Sex-specific phenotypic integration: Endocrine profiles, coloration, and behavior in fledgling boobies

Behavioral Ecology

Volumn 25, Issue 1, 2014, Pages 76-87

  Fargallo, Juan A ^a,b   Velando, Alberto ^c   López Rull, Isabel ^b   Gañán, Natalia ^b   Lifshitz, Natalia ^b   Wakamatsu, Kazumasa ^d   Torres, Roxana ^b  

^a MUSEO NACIONAL DE CIENCIAS NATURALES   (Spain)

^b INSTITUTO DE ECOLOGÍA   (Mexico)

^c UNIVERSITY OF VIGO   (Spain)

^d FUJITA HEALTH UNIVERSITY   (Japan)

Author keywords

Behavioral strategy; Corticosterone; Juvenile plumage; Melanin pigment; Personality; Pleiotropy; Sula dactylatra; Testosterone

Indexed keywords

AGE CLASS; BEHAVIORAL ECOLOGY; BODY MASS; COLOR; ENDOCRINE DISRUPTOR; EUSOCIALITY; JUVENILE; LIFE HISTORY TRAIT; MELANIN; NATURAL SELECTION; PHENOTYPIC PLASTICITY; PLEIOTROPY; PLUMAGE; RESOURCE ALLOCATION; SEABIRD; TESTOSTERONE;

EID: 84890610999     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/art088     Document Type: Article

References (110)

1. Adkins-Regan E. 2005. Hormones and animal social behavior. Princeton and Oxford, UK: Princeton University Press.
2. Alonso-Álvarez C, Velando A. 2001. Effect of testosterone on the behaviour of yellow-legged gulls (Larus cachinans) in a high-density colony during the courtship period. Ethol Ecol Evol. 13:341-349.
3. Andersson M. 1994. Sexual selection. Princeton, UK: Princeton University Press.
4. Arbuckle JL. 2010. IBM SPSS Amos 19 User's Guide. Chicago (IL): SPSS Inc.
5. Ariyomo TO, Carter M, Watt PJ. 2013. Heritability of boldness and aggressiveness in the zebrafish. Behav Genet. 43:161-167.
6. Badyaev AV. 2002. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol Evol. 17:369-378.
7. Bagnara JT, Matsumoto J, Ferris W, Frost SK, Turner WA Jr, Tchen TT, Taylor JD. 1979. Common origin of pigment cells. Science. 203:410-415.
8. Bell AM, Hankison SJ, Laskowski KL. 2009. The repeatability of behaviour: a meta-analysis. Anim Behav. 77:771-783.
9. Bergeon Burns CM, Rosvall KA, Ketterson ED. 2013. Neural steroid sensitivity and aggression: comparing individuals of two songbird subspecies. J Evol Biol. 26:820-831.
10. Blanckenhorn WU. 2005. Behavioural causes and consequences of sexual size dimorphism. Ethology. 111:977-1016.
11. Blas J, Baos R, Bortolotti GR, Marchant TA, Hiraldo F. 2006. Age-related variation in the adrenocortical response to stress in nestling white storks (Ciconia ciconia) supports the developmental hypothesis. Gen Comp Endocrinol. 148:172-180.
12. Bókony V, Garamszegi LZ, Hirschenhauser K, Liker A. 2008. Testosterone and melanin-based black plumage coloration: a comparative study. Behav Ecol Sociobiol. 62:1229-1238.
13. Bortolotti GR. 1986. Evolution of growth rates in eagles: sibling competition vs. energy considerations. Ecology. 67:182-194.
14. Budaev SV. 1999. Sex differences in the Big Five personality factors: testing an evolutionary hypothesis. Pers Individ Dif. 26:801-813.
15. Carter AJ, Goldizen AW, Tromp SA. 2010. Agamas exhibit behavioral syndromes: bolder males bask and feed more but may suffer higher predation. Behav Ecol. 21:655-661.
16. Catoni C, Peters A, Schaefer HM. 2009. Dietary flavonoids enhance conspicuousness of a melanin-based trait in male blackcaps but not of the female homologous trait or of sexually monochromatic traits. J Evol Biol. 22:1649-1657.
17. Cone RD. 2006. Studies on the physiological functions of the melanocortin system. Endocr Rev. 27:736-749.
18. Dall SRX, Houston AI, McNamara JM. 2004. The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett. 7:734-739.
19. de Boer SF, van der Vegt BJ, Koolhaas JM. 2003. Individual variation in aggression of feral rodent strains: a standard for the genetics of aggression and violence? Behav Genet. 33:485-501.
20. Delhey K, Burger C, Fiedler W, Peters A. 2010. Seasonal changes in colour: a comparison of structural, melanin-and carotenoid-based plumage colours. PLoS One. 5:e11582.
21. Dingemanse NJ, Both C, Drent PJ, Tinbergen JM. 2004. Fitness consequences of avian personalities in a fluctuating environment. Proc Biol Sci. 271:847-852.
22. Dingemanse NJ, Dochtermann N, Wright J. 2010. A method for exploring the structure of behavioral syndromes to allow formal comparisons within and among data sets. Anim Behav. 79:439-450.
23. Dingemanse NJ, Réale D. 2005. Natural selection and animal personality. Behaviour. 142:1165-1190.
24. Drent PJ, van Oers K, van Noordwijk AJ. 2003. Realized heritability of personalities in the great tit (Parus major). Proc Biol Sci. 270:45-51.
25. Drummond H, Osorno JL, Torres R, García Chavelas C, Larson HM. 1991. Sexual size dimorphism and sibling competition: implications for avian sex ratios. Am Nat. 138:623-641.
26. Ducrest AL, Keller L, Roulin A. 2008. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol. 23:502-510.
27. Edelaar P, Serrano D, Carrete M, Blas J, Potti J, Tella JL. 2012. Tonic immobility is a measure of boldness towards predators: an application of Bayesian structural equation modeling. Behav Ecol. 23:619-626.
28. Emerson BC, Kolm N. 2005. Species diversity can drive speciation. Nature. 434:1015-1017.
29. Evans M, Goldsmith AR, Norris SRA. 2000. The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol. 47:156-163.
30. Fairbairn DJ. 1997. Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Ann Rev Ecol Evol Syst. 28:659-687.
31. Fargallo JA, Laaksonen T, Korpimäki E, Pöyri V, Griffith SC, Valkama J. 2003. Size-mediated dominance and begging behaviour in Eurasian kestrel broods. Evol Ecol Res. 5:549-558.
32. Fargallo JA, Laaksonen T, Korpimäki E, Wakamatsu K. 2007a. A melanin-based trait reflects environmental growth conditions of nestling male Eurasian kestrels. Evol Ecol. 21:157-171.
33. Fargallo JA, Martínez-Padilla J, Toledano-Díaz A, Santiago-Moreno J, Dávila JA. 2007b. Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels. J Anim Ecol. 76:201-209.
34. Fernández-Juricic E, Jiménez MD, Lucas E. 2002. Factors affecting intra-and inter-specific variations in the difference between alert distances and flight distances for birds in forested habitats. Can J Zool. 80:1212-1220.
35. Ferree ED, Wikelski MC, Anderson DJ. 2004. Hormonal correlates of siblicide in Nazca boobies: support for the challenge hypothesis. Horm Behav. 46:655-662.
36. Fitze PS, Richner H. 2002. Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav Ecol. 13:401-407.
37. Forsman A, Ahnesjö J, Caesar S, Karlsson M. 2008. A model of ecological and evolutionary consequences of color polymorphism. Ecology. 89:34-40.
38. Frey FM. 2007. Phenotypic integration and the potential for independent color evolution in a polymorphic spring ephemeral. Am J Bot. 94:437-444.
39. Galván I, Amo L, Sanz JJ. 2008. Ultraviolet-blue reflectance of some nestling plumage patches mediates parental favouritism in great tits Parus major. J Avian Biol. 39:277-282.
40. Galván I, Mousseau TA, Møller AP. 2011. Bird population declines due to radiation exposure at Chernobyl are stronger in species with pheomelanin-based coloration. Oecologia. 165:827-835.
41. Gasparini J, Bize P, Piault R, Wakamatsu K, Blount JD, Ducrest AL, Roulin A. 2009. Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls. J Anim Ecol. 78:608-616.
42. Godin JG, Dugatkin LA. 1996. Female mating preference for bold males in the guppy, Poecilia reticulata. Proc Natl Acad Sci USA. 93:10262-10267.
43. Gompel N, Carroll SB. 2003. Genetic mechanisms and constraints governing the evolution of correlated traits in drosophilid flies. Nature. 424:931-935.
44. Grace JB. 2006. Structural equation modelling and natural systems. Cambridge, UK: Cambridge University Press.
45. Griffith SC, Owens PF, Burke T. 1999. Environmental determination of a sexually selected trait. Nature. 400:358-359.
46. Griffiths R, Double MC, Orr K, Dawson RJ. 1998. A DNA test to sex most birds. Mol Ecol. 7:1071-1075.
47. Groothuis T, Meeuwissen G. 1992. The influence of testosterone on the development and fixation of the form of displays in two age classes of young Black-headed Gulls. Anim Behav. 43:189-208.
48. Hoekstra HE. 2006. Genetics, development and evolution of adaptive pigmentation in vertebrates. Heredity (Edinb). 97:222-234.
49. Hubbard JK, Uy JA, Hauber ME, Hoekstra HE, Safran RJ. 2010. Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet. 26:231-239.
50. Ito S, Nakanishi Y, Valenzuela RK, Brilliant MH, Kolbe L, Wakamatsu K. 2011. Usefulness of alkaline hydrogen peroxide oxidation to analyze eumelanin and pheomelanin in various tissue samples: application to chemical analysis of human hair melanins. Pigment Cell Melanoma Res. 22:474-486.
51. Ito S, Wakamatsu K. 2008. Chemistry of mixed melanogenesis-Pivotal roles of dopaquinone. Photochem Photobiol. 84:582-592.
52. Jawor JM, Breitwisch R. 2003. Melanin ornaments, honesty, and sexual selection. Auk. 120:249-265.
53. Jones IL. 1990. Plumage variability functions for status signaling in least auklets. Anim Behav. 39:967-975.
54. Kepler CB. 1969. Breeding biology of the Blue-faced booby Sula dactylatra personata on Green Island Kure Atoll. Cambridge, UK: Nuttall Ornithological Club.
55. Ketterson ED, Atwell JW, McGlothlin JW. 2009. Phenotypic integration and independence: hormones, performance, and response to environmental change. Integr Comp Biol. 49:365-379.
56. Kim SY, Fargallo JA, Vergara P, Martínez-Padilla J. 2013. Multivariate heredity of melanin-based coloration, body mass and immunity. Heredity (Edinb). 111:139-146.
57. Koolhaas JM, de Boer SF, Coppens CM, Buwalda B. 2010. Neuroendocrinology of coping styles: towards understanding the biology of individual variation. Front Neuroendocrinol. 31:307-321.
58. Koolhaas JM, Korte SM, de Boer SF, Van der Vegt BJ, Van Reenen CG, Hopster H, De Jong IC, Ruis MAW, Blokhuis HJ. 1999. Coping styles in animals: current status in behavior and stress-physiology. Neurosci Biobehav Rev. 23:925-935.
59. Korte SM, Koolhaas JM, Wingfield JC, McEwen BS. 2005. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neurosci Biobehav Rev. 29:3-38.
60. Ligon RA, Hill GE. 2010. Feeding decisions of eastern bluebirds are situationally influenced by fledgling plumage color. Behav Ecol. 21:456-464.
61. López-Rull I, Celis P, Salaberria C, Puerta M, Gil D. 2011. Post-fledging recruitment in relation to nestling plasma testosterone and immunocompetence in the spotless starling. Funct Ecol. 25:500-508.
62. Lyon BE, Eadie JM, Hamilton LD. 1994. Parental choice selects for ornamental plumage in coot chicks. Nature. 371:240-243.
63. McGraw KJ. 2006. Mechanics of melanin-based coloration. In: Hill GE, McGraw KJ, editors. Bird coloration, volume I: mechanisms and measurements. Cambridge, UK: Harvard University Press. p. 243-294.
64. McKinnon JS, Pierotti ME. 2010. Colour polymorphism and correlated characters: genetic mechanisms and evolution. Mol Ecol. 19:5101-5125.
65. Marchetti C, Drent PJ. 2000. Individual differences in the use of social information in foraging by captive great tits. Anim Behav. 60:131-140.
66. Martín J, De Neve L, Polo V, Fargallo JA, Soler M. 2006. Health-dependent vulnerability to predation affects escape responses of unguarded chinstrap penguin chicks. Behav Ecol Sociobiol. 60:778-784.
67. Maynard Smith J. 1982. Evolution and the theory of games. Cambridge, UK: Cambridge University Press.
68. Meunier J, Pinto SF, Burri R, Roulin A. 2011. Eumelanin-based coloration and fitness parameters in birds: a meta-analysis. Behav Ecol Sociobiol. 65:559-567.
69. Montgomerie R. 2006. Analyzing colors. In: Hill GE, McGraw KJ, editors. Bird coloration, volume I: mechanisms and measurements. Cambridge, UK: Harvard University Press. p. 90-147.
70. Moreno J, Soler JJ. 2011. Sources of distinctness of juvenile plumage in Western Palearctic passerines. Biol J Linn Soc. 102:440-454.
71. Morgan C, Cone RD. 2006. Melanocortin-5 receptor deficiency in mice blocks a novel pathway influencing pheromone-induced aggression. Behav Genet. 36:291-300.
72. Morrell LJ, Lindström J, Ruxton GD. 2005. Why are small males aggressive? Proc Biol Sci. 272:1235-1241.
73. Mundy NI. 2005. A window on the genetics of evolution: MC1R and plumage colouration in birds. Proc Biol Sci. 272:1633-1640.
74. Nelson JB. 1978. The Sulidae. Oxford, UK: Oxford University Press.
75. Nelson JB. 2005. Pelicans, cormorants and their relatives: Pelecanidae, Sulidae, Phalacrocoracidae, Anhingidae, Fregatidae, Phaethontidae. Oxford, UK: Oxford University Press.
76. Pigliucci M, Preston K. 2004. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford, UK: Oxford University Press.
77. Penteriani V, Delgado MD, Alonso-Álvarez C, Pina NV, Sergio F, Bartolommei P, Thompson LJ. 2007. The importance of visual cues for nocturnal species: eagle owl fledglings signal with white mouth feathers. Ethology. 113:934-943.
78. Price T, Langen T. 1992. Evolution of correlated characters. Trends Ecol Evol. 7:307-310.
79. Quinn JL, Cresswell W. 2005. Personality, anti-predation behaviour and behavioural plasticity in the chaffinch Fringilla coelebs. Behaviour. 142:1383-1408.
80. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ. 2007. Integrating animal temperament within ecology and evolution. Biol Rev Camb Philos Soc. 82:291-318.
81. Rohwer SA. 1975. The social significance of avian winter plumage variability. Evolution. 29:593-610.
82. Rosvall KA, Bergeon Burns CM, Barske J, Goodson JL, Schlinger BA, Sengelaub DR, Ketterson ED. 2012. Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution. Proc Biol Sci. 279:3547-3555.
83. Roulin A, Almasi B, Meichtry-Stier KS, Jenni L. 2011. Eumelanin-and pheomelanin-based colour advertise resistance to oxidative stress in opposite ways. J Evol Biol. 24:2241-2247.
84. Roulin A, Ducrest AL. 2011. Association between melanism, physiology and behaviour: a role for the melanocortin system. Eur J Pharmacol. 660:226-233.
85. Sapolsky RM, Romero LM, Munck AU. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev. 21:55-89.
86. Santos JC, Cannatella DC. 2011. Phenotypic integration emerges from aposematism and scale in poison frogs. Proc Natl Acad Sci USA. 108:6175-6180.
87. Schuett W, Tregenza T, Dall SR. 2010. Sexual selection and animal personality. Biol Rev Camb Philos Soc. 85:217-246.
88. Schwabl H. 1993. Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA. 90:11446-11450.
89. Selander RK. 1972. Sexual selection and dimorphism in birds. In Campbell BG, editor. Sexual selection and the descent of man 1871-1971. Chicago (IL): Aldine Atherton. p. 180-230.
90. Senar JC. 2006. Color displays as intrasexual signals of aggression and dominance. In: Hill GE, McGraw KJ, editors. Bird coloration, volume II: function and evolution. Cambridge, UK: Harvard University Press. p. 41-89.
91. Sih A, Bell AM, Johnson JC, Ziemba RE. 2004. Behavioral syndromes: an intergrative overiew. Q Rev Biol. 79:241-277.
92. Spinney LH, Bentley GE, Hau M. 2006. Endocrine correlates of alternative phenotypes in the white-throated sparrow (Zonotrichia albicollis). Horm Behav. 50:762-771.
93. Stoehr AM, Kokko H. 2006. Sexual dimorphism in immunocompetence: what does life-history theory predict? Behav Ecol. 17:751-756.
94. Tringali A, Bowman R. 2012. Plumage reflectance signals dominance in Florida scrub-jay, Aphelocoma coerulescens, juveniles. Anim Behav. 84:1527-1522.
95. Tuttle EM. 2003. Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence. Behav Ecol. 14:425-432.
96. van Oers K, Buchanan KL, Thomas TE, Drent PJ. 2011. Correlated response to selection of testosterone levels and immunocompetence in lines selected for avian personality. Anim Behav. 81:1055-1061.
97. Veenema AH, Meijer OC, de Kloet ER, Koolhaas JM, Bohus BG. 2003. Differences in basal and stress-induced HPA regulation of wild house mice selected for high and low aggression. Horm Behav. 43:197-204.
98. Velando A. 2000. The importance of hatching date for dominance in young shags. Anim Behav. 60:181-185.
99. Verbeek MEM, Boon A, Drent PJ. 1996. Exploration, aggressive behaviour and dominance in pair-wise confrontations of juvenile male great tits. Behaviour. 133:945-963.
100. Vergara P, Fargallo JA. 2008. Sex, melanic coloration, and sibling competition during the postfledging dependence period. Behav Ecol. 19:847-853.
101. Vergara P, Fargallo JA, Martínez-Padilla J. 2010. Reaching independence: food supply, parent quality and offspring phenotypic characters in kestrels. Behav Ecol. 21:207-512.
102. Vergara P, Martínez-Padilla J. 2012. Social context decouples the relationship between a sexual ornament and testosterone levels in a male wild bird. Horm Behav. 62:407-412.
103. Viñuela J, Amat JA, Ferrer M. 1995. Nest defence of nesting chinstrap penguins (Pygoscelis antarctica) against intruders. Ethology. 99:323-331.
104. Weimerskirch H, Le Corre M, Gadenne H, Pinaud D, Kato A, Ropert-Coudert Y, Bost CA. 2009. Relationship between reversed sexual dimorphism, breeding investment and foraging ecology in a pelagic seabird, the masked booby. Oecologia. 161:637-649.
105. Wakamatsu K, Ito S, Rees JL. 2002. The usefulness of 4-amino-3- hydroxyphenylalanine as a specific marker of pheomelanin. Pigment Cell Res. 15:225-232.
106. Wilson ADM, Godin J-GJ. 2009. Boldness and behavioral syndromes in the bluegill sunfish, Lepomis macrochirus. Behav Ecol. 20:231-237.
107. Wilson DS, Clark AB, Coleman C, Dearstyne T. 1994. Shyness and boldness in humans and other animals. Trends Ecol Evol. 9:442-446.
108. Wilson MJ. 1983. Inhibition of development of both androgen-dependent and androgen-independent pigment cells in scrotal skin dermis of the rat by antiandrogen treatment during fetal growth. Endocrinology. 112:321-325.
109. Wingfield JC, Hegner RE, Dufty AM, Ball GF. 1990. The 'challenge hypothesis': theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat. 136:829-846.
110. Yabuuchi M, Bando K, Hiramatsu M, Takahashi S, Takeuchi S. 2010. Local agouti signaling protein/melanocortin signaling system that possibly regulates lipid metabolism in adipose tissues of chickens. J Poult Sci. 47:176-182.