Sexually selected dichromatism in the hihi Notiomystis cincta: Multiple colours for multiple receivers

Journal of Evolutionary Biology

Volumn 27, Issue 8, 2014, Pages 1522-1535

  Walker, L K ^a,b,c   Ewen, J G ^b   Brekke, P ^b   Kilner, R M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE OF ZOOLOGY   (United Kingdom)

^c RSPB CENTRE FOR CONSERVATION SCIENCE   (United Kingdom)

Author keywords

Bateman gradient; Plumage colour; Selection gradient; Sexual dichromatism; Sexual selection

Indexed keywords

ADAPTATION; COLOR; GENETIC ANALYSIS; PASSERINE; PLUMAGE; POPULATION STRUCTURE; REPRODUCTIVE SUCCESS; SEXUAL SELECTION;

NEW ZEALAND;

AVES; NOTIOMYSTIS CINCTA;

MICROSATELLITE DNA;

ANIMAL; COMPETITIVE BEHAVIOR; FEATHER; FEMALE; GENETICS; GENOTYPE; MALE; MATE CHOICE; NEW ZEALAND; PHYSIOLOGY; PIGMENTATION; REPRODUCTION; SONGBIRD; STATISTICAL MODEL;

ANIMALS; COMPETITIVE BEHAVIOR; FEATHERS; FEMALE; GENOTYPE; MALE; MATING PREFERENCE, ANIMAL; MICROSATELLITE REPEATS; MODELS, STATISTICAL; NEW ZEALAND; PASSERIFORMES; PIGMENTATION; REPRODUCTION;

EID: 84904425320     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12417     Document Type: Article

References (88)

1. Adler, M. 2010. Sexual conflict in waterfowl: why do females resist extrapair copulations? Behav. Ecol. 21: 182-192.
2. Akcay, C., Searcy, W.A., Campbell, S.E., Reed, V.A., Templeton, C.N., Hardwick, K.M. et al. 2011. Who initiates extrapair mating in song sparrows? Behav. Ecol. 23: 44-50.
3. Andersson, S., Pryke, S.R., Ornborg, J., Lawes, M.J. & Andersson, M. 2002. Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird. Am. Nat. 160: 683-691.
4. Arnold, S.J. 1994. Bateman's principles and the measurement of sexual selection in plants and animals. Am. Nat. 144: S126-S149.
5. Arnold, S.J. & Duvall, D. 1994. Animal mating systems: a synthesis based on selection theory. Am. Nat. 143: 317-348.
6. Baker, R.R. & Parker, G.A. 1979. The evolution of bird coloration. Phil. Trans. R. Soc. B. 287: 63-130.
7. Bateman, A.J. 1948. Intra-sexual selection in Drosophila. Heredity 2: 349-368.
8. Bergeron, P., Montiglio, P.-O., Réale, D., Humphries, M.M. & Garant, D. 2012. Bateman gradients in a promiscuous mating system. Behav. Ecol. Sociobiol. 66: 1125-1130.
9. Biard, C., Surai, P.F. & Møller, A.P. 2005. Effects of carotenoid availability during laying on reproduction in the blue tit. Oecologia 144: 32-44.
10. Brekke, P., Dawson, D.A., Horsburgh, G.J. & Ewen, J.G. 2009. Characterization of microsatellite loci in the hihi Notiomystis cincta (Notiomystidae, Aves). Mol. Ecol. Res. 9: 1255-1258.
11. Brekke, P., Cassey, P., Ariani, C. & Ewen, J.G. 2013. Evolution of extreme mating behaviour: patterns of extra-pair paternity in a species with forced extra-pair copulation. Behav. Ecol. Sociobiol. 67: 963-972.
12. Brooks, R. 2002. Variation in female mate choice within guppy populations: population divergence, multiple ornaments and the maintenance of polymorphism. Genetica 116: 343-358.
13. Brooks, R. & Couldridge, V. 1999. Multiple sexual ornaments coevolve with multiple mating preferences. Am. Nat. 154: 37-45.
14. Budden, A.E. & Dickinson, J.L. 2009. Signals of quality and age: the information content of multiple plumage ornaments in male western bluebirds Sialia mexicana. J. Avian Biol. 40: 18-27.
15. Castro, I., Minot, E.O., Fordham, R.A. & Birkhead, T.R. 1996. Polygynandry, face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Melihagidae). Ibis 138: 765-771.
16. Chain, A.S. & Lyon, B.E. 2008. Adaptive plasticity in female mate choice dampens sexual selection on male ornaments in the lark bunting. Science 319: 459-462.
17. Chiver, I., Stutchbury, B.J.M. & Morton, E.S. 2008. Do male plumage and song characteristics influence female off-territory forays and paternity in the hooded warbler? Behav. Ecol. Sociobiol. 62: 1981-1990.
18. Clutton-Brock, T.H. & Parker, G.A. 1995. Sexual coercion in animal societies. Anim. Behav. 49: 1345-1365.
19. Conover, W.J. 1971. Practical Nonparametric Statistics. John Wiley & Sons, New York.
20. Cuthill, I.C. 2006. Colour perception. In: Bird Colouration. Vol. I. Mechanisms and Measurements (G.E. Hill & K.J. McGraw, eds), pp. 3-40. Harvard University Press, Cambridge, MA.
21. Delhey, K., Johnsen, A., Peters, A., Andersson, S. & Kempenaers, B. 2003. Paternity analysis reveals opposing selection pressures on crown coloration in the blue tit (Parus caeruleus). Proc. R. Soc. B. 270: 2057-2063.
22. Double, M. & Cockburn, A. 2000. Pre-dawn infidelity: females control extra-pair mating in superb fairy-wrens. Proc. R. Soc B. 267: 465-470.
23. Eikenaar, C., Whitham, M., Komdeur, J., van der Velde, M. & Moore, I.T. 2011. Testosterone, plumage colouration and extra-pair paternity in male North-American barn swallows. PLoS One 6: e23288.
24. Endler, J.A. & Mielke, P.W. 2005. Comparing entire colour patterns as birds see them. Biol. J. Linn. Soc. 86: 405-431.
25. Estep, L.K., Mays, H. Jr, Keyser, A.J., Ballentine, B. & Hill, G.E. 2005. Effects of breeding density and plumage coloration on mate guarding and cuckoldry in blue grosbeaks (Passerina caerulea). Can. J. Zool. 83: 1143-1148.
26. Ewen, J.G. & Armstrong, D.P. 2000. Male provisioning is negatively correlated with attempted extrapair copulation frequency in the stitchbird (or hihi). Anim. Behav. 60: 429-433.
27. Ewen, J.G., Armstrong, D.P., Ebert, B. & Hansen, L.H. 2004. Extra-pair copulation and paternity defense in the hihi (or stitchbird) Notiomystis cincta. N. Z. J. Ecol. 28: 233-240.
28. Ewen, J.G., Surai, P.F., Stradi, R., Møller, A.P., Vittorio, B., Griffiths, R. et al. 2006. Carotenoids, colour and conservation in an endangered passerine, the hihi or stitchbird (Notiomystis cincta). Anim. Conserv. 9: 229-235.
29. Ewen, J.G., Thorogood, R. & Armstrong, D.P. 2011. Demographic consequences of adult sex ratio in a reintroduced hihi population. J. Anim. Ecol. 80: 448-455.
30. Fairbairn, D.J. & Preziosi, R.F. 1996. Sexual selection and the evolution of sexual size dimorphism in the water strider, Aquarius remigis. Evolution 50: 1549-1559.
31. Gerlach, N.M., McGlothlin, J.W., Parker, P.G. & Ketterson, E.D. 2012. Reinterpreting Bateman gradients: multiple mating and selection in both sexes of a songbird species. Behav. Ecol. 23: 1078-1088.
32. Götmark, F. 1993. Conspicuous coloration in male birds is favoured by predation in some species and disfavoured in others. Proc. R. Soc. B. 253: 143-146.
33. Götmark, F., Post, P., Olsson, J. & Himmelmann, D. 1997. Natural selection and sexual dimorphism: sex-biased sparrowhawk predation favours crypsis in female chaffinches. Oikos 80: 540-548.
34. Grafen, A. 1987. Measuring sexual selection: why bother? In: Sexual Selection: Testing the Alternatives (J.W. Bradbury & M.B. Andersson, eds), pp. 221-223. John Wiley & Sons, New York.
35. Grafen, A. 1990. Biological signals as handicaps. J. Theor. Biol. 144: 517-546.
36. Grueber, C.E., Nakagawa, S., Laws, R.J. & Jamieson, I.G. 2011. Multimodel inference in ecology and evolution: challenges and solutions. J. Evol. Biol. 24: 699-711.
37. Hart, N.S., Partridge, J.C., Cuthill, I.C. & Bennett, A.T. 2000. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J. Comp. Physiol. A. 186: 375-387.
38. Hemmings, N., West, M. & Birkhead, T.R. 2012. Causes of hatching failure in endangered birds. Biol. Lett. 8: 964-967.
39. Hinde, C.A., Johnstone, R.A. & Kilner, R.M. 2010. Parent-offspring conflict and coadaptation. Science 327: 1373-1376.
40. Hunt, J., Breuker, C.J., Sadowski, J.A. & Moore, A.J. 2009. Male-male competition, female mate choice and their interaction: determining total sexual selection. J. Evol. Biol. 22: 13-26.
41. Ingleby, F.C., Hosken, D.J., Flowers, K., Hawkes, M.F., Lane, S.M., Rapkin, J. et al. 2014. Environmental heterogeneity, multivariate sexual selection and genetic constraints on cuticular hydrocarbons in Drosophila simulans. J. Evol. Biol. 27: 700-713.
42. Jennions, M.D. & Kokko, H. 2010. Sexual selection. In: Evolutionary Behavioral Ecology (D.F. Westneat & C.F. Fox, eds), pp. 343-364. Oxford University Press, Oxford.
43. Jennions, M.D. & Petrie, M. 2000. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75: 21-64.
44. Jones, A.G. 2009. On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution 63: 1673-1684.
45. Jones, A.G., Arguello, J.R. & Arnold, S.J. 2002. Validation of Bateman's principles: a genetic study of sexual selection and mating patterns in the rough-skinned newt. Proc. R. Soc. B. 269: 2533-2539.
46. Jones, A.G., Rosenqvist, G., Berglund, A. & Avise, J.C. 2005. The measurement of sexual selection using Bateman's principles: an experimental test in the sex-role reversed pipefish Syngnathus typhle. Integr. Comp. Biol. 45: 874-884.
47. Kelber, A., Vorobyev, M. & Osorio, D. 2003. Animal colour vision-behavioural tests and physiological concepts. Biol. Rev. 78: 81-118.
48. Kennedy, P. 1992. A Guide to Econometrics. Blackwell, Oxford.
49. Kimball, R.T. & Ligon, J.D. 1999. Evolution of avian plumage dichromatism from a proximate perspective. Am. Nat. 154: 182-193.
50. Klug, H., Heuschele, J., Jennions, M.D. & Kokko, H. 2010. The mismeasurement of sexual selection. J. Evol. Biol. 23: 447-462.
51. Krakauer, A.H., Webster, M.S., Duval, E.H., Jones, A.G. & Shuster, S.M. 2011. The opportunity for sexual selection: not mismeasured, just misunderstood. J. Evol. Biol. 24: 2064-2071.
52. Lande, R. & Arnold, S.J. 1983. The measurement of selection on correlated characters. Evolution 37: 1210-1226.
53. Lehtonen, P.K., Primmer, C.R. & Laaksonen, T. 2009. Different traits affect gain of extrapair paternity and loss of paternity in the pied flycatcher, Ficedula hypoleuca. Anim. Behav. 77: 1103-1110.
54. Lessells, C.M. & Boag, P.T. 1987. Unrepeatable repeatabilities: a common mistake. Auk 104: 116-121.
55. Ligon, J.D. & Zwartjes, P.W. 1995. Ornate plumage of male red junglefowl does not influence mate choice by females. Anim. Behav. 49: 117-125.
56. Low, M. 2005. Female resistance and male force: context and patterns of copulation in the New Zealand stitchbird Notiomystis cincta. J. Avian Biol. 36: 436-448.
57. Low, M., Pärt, T. & Forslund, P. 2007. Age-specific variation in reproduction is largely explained by the timing of territory establishment in the New Zealand stitchbird Notiomystis cincta. J. Anim. Ecol. 76: 459-470.
58. Marchetti, K. 1998. The evolution of multiple male traits in the yellow-browed leaf warbler. Anim. Behav. 55: 361-376.
59. McGlothlin, J.W., Parker, P.G., Nolan, V. Jr & Ketterson, E.D. 2005. Correlational selection leads to genetic integration of body size and an attractive plumage trait in dark-eyed juncos. Evolution 59: 658-671.
60. McGraw, K.J. & Gregory, A.J. 2004. Carotenoid pigments in male American goldfinches: what is the optimal biochemical strategy for becoming colourful? Biol. J. Linn. Soc. 83: 273-280.
61. McGraw, K.J., Safran, R.J. & Wakamatsu, K. 2005. How feather colour reflects its melanin content. Funct. Ecol. 19: 816-821.
62. Mitchell-Olds, T. & Shaw, R.G. 1987. Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41: 1149-1161.
63. Nicholls, J.A., Double, M.C., Rowell, D.M. & Magrath, R.D. 2000. The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J. Avian Biol. 31: 165-176.
64. Oliver, W.R.B. 1955. New Zealand Birds. A.H. and A.W. Reed, Wellington, NZ.
65. Osorio, D. & Vorobyev, M. 2005. Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc. R. Soc. B. 272: 1745-1752.
66. Osorio, D. & Vorobyev, M. 2008. A review of the evolution of animal colour vision and visual communication signals. Vision. Res. 48: 2042-2051.
67. Part, T. & Qvarnström, A. 1997. Badge size in collared flycatchers predicts outcome of male competition over territories. Anim. Behav. 54: 893-899.
68. Perneger, T.V. 1998. What's wrong with Bonferroni adjustments? BMJ 316: 1236-1238.
69. Pizzari, T. & Birkhead, T.R. 2000. Female feral fowl eject sperm of subdominant males. Nature 405: 787-789.
70. Rubenstein, D.R. 2007. Female extrapair mate choice in a cooperative breeder: trading sex for help and increasing offspring heterozygosity. Proc. R. Soc. B. 274: 1895-1903.
71. Saino, N., Stradi, R., Ninni, P., Pini, E. & Møller, A.P. 1999. Carotenoid plasma concentration, immune profile, and plumage ornamentation of male barn swallows (Hirundo rustica). Am. Nat. 154: 441-448.
72. Saks, L., McGraw, K.J. & Hõrak, P. 2003. How feather colour reflects its carotenoid content. Funct. Ecol. 17: 555-561.
73. Sardell, R.J., Keller, L.F., Arcese, P., Bucher, T. & Reid, J.M. 2010. Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows, Melospiza melodia. Mol. Ecol. 19: 4352-4364.
74. Sheldon, B.C. & Ellegren, H. 1999. Sexual selection resulting from extrapair paternity in collared flycatchers. Anim. Behav. 57: 285-298.
75. Shine, R. & Madsen, T. 1994. Sexual dichromatism in snakes of the genus vipera: a review and a new evolutionary hypothesis. J. Herpetol. 28: 117-120.
76. Sokal, R.R. & Rohlf, F.J. 1995. Biometry: The Principles and Practice of Statistics in Biological Research, 3rd edn. W. H. Freeman and Company, New York.
77. Stevens, M., Stoddard, M.C. & Higham, J.P. 2009. Studying primate color: towards visual system-dependent methods. Int. J. Primatol. 30: 893-917.
78. Stoddard, M.C. & Prum, R.O. 2011. How colorful are birds? Evolution of the avian plumage color gamut. Behav. Ecol. 22: 1042-1052.
79. Tarvin, K.A. & Murphy, T.G. 2012. It isn't always sexy when both are bright and shiny: considering alternatives to sexual selection in elaborate monomorphic species. Ibis 154: 439-443.
80. Van Rooij, E.P. & Griffith, S.C. 2012. No evidence of assortative mating on the basis of putative ornamental traits in long-tailed finches Poephila acuticauda. Ibis 154: 444-451.
81. Vedder, O., Komdeur, J., van der Velde, M., Schut, E. & Magrath, M.J.L. 2011. Polygyny and extra-pair paternity enhance the opportunity for sexual selection in blue tits. Behav. Ecol. Sociobiol. 65: 741-752.
82. Walker, L.K., Stevens, M., Karadas, F., Kilner, R.M. & Ewen, J.G. 2013. A window on the past: male ornamental plumage reveals the quality of their early-life environment. Proc. R. Soc. B. 280: 20122852.
83. Wang, J. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166: 1963-1979.
84. Wang, J. & Santure, A.W. 2009. Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181: 1579-1594.
85. Webster, M.S., Pruett-Jones, S., Westneat, D.F. & Arnold, S.J. 1995. Measuring the effects of pairing success, extra-pair copulations and mate quality on the opportunity for sexual selection. Evolution 49: 1147-1157.
86. Westneat, D.F. 2006. No evidence of current sexual selection on sexually dimorphic traits in a bird with high variance in mating success. Am. Nat. 167: e171-e189.
87. Westneat, D.F. & Stewart, I.R.K. 2003. Extra-pair paternity in birds: causes, correlates, and conflict. Annu. Rev. Ecol. Evol. Syst. 34: 365-396.
88. Zahavi, A. & Zahavi, A. 1997. The Handicap Principle: A Missing Piece of Darwin's Puzzle. Oxford University Press, Oxford.