Gonadotropin hormone modulation of testosterone, immune function, performance, and behavioral trade-offs among male morphs of the lizard Uta stansburiana

American Naturalist

Volumn 171, Issue 3, 2008, Pages 339-357

  Mills, Suzanne C ^a,b,e   Hazard, Lisa ^a,c   Lancaster, Lesley ^a   Mappes, Tapio ^b   Miles, Donald ^a,d   Oksanen, Tuula A ^b   Sinervo, Barry ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^c MONTCLAIR STATE UNIVERSITY   (United States)

^d OHIO UNIVERSITY   (United States)

^e University Via Domitia   (France)

Author keywords

Follicle stimulating hormone; Luteinizing hormone; Reproduction; Survival

Indexed keywords

CORTISONE; FOLLITROPIN; LUTEINIZING HORMONE; TESTOSTERONE;

HORMONE; LIZARD; MORPHOLOGY; PHYSIOLOGY; PLEIOTROPY; REPRODUCTION; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; SEXUAL SELECTION; SURVIVAL; TESTOSTERONE; TRADE-OFF;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BLOOD; COLOR; ENDOCRINOLOGY; FEMALE; GENETIC SELECTION; GENETICS; IMMUNOLOGY; LIZARD; MALE; METABOLISM; PHENOTYPE; PHYSIOLOGY; SEXUAL BEHAVIOR; SEXUAL MATURATION; SOCIAL BEHAVIOR; STATISTICAL MODEL; UNITED STATES;

ANIMALS; CALIFORNIA; COLOR; CORTISONE; ENDOCRINOLOGY; FEMALE; FOLLICLE STIMULATING HORMONE; LINEAR MODELS; LIZARDS; LUTEINIZING HORMONE; MALE; MODELS, BIOLOGICAL; PHENOTYPE; SELECTION (GENETICS); SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION; SOCIAL BEHAVIOR; TESTOSTERONE;

SQUAMATA; UTA; UTA STANSBURIANA; VERTEBRATA;

EID: 40549094317     PISSN: 00030147     EISSN: None     Source Type: Journal    
DOI: 10.1086/527520     Document Type: Article

References (67)

1. Belliure, J., L. Smith, and G. Sorci. 2004. Effect of testosterone on T cell-mediated immunity in two species of Mediterranean lacertid lizards. Journal of Experimental Zoology A 301:411-418.
2. Bennett, A. F. 1978. Activity metabolism of the lower vertebrates. Annual Review of Physiology 40:447-469.
3. Bleay, C., and B. Sinervo. 2007. Discrete genetic variation in mate choice and a condition dependent preference function in the side-blotched lizard: implications for the formation and maintenance of co-adapted gene complexes. Behavioral Ecology 18:304-310.
4. Brandt, Y. 2003. Lizard threat display handicaps endurance. Proceedings of the Royal Society B: Biological Sciences 270:1061-1068.
5. Calsbeek, R., S. H. Alonzo, K. Zamudio, and B. Sinervo. 2002. Sexual selection and alternative mating behaviours generate demographic stochasticity in small populations. Proceedings of the Royal Society B: Biological Sciences 269:157-164.
6. Chastel, O., C. Barbraud, H. Weimerskirch, H. Lornée, A. Lacroix, and O. Tostain. 2005. High levels of LH and testosterone in a tropical seabird with an elaborate courtship display. General and Comparative Endocrinology 140:33-40.
7. Comendant, T., B. Sinervo, E. Svensson, and J. Wingfield. 2003. Social competition, corticosterone and survival in female lizard morphs. Journal of Evolutionary Biology 16:948-955.
8. DeNardo, D. F., and P. Licht. 1993. Effects of corticosterone on social behavior of male lizards. Hormones and Behavior 27:184-199.
9. Eberhard, W. G. 1980. Horned beetles. Scientific American 242:124-131.
10. Evans, M. R., A. R. Goldsmith, and S. R. Norris. 2000. The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behavioral Ecology and Sociobiology 47:156-163.
11. Folstad, I., and A. J. Karter. 1992. Parasites, bright males, and the immunocompetence handicap. American Naturalist 139:603-622.
12. Garland, T., Jr., and J. B. Losos. 1994. Ecological morphology of locomotor performance in squamate reptiles. Pages 240-302 in P. C. Wainwright and S. M. Reilly, eds. Ecological morphology: integrative organismal biology. University of Chicago Press, Chicago.
13. Gomez, J. M., and R. Zamora. 2000. Spatial variation in the selective scenarios of Hormatophylla spinosa (Cruciferae). American Naturalist 155:657-658.
14. Habert, R., H. Lejeune, and J. M. Saez. 2001. Origin, differentiation and regulation of fetal and adult Leydig cells. Molecular Cell and Endocrinology 179:47-74.
15. Ketterson, E. D., and V. Nolan Jr. 1992. Hormones and life histories: an integrative approach. American Naturalist 140(suppl.):S33-S62.
16. Krohmer, R. W. 1986. Effects of mammalian gonadotropins (oFSH and oLH) on testicular development in the immature water snake, Nerodia sipedon. General and Comparative Endocrinology 64:330-338.
17. Lessells, C. M., and P. T. Boag. 1987. Unrepeatable repeatabilities: a common mistake. Auk 104:116-121.
18. Li, C. C. 1981. Path analysis: a primer. Boxwood, Pacific Grove, CA.
19. Licht, P., and H. Papkoff. 1985. Reevaluation of the relative activities of the pituitary glycoprotein hormones (follicle-stimulating hormone, luteinizing hormone, and thyrotrophin) from the green sea turtle, Chelonia mydas. General and Comparative Endocrinology 58:443-451.
20. López, P., and J. Martin. 2005. Female Iberian wall lizards prefer male scents that signal a better cell-mediated immune response. Biology Letters 1:404-406.
21. 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.
22. Martin, L. B., II, P. Han, J. Lewittes, J. R. Kuhlman, K. C. Klasings, and M. Wikelski. 2006. Phytohemagglutinin-induced skin swelling in birds: histological support for a classic immunoecological technique. Functional Ecology 20:290-299.
23. Martins, E. P. 1993. Contextual use of the push-up display by the sagebrush lizard, Sceloporus graciosus. Animal Behaviour 45:25-36.
24. _. 1994. Structural complexity in a lizard communication system: the Sceloporus graciosus "push-up" display. Copeia 1994:944-955.
25. Meddle, S. L., L. M. Romero, L. B. Astheimer, W. A. Buttemer, I. T. Moore, and J. C. Wingfield. 2002. Steroid hormone interrelationships with territorial aggression in an arctic-breeding songbird, Gambel's white-crowned sparrow, Zonotrichia leucophyrs gambelii. Hormones and Behavior 42:212-221.
26. Miles, D. B., and R. G. Smith. 1987. A computerized racetrack for measuring sprint speed in cursorial animals. Functional Ecology 1:281-286.
27. Mills, S. C., A. Grapputo, E. Koskela, and T. Mappes. 2007. Quantitative measure of sexual selection with respect to the operational sex ratio: a comparison of selection indices. Proceedings of the Royal Society B: Biological Sciences 274:143-150.
28. Moore, M. C. 1991. Application of organization-activation theory to alternative male reproductive strategies: a review. Hormones and Behavior 25:154-179.
29. Moore, M. C., D. K. Hews, and R. Knapp. 1998. Hormonal control and evolution of alternative male phenotypes: generalizations of models for sexual differentiation. American Zoologist 38:133-151.
30. Mougeot, F., J. R. Irvine, L. Seivwright, S. M. Redpath, and S. Piertney. 2004. Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behavioral Ecology 15:930-937.
31. Norris, K., and M. R. Evans. 2000. Ecological immunology: life history trade-offs and immune defense in birds. Behavioral Ecology 11:19-26.
32. Peters, A. 2000. Testosterone treatment is immunosuppressive in superb fairy-wrens, yet free-living males with high testosterone are more immunocompetent. Proceedings of the Royal Society B: Biological Sciences 267:883-889.
33. Peters, A., A. G. Denk, K. Delhey, and B. Kempenaers. 2004. Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. Journal of Evolutionary Biology 17:1111-1120.
34. Phillips, J. A., F. Frye, A. Bercovitz, P. Calle, R. Millar, J. Rivier, and B. L. Lasley. 1987. Exogenous GnRH overrides the endogenous annual reproductive rhythm in green iguana, Iguana iguana. Journal of Experimental Zoology 241:227-236.
35. 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.
36. Roberts, M. L., K. L. Buchanan, D. Hasselquist, and M. R. Evans. 2007. Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Hormones and Behavior 51:126-134.
37. Robson, M. A., and D. B. Miles. 2000. Locomotor performance and dominance in male tree lizards, Urosaurus ornatus. Functional Ecology 14:338-344.
38. Rolff, J., and M. T. Siva-Jothy. 2002. Copulation corrupts immunity: a mechanism for a cost of mating in insects. Proceedings of the National Academy of Sciences of the USA 99:9916-9918.
39. Saez, J. M. 1994. Leydig cells: endocrine, paracrine, and autocrine regulation. Endocrine Reviews 15:574-626.
40. Saino, N., A. P. Møller, and A. M. Bolzern. 1995. Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis. Behavioral Ecology 6:397-404.
41. Salvador, A., J. P. Veiga, J. Martin, P. Lopez, M. Abelenda, and M. Puerta. 1996. The cost of producing a sexual signal: testosterone increases the susceptibility of male lizards to ectoparasitic infestation. Behavioral Ecology 7:145-150.
42. Sapolsky, R., 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.
43. Schulte-Hostedde, A. I., B. Zinner, J. S. Millar, and G. J. Hickling. 2005. Restitution of mass-size residuals: validating body condition indices. Ecology 86:155-163.
44. Shuster, S. M., and M. J. Wade. 1991. Equal mating success among male reproductive strategies in a marine isopod. Nature 350:606-610.
45. Sih, A., A. M. Bell, and J. C. Johnson. 2004. Behavioral syndromes: an ecological and evolutionary overview. Trends in Ecology & Evolution 19:372-378.
46. Simoni, M., J. Gromoll, and E. Nieschlag. 1997. The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocrine Reviews 18:739-773.
47. Sinervo, B. 2001. Runaway social games, genetic cycles driven by alternative male and female strategies, and the origin of morphs. Genetica 112:417-434.
48. Sinervo, B., and A. L. Basolo. 1996. Testing adaptation using phenotypic manipulations. Pages 148-185 in M. R. Rose and G. V. Lauder, eds. Adaptation. Academic Press, San Diego, CA.
49. Sinervo, B., and R. Calsbeek. 2003. Physiological epistasis, ontogenetic conflict and natural selection on physiology and life history. Integrative and Comparative Biology 43:419-430.
50. Sinervo, B., and R. B. Huey. 1990. Allometric engineering: an experimental test of the causes of interpopulational differences in locomotor performance. Science 248:1106-1109.
51. Sinervo, B., and P. Licht. 1991a. Hormonal and physiological control of clutch size, egg size, and egg shape in side-blotched lizards (Uta stansburiana): constraints on the evolution of lizard life histories. Journal of Experimental Zoology 257:252-264.
52. _. 1991b. Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards. Science 252:1300-1302.
53. Sinervo, B., and C. M. Lively. 1996. The rock-paper-scissors game and the evolution of alternative male strategies. Nature 380:240-243.
54. Sinervo, B., and E. Svensson. 2002. Correlational selection and the evolution of genomic architecture. Heredity 89:329-338.
55. Sinervo, B., E. Svensson, and T. Comendant. 2000a. Density cycles and an offspring quantity and quality game driven by natural selection. Nature 406:985-988.
56. Sinervo, B., D. B. Miles, W. A. Frankino, M. Klukowski, and D. F. DeNardo. 2000b. 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.
57. Sinervo, B., C. Bleay, and C. Adamopoulou. 2001. Social causes of correlational selection and the resolution of a heritable throat color polymorphism in a lizard. Evolution 55:2040-2052.
58. Sinervo, B., R. Calsbeek, T. Comendant, C. Both, C. Adamopoulou, and J. Clobert. 2006. Genetic and maternal determinants of effective dispersal: the effect of sire genotype and size at birth on side-blotched lizards. American Naturalist 168:88-99.
59. Svensson, E., B. Sinervo, and T. Comendant. 2001a. Condition, genotype-by-environment interaction, and correlational selection in lizard life-history morphs. Evolution 55:2053-2069.
60. _. 2001b. Density-dependent competition and selection on immune function in genetic lizard morphs. Proceedings of the National Academy of Sciences of the USA 98:12561-12565.
61. _. 2002. Mechanistic and experimental analysis of condition and reproduction in a polymorphic lizard. Journal of Evolutionary Biology 15:1034-1047.
62. Verhulst, S., S. J. Dieleman, and H. K. Parmentier. 1999. A tradeoff between immunocompetence and sexual ornamentation in domestic fowl. Proceedings of the National Academy of Sciences of the USA 96:4478-4481.
63. Wagner, G., and L. Altenberg. 1996. Complex adaptations and the evolution of evolvability. Evolution 50:967-976.
64. Warner, R. R., and S. G. Hoffmann. 1980. Local population size as a determinant of mating system and sexual composition in two tropical marine fishes (Thalassoma spp.). Evolution 34:508-518.
65. Wedekind, C., and I. Folstad. 1994. Adaptive or nonadaptive immunosuppression by sex hormones. American Naturalist 143:936-938.
66. Zamudio, K. R., and B. Sinervo. 2000. Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. Proceedings of the National Academy of Sciences of the USA 97:14427-14432.
67. Zera, A. J., and L. G. Harshman. 2001. The physiology of life history trade-offs in animals. Annual Review of Ecology and Systematics 32:95-106.