Variation in testosterone and corticosterone in amphibians and reptiles: Relationships with latitude, elevation, and breeding season length

American Naturalist

Volumn 180, Issue 5, 2012, Pages 642-654

  Eikenaar, Cas ^a   Husak, Jerry ^b   Escallón, Camilo ^c   Moore, Ignacio T ^c  

^a INSTITUTE OF AVIAN RESEARCH VOGELWARTE HELGOLAND   (Germany)

^b Department of Biology   (Germany)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Amphibians; Breeding season; Corticosterone; Elevation; Latitude; Reptiles; Testosterone

Indexed keywords

CORTICOSTERONE; TESTOSTERONE;

AMPHIBIAN; BREEDING SEASON; ELEVATION; GEOGRAPHICAL VARIATION; HORMONE; INTERSPECIFIC VARIATION; LATITUDE; LIFE HISTORY TRAIT; PHYLOGENETICS; REPTILE; SPERM COMPETITION; STEROID; TESTOSTERONE;

AMPHIBIA; ANIMAL; ARTICLE; BLOOD; BREEDING; GEOGRAPHY; MALE; PHYLOGENY; PHYSIOLOGY; REPTILE; SEASON; TIME;

AMPHIBIANS; ANIMALS; BREEDING; CORTICOSTERONE; GEOGRAPHY; MALE; PHYLOGENY; REPTILES; SEASONS; TESTOSTERONE; TIME FACTORS;

EID: 84867703819     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/667891     Document Type: Article

References (66)

1. Andersson, M. 1994. Sexual selection. Princeton University Press, Princeton, NJ.
2. Angilletta, M. J., Jr., P. H. Niewiarowski, A. E. Dunham, A. D. Leaché, and W. P. Porter. 2004. Bergmann's clines in ectotherms: illustrating a life-historical perspective with sceloporine lizards. American Naturalist 164:E168-E183.
3. Arnold, S. J., and D. Duvall. 1994. Animal mating systems: a synthesis based on selection theory. American Naturalist 143:317-348.
4. Böhning-Gaese, K., B. Halbe, N. Lemoine, and R. Oberrath. 2000. Factors influencing the clutch size, number of broods and annual fecundity of North American and European land birds. Evolutionary Ecology Research 2:823-839.
5. Bókony, V., A. Z. Lendvai, A. Liker, F. Angelier, J. C. Wingfield, and O. Chastel. 2009. Stress response and the value of reproduction: are birds prudent parents? American Naturalist 173:589-598.
6. Corl, A., A. R. Davis, S. R. Kuchta, T. Comendant, and B. Sinervo. 2010. Alternative mating strategies and the evolution of sexual size dimorphism in the side-blotched lizard, Uta stansburiana: a population-level comparative analysis. Evolution 64:79-96.
7. Cox, R. M., and H. B. John-Alder. 2007. Increased mite parasitism as a cost of testosterone in male striped plateau lizards, Sceloporus virgatus. Functional Ecology 21:327-334.
8. De Ridder, E., R. Pinxten, and M. Eens. 2000. Experimental evidence of a testosterone-induced shift from paternal to mating behavior in a facultatively polygynous songbird. Behavioral Ecology and Sociobiology 49:24-30.
9. Duellman, W. E., and L. Trueb. 1986. Biology of amphibians. Mc-Graw-Hill, New York.
10. Emerson, S. B. 2001. Male advertisement calls. Behavioral variation and physiological processes. Pages 36-44 in M. S. Ryan, ed. Anuran communication. Smithsonian Institution, Washington, DC.
11. Emerson, S. B., and D. L. Hess. 2001. Glucocorticoids, androgens, testis mass, and the energetics of vocalization in breeding male frogs. Hormones and Behavior 39:59-69.
12. Enstrom, D. A., E. D. Ketterson, and V. Nolan. 1997. Testosterone and mate choice in the dark-eyed junco. Animal Behaviour 54: 1135-1146.
13. Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1-15.
14. Fitch, H. S. 1970. Reproductive cycles in lizards and snakes. University of Kansas Museum of Natural History Miscellaneous Publications 52. Lawrence, University of Kansas Museum of Natural History.
15. Folstad, I., and A. J. Karter. 1992. Parasites, bright males, and the immunocompetence handicap. American Naturalist 139:603-622.
16. Fox, S. F., J. K. McCoy, and T. A. Baird. 2003. Lizard social behavior. Johns Hopkins University Press, Baltimore, MD.
17. Garamszegi, L. Z., K. Hirschenhauser, V. Bókony, M. Eens, S. Hurtrez-Boussès, A. P. Møller, R. F. Oliveira, and J. C. Wingfield. 2008. Latitudinal distribution, migration, and testosterone levels in birds. American Naturalist 172:533-546.
18. Garland, T., Jr., P. E. Midford, and A. R. Ives. 1999. An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral states. American Zoologist 39:374-388.
19. Ghalambor, C. K., and T. E. Martin. 2001. Fecundity-survival tradeoffs and parental risk-taking in birds. Science 292:494-498.
20. Goymann, W., I. T. Moore, A. Scheuerlein, K. Hirschenhauser, A. Grafen, and J. C. Wingfield. 2004. Testosterone in tropical birds: effects of environmental and social factors. American Naturalist 164:327-334.
21. Halliday, T., and M. Tejedo. 1995. Intrasexual selection and alternative mating behavior. Pages 419-468 in H. Heatwole and B. K. Sullivan, eds. Amphibian biology. Volume 2. Social behaviour. Surrey Beatty, Chipping Norton, Australia.
22. Hare, K. M., S. Pledger, M. B. Thompson, J. H. Miller, and C. H. Daugherty. 2007. Low costs of locomotion in lizards that are active at low temperatures. Physiological and Biochemical Zoology 80: 46-58.
23. Hartel, T., I. Sas, A. P. Pernetta, and I. C. Geltsch. 2007. The reproductive dynamics of temperate amphibians: a review. North-Western Journal of Zoology 3:127-125.
24. Hau, M., R. E. Ricklefs, M. Wikelski, K. A. Lee, and J. D. Brawn. 2010. Corticosterone, testosterone and life-history strategies of birds. Proceedings of the Royal Society B: Biological Sciences 277: 3203-3212.
25. Heatwole, H., and B. K. Sullivan, eds. 1995. Amphibian biology. Volume 2. Social behaviour. Surrey Beatty, Chipping Norton, Australia.
26. Hirschenhauser, K., and R. F. Oliveira. 2006. Social modulation of androgens in male vertebrates: meta-analysis of the challenge hypothesis. Animal Behaviour 71:265-277.
27. Hirschenhauser, K., H. Winkler, and R. F. Oliveira. 2003. Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Hormones and Behavior 43:508-519.
28. Husak, J. F., D. J. Irschick, J. P. Henningsen, K. S. Kirkbride, S. P. Lailvaux, and I. T. Moore. 2009. Hormonal response of male green anole lizards (Anolis carolinensis) to GnRH challenge. Journal of Experimental Zoology A 311:105-114.
29. Husak, J. F., D. J. Irschick, J. J. Meyers, S. P. Lailvaux, and I. T. Moore. 2007. Hormones, sexual signals and performance of green anole lizards (Anolis carolinensis). Hormones and Behavior 52:360-367.
30. Landys, M. M., M. Ramenofsky, and J. C. Wingfield. 2006. Actions of glucocorticoids at a seasonal baseline as compared to stressrelated levels in the regulation of periodic life processes. General and Comparative Endocrinology 148:132-149.
31. Leaché, A. D., D.-S. Helmer, and C. Moritz. 2010. Phenotypic evolution in high-elevation populations of western fence lizards (Sceloporus occidentalis) in the Sierra Nevada Mountains. Biological Journal of the Linnean Society 100:630-641.
32. Maddison, W. P., and D. R. Maddison. 2009. Mesquite: a modular system for evolutionary analysis. Version 2.72. http://mesquiteproject.org.
33. Marler, C. A., and M. C. Moore. 1988. Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behavioral Ecology and Sociobiology 23:21-26.
34. Marler, C. A., G. Walsberg, M. L. White, and M. Moore. 1995. Increased energy expenditure due to increased territorial defense in male lizards after phenotypic manipulation. Behavioral Ecology and Sociobiology 37:225-231.
35. Midford, P. E., T. Garland Jr., and W. P. Maddison. 2005. PDAP package of Mesquite. Version 1.07. http://mesquiteproject.org/pdap_mesquite/index.html.
36. Miles, D. B., R. Calsbeek, and B. Sinervo. 2007. Corticosterone, locomotor performance, and metabolism in side-blotched lizards (Uta stansburiana). Hormones and Behavior 51:548-554.
37. Moore, I. T., M. J. Greene, and R. T. Mason. 2001. Environmental and seasonal adaptations of the adrenocortical and gonadal responses to capture stress in two population of the male garter snake, Thamnophis sirtalis. Journal of Experimental Zoology 289: 99-108.
38. Moore, I. T., and T. S. Jessop. 2003. Stress, reproduction and adrenocortical modulation in amphibians and reptiles. Hormones and Behavior 43:39-47.
39. Morrison, C., and J. Hero. 2003. Geographic variation in life history characteristics of amphibians: a review. Journal of Animal Ecology 72:270-279.
40. Niewiarowski, P. H. 1994. Understanding geographic life-history variationin lizards. Pages 31-50 in L. J. Vitt and E. R. Pianka, eds. Lizard ecology: historical and experimental perspectives. Princeton University Press, Princeton, NJ.
41. Oliveira, R. F. 2004. Social modulation of androgens in vertebrates: mechanisms and function. Advances in the Study of Behavior 34: 165-239.
42. Pyron, R. A., and J. J. Wiens. 2011. A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61:543-583.
43. Rasbash, J., F. Steele, W. Browne, and B. Prosser. 2004. A user's guide to MLwiN, version 2.02. Centre for Multilevel Modeling, London.
44. Ricklefs, R. 1969. The nesting cycle of songbirds in tropical and temperate regions. Living Bird 8:165-175.
45. Ricklefs, R. E., and M. Wikelski. 2002. The physiology/life-history nexus. Trends in Ecology & Evolution 17:462-463.
46. Rivas, J. A., and G. M. Burghardt. 2005. Snake mating systems, behavior, and evolution: the revisionary implications of recent findings. Journal of Comparative Psychology 119:447-454.
47. Roberts, M. L., K. L. Buchanan, and M. R. Evans. 2004. Testing the immunocompetence handicap hypothesis: a review of the evidence. Animal Behaviour 68:227-239.
48. Romero, L. M. 2002. Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. General and Comparative Endocrinology 128:1-24.
49. Romero, L. M., M. J. Dickens, and N. E. Cyr. 2009. The reactive scope model: a new model integrating homeostasis, allostasis, and stress. Hormones and Behavior 55:375-389.
50. Romero, L. M., and J. M. Reed. 2005. Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comparative Biochemistry and Physiology A 140:73-79.
51. Salkeld, D. J., M. Trivedi, and L. Schwarzkopf. 2008. Parasite loads are higher in the tropics: temperate to tropical variation in a single host-parasite system. Ecography 31:538-544.
52. Sapolsky, R. M., L. M. Romero, and A. U. Munck. 2000. How do glucocorticoids influence stress responses? integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21:55-89.
53. Schuett, G. W., D. L. Hardy Sr., H. W. Greenes, R. L. Earley, M. S. Grober, E. A. van Kirk, and W. J. Murdoch. 2005. Sympatric rattlesnakes with contrasting mating systems show differences in seasonal patterns of plasma sex steroids. Animal Behaviour 70:257-266.
54. Shuster, S., and M. J. Wade. 2003. Mating systems and strategies. Princeton University Press, Princeton, NJ.
55. Sinervo, B., D. B. Miles, W. A. Frankino, M. Klukowski, and D. F. DeNardo. 2000. Testosterone, endurance, and Darwinian fitness: natural and sexual selection on the physiological bases of alternative male behaviors in side-blotched lizards. Hormones and Behavior 38:222-233.
56. Stamps, J. A. 1983. Sexual selection, sexual dimorphism, and territoriality. Pages 169-204 in R. B. Huey, E. R. Pianka, and T. W. Schoener, eds. Lizard ecology: studies of a model organism. Harvard University Press, Cambridge, MA.
57. Sullivan, B. K., and M. A. Kwiatkowski. 2007. Courtship displays in anurans and lizards: theoretical and empirical contributions to our understanding of costs and selection on males due to female choice. Functional Ecology 21:666-675.
58. Sullivan, B. K., and G. E. Walsberg. 1985. Call rate and aerobic capacity in Woodhouse's toad (Bufo woodhousei). Herpetologica 41:404-407.
59. Townsend, T. M., A. Larson, E. Louis, and J. R. Macey. 2004. Molecular phylogenetics of squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. Systematic Biology 53:735-757.
60. Townsend, T. M., D. G. Mulcahy, J. W. Sites Jr., C. A. Kuczynski, J. J. Wiens, and T. W. Reeder. 2011. Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation. MolecularPhylogenetics and Evolution 61:363-380.
61. Vitousek, M. N., D. R. Rubenstein, K. N. Nelson, and M. Wikelski. 2008. Are hotshots always hot? a longitudinal study of hormones, behavior, and reproductive success in male marine iguanas. General and Comparative Endocrinology 157:227-232.
62. Ward, S., J. R. Speakman, and P. J. B. Slater. 2003. The energy cost of song in the canary, Serinus canaria. Animal Behaviour 66:893-902.
63. Wells, K. D. 2007. The ecology and behavior of amphibians. University of Chicago Press, Chicago.
64. Wilczynski, W., and E. J. Yang. 2002. Relationships between hormones and aggressive behavior in green anole lizards: an analysis using structural equation modeling. Hormones and Behavior 42:192-205.
65. Wingfield, J. C., R. E. Hegner, A. M. Dufty Jr., and G. F. Ball. 1990. The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. American Naturalist 136:829-846.
66. Wingfield, J. C., S. E. Lynn, and K. K. Soma. 2001. Avoiding the "costs" of testosterone: ecological bases of hormone-behavior interactions. Brain, Behavior and Evolution 57:239-251.