Key ornamental innovations facilitate diversification in an avian radiation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 26, 2013, Pages 10687-10692

  Maia, Rafael ^a   Rubenstein, Dustin R ^b   Shawkey, Matthew D ^a  

^a UNIVERSITY OF AKRON   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Biophotonics; Macroevolution; Phylogenetics; Structural color; Sturnidae

Indexed keywords

ADAPTIVE RADIATION; ANIMAL CELL; ARTICLE; BIODIVERSITY; COLOR; COMPETITION; MELANOSOME; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; SEXUAL SELECTION; STARLING;

BIOPHOTONICS; MACROEVOLUTION; PHYLOGENETICS; STRUCTURAL COLOR; STURNIDAE;

AFRICA; ANIMALS; BIODIVERSITY; ECOSYSTEM; EVOLUTION, MOLECULAR; FEMALE; MALE; MATING PREFERENCE, ANIMAL; MELANOSOMES; MODELS, GENETIC; PHYLOGENY; PIGMENTATION; STARLINGS;

AVES; STURNIDAE;

EID: 84879531337     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220784110     Document Type: Article

References (86)

1. Schluter D (2000) The Ecology of Adaptive Radiation (Oxford Univ Press, New York).
2. Simpson GG (1953) The Major Features of Evolution (Columbia Univ Press, New York).
3. Yoder JB, et al. (2010) Ecological opportunity and the origin of adaptive radiations. J Evol Biol 23(8):1581-1596.
4. Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457(7231):830-836.
5. Grant PR, Grant BR (2008) How & Why Species Multiply: The Radiation of Darwin's Finches (Princeton Univ Press, Princeton).
6. Kambysellis MP, et al. (1995) Pattern of ecological shifts in the diversification of Hawaiian Drosophila inferred from a molecular phylogeny. Curr Biol 5(10):1129-1139.
7. Morales-Hojas R, Vieira J (2012) Phylogenetic patterns of geographical and ecological diversification in the subgenus Drosophila. PLoS ONE 7(11):e49552.
8. Losos JB (2009) Lizards in an Evolutionary Tree: The Ecology of Adaptive Radiation in Anoles (Univ of California Press, Berkeley, California).
9. Wagner CE, Harmon LJ, Seehausen O (2012) Ecological opportunity and sexual selection together predict adaptive radiation. Nature 487(7407):366-369.
10. Salzburger W (2009) The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 18(2):169-185.
11. Etienne RS, Haegeman B (2012) A conceptual and statistical framework for adaptive radiations with a key role for diversity dependence. Am Nat 180(4):E75-E89.
12. Losos JB, Mahler DL (2010) Evolution Since Darwin: The First 150 Years, eds Bell MA, Futuyma DJ, Eanes WF, Levinton JS (Sinauer, Sunderland, MA), pp 381-420.
13. Hunter JP (1998) Key innovations and the ecology of macroevolution. Trends Ecol Evol 13(1):31-36.
14. Heard SB, Hauser DL (1995) Key evolutionary innovations and their ecological mechanisms. Hist Biol 10(2):151-173.
15. Liem K (1973) Evolutionary strategies and morphological innovations: Cichlid pharyngeal jaws. Syst Biol 22(4):425-441.
16. Price SA, et al. (2010) Functional innovations and morphological diversification in parrotfish. Evolution 64(10):3057-3068.
17. Wainwright PC, et al. (2012) The evolution of pharyngognathy: A phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. Syst Biol 61(6):1001-1027.
18. Jønsson KA, et al. (2012) Ecological and evolutionary determinants for the adaptive radiation of the Madagascan vangas. Proc Natl Acad Sci USA 109(17):6620-6625.
19. West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Q Rev Biol 58(2):155-183.
20. Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci USA 78(6):3721-3725.
21. Carson HL (1997) Sexual selection: A driver of genetic change in Hawaiian Drosophila. J Hered 88(5):343-352.
22. Mendelson TC, Shaw KL (2005) Sexual behaviour: Rapid speciation in an arthropod. Nature 433(7024):375-376.
23. Sauer J, Hausdorf B (2009) Sexual selection is involved in speciation in a land snail radiation on Crete. Evolution 63(10):2535-2546.
24. Carlson BA, et al. (2011) Brain evolution triggers increased diversification of electric fishes. Science 332(6029):583-586.
25. Ryan MJ (1986) Neuroanatomy influences speciation rates among anurans. Proc Natl Acad Sci USA 83(5):1379-1382.
26. Seehausen O, et al. (2008) Speciation through sensory drive in cichlid fish. Nature 455(7213):620-626.
27. Edwards SV, et al. (2005) Speciation in birds: Genes, geography, and sexual selection. Proc Natl Acad Sci USA 102(Suppl 1):6550-6557.
28. Price T (2008) Speciation in Birds (Roberts and Co., Greenwood Village, CO).
29. Price T, Pavelka M (1996) Evolution of a colour pattern: History, development, and selection. J Evol Biol 9(4):451-470.
30. Prum RO, LaFountain AM, Berro J, Stoddard MC, Frank HA (2012) Molecular diversity, metabolic transformation, and evolution of carotenoid feather pigments in cotingas (Aves: Cotingidae). J Comp Physiol B 182(8):1095-1116.
31. StoddardMC, Prum RO (2011) How colorful are birds? Evolution of the avian plumage color gamut. Behav Ecol 22(5):1042-1052.
32. Price JJ, Friedman NR, Omland KE (2007) Song and plumage evolution in the New World orioles (Icterus) show similar lability and convergence in patterns. Evolution 61(4):850-863.
33. Prager M, Andersson S (2010) Convergent evolution of red carotenoid coloration in widowbirds and bishops (Euplectes spp.). Evolution 64(12):3609-3619.
34. Durrer H (1977) Schillerfarben der vogelfeder als evolutionsproblem [Iridescent colors of bird feathers as an evolutionary question]. Denkschr Schweiz Naturforsch Ges 91:1-127.
35. Greenewalt C, Brandt W, Friel D (1960) Iridescent colors of hummingbird feathers. J Opt Soc Am 50(10):1005-1013.
36. Eliason CM, Shawkey MD (2012) A photonic heterostructure produces diverse iridescent colours in duck wing patches. J R Soc Interface 9(74):2279-2289.
37. Shawkey MD, Hauber ME, Estep LK, Hill GE (2006) Evolutionary transitions and mechanisms of matte and iridescent plumage coloration in grackles and allies (Icteridae). J R Soc Interface 3(11):777-786.
38. Durrer H (1970) Schillerfarben der stare (Sturnidae) [Iridescent colors of the starlings (Sturnidae)]. J Ornithol 111(2):133-153.
39. Rubenstein DR, Lovette IJ (2009) Reproductive skew and selection on female ornamentation in social species. Nature 462(7274):786-789.
40. Bennett ATD, Cuthill IC, Partridge JC, Lunau K (1997) Ultraviolet plumage colors predict mate preferences in starlings. Proc Natl Acad Sci USA 94(16):8618-8621.
41. Komdeur J, Oorebeek M, van Overveld T, Cuthill IC (2005) Mutual ornamentation, age, and reproductive performance in the European starling. Behav Ecol 16:805-817.
42. Craig AJFK, Hartley AH (1985) The arrangement and structure of feathermelanin granules as a taxonomic character in African Starlings (Sturnidae). Auk 102(3):629-632.
43. Stoddard MC, Prum RO (2008) Evolution of avian plumage color in a tetrahedral color space: A phylogenetic analysis of new world buntings. Am Nat 171(6):755-776.
44. Beaulieu JM, Jhwueng D-C, Boettiger C, O'Meara BC (2012) Modeling stabilizing selection: Expanding the Ornstein-Uhlenbeck model of adaptive evolution. Evolution 66(8):2369-2383.
45. Endler JA, Westcott DA, Madden JR, Robson T (2005) Animal visual systems and the evolution of color patterns: Sensory processing illuminates signal evolution. Evolution 59(8):1795-1818.
46. FitzJohn RG (2012) Diversitree: Comparative phylogenetic analyses of diversification in R. Methods Ecol Evol 3(6):1084-1092.
47. Price TD (2010) The roles of time and ecology in the continental radiation of the Old World leaf warblers (Phylloscopus and Seicercus). Philos Trans R Soc Lond B Biol Sci 365(1547):1749-1762.
48. Arak A, Enquist M, Arak A, Enquist M (1993) Hidden preferences and the evolution of signals. Philos Trans R Soc Lond B Biol Sci 340:207-213.
49. Enquist M, Arak A (1993) Selection of exaggerated male traits by female aesthetic senses. Nature 361(6411):446-448.
50. Verzijden MN, et al. (2012) The impact of learning on sexual selection and speciation. Trends Ecol Evol 27(9):511-519.
51. Irwin DE, Price T (1999) Sexual imprinting, learning and speciation. Heredity 82(4): 347-354.
52. Burley NT, Symanski R (1998) "A taste for the beautiful": Latent aesthetic mate preferences for white crests in two species of Australian grassfinches. Am Nat 152(6): 792-802.
53. Schluter D (2009) Evidence for ecological speciation and its alternative. Science 323(5915):737-741.
54. Mani GS, Clarke BC (1990) Mutational order: A major stochastic process in evolution. Proc R Soc Lond B Biol Sci 240(1297):29-37.
55. Prum RO (2010) The Lande-Kirkpatrick mechanism is the null model of evolution by intersexual selection: Implications for meaning, honesty, and design in intersexual signals. Evolution 64(11):3085-3100.
56. Price T (1998) Sexual selection and natural selection in bird speciation. Philos Trans R Soc B 353:251-260.
57. Meadows MG, Roudybush TE, McGraw KJ (2012) Dietary protein level affects iridescent coloration in Anna's hummingbirds, Calypte anna. J Exp Biol 215(16):2742-2750.
58. McGraw KJ, Mackillop EA, Dale J, Hauber ME (2002) Different colors reveal different information: How nutritional stress affects the expression of melanin- and structurally based ornamental plumage. J Exp Biol 205(23):3747-3755.
59. Hill GE, Doucet SM, Buchholz R (2005) The effect of coccidial infection on iridescent plumage coloration in wild turkeys. Anim Behav 69(2):387-394.
60. Eliason CM, Shawkey MD (2011) Decreased hydrophobicity of iridescent feathers: A potential cost of shiny plumage. J Exp Biol 214(13):2157-2163.
61. Uyeda JC, Arnold SJ, Hohenlohe PA, Mead LS (2009) Drift promotes speciation by sexual selection. Evolution 63(3):583-594.
62. Fjeldså J, Bowie RC (2008) New perspectives on the origin and diversification of Africa's forest avifauna. Afr J Ecol 46(3):235-247.
63. Jetz W, Rahbek C, Colwell RK (2004) The coincidence of rarity and richness and the potential signature of history in centres of endemism. Ecol Lett 7(12):1180-1191.
64. Cracraft J (1990) Evolutionary Innovations, ed Nitecki MH (Univ of Chicago Press, Chicago), pp 21-44.
65. Kraaijeveld K, Kraaijeveld-Smit FJL, Maan ME (2011) Sexual selection and speciation: The comparative evidence revisited. Biol Rev Camb Philos Soc 86(2):367-377.
66. Rabosky DL, Glor RE (2010) Equilibrium speciation dynamics in a model adaptive radiation of island lizards. Proc Natl Acad Sci USA 107(51):22178-22183.
67. Lovette IJ, Rubenstein DR (2007) A comprehensive molecular phylogeny of the starlings (Aves: Sturnidae) and mockingbirds (Aves: Mimidae): Congruent mtDNA and nuclear trees for a cosmopolitan avian radiation. Mol Phylogenet Evol 44(3):1031-1056.
68. Lovette IJ, McCleery BV, Talaba AL, Rubenstein DR (2008) A complete species-level molecular phylogeny for the "Eurasian" starlings (Sturnidae: Sturnus, Acridotheres, and allies): Recent diversification in a highly social and dispersive avian group. Mol Phylogenet Evol 47(1):251-260.
69. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214.
70. Weir JT, Schluter D (2008) Calibrating the avian molecular clock. Mol Ecol 17(10): 2321-2328.
71. Nylander JAA, Wilgenbusch JC, Warren DL, Swofford DL (2008) AWTY (are we there yet?): A system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics 24(4):581-583.
72. Maia R, D'Alba L, Shawkey MD (2011) What makes a feather shine? A nanostructural basis for glossy black colours in feathers. Proc Biol Sci 278(1714):1973-1980.
73. Pagel M, Meade A (2006) Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. Am Nat 167(6):808-825.
74. Pagel M, Meade A, Barker D (2004) Bayesian estimation of ancestral character states on phylogenies. Syst Biol 53(5):673-684.
75. Kass R, Raferty A (1995) Bayes factors. J Am Stat Assoc 90(430):773-795.
76. Goldberg EE, Igić B (2008) On phylogenetic tests of irreversible evolution. Evolution 62(11):2727-2741.
77. Hart NS (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20(5): 675-703.
78. Endler JA, Day LB (2006) Ornament colour selection, visual contrast and the shape of colour preference functions in great bowerbirds, Chlamydera nuchalis. Anim Behav 72:1405-1416.
79. Maia R, Eliason CM, Bitton P-P, Doucet SM, Shawkey MD (2013) pavo: an R package for the analysis, visualization and organization of spectral data. Methods Ecol Evol, 10.1111/2041-210X.12069.
80. Huelsenbeck JP, Nielsen R, Bollback JP (2003) Stochastic mapping of morphological characters. Syst Biol 52(2):131-158.
81. Boettiger C, Coop G, Ralph P (2012) Is your phylogeny informative? Measuring the power of comparative methods. Evolution 66(7):2240-2251.
82. Revell LJ (2012) phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217-223.
83. Rabosky DL (2010) Extinction rates should not be estimated from molecular phylogenies. Evolution 64(6):1816-1824.
84. Hugall AF, Stuart-Fox D (2012) Accelerated speciation in colour-polymorphic birds. Nature 485(7400):631-634.
85. Price SA, Hopkins SSB, Smith KK, Roth VL (2012) Tempo of trophic evolution and its impact on mammalian diversification. Proc Natl Acad Sci USA 109(18):7008-7012.
86. Hadfield JD, Nakagawa S (2010) General quantitative genetic methods for comparative biology: Phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J Evol Biol 23(3):494-508.