Eumelanin-based coloration and fitness parameters in birds: A meta-analysis

Behavioral Ecology and Sociobiology

Volumn 65, Issue 4, 2011, Pages 559-567

  Meunier, Joël ^a,b   Pinto, Susana Figueiredo ^a   Burri, Reto ^a   Roulin, Alexandre ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Condition dependent; Fitness; Melanin based coloration; Meta analysis; Natural and sexual selection

Indexed keywords

BIRD; BROOD SIZE; CLUTCH SIZE; COLOR; DIMORPHISM; FITNESS; MELANIN; META-ANALYSIS; POLYMORPHISM; SEXUAL SELECTION; SURVIVAL;

ANIMALIA; AVES;

EID: 79952710370     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-010-1092-z     Document Type: Review

References (105)

1. Alström P, Ericson PGP, Olsson U, Sundberg P (2006) Phylogeny and classification of the avian superfamily Sylvioidea. Mol Phyl Evol 38: 381-297.
2. Amat JA (2005) Does the expression of a male plumage trait in female Kentish plovers (Charadrius alexandrinus) signal individual quality? J Ornithol 146: 287-290.
3. Anderson TM, vonHoldt BM, Candille SI, Musiani M, Greco C, Stahler DR, Smith DW, Padhukasahasram B, Randi E, Leonard JA, Bustamante CD, Ostrander EA, Tang H, Wayne RK, Barsh GS (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323: 1339-1343.
4. Antoniazza S, Burri R, Fumagalli L, Goudet J, Roulin A (2010) Local adaptation maintains clinal variation in melanin-based coloration of European barn owls (Tyto alba). Evolution 64: 1944-1954.
5. Bize P, Gasparini J, Klopfenstein A, Altwegg R, Roulin A (2006) Melanin-based coloration is a nondirectionally selected sex-specific signal of offspring development in the Alpine Swift. Evolution 60: 2370-2380.
6. Bókony V, Liker A, Lendvai AZ, Kulcsár A (2008) Risk-taking and survival in the house sparrow Passer domesticus: are plumage ornaments costly? Ibis 150: 139-151.
7. Bond AB, Kamil AC (1998) Apostatic selection by blue jays produces balanced polymorphism in virtual prey. Nature 395: 594-596.
8. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Sorci G (2003) Assessing the cost of mounting an immune response. Am Nat 161: 367-379.
9. Bonser RHC (1995) Melanin and the abrasion resistance of feathers. Condor 97: 590-591.
10. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR (2009) Introduction to meta-analysis. John Wiley & Sons, Ltd, Chichester.
11. Bortolotti GR, Blas J, Negro JJ, Tella JL (2006) A complex plumage pattern as an honest social signal. Anim Behav 72: 423-430.
12. Brommer JE, Ahola K, Karstinen T (2005) The colour of fitness: plumage coloration and lifetime reproductive success in the tawny owl. Proc R Soc Lond B Biol Sci 272: 935-940.
13. Brown JW, Payne RB, Mindell DP (2007) Comment. Nuclear DNA does not reconcile 'rocks' and 'clocks' in Neoaves: a comment on Ericson et al. Biol Lett 3: 257-259.
14. Buchanan KL, Evans MR, Goldsmith AR, Bryant DM, Rowe LV (2001) Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signalling? Proc R Soc Lond B Biol Sci 268: 1337-1344.
15. Burtt EH (1979) Tips on wings and other things. In: Burtt EH (ed) The behavioural significance of color. Garland STPM Press, New York, pp 75-100.
16. Chakarov N, Boerner M, Krüger O (2008) Fitness in common buzzards at the cross-point of opposite melanin-parasite interactions. Funct Ecol 22: 1062-1069.
17. Childress RB, Bennun LA (2002) Sexual character intensity and its relationship to breeding timing, fecundity and mate choice in the great cormorant Phalacrocorax carbo lucidus. J Avian Biol 33: 23-30.
18. Clusella Trullas S, van Wyk JH, Spotila JR (2007) Thermal melanism in ectotherms. J Therm Biol 32: 235-245.
19. Cooch G (1961) Ecological aspects of the blue-snow goose complex. Auk 78: 72-89.
20. Cooke F, Findlay CS, Rockwell RF, Smith JA (1985) Life history studies of the lesser snow goose (Anser caerulescens caerulescens): III. The selective value of plumage polymorphism: net fecundity. Evolution 39: 165-177.
21. Cooke F, Rockwell RF, Lank DB (1995) The snow geese of La Pérouse Bay, natural selection in the wild. Oxford University Press, Oxford.
22. Dale J (2000) Ornamental plumage does not signal male quality in red-billed queleas. Proc R Soc Lond B Biol Sci 267: 2143-2149.
23. Davis JWF (1976) Breeding success and experience in the Arctic skua, Stercorarius parasiticus (L.). J Anim Ecol 45: 531-535.
24. Doucet SM, Mennill DJ, Montgomerie R, Boag PT, Ratcliffe LM (2005) Achromatic plumage reflectance predicts reproductive success in male black-capped chickadees. Behav Ecol 16: 218-222.
25. Ducrest A-L, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23: 502-510.
26. Ericson P, Anderson C, Britton T, Elzanowski A, Johansson U, Källersjö M, Ohlson J, Parsons T, Zuccon D, Mayr G (2006) Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2: 543-547.
27. Fain MG, Houde P (2004) Parallel Radiations in the primary clades of birds. Evolution 58: 2558-2573.
28. Fargallo JA, Laaksonen T, Korpimäki E, Wakamatsu K (2007) A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol Ecol 21: 157-171.
29. Ferguson-Lees J, Christie DA (2001) Raptors of the world. Helm Identification Guides, London.
30. Fitze PS, Richner H (2002) Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav Ecol 13: 401-407.
31. Galeotti P, Sacchi R (2003) Differential parasitaemia in the tawny owl (Strix aluco): effects of colour morph and habitat. J Zool 261: 91-99.
32. Galván I, Alonso-Alvarez C (2008) An intracellular antioxidant determines the expression of a melanin-based signal in a bird. PLoS Biol 3: e3335.
33. Gasparini J, Bize P, Piault R, Kazumasa W, Blount J, Roulin A (2009) Strength and cost of mounting an immune response are associated with a heritable melanin-based color trait in female tawny owls. J Anim Ecol 78: 608-616.
34. Götmark F (1987) White underparts in gull function as hunting camouflage. Anim Behav 35: 1786-1792.
35. Götmark F (1993) Conspicuous coloration in male birds is favoured by predation in some species and disfavoured in others. Proc R Soc Lond B Biol Sci 253: 143-146.
36. Grant BR (1990) The significance of subadult plumage in Darwin's finches, Geospiza fortis. Behav Ecol 1: 161-170.
37. Grant BR, Grant PR (1987) Mate choice in Darwin's finches. Biol J Linn Soc 32: 247-270.
38. Griffith SC (2000) A trade-off between reproduction and a condition-dependent sexually selected ornament in the house sparrow Passer domesticus. Proc R Soc Lond B Biol Sci 267: 1115-1119.
39. Griffith SC, Owens IPF, Burke T (1999) Female choice and annual reproductive success favour less-ornamented male house sparrows. Proc R Soc Lond B Biol Sci 266: 765-770.
40. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763-1768.
41. Hanssen SV, Folstad I, Erikstad KE (2006) White plumage reflects individual quality in female eiders. Anim Behav 71: 337-343.
42. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2008) A label of health: a previous immune challenge is reflected in the expression of a female plumage trait. Biol Lett 4: 379-381.
43. Hatch SA (1991) Evidence for color phase effects on the breeding and life history of northern fulmars. Condor 93: 4090-4417.
44. Hoekstra HE, Krenz JG, Nachman MW (2005) Local adaptation in the rock pocket mouse (Chaetodipus intermedius): natural selection and phylogenetic history of populations. Heredity 94: 217-228.
45. Horth L (2003) Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki). Proc R Soc Lond B Biol Sci 266270: 1033-1040.
46. Hughes JM, Lange CL, Mather PB, Robinson A (2002) A comparison of fitness components among different plumage morphs of the Australian Magpie. Gymnorhina tibicen Emu 102: 331-338.
47. Järvi T, Røskaft E, Bakken M, Zumsteg B (1987) Evolution of variation in male secondary sexual characteristics. A test of eight hypotheses applied to pied flycatchers. Behav Ecol Sociobiol 20: 161-169.
48. Jawor JM, Breitwisch R (2003) Melanin ornaments, honesty, and sexual selection. Auk 120: 249-265.
49. Jensen H, Sæther BE, Ringsby TH, Tufto J, Griffith SC, Ellegren H (2003) Sexual variation in heritability and genetic correlations of morphological traits in house sparrow (Passer domesticus). J Evol Biol 16: 1296-1307.
50. Jensen H, Sæther BE, Ringsby TH, Tufto J, Griffith SC, Ellegren H (2004) Lifetime reproductive success in relation to morphology in the house sparrow Passer domesticus. J Anim Ecol 73: 599-611.
51. Johannesson K, Ekendahl A (2002) Selective predation favouring cryptic individuals of marine snails (Littorina). Biol J Linn Soc 76: 137-144.
52. Johansson US, Fjeldså J, Bowie RCK (2008) Phylogenetic relationships within Passerida (Aves: Passeriformes): a review and a new molecular phlogeny based on three nuclear intron marklers. Mol Phyl Evol 48: 858-876.
53. Jones JS, Leith BH, Rawlings P (1977) Polymorphism in Cepaea: a problem with too many solutions? Annu Rev Ecol Syst 8: 109-143.
54. Kimball RT, Braun EL (2008) A multigene phylogeny of Galliformes supports a single origin of erectile ability in non-feathered facial traits. J Avian Biol 39: 438-445.
55. Kingma S, Szentirmai I, Székely T, Bókony V, Bleeker M, Liker A, Komdeur J (2008) Sexual selection and the function of a melanin-based plumage ornament in polygamous penduline tits Remiz pendulinus. Behav Ecol Sociobiol 62: 1277-1288.
56. Kristín A, Valera F, Hoi C, Hoi H (2007) Do melanin-based tail patterns predict individual quality and sex in Lesser Grey Shrikes Lanius minor? J Ornithol 148: 1-8.
57. Lajeunesse MJ (2009) Meta-analysis and the comparative phylogenetic method. Am Nat 174: 369-381.
58. Lemon RE, Weary DM, Norris KJ (1992) Male morphology and behavior correlate with reproductive success in the American redstart (Setophaga ruticilla). Behav Ecol Sociobiol 29: 399-403.
59. Lendvai AZ, Liker A (2004) Male badge size is related to clutch volume in the Kentish plover. Ornis Hung 14: 1-7.
60. Losey JE, Uves AR, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintaine by opposite patterns of parasitism and predation. Nature 388: 269-272.
61. Lovette IJ, Bermingham E (2002) What is a wood-warbler? Molecular characterization of a monophyletic Parulidae. Auk 119: 695-714.
62. Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2. 6 http://mesquiteproject. org.
63. McGraw KJ (2005) The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants? Anim Behav 69: 757-764.
64. McGraw KJ, Hill GE (2000) Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc R Soc Lond B Biol Sci 267: 1525-1531.
65. 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: 3747-3755.
66. McKinnon EA, Robertson RJ (2008) The signal function of a melanin-based plumage ornament in golden-winged warblers. Wilson J Ornithol 120: 366-370.
67. Mackintosh JA (2001) The antimicrobial properties of melanocytes, melanosomes and melanin and the evolution of black skin. J Theor Biol 212: 101-128.
68. Møller A, Flensted-Jensen E, Mardal W (2007) Black beak tip coloration as a signal of phenotypic quality in a migratory seabird. Behav Ecol Sociobiol 61: 1561-1571.
69. Møller A, Jennions M (2002) How much variance can be explained by ecologists and evolutionary biologists? Oecologia 132: 492-500.
70. Møller AP, Jennions MD (2001) Testing and adjusting for publication bias. Trends Ecol Evol 16: 580-586.
71. Mundy NI, Badcock NS, Hart T, Scribner K, Janssen K, Nadeau NJ (2004) Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303: 1870-1873.
72. Nakagawa S, Ockendon N, Gillespie DOS, Hatchwell BJ, Burke T (2007) Assessing the function of house sparrows' bib size using a flexible meta-analysis method. Behav Ecol 18: 831-840.
73. Norris KJ (1990) Female choice and the evolution of the conspicuous plumage coloration of monogamous male great tits. Behav Ecol Sociobiol 26: 129-138.
74. O'Donald P (1983) The arctic skua. Cambridge University Press, Cambridge.
75. Paradis E, Claude J, Strimmer K (2004) APE: analysis of phylogenetics and evolution in R language Bioinformatics. Bioinformatics 20: 289-290.
76. Philips RA, Furness RW (1998) Polymorphism, mating preferences and sexual selection in the Arctic skua. J Zool Lond 245: 245-252.
77. Potti J, Montalvo S (1991) Male colour variation in Spanish pied flycatchers Ficedula hypoleuca. Ibis 133: 293-299.
78. R Development Core Team (2009) R: a language and environment for statistical computing.
79. Rice WR, Gaines SD (1994a) Extending nondirectional heterogeneity tests to evaluate simply ordered alterntive hypotheses. Proc Natl Acad Sci USA 91: 225-226.
80. Rice WR, Gaines SD (1994b) The ordered-heterogeneity family of tests. Biometrics 50: 746-746.
81. Rockwell RF, Scott Findlay C, Cooke F, Smith JA (1985) Life history studies of the Lesser Snow Goose (Anser caerulescens caerulescens): IV. The selective value of plumage polymorphism: net viability, the timing of maturation, and breeding propensity. Evolution 39: 178-189.
82. Rosenberg MS (2005) The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution 59: 464-468.
83. Rosenberg MS, Adams DC, Gurevith J (2000) MetaWin: statistical software for meta-analysis. Sinauer Associates, Sunderland.
84. Rosenthal R (1991) Meta-analytic procedures for social research. Applied Social Research Methods. Sage Publications, Newbury.
85. Roulin A (2004) The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev 79: 815-848.
86. Roulin A, Altwegg R (2007) Breeding rate is associated with pheomelanism in male and with eumelanism in female barn owls. Behav Ecol 18: 563-570.
87. Roulin A, Richner H, Ducrest A-L (1998) Genetic, environmental and condition-dependent effects on female and male plumage ornamentation. Evolution 52: 1451-1460.
88. Roulin A, Ducrest A-L, Ravussin P-A, Altwegg R (2003) Female plumage coloration covaries with reproductive strategies in the tawny owl. J Avian Biol 34: 251-258.
89. Roulin A, Wink M (2004) Predator-prey polymorphism: relationships and the evolution of colour a comparative analysis in diurnal raptors. Biol J Linn Soc 81: 565-578.
90. Roulin A, Almais B, Rossi-Pedruzzi A, Ducrest A-L, Wakamatsu K, Miksik I, Blount JD, Jenni-Eiermann S, Jenni L (2008) Corticosterone mediates the condition-dependent component of melanin-based coloration. Anim Behav 75: 1351-1358.
91. Roulin A, Wink M, Salamin N (2009) Selection on a eumelanic ornament is stronger in the tropics than in temperate zones in the worldwide-distributed barn owl. J Evol Biol 22: 345-354.
92. Roulin A, Altwegg R, Jensen H, Steinsland I, Schaub M (2010) Sex-dependent selection on an autosomal melanic female ornament promotes the evolution of sex ratio bias. Ecol Lett 13: 616-626.
93. Sanderson MJ (2002) Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol Biol Evol 19: 101-109.
94. Schroeder J, Lourenço P, van der Velde M, Hooijmeijer J, Both C, Piersma T (2009) A possible case of contemporary selection leading to a decrease in sexual plumage dimorphism in a grassland-breeding shorebird. Behav Ecol 20: 797-807.
95. Sheldon BC, West SA (2004) Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. Am Nat 163: 40-54.
96. Siefferman L, Hill GE (2005) Evidence for sexual selection on strucutral plumage coloration in female Eastern Bluebirds (Sialia sialis). Evolution 59: 1819-1828.
97. Sokal RR, Rohlf FJ (1995) BIOMETRY: The principles and practice of statistics in biological research. W. H. Freeman and Company, New York.
98. Swofford DL (2003) PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland.
99. Tella JL, Forero MG, Donazar JA, Hiraldo F (1997) Is the expression of male traits in female lesser kestrels related to sexual selection? Ethology 103: 72-81.
100. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
101. Thusius KJ, Peterson KA, Dunn PO, Whittingham LA (2001) Male mask size is correlated with mating success in the common yellowthroat. Anim Behav 62: 435-446.
102. Treplin S, Siegert R, Bleidorn C, Thompson HS, Fotso R, Tiedemann R (2008) Molecular phylogeny of songbirds (Aves: Passeriformes) and the relative utility of common nuclear marker loci. Cladistics 24: 328-349.
103. Vaclav R, Hoi H (2002) Different reproductive tactics in house sparrows signalled by badge size: is there a benefit to being average? Ethology 108: 569-582.
104. Vergara P, Fargallo JA, Martínez-Padilla J, Lemus JA (2009) Inter-annual variation and information content of melanin-based coloration in female Eurasian kestrels. Biol J Linn Soc 97: 781-790.
105. West SA, Shuker DM, Sheldon BC (2005) Sex-ratio adjustment when relatives interact: a test of constraints on adaptation. Evolution 59: 1211-1228.