and I. P. F. Owens. 1998. Costly sexual signals: are carotenoid rare, risky, or required? Trends Ecol. Evol. 13:510-515.
55. Omland, K. E. 1999. The assumptions and challenges of ancestral state reconstruction. Syst. Biol. 48:604-611.
56. Omland, K. E., and S. M. Lanyon. 2000. Reconstructing plumage evolution in orioles (Icterus): repeated convergence and reversal in patterns. Evolution 54:2119-2133.
57. Pagel, M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proc. R. Soc. Lond. B 255:36-45.
58. Paradis, E., J. Claude, and K. Strimmer. 2004. APE: analysis of phylogenetics and evolution in R language. Bioinformatics 20:289-290.
59. Powell, A. F. L. A. 2013. Molecular phylogenetics of the New World blackbirds (Icteridae). Ph.D. dissertation, University of Minnesota.
60. Prager, M., and S. Andersson. 2009. Differential ability of carotenoid C4-oxygenation in yellow and red bishop species (Euplectes spp.). Comp. Biochem. Physiol. B 154:373-380.
61. Prager, M., and S. Andersson. 2010. Convergent evolution of red carotenoid coloration in widowbirds and Bishops (Euplectes spp.). Evolution 64:3609-3619.
62. Price, J. J., N. R. Friedman, and K. E. Omland. 2007. Song and plumage evolution in the New World orioles (Icterus) show similar lability and convergence in patterns. Evolution 61:850-863.
63. Price, J. J., and S. M. Lanyon. 2002. A robust phylogeny of the oropendolas: polyphyly revealed by mitochondrial sequence data. Auk 119:335-348.
64. Price, J. J., S. M. Lanyon, and K. E. Omland. 2009. Losses of female song with changes from tropical to temperate breeding in the New World blackbirds. Proc. R. Soc. Lond. B 276:1971-1980.
65. Prum, R. O., A. M. LaFountain, J. Berro, M. C. Stoddard, and H. A. Frank. 2012. Molecular diversity, metabolic transformation, and evolution of carotenoid feather pigments in cotingas (Aves: Cotingidae). J. Comp. Physiol. B 182:1095-1116.
66. R Core Team. 2012. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www.R-project.org/.
67. Reed, R. D., and M. S. Serfas. 2004. Butterfly wing pattern evolution is associated with changes in a notch/distal-less temporal pattern formation process. Curr. Biol. 14:1159-1166.
68. Reed, R. D., R. Papa, A. Martin, H. M. Hines, B. A. Countermain, C. Pardo-Diaz, C. D. Jiggins, N. L. Chamberlain, M. R. Kronforst, R. Chen et al. 2011. optix drives the repeated convergent evolution of butterfly wing pattern mimicry. Science 333:1137-1141.
69. Robinson, S. R. 1994. Early vertebrate colour vision. Nature 367:121.
70. Rowe, M., and K. J. McGraw. 2009. Carotenoids in the seminal fluid of wild birds: interspecific variation in fairy-wrens. Condor 110:694-700.
71. Smith, S. D., and M. D. Rausher. 2011. Gene loss and parallel evolution contribute to species difference in flower color. Mol. Biol. Evol. 28:2799-2810.
72. 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.
73. Stradi, R., E. Rossi, G. Gelantano, and B. Bellardi. 1996. Carotenoids in bird plumage: the pattern in three Loxia species and in Pinicola enucleator. Comp. Biochem. Physiol. B 113:427-432.
74. Toomey, M. B., and K. J. McGraw. 2007. Modified saponification and HPLC methods for analyzing carotenoids from the retina of quail: implications for its use as a nonprimate model species. Invest. Ophthalmol. Vis. Sci. 48:3976-3982.
75. Westneat, D. F., A. B. Clark, and K. C. Rambo. 1995. Within-brood patterns of paternity and paternal behavior in red-winged blackbirds. Behav. Ecol. Sociobiol. 37:349-356.
76. Wiens, J. J., C. A. Kuczynski, W. E. Duellman, and T. W. Reeder. 2007. Loss and re-evolution of complex life cycles in marsupial frogs: does ancestral trait reconstruction mislead? Evolution 61:1886-1899.