Seasonal variation in testosterone and performance in males of a non-territorial lizard species

Physiology and Behavior

Volumn 100, Issue 4, 2010, Pages 357-363

  Gowan, Timothy A ^a   McBrayer, Lance D ^a   Rostal, David C ^a  

^a GEORGIA SOUTHERN UNIVERSITY   (United States)

Author keywords

Aspidoscelis sexlineata; Bite force; Lizard; Locomotion; Performance; Testosterone

Indexed keywords

TESTOSTERONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BREEDING; CONTROLLED STUDY; HORMONE DETERMINATION; LIZARD; LOCOMOTION; MALE; MASTICATION; MATING; MOTOR PERFORMANCE; NONHUMAN; PRIORITY JOURNAL; SEASONAL VARIATION; ANIMAL; BLOOD; COMPARATIVE STUDY; FEMALE; MOTOR ACTIVITY; PHYSIOLOGY; SEASON; SEXUAL BEHAVIOR;

ANIMALS; BITE FORCE; FEMALE; LIZARDS; MALE; MOTOR ACTIVITY; SEASONS; SEXUAL BEHAVIOR, ANIMAL; TESTOSTERONE;

EID: 77952959550     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.03.014     Document Type: Article

References (86)

1. Crews D., Moore M.C. Evolution of mechanisms controlling mating behavior. Science 1986, 231(4734):121-125.
2. Hau M. Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. BioEssays 2007, 29:133-144.
3. Wingfield J.C., Hegner R.E., Dufty A.M., Ball G.F. The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 1990, 136(6):829-846.
4. Balthazart J. Hormonal correlates of behavior. Avian biology 1983, vol. 7:221-365. Academic Press, New York. D.S. Farner, J.R. King, K.C. Parkes (Eds.).
5. McKinney R.B., Marion K.R. Plasma androgens and their association with the reproductive cycle of the male fence lizard, Sceloporus undulatus. Comp Biochem Physiol 1985, 82A(3):515-519.
6. Saino N., Moller A.P. Testosterone correlates of mate guarding, singing and aggressive behavior in male barn swallows, Hirundo rustica. Anim Behav 1995, 40:465-472.
7. Arnold S.J. Morphology, performance, and fitness. Am Zool 1983, 23:347-361.
8. Husak J.F., Fox S.F., Lovern M.B., Van Den Bussche R.A. Faster lizards sire more offspring: sexual selection on whole-animal performance. Evolution 2006, 60(10):2122-2130.
9. Irschick D.J., Meyers J.J. An analysis of the relative roles of plasticity and natural selection in the morphology and performance of a lizard (Urosaurus ornatus). Oecologia 2007, 153:489-499.
10. Ryan M.J., Keddy-Hector A. Directional patterns of female mate choice and the role of sensory biases. Am Nat 1992, 139(Suppl):S4-S35.
11. Prohl H. Variation in male calling behaviour and relation to male mating success in the strawberry poison frog (Dendrobates pumilio). Ethol 2003, 109:273-290.
12. Lappin A.K., Husak J.F. Weapon performance, not size, determines mating success and potential reproductive output in the collared lizard (Crotaphytus collaris). Am Nat 2005, 166(3):426-436.
13. Huyghe K., Vanhooydonck B., Scheers H., Molina-Borja M., Van Damme R. Morphology, performance and fighting capacity in male lizards, Gallotia galloti. Funct Ecol 2005, 19:800-807.
14. Husak J.F., Lappin K.A., Fox S.F., Lemos-Espinal J.A. Bite-force performance predicts dominance in male venerable collared lizards (Crotaphytus antiquus). Copeia 2006, 2006(2):301-306.
15. Lailvaux S.P., Herrel A., Vanhooydonck B., Meyers J.J., Irschick D.J. Performance capacity, fighting tactics and the evolution of life stage male morphs in the green anole lizard (Anolis carolinensis). Proc R Soc Lond B 2004, 271:2501-2508.
16. Robson M.A., Miles D.B. Locomotor performance and dominance in male tree lizards, Urosaurus ornatus. Funct Ecol 2000, 14:338-344.
17. Perry G., LeVering K., Girard I., Garland T. Locomotor performance and social dominance in male Anolis cristatellus. Anim Behav 2004, 67:37-47.
18. Winkler S.M., Wade J. Aromatase activity and regulation of sexual behaviors in the green anole lizard. Physiol Behav 1998, 64:731-777.
19. Lynch L., Blackburn D. Effects of testosterone administration and gonadectomyon nuptial pad morphology in overwintering male leopard frogs, Rana pipiens. Amphibia Reptilia 1995, 16:113-121.
20. Buchanan K.L., Evans M.R., Goldsmith A.R., Bryant D.M., Rowe L.V. Testosterone influences basal metabolic rate in male house sparrows: a new cost of dominance signaling?. Proc R Soc Lond B 2001, 268:1337-1344.
21. Olsson M., Wapstra E., Madsen T., Silverin B. Testosterone, ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proc R Soc Lond B 2000, 267:2339-2343.
22. Sinervo B., Miles D.B., Frankino W.A., Klukowski M., DeNardo D.F. Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Horm Behav 2000, 38:222-233.
23. Husak J.F., Irschick D.J., Meyers J.J., Lailvaux S.P., Moore I.T. Hormones, sexual signals, and performance of green anole lizards (Anolis carolinensis). Horm Behav 2007, 52:360-367.
24. Irschick D.J., Ramos M., Buckley C., Elstrott J., Carlisle E., Lailvaux S.P., Bloch N., Herrel A., Vanhooydonck B. Are morphology-performance relationships invariant across different seasons? A test with the green anole lizard (Anolis carolinensis). Oikos 2006, 114:49-59.
25. Huyghe K., Husak J.F., Herrel A., Tadic Z., Moore I.T., Van Damme R., Vanhooydonck B. Relationships between hormones, physiological performance and immunocompetence in a color-polymorphic lizard species, Podarcis melisellensis. Horm Behav 2009, 55:488-494.
26. Miles D.B. Covariation between morphology and locomotory performance in sceloporine lizards. Lizard ecology: historical and experimental perspectives 1994, 207-235. Princeton University Press, Princeton. L.J. Vitt, E.R. Pianka (Eds.).
27. Garland T., Losos J.B. Ecological morphology of locomotor performance in squamate reptiles. Ecological morphology: integrative organismal biology 1994, 240-302. University of Chicago Press, Chicago. P.C. Wainwright, S.M. Reilly (Eds.).
28. Miles D.B., Losos J.B., Ischick D.J. Morphology, performance, and foraging mode. Lizard ecology: the evolutionary consequences of foraging mode 2007, 49-93. Cambridge University Press, Cambridge. S.M. Reilly, L.D. McBrayer, D.B. Miles (Eds.).
29. Garland T. Physiological correlates of locomotory performance in a lizard: an allometric approach. Am J Physiol Regul Integr Comp Physiol 1984, 247:R806-R815.
30. John-Alder H.B. Testosterone improves exercise endurance in a lizard (Anolis sagrei). Am Zool 1994, 34:120A. Abstract.
31. Klukowski M., Jenkinson N.M., Nelson C.E. Effects of testosterone on locomotor performance and growth in field-active northern fence lizards, Sceloporus undulatus hyacinthinus. Physiol Zool 1998, 71(5):506-514.
32. Stamps J.A. Sexual selection, sexual dimorphism, and territoriality. Lizard ecology: studies of a model organism 1983, 169-204. Harvard University Press, Cambridge, MA. R.B. Huey, E.R. Pianka, T.W. Schoener (Eds.).
33. Fitch H.S. Natural history of the six-lined racerunner (Cnemidophorus sexlineatus). Univ Kan Publ Mus Nat Hist 1958, 11:11-62.
34. Carpenter C.C. Patterns of behavior in two Oklahoma lizards. Am Midl Nat 1962, 67(1):132-151.
35. Jenssen T.A., Greenberg N., Hovde K.A. Behavioral profile of free-ranging male lizards, Anolis carolinensis, across breeding and post-breeding seasons. Herpetol Monogr 1995, 9:41-62.
36. Clark D.R. Ecological observations on a Texas population of six-lined racerunners, Cnemidophorus sexlineatus (Reptilia, Lacertilia, Teiidae). J Herpetol 1976, 10(2):133-138.
37. Anderson, R.A. Foraging behavior, behavior of reproduction, and sexual selection in a widely-foraging lizard, Cnemidophorus tigris. Unpublished Ph.D. Dissertation, University of California, Los Angeles 1986.
38. Anderson R.A., Vitt L.J. Sexual selection versus alternative causes of sexual dimorphism in teiid lizards. Oecologia 1990, 84:145-157.
39. Garland T. Locomotor performance and activity metabolism of Cnemidophorus tigris in relation to natural behaviors. Biology of whiptail lizards (genus Cnemidophorus) 1993, p163-p210. Oklahoma Museum of Natural History, Norman, OK. J.W. Wright, L.J. Vitt (Eds.).
40. Carpenter C.C.A. A population of the six-lined racerunner (Cnemidophorus sexlineatus). Herpetologica 1959, 15:81-86.
41. Carpenter C.C. Aggressive behavior and social dominance in the six-lined racerunner (Cnemidophorus sexlineatus). Anim Behav 1960, 8:61-66.
42. Leuck B.E. Comparative, social behavior of bisexual and unisexual whiptail lizards (Cnemidophorus). J Herpetol 1985, 19(4):492-506.
43. Brackin M.F. The relation of rank to physiological state in Cnemidophorus sexlineatus dominance hierarchies. Herpetologica 1978, 34(2):185-191.
44. Maclean G.S., Lee K.J., Wilson K.J. A simple method of obtaining blood from lizards. Copeia 1973, 1973(2):338-339.
45. Lindzey J., Crews D. Hormonal control of courtship and copulatory behavior in male Cnemidophorus inornatus, a direct sexual ancestor of a unisexual, parthenogenetic lizard. Gen Comp Endrocinol 1986, 64:411-418.
46. Witz B.W. Aspects of the thermal biology of the six-lined racerunner, Cnemidophorus sexlineatus (Squamata:Teiidae) in West-Central Florida. J Therm Biol 2001, 26:529-535.
47. Anderson R.A., McBrayer L.D., Herrel A. Bite force in vertebrates: opportunities and caveats for use of a nonpareil whole-animal performance measure. Biol J Linn Soc 2008, 93:709-720.
48. McBrayer L.D. The relationship between skull morphology, biting performance and foraging mode in Kalahari lacertid lizards. Zool J Linn Soc 2004, 140:403-416.
49. Herrel A., De Grauw E., Lemos-Espinal J.A. Head shape and bite performance in Xenosaurid lizards. J Exp Zool 2001, 290:101-107.
50. Cullum A.J. Comparisons of physiological performance in sexual and asexual whiptail lizards (genus Cnemidophorus): implications for the role of heterozygosity. Am Nat 1997, 150(1):24-47.
51. Cullum A.J. Sexual dimorphism in physiological performance of whiptail lizards (genus Cnemidophorus). Physiol Zool 1998, 71(5):541-552.
52. Cullum A.J. Phenotypic variability of physiological traits in populations of sexual and asexual whiptail lizards (genus Cnemidophorus). Evol Ecol Res 2000, 2:841-855.
53. Rodriguez L., Begtashi I., Zanuy S., Carrillo M. Development and validation of an enzyme immunoassay for testosterone: effects of photoperiod on plasma testosterone levels and gonadal development in male sea bass (Dicentrarchus labrax, L.) at puberty. Fish Physiol Biochem 2000, 23:141-150.
54. Olsson M., Healey M., Astheimer L. Afternoon T: testosterone level is higher in red than yellow male polychromatic lizards. Physiol Behav 2007, 91:531-534.
55. Gil D., Bulmer E., Celis P., Puerta M. Increased sibling competition does not increase testosterone or corticosterone levels in nestlings of the spotted starling (Sturnus unicolor). Horm Behav 2008, 54:238-243.
56. Schradin C., Scantlebury M., Pillay N., Konig B. Testosterone levels in dominant sociable males are lower than in solitary roamers: physiological differences between three male reproductive tactics in a sociably flexible mammal. Am Nat 2009, 173:376-388.
57. Midgley A.R., Niswender G.D., Rebar R.W. Principles for the assessment of the reliability of radioimmunoassay methods (precision, accuracy, sensitivity, specificity). Acta Endocr Suppl 1969, 142:163-184.
58. Borque C., Perez-Garnelo S.S., Lopez M., Talavera C., Delclaux M., de la Fuente J. Validating a commercially available enzyme immunoassay for the determination of 17β-estradiol and progesterone in the feces of cheetahs (Acinonyx jubatus): a case report. J Zoo Wildl Med 2005, 36(1):54-61.
59. Brackin M.F. The seasonal reproductive, fat body, and adrenal cycles of male six-lined racerunners (Cnemidophorus sexlineatus) in central Oklahoma. Herpetologica 1979, 35(3):216-222.
60. Etheridge K., Wit L.C., Sellers J.C., Trauth S.E. Seasonal changes in reproductive condition and energy stores in Cnemidophorus sexlineatus. J Herpetol 1986, 20(4):554-559.
61. Sokal R.R., Rohlf F.J. Biometry 1995, W.H. Freeman & Co, New York. 3rd ed.
62. Griggs R.C., Kingston W., Jozefowicz R.F., Herr B.E., Forbes G., Halliday D. Effect of testosterone on muscle mass and muscle protein synthesis. J Appl Physiol 1989, 66(1):498-503.
63. Cree A., Guillette L.J., Cockrem J.F., Joss J.M. Effects of capture and temperature stress on plasma steroid concentrations in male tuatara (Sphenodon punctatus). J Exp Zool 1990, 253(1):38-46.
64. Lance V.A., Rostal D.C. The annual reproductive cycle of the male and female desert tortoise: physiology and endocrinology. Chelonian Conserv Biol 2002, 4:302-312.
65. Johnson L.F., Jacob J.S. Pituitary activity and reproductive cycle of male Cnemidophorus sexlineatus in West Tennessee. J Herpetol 1984, 18(4):396-405.
66. Grassman M., Hess D.L. Sex differences in adrenal function in the lizard Cnemidophorus sexlineatus: I. Seasonal variation in the field. J Exp Biol 1992, 264:177-182.
67. Borg B. Androgens in teleost fishes. Comp Biochem Physiol 1994, 109C(3):219-245.
68. Tokarz R.R., McMann S., Seitz L., John-Alder H. Plasma corticosterone and testosterone levels during the annual reproductive cycle of male brown anoles (Anolis sagrei). Physiol Zool 1998, 71(2):139-146.
69. Amey A.P., Whittier J.M. Seasonal patterns of plasma steroid hormones in males and females of the bearded dragon lizard, Pogona barbata. Gen Comp Endocrinol 2000, 117:335-342.
70. Arslan M., Lobo J., Zaidi A.A., Jalali S., Qazi M.H. Annual androgen rhythm in the spiny-tailed lizard, Uromastix hardwicki. Gen Comp Endocrinol 1978, 36:16-22.
71. Mills S.C., Hazard L., Lancaster L., Mappes T., Miles D., Oksanen T.A., Sinervo B. Gonadotropin hormone modulation of testosterone, immune function, performance, and behavioral trade-offs among male morphs of the lizard Uta stansburiana. Am Nat 2008, 171(3):339-357.
72. Crews D. Gamete production, sex hormone secretion, and mating behavior uncoupled. Horm Behav 1984, 18:22-28.
73. John-Alder H.B., Cox R.M., Haenel G.J., Smith L.C. Hormones, performance and fitness: natural history and endocrine experiments on a lizard (Sceloporus undulatus). Integr Comp Biol 2009, 49:393-407.
74. Brantley R.K., Marchaterre M.A., Bass A.H. Androgen effects on vocal muscle structure in a teleost fish with inter- and intra-sexual dimorphism. J Morphol 1993, 216(3):305-318.
75. Effect of anabolic steroids on mitochondria and sarcotubular system skeletal muscle. J Appl Physiol 1991, 70:1038-1043.
76. Garland T., Else P.L. Seasonal, sexual, and individual variation in endurance and activity metabolism in lizards. Am J Physiol Regul Integr Comp Physiol 1987, 252:R439-R449.
77. Thorarensen H., Young G., Davie P.S. 11-Ketotestosterone stimulates growth of heart and red muscle in rainbow trout. Can J Zool 1996, 74:912-917.
78. Holloway A.C., Leatherland J.F. Neuroendocrine regulation of growth hormone secretion in teleost fishes with emphasis on the involvement of gonadal sex steroids. Rev Fish Biol Fisheries 1998, 8:409-429.
79. Cox R.M., John-Alder H.B. Testosterone has opposite effects on male growth in lizards (Sceloporus spp.) with opposite patterns of sexual size dimorphism. J Exp Biol 2005, 208:4679-4687.
80. Bhasin S., Storer T.W., Berman N., Yarasheski K.E., Clevenger B., Phillips J., Lee W.P., Bunnell T.J., Casaburi R. Testosterone replacement increases fat-free mass and muscle size in hypogonadal men. J Clin Endocrinol Metab 1997, 82:407-413.
81. Herrel A., McBrayer L.D., Larson P.M. Functional basis for sexual differences in bite force in the lizard Anolis carolinensis. Biol J Linn Soc 2007, 91:111-119.
82. Lappin A.K., Hamilton P.S., Sullivan B.K. Bite-force performance and head shape in a sexually dimorphic crevice-dwelling lizard, the common chuckwalla [Sauromalus ater (=obesus)]. Biol J Linn Soc 2006, 88:215-222.
83. Huyghe K., Husak J.F., Moore I.T., Vanhooydonck B., Van Damme R., Molina-Borja M., Herrel A. Effects of testosterone on morphology, performance, and muscle mass in a lizard. J Exp Biol 2010, 313A:9-16.
84. Dittami J.P., Reyer H. A factor analysis of seasonal, behavioral, hormonal and body weight changes in adult male barheaded geese, Anser indicus. Behav 1984, 90:114-124.
85. Hews D.K., Moore M.C. Hormones and sex-specific traits: critical questions. Parasites and pathogens: effects on host hormones and behavior 1997, 277-292. Chapman & Hall, New York. N.E. Beckage (Ed.).
86. Ketterson E.D., Nolan V. Adaptation, exaptation, and constraint: a hormonal perspective. Am Nat 1999, 154(Suppl):S4-S25.