Species differences in the winner effect disappear in response to post-victory testosterone manipulations

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1724, 2011, Pages 3497-3503

  Fuxjager, Matthew J ^a   Montgomery, Jon L ^a   Marler, Catherine A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Behavioural evolution; Peromyscus mice; Social behaviour; Testosterone; The challenge hypothesis; Winner effect

Indexed keywords

ADAPTATION; ENDOCRINE DISRUPTOR; ENDOGENOUS CUE; EVOLUTIONARY BIOLOGY; HYPOTHESIS TESTING; INTERSPECIFIC VARIATION; PHENOTYPIC PLASTICITY; PHYSIOLOGICAL RESPONSE; QUALITATIVE ANALYSIS; RODENT; SOCIAL BEHAVIOR; TESTOSTERONE;

MUS; PEROMYSCUS; PEROMYSCUS CALIFORNICUS; PEROMYSCUS LEUCOPUS;

EID: 80054939790     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2011.0301     Document Type: Article

References (43)

1. Adkins-Regan, E. 2005 Hormones and animal social behavior. Princeton, NJ: Princeton University Press.
2. Hau, M. 2007 Regulation of male traits by testosterone: implications for the evolution of vertebrate life histories. Bioessays 29, 133-144. (doi:10.1002/bies.20524)
3. Marler, C. A. & Moore, M. C. 1988 Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behav. Ecol. Sociobiol. 23, 21-26. (doi:10.1007/BF00303053)
4. Ketterson, E. D. & Nolan, V. 1999 Adaptation, exaptation, and constraint: a hormonal perspective. Am. Nat. 154, S4-S25. (doi:10.1086/303280)
5. Lynn, S. E., Hayward, L. S., Benowitz-Fredericks, Z.M. & Wingfield, J. C. 2002 Behavioural insensitivity to supplementary testosterone during the parental phase in the chestnut-collared longspur, Calcarius ornatus. Anim. Behav. 63, 795-803. (doi:10.1006/anbe.2001.1980)
6. Hsu, Y. Y., Earley, R. L. & Wolf, L. L. 2006 Modulation of aggressive behaviour by fighting experience: mechanisms and contest outcomes. Biol. Rev. 81, 33-74. (doi:10.1017/S146479310500686X)
7. Dugatkin, L. A. & Druen, M. 2004 The social implications of winner and loser effects. Proc. R. Soc. Lond. B 271, S488-S489. (doi:10.1098/rsbl.2004.0235)
8. Guhl, A. M., Collias, N. E. & Allee, W. C. 1945 Mating behavior and the social hierarchy in small flocks of white leghorns. Physiol. Zool. 18, 365-390.
9. Fournier, F. & Fest-Bianchet, M. 1995 Social dominance in adult female mountain goats. Anim. Behav. 49, 1449-1459. (doi:10.1016/0003-3472(95)90066-7)
10. Fuxjager, M. J. & Marler, C. A. 2010 How and why the winner effect forms: influences of contest environment and species differences. Behav. Ecol. 21, 37-45. (doi:10.1093/beheco/arp148)
11. Oyegbile, T. O. & Marler, C. A. 2006 Weak winner effect in a less aggressive mammal: correlations with corticosterone but not testosterone. Physiol. Behav. 89, 171-179. (doi:10.1016/j.physbeh.2006.05.044)
12. Oyegbile, T. O. & Marler, C. A. 2005 Winning fights elevates testosterone levels in California mice and enhances future ability to win fights. Horm. Behav. 48, 259-267. (doi:10.1016/j.yhbeh.2005.04.007)
13. Fuxjager, M. J., Mast, G., Becker, E. A. & Marler, C. A. 2009 The 'home advantage' is necessary for a full winner effect and changes in post-encounter testosterone. Horm. Behav. 56, 214-219. (doi:10.1016/j.yhbeh.2009.04.009)
14. Oliveira, R. F., Silva, A. & Canario, A. V. M. 2009 Why do winners keep winning? Androgen mediation of winner but not loser effects. Proc. R. Soc. B 276, 2249-2256. (doi:10.1098/rspb.2009.0132)
15. Gleason, E. D., Fuxjager, M. J., Oyegbile, T. O. & Marler, C. A. 2009 Testosterone release and social context: when it occurs and why. Front. Neuroendocrin. 30, 460-469. (doi:10.1016/j.yfrne.2009.04.009)
16. Marler, C. A., Oyegbile, T. O., Plavicki, J. & Trainor, B. C. 2005 Response to Wingfield's commentary on 'A continuing saga: the role of testosterone in aggression'. Horm. Behav. 48, 256-258. (doi:10.1016/j.yhbeh.2005.05.010)
17. Fuxjager, M. J., Forbes-Lorman, R. M., Coss, D. J., Auger, C. J., Auger, A. P. & Marler, C. A. 2010 Winning territorial disputes selectively enhances androgen sensitivity in neural pathways related to motivation and social aggression. Proc. Natl Acad. Sci. USA 107, 12393-12398. (doi:10.1073/pnas.1001394107)
18. McGlothlin, J. W., Whittaker, D. J., Schrock, S. E., Gerlach, N. M., Jawor, J. M., Snajdr, E. A. & Ketterson, E. D. 2010 Natural selection on testosterone production in a wild songbird population. Am. Nat. 175, 687-701. (doi:10.1086/652469)
19. Voigt, C. & Goymann, W. 2007 Sex-role reversal is reflected in the brain of African black coucals (Centropus grillii). Dev. Neurobiol. 67, 1560-1573. (doi:10.1002/dneu.20528)
20. Hirschenhauser, K. & Oliveira, R. F. 2006 Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Anim. Behav. 71, 265-277. (doi:10.1016/j.anbehav.2005.04.014)
21. Wingfield, J. C., Hegner, R. E., Dufty, A. M. & Ball, G. F. 1990 The challenge hypothesis: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136, 829-846. (doi:10.1086/285134)
22. Goymann, W., Landys, M. M. & Wingfield, J. C. 2007 Distinguishing seasonal androgen responses from male-male androgen responsiveness: revisiting the challenge hypothesis. Horm. Behav. 51, 463-476. (doi:10.1016/j.yhbeh.2007.01.007)
23. Ribble, D. O. & Salvioni, M. 1990 Social organization and nest-co-occupancy in Peromyscus californicus, a monogamous rodent. Behav. Ecol. Sociobiol. 26, 9-15.
24. Gubernick, D. J. & Teferi, T. 2000 Adaptive significance of male parental care in a monogamous mammal. Proc. R. Soc. Lond. B 267, 147-150. (doi:10.1098/rspb.2000.0979)
25. Wolff, J. O. 1986 Life history strategies of whitefooted mice (Peromyscus leucopus). V. J. Sci. 37, 208-220.
26. Xia, X. & Millar, J. S. 1991 Genetic evidence of promiscuity in Peromyscus leucopus. Behav. Ecol. Sociobiol. 28, 171-178. (doi:10.1007/2FBF00172168)
27. Trainor, B. C., Bird, I. M. & Marler, C. A. 2004 Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm. Behav. 45, 115-121. (doi:10.1016/j.yhbeh.2003.09.006)
28. Holm, S. 1979 A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6, 65-70.
29. Zar, J. H. 1999 Biostatistical Analysis. Upper Saddle River, NJ: Prentice Hall.
30. Hasen, N. S. & Gammie, S. C. 2005 Differential fos activation in virgin and lactating mice in response to an intruder. Physiol. Behav. 84, 681-695. (doi:10.1016/j.physbeh.2005.02.010)
31. Solomon, M. B., Karom, M. C., Norvelle, A., Markham, C. M., Erwin, W. D. & Huhman, K. L. 2009 Gonadal hormones modulate the display of conditioned defeat in male Syrian hamsters. Horm. Behav. 56, 423-428. (doi:10.1016/j.yhbeh.2009.07.011)
32. Freeman, G. H. & Halton, J. H. 1951 Note on the exact treatment of contingency, goodness of fit and other problems of significance. Biometrika 38, 141-149. (doi:10.2307/2F2332323)
33. Gleason, E. D. 2010 Testosterone response to courtship in the male California mouse: does it predict future pair or paternal behavior? PhD dissertation, University of Wisconsin at Madison, USA.
34. Jawor, J. M., McGlothlin, J.W., Casto, J. M., Greives, T. J., Snajdr, E. A., Bentley, G. E. & Ketterson, E. D. 2006 Seasonal and individual variation in response to Gn RH challenge in male dark-eyed juncos (Junco hyemalis). Gen. Comp. Endocrinol. 149, 182-189. (doi:10.1016/2Fj.ygcen.2006.05.013)
35. Millesi, E., Hoffmann, I. E., Steurer, S., Metwaly, M. & Dittami, J. P. 2002 Vernal changes in the behavioral and endocrine responses to GnRH application in male European ground squirrels. Horm. Behav. 41, 51-58. (doi:10.1006/hbeh.2001.1735)
36. Fuxjager, M. J., Montgomery, J. L., Becker, E. A. & Marler, C. A. 2010 Deciding to win: interactive effects of residency, resources and 'boldness' on contest outcome in white-footed mice. Anim. Behav. 80, 921-927. (doi:10.1016/j.anbehav.2010.08.018)
37. Nyby, J. G. 2008 Reflexive testosterone release: a model system for studying the nongenomic effects of testosterone upon male behavior. Front. Neuroendocrin. 29, 199-210. (doi:10.1016/j.yfrne.2007.09.001)
38. Apfelbeck, B. & Goymann, W. In press. Ignoring the challenge? Male black redstarts (Phoenicurus ochruros) do not increase testosterone levels during territorial conflicts but they do so in response to gonadotropin-releasing hormone. Proc. R. Soc. B 278, 3233-3242. (doi:10.1098/rspb.2011.0098)
39. Cushing, B. S., Perry, A., Musatov, S., Ogawa, S. & Papademetriou, E. 2008 Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior. J. Neurosci. 28, 10399-10403. (doi:10.1523/JNEUROSCI.1928-08.2008)
40. Goodson, J. L., Schrock, S. E., Klatt, J. D., Kabelik, D. & Kingsbury, M. A. 2009 Mesotocin and nonpeptide receptors promote songbird flocking behavior. Science 325, 862-866. (doi:10.1126/science.1174929)
41. Sperry, T. S., Wacker, D. W. & Wingfield, J. C. 2010 The role of androgen receptors in regulating territorial aggression in male song sparrows. Horm. Behav. 57, 86-95. (doi:10.1016/j.yhbeh.2009.09.015)
42. Juntti, S. A., Tollkuhn, J., Wu, M. V., Fraser, E. J., Soderborg, T., Tan, S., Honda, S., Harada, N. & Shah, N. M. 2010 The androgen receptor governs the execution, but not programming, of male sexual and territorial behaviors. Neuron 66, 260-272. (doi:10.1016/j.neuron.2010.03.024)
43. Couppis, M. H. & Kennedy, C. H. 2008 The rewarding effect of aggression is reduced by nucleus accumbens dopamine receptor antagonism in mice. Psychopharmacology 197, 449-456. (doi:10.1007/s00213-007-1054-y)