Experimentally-elevated testosterone, female parental care, and reproductive success in a songbird, the Dark-eyed Junco (Junco hyemalis)

Hormones and Behavior

Volumn 54, Issue 4, 2008, Pages 571-578

  O'Neal, Dawn M ^a   Reichard, Dustin G ^a   Pavilis, Katie ^b   Ketterson, Ellen D ^a  

^a INDIANA UNIVERSITY   (United States)

^b Columbia University ^*  (United States)

Author keywords

Female testosterone; Nest defense; Nest success; Nest survival; Nestling brooding; Nestling feeding; Parental care

Indexed keywords

TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; FERTILITY; FITNESS; FLEDGLING; JUNCO HYEMALIS; MALE; MATING; NESTLING; NONHUMAN; PARENTAL BEHAVIOR; PREDATOR; PRIORITY JOURNAL; PROGENY; QUANTITATIVE ANALYSIS; REPRODUCTION; SONGBIRD; SURVIVAL;

ANIMALS; CLUTCH SIZE; FEEDING BEHAVIOR; FEMALE; FERTILITY; MALE; MATERNAL BEHAVIOR; NESTING BEHAVIOR; REPRODUCTION; SONGBIRDS; TERRITORIALITY; TESTOSTERONE;

EID: 49849101283     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2008.05.017     Document Type: Article

References (79)

1. Arnold A.P. Genetically triggered sexual differentiation of brain and behavior. Horm. Behav. 30 (1996) 495-505
2. Arnold A.P. Sex chromosomes and brain gender. Nat. Rev. Neurosci 5 (2004) 701-708
3. Ball G.F., and Balthazart J. Hormonal regulation of brain circuits mediating male sexual behavior in birds. Physiol. Behav. 83 (2004) 329-346
4. Balthazart J., and Ball G.F. Sexual-differentiation of brain and behavior in birds. Trends Endocrinol. Metab. 6 (1995) 21-29
5. Bart J., and Robson D.S. Estimating survivorship when the subjects are visited periodically. Ecology 63 (1982) 1078-1090
6. Blanckenhorn W.U. The evolution of body size: what keeps organisms small?. Q. Rev. Biol. 75 (2000) 385-407
7. Buchanan K.L., Evans M.R., Goldsmith A.R., Bryant D.M., and Rowe L.V. Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signaling? Proc. R. Soc. Lond. B. Biol. Sci. 268 (2001) 1337-1344
8. Burnham K.P., and Anderson D.R. Model Selection and Multimodel Inference: A Practical Iinformation-Theoretic Approach (2002), Springer, New York
9. Cawthorn J., Morris D., Ketterson E.D., and Nolan V. Influence of experimentally elevated testosterone on nest defense in dark-eyed juncos. Anim. Behav. 56 (1998) 617-621
10. Chalfoun A.D., Thompson F.R., and Ratnaswamy M.J. Nest predators and fragmentation: a review and meta-analysis. Conserv. Biol. 16 (2002) 306-318
11. Chandler C.R., Ketterson E.D., Nolan V., and Ziegenfus C. Effects of testosterone on spatial activity in free-ranging male dark-eyed juncos, Junco hyemalis. Anim. Behav. 47 (1994) 1445-1455
12. Cheverud J.M., and Routman E.J. Epistasis and its contribution to genetic variance-components. Genetics 139 (1995) 1455-1461
13. Clotfelter E.D., Chandler C.R., Nolan V., and Ketterson E.D. The influence of exogenous testosterone on the dynamics of nestling provisioning in dark-eyed juncos. Ethology 113 (2007) 18-25
14. Clotfelter E.D., O'Neal D.M., Gaudioso J.M., Casto J.M., Parker-Renga I.M., Snajdr E.A., Duffy D.L., Nolan V., and Ketterson E.D. Consequences of elevating plasma testosterone in females of a socially monogamous songbird: evidence of constraints on male evolution?. Horm. Behav. 46 (2004) 171-178
15. Clutton-Brock T.H. The Evolution of Parental Care (1991), Princeton University Press, Princeton
16. Clutton-Brock T.H., and Godfray C. Parental investment. In: Krebs J.R., and Davies N.B. (Eds). Behavioural Ecology: An Evolutionary Approach (1991), Blackwell Publishing, Boston 234-262
17. Cordero P.J., Veiga J.P., Moreno J., and Parkin D.T. Extra-pair paternity in the facultatively polygynous spotless starling, Sturnus unicolor. Behav. Ecol. Sociobiol 54 (2003) 1-6
18. Dawson R.D., Lawrie C.C., and O'Brien E.L. The importance of microclimate variation in determining size, growth and survival of avian offspring: experimental evidence from a cavity nesting passerine. Oecologia 144 (2005) 499-507
19. Dinsmore S.J., White G.C., and Knopf F.L. Advanced techniques for modeling avian nest survival. Ecology 83 (2002) 3476-3488
20. Enstrom D.A., Ketterson E.D., and Nolan V. Testosterone and mate choice in the dark-eyed junco. Anim. Behav. 54 (1997) 1135-1146
21. Finch C.E., and Rose M.R. Hormones and the physiological architecture of life-history evolution. Q. Rev. Biol. 70 (1995) 1-52
22. Garamszegi L.Z., Eens M., Hurtrez-Bousses S., and Moller A.P. Testosterone, testes size, and mating success in birds: a comparative study. Horm. Behav. 47 (2005) 389-409
23. Goymann W., Landys M.M., and Wingfield J.C. Distinguishing seasonal androgen responses from male-male androgen responsiveness: revisiting the challenge hypothesis. Horm. Behav. 51 (2007) 463-476
24. Hiipakka R.A., and Liao S.S. Molecular mechanism of androgen action. Trends Endocrinol. Metab. 9 (1998) 317-324
25. Hirschenhauser K., Winkler H., and Oliveira R.F. Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Horm. Behav. 43 (2003) 508-519
26. Houston A., and Davies N. The evolution of cooperation and life history in the dunnock Prunella modularis. In: Sibely R., and Smith R. (Eds). Behavioural Ecology (1985), Blackwell Scientific, Oxford 471-478
27. Hunt K.E., Hahn T.P., and Wingfield J.C. Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus). Behav. Ecol. Sociobiol. 45 (1999) 360-369
28. Hunt K.E., and Wingfield J.C. Effect of estradiol implants on reproductive behavior of female Lapland longspurs (Calcarius lapponicus). Gen. Comp. Endocrinol. 137 (2004) 248-262
29. James W.C., Smallwood K.S., Morrison M.L., and Loffland H.L. Influence of mammal activity on nesting success of passerines. J. Wildl. Manag. 70 (2006) 522-531
30. Jones K.M., Ruxton G.D., and Monaghan P. Model parents: is full compensation for reduced partner nest attendance compatible with stable biparental care?. Behav. Ecol 13 (2002) 838-843
31. Ketterson E.D., and Nolan V. Male parental behavior in birds. Annu. Rev. Ecol. Syst. 25 (1994) 601-628
32. Ketterson E.D., Nolan V., Casto J.M., Buerkle C.A., Clotfelter E., Grindstaff J.L., Jones K.J., Lipar J.L., McNabb F.M.A., Neudorf D.L., Parker-Renga I., Snajdr E., and Schoech S.J. Testosterone, phenotype and fitness: a research program in evolutionary behavioral endocrinology. In: Dawnson A., and Chaturvedi C.M. (Eds). Avian Endocrinology (2001), Narosa Publishing House, New Delhi, India 1-17
33. Ketterson E.D., Nolan V., Cawthorn M.J., Parker P.G., and Ziegenfus C. Phenotypic engineering: using hormones to explore the mechanistic and functional bases of phenotypic variation in nature. Ibis 138 (1996) 70-86
34. Ketterson E.D., Nolan V., and Sandell M. Testosterone in females: mediator of adaptive traits, constraint on sexual dimorphism, or both?. Am. Nat. 166 (2005) S85-S98
35. Ketterson E.D., Nolan V., Wolf L., and Ziegenfus C. Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). Am. Nat. 140 (1992) 980-999
36. Knight J. Early birds make the most of global warming. New. Sci. 155 (1997) 15
37. Knight R.L., and Temple S.A. Why does intensity of avian nest defense increase during the nesting cycle. Auk. 103 (1986) 318-327
38. Lande R., and Arnold S.J. The measurement of selection on correlated characters. Evolution 37 (1983) 1210-1226
39. Listoen C., Karlsen R.F., and Slagsvold T. Risk taking during parental care: a test of the harm-to-offspring hypothesis. Behav. Ecol. 11 (2000) 40-43
40. Lynn S.E., Hayward L.S., Benowitz-Fredericks Z.M., and Wingfield J.C. Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur, Calcarius ornatus. Anim. Behav. 63 (2002) 795-803
41. Lynn S.E., Houtman A.M., Weathers W.W., Ketterson E.D., and Nolan V. Testosterone increases activity but not daily energy expenditure in captive male dark-eyed juncos, Junco hyemalis. Anim. Behav. 60 (2000) 581-587
42. Lynn S.E., Walker B.G., and Wingfield J.C. A phylogenetically controlled test of hypotheses for behavioral insensitivity to testosterone in birds. Horm. Behav. 47 (2005) 170-177
43. Mank J.E. The evolution of sexually selected traits and antagonistic androgen expression in actinopterygiian fishes. Am. Nat. 169 (2007) 142-149
44. Markman S., Pinshow B., and Wright J. The manipulation of food resources reveals sex-specific trade-offs between parental self-feeding and offspring care. Proc. R. Soc. Lond. B. Biol. Sci. 269 (2002) 1931-1938
45. Martin J.L., and Joron M. Nest predation in forest birds: influence of predator type and predator's habitat quality. Oikos 102 (2003) 641-653
46. McGlothlin J.W., Neudorf D.L.H., Casto J.M., Nolan V., and Ketterson E.D. Elevated testosterone reduces choosiness in female dark-eyed juncos (Junco hyemalis): evidence for a hormonal constraint on sexual selection? Proc. R. Soc. Lond. B. Biol. Sci. 271 (2004) 1377-1384
47. Moller A.P., Garamszegi L.Z., Gil D., Hurtrez-Bousses S., and Eens M. Correlated evolution of male and female testosterone profiles in birds and its consequences. Behav. Ecol. Sociobiol. 58 (2005) 534-544
48. Monros J.S., Belda E.J., and Barba E. Post-fledging survival of individual great tits: the effect of hatching date and fledging mass. Oikos 99 (2002) 481-488
49. Montgomerie R.D., and Weatherhead P.J. Risks and rewards of nest defense By parent birds. Quarterly Review Of Biology 63 (1988) 167
50. Navara K.J., Hill G.E., and Mendonca M.T. Variable effects of yolk androgens on growth, survival, and immunity in eastern bluebird nestlings. Physiol. Biochem. Zool. 78 (2005) 570-578
51. Palestis B.G. Nesting stage and nest defense by common terns. Waterbirds 28 (2005) 87-94
52. Perrins C.M., and McCleery R.H. The effect of fledging mass on the lives of great tits Parus major. Ardea 89 (2001) 135-142
53. Raouf S.A., Parker P.G., Ketterson E.D., Nolan V., and Ziegenfus C. Testosterone affects reproductive success by influencing extra-pair fertilizations in male dark-eyed juncos (Aves: Junco hyemalis). Proc. R. Soc. Lond. Series. B. Biol. Sci. 264 (1997) 1599-1603
54. Rastogi A.D., Zanette L., and Clinchy M. Food availability affects diurnal nest predation and adult antipredator behaviour in song sparrows, Melospiza melodia. Anim. Behav. 72 (2006) 933-940
55. Ratnieks F.L.W. Evolution of unstable and stable biparental care. Behav. Ecol. 7 (1996) 490-493
56. Reed W.L., Clark M.E., Parker P.G., Raouf S.A., Arguedas N., Monk D.S., Snajdr E., Nolan Jr. V., and Ketterson E.D. Physiological effects on demography: a long-term experimental study of testosterone's effects on fitness. Am. Nat. 167 (2006) 667-683
57. Ricklefs R.E., and Wikelski M. The physiology/life-history nexus. Trends. Ecol. Evol. 17 (2002) 462-468
58. Sandell M.I. Exogenous testosterone increases female aggression in the European starling (Sturnus vulgaris). Behav. Ecol. Sociobiol. 62 (2007) 255-262
59. Schwagmeyer P.L., Schwabl H.G., and Mock D.W. Dynamics of biparental care in house sparrows: hormonal manipulations of paternal contributions. Anim. Behav. 69 (2005) 481-488
60. Simerly R.B. Wired for reproduction: organization and development of sexually dimorphic circuits in the mammalian forebrain. Ann. Rev. Neurosci. 25 (2002) 507-536
61. Staub N.L., and DeBeer M. The role of androgens in female vertebrates. Gen. Comp. Endocrinol. 108 (1997) 1-24
62. Stienen E.W.M., and Brenninkmeijer A. Variation in growth in sandwich tern chicks Sterna sandvicensis and the consequences for pre- and post-fledging mortality. Ibis 144 (2002) 567-576
63. Stoehr A.M., and Hill G.E. Testosterone and the allocation of reproductive effort in male house finches (Carpodacus mexicanus). Behav. Ecol. and. Sociobiol. 48 (2000) 407-411
64. Tirpak J.M., Giuliano W.M., Miller C.A., Allen T.J., Bittiner S., Edwards J.W., Friedhof S., Igo W.K., Stauffer D.F., and Norman G.W. Ruffed grouse nest success and habitat selection in the central and southern Appalachians. J. Wildl. Manag. 70 (2006) 138-144
65. Trivers R.L. Parental investment and sexual selection. In: Campbell B. (Ed). Sexual Selection and the Descent of Man (1972), Aldine, Chicago 136-179
66. Tryjanowski P., and Golawski A. Sex differences in nest defense by the red-backed shrike Lanius collurio: effects of offspring age, brood size, and stage of breeding season. J. Ethology 22 (2004) 13-16
67. Van Duyse E., Pinxten R., and Eens M. Effects of testosterone on song, aggression, and nestling feeding behavior in male great tits, Parus major. Horm. Behav. 41 (2002) 178-186
68. Van Roo B.L. Exogenous testosterone inhibits several forms of male parental behavior and stimulates song in a monogamous songbird: The blue-headed vireo (Vireo solitarius). Horm. Behav. 46 (2004) 678-683
69. Van Roo B.L., Ketterson E.D., and Sharp P.J. Testosterone and prolactin in two songbirds that differ in paternal care: the blue-headed vireo and the red-eyed vireo. Horm. Behav. 44 (2003) 435-441
70. Veiga J.P., Vinuela J., Cordero P.J., Aparicio J.M., and Polo V. Experimentally increased testosterone affects social rank and primary sex ratio in the spotless starling. Horm. Behav. 46 (2004) 47-53
71. White G.C., and Burnham K.P. Program MARK: survival estimation from populations of marked animals. Bird. Study 46 (1999) 120-139
72. Wikelski M., Lynn S., Breuner C., Wingfield J.C., and Kenagy G.J. Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J. Comp. Physiol. A. 185 (1999) 463-470
73. Wingfield J.C. Androgens and mating systems: testosterone-induced polygyny in normally monogamous birds. Auk. 101 (1984) 665-671
74. Wingfield J.C. A continuing saga: the role of testosterone in aggression. Horm. Behav. 48 (2005) 253-255
75. Wingfield J.C., Ball G.F., Dufty A.M., Hegner R.E., and Ramenofsky M. Testosterone and aggression in birds. Am. Scientist 75 (1987) 602-608
76. Wingfield J.C., Hegner R.E., Dufty A.M., and Ball G.F. The challenge hypothesis: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136 (1990) 829-846
77. Wingfield J.C., Jacobs J., Tramontin A.D., Perfito N., Meddle S., Maney D.L., and Soma K.K. Toward and ecological basis of hormone-behavior interactions in reproduction of birds. In: Wallen K., and Schneider J.E. (Eds). Reproduction in Context: Social and Environmental Influences on Reproduction (2000), MIT Press, Cambridge 85-128
78. Wolf L., Ketterson E.D., and Nolan V. Paternal influence on growth and survival of dark-eyed junco young: do parental males benefit. Anim. Behav. 36 (1988) 1601-1618
79. Zysling D.A., Greives T.J., Breuner C.W., Casto J.M., Demas G.E., and Ketterson E.D. Behavioral and physiological responses to experimentally elevated testosterone in female dark-eyed juncos (Junco hyemalis carolinensis). Horm. Behav. 50 (2006) 200-207