More ornamented females produce higher-quality offspring in a socially monogamous bird: An experimental study in the great tit (Parus major)

Frontiers in Zoology

Volumn 10, Issue 1, 2013, Pages

  Remeš, Vladimír ^a   Matysioková, Beata ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

Carotenoids; Coloration; Great tit; Immunity; Melanins; Mutual choice; Ornaments; Parental care

Indexed keywords

ANIMALIA; AVES; PARUS MAJOR; PASSERIFORMES;

EID: 84875321221     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-10-14     Document Type: Article

References (77)

1. Hill GE. McGraw KJ: Bird Coloration, Volume 1 2006, Mechanisms and Measurements. Cambridge: Harvard University Press.
2. Hill GE. McGraw KJ: Bird Coloration, Volume 2 2006, Function and Evolution. Cambridge: Harvard University Press.
3. Ruxton GD, Sherratt TN, Speed MP. Avoiding Attack: The Evolutionary Ecology of Crypsis, Warning Signals and Mimicry 2004, Oxford: Oxford University Press.
4. Andersson M. Sexual Selection 1994, Princeton: Princeton University Press.
5. Dunn PO, Whittingham LA, Pitcher TE. Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 2001, 55:161-175.
6. Møller AP, Alatalo RV. Good-genes effects in sexual selection. Proc R Soc B 1999, 266:85-91.
7. Møller AP, Jennions MD. How important are direct fitness benefits of sexual selection?. Naturwissenschaften 2001, 88:401-415. 10.1007/s001140100255, 11729807.
8. Fisher RA. The Genetical Theory of Natural Selection 1930, Oxford: Clarendon Press.
9. Clutton-Brock T. Sexual Selection in Males and Females. Science 2007, 318:1882-1885. 10.1126/science.1133311, 18096798.
10. Cockburn A. Prevalence of different modes of parental care in birds. Proc R Soc B 2006, 273:1375-1383. 10.1098/rspb.2005.3458, 1560291, 16777726.
11. Amundsen T, Pärn H. Female Coloration: Review of Functional and Nonfunctional Hypotheses. Bird Coloration, Vol. 2: Function and Evolution 2006, 280-348. Cambridge: Harvard University Press, Hill GE, McGraw KJ.
12. Poissant J, Wilson AJ, Coltman DW. Sex-specific genetic variance and the evolution of sexual dimorphism: a systematic review of cross-sex genetic correlations. Evolution 2010, 64:97-107. 10.1111/j.1558-5646.2009.00793.x, 19659596.
13. Rubenstein DR, Lovette IJ. Reproductive skew and selection on female ornamentation in social species. Nature 2009, 462:786-789. 10.1038/nature08614, 20010686.
14. LeBas NR. Female finery is not for males. Trends Ecol Evol 2006, 21:170-173. 10.1016/j.tree.2006.01.007, 16701080.
15. Kraaijeveld K, Kraaijeveld-Smit FJL, Komdeur J. The evolution of mutual ornamentation. Anim Behav 2007, 74:657-677.
16. Clutton-Brock T. Sexual selection in females. Anim Behav 2009, 77:3-11.
17. Berglund A, Rosenqvist G. Male pipefish prefer ornamented females. Anim Behav 2001, 61:345-350.
18. Griggio M, Valera F, Casas A, Pilastro A. Males prefer ornamented females: a field experiment of male choice in the rock sparrow. Anim Behav 2005, 69:1243-1250.
19. Amundsen T, Forsgren E, Hansen LTT. On the function of female ornaments: male bluethroats prefer colourful females. Proc R Soc B 1997, 264:1579-1586.
20. Janhunen M, Kekäläinen J, Kortet R, Hyvärinen P, Piironen J. No evidence for an indirect benefit from female mate preference in Arctic charr Salvelinus alpinus, but female ornamentation decreases offspring viability. Biol J Linn Soc 2011, 103:602-611.
21. Kekäläinen J, Huuskonen H, Tuomaala M, Kortet R. Both male and female sexual ornaments reflect offspring performance in a fish. Evolution 2010, 64:3149-3157. 10.1111/j.1558-5646.2010.01084.x, 20629728.
22. Weiss SL, Kennedy EA, Bernhard JA. Female-specific ornamentation predicts offspring quality in the striped plateau lizard, Sceloporus virgatus. Behav Ecol 2009, 20:1063-1071.
23. Roulin A, Jungi TW, Pfister H, Dijkstra C. Female barn owls (Tyto alba) advertise good genes. Proc R Soc B 2000, 267:937-941. 10.1098/rspb.2000.1093, 1690619, 10853738.
24. Roulin A, Riols C, Dijkstra C, Ducrest A. Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol 2001, 12:103-110.
25. Roulin A. Proximate basis of the covariation between a melanin-based female ornament and offspring quality. Oecologia 2004, 140:668-675.
26. Velando A, Lessells CM, Márquez JC. The function of female and male ornaments in the Inca Tern: evidence for links between ornament expression and both adult condition and reproductive performance. J Avian Biol 2001, 4:311-318.
27. Rohde PA, Johnsen A, Lifjeld JT. Female plumage coloration in the Bluethroat: no evidence for an indicator of maternal quality. Condor 1999, 101:96-104.
28. Siefferman L, Hill GE. Evidence for sexual selection on structural plumage coloration in female eastern bluebirds (Sialia sialis). Evolution 2005, 59:1819-1828.
29. Doutrelant C, Grégoire A, Grnac N, Gomez D, Lambrechts MM, Perret P. Female coloration indicates female reproductive capacity in blue tits. J Evol Biol 2008, 21:226-233.
30. Evans SR, Hinks AE, Wilkin TA, Sheldon BC. Age, sex and beauty: methodological dependence of age- and sex-dichromatism in the great tit Parus major. Biol J Linn Soc 2010, 101:777-796.
31. Delhey K, Peters A. Quantifying variability of avian colours: are signalling traits more variable?. PLoS ONE 2008, 3:e1689. 10.1371/journal.pone.0001689, 2253496, 18301766.
32. Hegyi G, Szigeti B, Török J, Eens M. Melanin, carotenoid and structural plumage ornaments: information content and role in great tits Parus major. J Avian Biol 2007, 38:698-708.
33. Roulin A, Gasparini J, Bize P, Ritschard M, Richner H. Melanin-based colorations signal strategies to cope with poor and rich environments. Behav Ecol Sociobiol 2008, 62:507-519.
34. Matysioková B, Remeš V. Incubation Feeding and Nest Attentiveness in a Socially Monogamous Songbird: Role of Feather Colouration, Territory Quality and Ambient Environment. Ethology 2010, 116:596-607.
35. Remeš V, Matysioková B, Klejdus B. Egg yolk antioxidant deposition as a function of parental ornamentation, age, and environment in great tits Parus major. J Avian Biol 2011, 42:387-396.
36. Chew BP, Park JS. Carotenoid Action on the Immune Response. J Nutr 2004, 134:S257-S261.
37. Remeš V. Yolk androgens in great tit eggs are related to male attractiveness, breeding density and territory quality. Behav Ecol Sociobiol 2011, 65:1257-1266.
38. Saino N, Martinelli R, Biard C, Gil D, Spottiswoode CN, Rubolini D, Surai PF, Møller AP. Maternal immune factors and the evolution of secondary sexual characters. Behav Ecol 2007, 18:513-520.
39. Hasselquist D, Nilsson J-T. Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Philos T R Soc B 2009, 364:51-60.
40. Ducrest A-L, Keller L, Roulin V. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 2008, 23:502-510. 10.1016/j.tree.2008.06.001, 18644658.
41. Tripet F, Glaser M, Richner H. Behavioural responses to ectoparasites: time-budget adjustments and what matters to Blue Tits Parus caeruleus infested by fleas. Ibis 2002, 144:461-469.
42. Hutrez-Bousses S, Perret P, Renaud F, Blondel J. High blowfly parasitic loads affect breeding success in a Mediterranean population of blue tits. Oecologia 1997, 112:514-517.
43. Simon A, Thomas D, Blondel J, Perret P, Lambrechts MM. Physiological Ecology of Mediterranean Blue Tits (Parus caeruleus L.): Effects of Ectoparasites (Protocalliphora spp.) and Food Abundance on Metabolic Capacity of Nestlings. Physiol Biochem Zool 2004, 77:492-501. 10.1086/383512, 15286922.
44. Remeš V, Krist M. Nest design and the abundance of parasitic Protocalliphora blow flies in two hole-nesting passerines. Ecoscience 2005, 12:549-553.
45. Griffith SC, Parker TH, Olson VA. Melanin- versus carotenoid-based sexual signals: is the difference really so black and red?. Anim Behav 2006, 71:749-763.
46. Norris KJ. Heritable variation in a plumage indicator of viability in male great tits Parus major. Nature 1993, 362:537-539.
47. Norris KJ. Female choice and the quality of parental care in the great tit Parus major. Behav Ecol Sociobiol 1990, 27:275-281.
48. Quesada J, Senar JC. The role of melanin- and carotenoid-based plumage coloration in nest defence in the Great Tit. Ethology 2007, 113:640-647.
49. Järvi T, Bakken M. The function of the variation in the breast stripe of the great tit (Parus major). Anim Behav 1984, 32:590-596.
50. Matrková J, Remeš V. Environmental and Genetic Effects on Pigment-Based vs Structural Component of Yellow Feather Colouration. PLoS ONE 2012, 7:e36640. 10.1371/journal.pone.0036640, 3349711, 22590581.
51. Matysioková B, Remeš V. Responses to increased costs of activity during incubation in a songbird with female-only incubation: does feather colour signal coping ability?. J Ornithol 2011, 152:337-346.
52. Matysioková B, Remeš V. Assessing the usefulness of ptilochronology in the study of melanin- and ornaments in the Great Tit Parus major. Ibis 2010, 152:397-401.
53. Hõrak P, Ots I, Vellau H, Spottiswoode C, Pape Møller A. Carotenoid-based plumage coloration reflects hemoparasite infection and local survival in breeding great tits. Oecologia 2001, 126:166-173.
54. Mand R, Tilgar V, Moller A. Negative relationship between plumage colour and breeding output in female great tits, Parus major. Evol Ecol Res 2005, 7:1013-1023.
55. Schwagmeyer PL, Mock DW. Parental provisioning and offspring fitness: size matters. Anim Behav 2008, 75:291-298.
56. Tinbergen JM, Boerlijst MC. Nestling weight and survival in individual Great Tits (Parus major). J Anim Ecol 1990, 59:1113-1127.
57. Perrins CM. Population fluctuations and clutch-size in the Great Tit, Parus major L. J Anim Ecol 1965, 34:601-647.
58. Perrins CM, McCleery RH. The effect of fledging mass on the lives of Great Tits Parus major. Ardea 2001, 89:135-142.
59. Naef-Daenzer B, Widmer F, Nuber M. Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J Anim Ecol 2001, 70:730-738.
60. Greno JL, Belda EJ, Barba E. Influence of temperatures during the nestling period on post-fledging survival of great tit Parus major in a Mediterranean habitat. J Avian Biol 2008, 39:41-49.
61. Kennedy MW, Nager RG. The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol Evol 2006, 21:653-655. 10.1016/j.tree.2006.09.017, 17028055.
62. Møller AP, Martín-Vivaldi S, Merino S, Soler JJ. Density-dependent and geographical variation in bird immune response. Oikos 2006, 115:463-474.
63. Isabel L-R, Celis P, Salaberria C, Puerta M, Gil D. Post-fledging recruitment in relation to nestling plasma testosterone and immunocompetence in the spotless starling. Funct Ecol 2011, 25:500-508.
64. Moreno J, Merino S, Sanz JJ, Arriero E, Morales J, Tomás G. Nestling cell-mediated immune response, body mass and hatching date as predictors of local recruitment in the pied flycatcher Ficedula hypoleuca. J Avian Biol 2005, 36:251-260.
65. Cichon M, Dubiec A. Cell-mediated immunity predicts the probability of local recruitment in nestling blue tits. J Evol Biol 2005, 18:962-966. 10.1111/j.1420-9101.2005.00910.x, 16033568.
66. Møller AP, Saino N. Immune response and survival. Oikos 2004, 104:299-304.
67. Nordeide JT, Rudolfsen G, Egeland ES. Ornaments or offspring? Female sticklebacks (Gasterosteus aculeatus L.) trade off carotenoids between spines and eggs. J Evol Biol 2006, 19:431-439. 10.1111/j.1420-9101.2005.01018.x, 16599919.
68. Svensson PA, Pélabon C, Blount JD, Surai PF, Amundsen T. Does female nuptial coloration reflect egg carotenoids and clutch quality in the Two-Spotted Goby (Gobiusculus flavescens, Gobiidae)?. Funct Ecol 2006, 20:689-698.
69. Lambrechts MM, Adriaensen F, Ardia DR, Artemyev AV, Atiénzar F, Bańbura J, Barba E, Bouvier J-C, Camprodon J, Cooper CB, Dawson RD, Eens M, Eeva T, Faivre B, Garamszegi LZ, Goodenough AE, Gosler AG, Grégoire A, Griffith SC, Gustafsson L, Johnson LS, Kania W, Keišs O, Llambias PE, Mainwaring MC, Mänd R, Massa B, Mazgajski TD, Møller AP, Moreno J. The Design of Artificial Nestboxes for the Study of Secondary Hole-Nesting Birds: A Review of Methodological Inconsistencies and Potential Biases. Acta Ornithol 2010, 45:1-26.
70. Svensson L. Identification Guide to European Passerines 1992, London: British Trust for Ornithology, 4.
71. Isaksson C, Ornborg J, Prager M, Andersson S. Sex and age differences in reflectance and biochemistry of carotenoid-based colour variation in the great tit Parus major. Biol J Linn Soc 2008, 95:758-765.
72. Ferns PN, Hinsley SA. Immaculate tits: head plumage pattern as an indicator of quality in birds. Anim Behav 2004, 67:261-272.
73. Lessells CM, Boag P. Unrepeatable repeatabilities: a common mistake. Auk 1987, 104:116-121.
74. Andersson S, Prager M. Quantifying colors. Bird coloration I 2006, 41-89. Cambridge: Harvard University Press, Hill GE, McGraw KJ.
75. Quesada J, Senar JC. Comparing plumage colour measurements obtained directly from live birds and from collected feathers: the case of the great tit Parus major. J Avian Biol 2006, 37:609-616.
76. Anderson DR. Model Based Inference in the Life Sciences: a Primer on Evidence 2007, New York: Springer.
77. Grafen A, Hails R. Modern statistics for the life sciences 2002, Oxford: Oxford University Press.