Life History Trade-Offs and Behavioral Sensitivity to Testosterone: An Experimental Test When Female Aggression and Maternal Care Co-Occur

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Rosvall, Kimberly A ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TESTOSTERONE;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; BREEDING; CONTROLLED STUDY; FEMALE; HORMONE SENSITIVITY; INCUBATION TEMPERATURE; LIFE HISTORY; MATERNAL CARE; NONHUMAN; SEXUAL BEHAVIOR; SWALLOW (BIRD); TACHYCINETA BICOLOR;

ANIMALS; BEHAVIOR, ANIMAL; FEMALE; MALE; SWALLOWS; TESTOSTERONE;

ANIMALIA; PASSERI; TACHYCINETA; TACHYCINETA BICOLOR;

EID: 84872340686     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0054120     Document Type: Article

References (99)

1. Magrath MJL, Komdeur J, (2003) Is male care compromised by additional mating opportunity? Trends in Ecology & Evolution 18: 424-430.
2. Stearns SC (1992) The evolution of life histories. Oxford: Oxford University Press.
3. Roff DA, Mostowy S, Fairbairn DJ, (2002) The evolution of trade-offs: Testing predictions on response to selection and environmental variation. Evolution 56: 84-95.
4. Wingfield JC, Lynn SE, Soma KK, (2001) Avoiding the 'costs' of testosterone: Ecological bases of hormone-behavior interactions. Brain Behavior and Evolution 57: 239-251.
5. Adkins-Regan E (2005) Hormones and animal social behavior. Princeton, NJ: Princeton University Press.
6. McGlothlin JW, Jawor JM, Ketterson ED, (2007) Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. American Naturalist 170: 864-875.
7. Folstad I, Karter AJ, (1992) Parasites, bright males, and the immunocompetence handicap. American Naturalist 139: 603-622.
8. Knapp R, Wingfield JC, Bass AH, (1999) Steroid hormones and paternal care in the plainfin midshipman fish (Porichthys notatus). Hormones and Behavior 35: 81-89.
9. Hirschenhauser K, Oliveira RF, (2006) Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Animal Behaviour 71: 265-277.
10. Ketterson ED, Nolan V, (1999) Adaptation, exaptation, and constraint: A hormonal perspective. American Naturalist 154: S4-S25.
11. Hau M, (2007) Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. Bioessays 29: 133-144.
12. Zera AJ, Harshman LG, (2001) The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics 32: 95-126.
13. Soma KK, Scotti MAL, Newman AEM, Charlier TD, Demas GE, (2008) Novel mechanisms for neuroendocrine regulation of aggression. Frontiers in Neuroendocrinology 29: 476-489.
14. Buntin JD (1996) Neural and hormonal control of parental behavior in birds. In: Rosenblatt JS, Snowdon CT, editors. Advances in the Study of Behavior: Academic Press. 161-213.
15. De Ridder E, Pinxten R, Eens M, (2000) Experimental evidence of a testosterone-induced shift from paternal to mating behaviour in a facultatively polygynous songbird. Behavioral Ecology and Sociobiology 49: 24-30.
16. Schwagmeyer PL, Schwabl HG, Mock DW, (2005) Dynamics of biparental care in house sparrows: hormonal manipulations of paternal contributions. Animal Behaviour 69: 481-488.
17. Van Roo BL, (2004) Exogenous testosterone inhibits several forms of male parental behavior and stimulates song in a monogamous songbird: The blue-headed vireo (Vireo solitarius). Hormones and Behavior 46: 678-683.
18. McDonald PG, Buttemer WA, Astheimer LB, (2001) The influence of testosterone on territorial defence and parental behavior in male free-living rufous whistlers, Pachycephala rufiventris. Hormones and Behavior 39: 185-194.
19. Lynn SE, Prince LE, Schook DM, Moore IT, (2009) Supplementary testosterone inhibits paternal care in a tropically breeding sparrow, Zonotrichia capensis. Physiological and Biochemical Zoology 82: 699-708.
20. Ketterson ED, Nolan V, Wolf L, Ziegenfus C, (1992) Testosterone and avian life histories- effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). American Naturalist 140: 980-999.
21. Silverin B, (1980) Effects of long-acting testosterone treatment on free-living pied flycatchers, Ficedula hypoleuca, during the breeding period. Animal Behaviour 28: 906-912.
22. Hegner RE, Wingfield JC, (1987) Effects of experimental manipulation of testosterone levels on parental investment and breeding success in male house sparrows. Auk 104: 462-469.
23. Wingfield JC, (1984) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia. 2. Agonistic interactions as environmental information stimulating secretion of testosterone. General and Comparative Endocrinology 56: 417-424.
24. Beletsky LD, Gori DF, Freeman S, Wingfield JC (1995) Testosterone and polygyny in birds. In: Power DM, editor. Current Ornithology. New York, NY: Plenum Press.
25. Clark MM, Galef BG, (1999) A testosterone-mediated trade-off between parental and sexual effort in male mongolian gerbils (Meriones unguiculatus). Journal of Comparative Psychology 113: 388-395.
26. Hunt KE, Hahn TP, Wingfield JC, (1999) Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus). Behavioral Ecology and Sociobiology 45: 360-369.
27. Hunt KE, Hahn TP, Wingfield JC, (1997) Testosterone implants increase song but not aggression in male Lapland longspurs. Animal Behaviour 54: 1177-1192.
28. Trainor BC, Marler CA, (2001) Testosterone, paternal behavior, and aggression in the monogamous California mouse (Peromyscus californicus). Hormones and Behavior 40: 32-42.
29. Lynn SE, (2008) Behavioral insensitivity to testosterone: Why and how does testosterone alter paternal and aggressive behavior in some avian species but not others? General and Comparative Endocrinology 157: 233-240.
30. Lynn SE, Walker BG, Wingfield JC, (2005) A phylogenetically controlled test of hypotheses for behavioral insensitivity to testosterone in birds. Hormones and Behavior 47: 170-177.
31. Ketterson ED, Nolan V, Sandell M, (2005) Testosterone in females: Mediator of adaptive traits, constraint on sexual dimorphism, or both? American Naturalist 166: S85-S98.
32. Møller AP, Garamszegi LZ, Gil D, Hurtrez-Bousses S, Eens M, (2005) Correlated evolution of male and female testosterone profiles in birds and its consequences. Behavioral Ecology and Sociobiology 58: 534-544.
33. Wingfield JC, Hunt KE, (2002) Arctic spring: hormone-behavior interactions in a severe environment. Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 132: 275-286.
34. Lynn SE, Hayward LS, Benowitz-Fredericks ZM, Wingfield JC, (2002) Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur, Calcarius ornatus. Animal Behaviour 63: 795-803.
35. Goymann W, (2009) Social modulation of androgens in male birds. General and Comparative Endocrinology 163: 149-157.
36. Wingfield JC, Hegner RE, Dufty AM, Ball GF, (1990) The Challenge Hypothesis- theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist 136: 829-846.
37. Reed WL, Clark ME, Parker PG, Raouf SA, Arguedas N, et al. (2006) Physiological effects on demography: A long-term experimental study of testosterone's effects on fitness. American Naturalist 167: 667-683.
38. Trivers RL (1972) Parental investment and sexual selection. In: Cambell B, editor. Sexual Selection and the Descent of Man, 1871-1971. London: Heinemann. 136-179.
39. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton, NJ: Princeton University Press.
40. Clutton-Brock T, (2007) Sexual selection in males and females. Science 318: 1882-1885.
41. Rosvall KA, (2011) Intrasexual competition in females: evidence for sexual selection? Behavioral Ecology 22: 1131-1140.
42. Clutton-Brock T, (2009) Sexual selection in females. Animal Behaviour 77: 3-11.
43. Stockley P, Bro-Jørgensen J, (2011) Female competition and its evolutionary consequences in mammals. Biological Reviews of the Cambridge Philosophical Society 86: 341-366.
44. Staub NL, DeBeer M, (1997) The role of androgens in female vertebrates. General and Comparative Endocrinology 108: 1-24.
45. Zysling DA, Greives TJ, Breuner CW, Casto JM, Demas GE, et al. (2006) Behavioral and physiological responses to experimentally elevated testosterone in female dark-eyed juncos (Junco hyemalis carolinensis). Hormones and Behavior 50: 200-207.
46. Veiga JP, Polo V, (2008) Fitness consequences of increased testosterone levels in female spotless starlings. American Naturalist 172: 42-53.
47. O'Neal DM, Reichard DG, Pavilis K, Ketterson ED, (2008) Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the Dark-eyed junco (Junco hyemalis). Hormones and Behavior 54: 571-578.
48. Sandell MI, (2007) Exogenous testosterone increases female aggression in the European starling (Sturnus vulgaris). Behavioral Ecology and Sociobiology 62: 255-262.
49. Clotfelter ED, O'Neal DM, Gaudioso JM, Casto JM, Parker-Renga IM, et al. (2004) Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution? Hormones and Behavior 46: 171-178.
50. De Ridder E, Pinxten R, Mees V, Eens M, (2002) Short- and long-term effects of male-like concentrations of testosterone on female European starlings (Sturnus vulgaris). Auk 119: 487-497.
51. Kriner E, Schwabl H, (1991) Control of winter song and territorial aggression of female robins (Erithacus rubecula) by testosterone. Ethology 87: 37-44.
52. Rosvall KA, (2010) Do males offset the cost of female aggression? An experimental test in a biparental songbird. Behavioral Ecology 21: 161-168.
53. Rosvall KA, (2011) Cost of female intrasexual aggression in terms of offspring quality: a cross-fostering study. Ethology 117: 1-13.
54. Robertson RJ, Stutchbury BJ, Cohen RR, (1992) Tree swallow (Tachycineta bicolor). The Birds of North America, No 11: Academy of Natural Sciences, Philadelphia, PA and American Ornithologists' Union, Washington, D. C: 1-26.
55. Hunt K, Wingfield JC, Astheimer LB, Buttemer WA, Hahn TP, (1995) Temporal patterns of territorial behavior and circulating testosterone in the Lapland longspur and other arctic Passerines. American Zoologist 35: 274-284.
56. Lynn SE, Wingfield JC, (2008) Dissociation of testosterone and aggressive behavior during the breeding season in male chestnut-collared longspurs, Calcarius ornatus. General and Comparative Endocrinology 156: 181-189.
57. Poole A, editor (2005) The Birds of North America. Ithaca, NY: Cornell Laboratory of Ornithology.
58. Ardia DR, Perez JH, Clotfelter ED, (2010) Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proceedings of the Royal Society B: Biological Sciences 277: 1881-1888.
59. Lombardo MP, Bosman RM, Faro CA, Houtteman SG, Kluisza TS, (1995) Effect of feathers as nest insulation on incubation behavior and reproductive performance of tree swallows (Tachycineta bicolor). Auk 112: 973-981.
60. McCarty JP, (2001) Variation in growth of nestling tree swallows across multiple temporal and spatial scales. Auk 118: 176-190.
61. Stutchbury BJ, Robertson RJ, (1985) Floating populations of female tree swallows. Auk 102: 651-654.
62. Leffelaar D, Robertson RJ, (1985) Nest usurpation and female competition for breeding opportunities by tree swallows. Wilson Bulletin 97: 221-224.
63. Stutchbury BJ, Robertson RJ, (1987) Behavioral tactics of subadult female floaters in the tree swallow. Behavioral Ecology and Sociobiology 20: 413-419.
64. Rosvall KA, (2008) Sexual selection on aggressiveness in females: evidence from an experimental test with tree swallows. Animal Behaviour 75: 1603-1610.
65. Stutchbury BJ, Robertson RJ, (1987) Signaling subordinate and female status- two hypotheses for the adaptive significance of subadult plumage in female tree swallows. Auk 104: 717-723.
66. Ketterson ED, Atwell JW, McGlothlin JW, (2009) Phenotypic integration and independence: Hormones, performance, and response to environmental change. Integrative and Comparative Biology 49: 365-379.
67. Dunn PO, Robertson RJ, Michaudfreeman D, Boag PT, (1994) Extra-pair paternity in tree swallows- Why do females mate with more than one male. Behavioral Ecology and Sociobiology 35: 273-281.
68. Desteven D, (1978) Influence of age on breeding biology of tree swallow Iridoprocne bicolor. Ibis 120: 516-523.
69. Ardia DR, Clotfelter ED, (2007) Individual quality and age affect responses to an energetic constraint in a cavity-nesting bird. Behavioral Ecology 18: 259-266.
70. Stutchbury BJ, Robertson RJ, (1988) Within-season and age-related patterns of reproductive-performance in female tree swallows (Tachycineta bicolor). Canadian Journal of Zoology 66: 827-834.
71. Hussell DJT, (1983) Age and plumage color in female tree swallows. Journal of Field Ornithology 54: 312-318.
72. Fusani L, (2008) Endocrinology in field studies: Problems and solutions for the experimental design. General and Comparative Endocrinology 157: 249-253.
73. Bishop CA, Van Der Kraak GJ, Ng P, Smits JEG, Hontela A, (1998) Health of tree swallows (Tachycineta bicolor) nesting in pesticide-sprayed apple orchards in Ontario, Canada. II. Sex and thyroid hormone concentrations and testes development. Journal of Toxicology and Environmental Health-Part A 55: 561-581.
74. Lande R, Arnold SJ, (1983) The measurement of selection on correlated characters. Evolution 37: 1210-1226.
75. Mank JE, (2007) The evolution of sexually selected traits and antagonistic androgen expression in actinopterygiian fishes. American Naturalist 169: 142-149.
76. Schoech SJ, Ketterson ED, Nolan V, Sharp PJ, Buntin JD, (1998) The effect of exogenous testosterone on parental behavior, plasma prolactin, and prolactin binding sites in dark-eyed juncos. Hormones and Behavior 34: 1-10.
77. Wang JM, Beissinger SR, (2009) Variation in the onset of incubation and its influence on avian hatching success and asynchrony. Animal Behaviour 78: 601-613.
78. Wang JM, Beissinger SR, (2011) Partial incubation in birds: its occurrence, function, and quantification. Auk 128: 454-466.
79. Cresswell W, Holt S, Reid JM, Whitfield DP, Mellanby RJ, et al. (2004) The energetic costs of egg heating constrain incubation attendance but do not determine daily energy expenditure in the pectoral sandpiper. Behavioral Ecology 15: 498-507.
80. Hepp GR, Kennamer RA, Johnson MH, (2006) Maternal effects in Wood Ducks: incubation temperature influences incubation period and neonate phenotype. Functional Ecology 20: 307-314.
81. Perez JH, Ardia DR, Chad EK, Clotfelter ED, (2008) Experimental heating reveals nest temperature affects nestling condition in tree swallows (Tachycineta bicolor). Biology Letters 4: 468-471.
82. Gebhardt-Henrich S, Richner H (1998) Causes of growth variation and its consequences for fitness. In: Starck JM, Ricklefs RE, editors. Avian growth and development: evolution within the altricial-precocial spectrum. Oxford: Oxford University Press. 324-339.
83. Raouf SA, Parker PG, Ketterson ED, Nolan V, Ziegenfus C, (1997) Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis). Proceedings of the Royal Society B: Biological Sciences 264: 1599-1603.
84. Langmore NE, Davies NB, (1997) Female dunnocks use vocalizations to compete for males. Animal Behaviour 53: 881-890.
85. Eens M, Pinxten R, (2000) Sex-role reversal in vertebrates: behavioural and endocrinological accounts. Behavioural Processes 51: 135-147.
86. Elekonich MM, Wingfield JC, (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia). Ethology 106: 493-510.
87. Jawor JM, Young R, Ketterson ED, (2006) Females competing to reproduce: Dominance matters but testosterone may not. Hormones and Behavior 49: 362-368.
88. While GM, Isaksson C, McEvoy J, Sinn DL, Komdeur J, et al. (2010) Repeatable intra-individual variation in plasma testosterone concentration and its sex-specific link to aggression in a social lizard. Hormones and Behavior 58: 208-213.
89. Sandell MI, (1998) Female aggression and the maintenance of monogamy: female behaviour predicts male mating status in European starlings. Proceedings of the Royal Society B: Biological Sciences 265: 1307-1311.
90. Cain KE, Ketterson ED, (2012) Competitive females are successful females; phenotype, mechanism, and selection in a common songbird. Behavioral Ecology and Sociobiology 66: 241-252.
91. Goodson JL, (2005) The vertebrate social behavior network: Evolutionary themes and variations. Hormones and Behavior 48: 11-22.
92. Gahr M, Metzdorf R, (1997) Distribution and dynamics in the expression of androgen and estrogen receptors in vocal control systems of songbirds. Brain Research Bulletin 44: 509-517.
93. Canoine V, Fusani L, Schlinger B, Hau M, (2007) Low sex steroids, high steroid receptors: Increasing the sensitivity of the nonreproductive brain. Developmental Neurobiology 67: 57-67.
94. Voigt C, Goymann W, (2007) Sex-role reversal is reflected in the brain of African black coucals (Centropus grillii). Developmental Neurobiology 67: 1560-1573.
95. Rosvall KA, Bergeon Burns CM, Barske J, Goodson JL, Schlinger BA, et al. (2012) Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution. Proceedings of the Royal Society B: Biological Sciences 279: 3547-3555.
96. Goymann W, Wittenzellner A, Schwabl I, Makomba M, (2008) Progesterone modulates aggression in sex-role reversed female African black coucals. Proceedings of the Royal Society B: Biological Sciences 275: 1053-1060.
97. Oliveira RF, (2009) Social behavior in context: Hormonal modulation of behavioral plasticity and social competence. Integrative and Comparative Biology 49: 423-440.
98. Swett MB, Breuner CW, (2008) Interaction of testosterone, corticosterone and corticosterone binding globulin in the white-throated sparrow (Zonotrichia albicollis). Comparative Biochemistry and Physiology A-Molecular & Integrative Physiology 151: 226-231.
99. Ball GF, Balthazart J, (2008) Individual variation and the endocrine regulation of behaviour and physiology in birds: a cellular/molecular perspective. Philosophical Transactions of the Royal Society B: Biological Sciences 363: 1699-1710.