Alternative male reproductive tactics and the immunocompetence handicap in the Azorean rock-pool blenny, Parablennius parvicornis

Proceedings of the Royal Society B: Biological Sciences

Volumn 273, Issue 1589, 2006, Pages 901-909

  Ros, Albert F H ^a   Bouton, Niels ^b   Santos, Ricardo S ^b   Oliveira, Rui F ^a  

^a INSTITUTO SUPERIOR DE PSICOLOGIA APLICADA   (Portugal)

^b UNIVERSITY OF THE AZORES   (Portugal)

Author keywords

11 ketotestosterone; Alternative reproductive tactics; Haemagglutination; Leukocytes; Sheep red blood cells; Testosterone

Indexed keywords

11 OXOTESTOSTERONE; ANDROGEN; HUMORAL ANTIBODY; TESTOSTERONE; 11-KETOTESTOSTERONE; DRUG DERIVATIVE;

ANDROGEN; ANTIGEN; HYPOTHESIS TESTING; IMMUNE RESPONSE; IMMUNOCOMPETENCE; MORPHOTYPE; PERCIFORM; REPRODUCTIVE STRATEGY; SECONDARY SEXUAL CHARACTERISTICS; TESTOSTERONE;

ANTIBODY RESPONSE; ARTICLE; BLOOD CELL COUNT; CONTROLLED STUDY; DISABILITY; FERTILIZATION; IMMUNITY; IMMUNOCOMPETENCE; INJURY; LEUKOCYTE; MALE; MALE GENITAL SYSTEM; MORPHOTYPE; NONHUMAN; PARABLENNIUS PARVICORNIS; PRIORITY JOURNAL; REPRODUCTION; SHEEP ERYTHROCYTE; SPAWNING; TELEOST; ANIMAL; BLOOD; CYTOLOGY; ERYTHROCYTE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE; PERCIFORMES; PHYSIOLOGY; SEXUAL BEHAVIOR; SEXUAL DEVELOPMENT; SHEEP;

OVIS ARIES; PARABLENNIUS PARVICORNIS;

ANDROGENS; ANIMALS; BLOOD CELL COUNT; ERYTHROCYTES; IMMUNE TOLERANCE; LYMPHOCYTES; MALE; PERCIFORMES; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; SHEEP; TESTOSTERONE;

EID: 33744521395     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2005.3407     Document Type: Article

References (60)

1. Aitken, I. D. & Parry, S. H. 1974 The comparative serological response of the chicken, pheasant and quail to soluble and a particulate antigen. Immunology 27, 623-629.
2. Borg, B. 1994 Androgens in teleost fishes. Comp. Biochem. Physiol. C 109, 219-245. (doi:10.1016/0305-0491(94) 90005-1)
3. Brantley, R. K., Wingfield, J. C. & Bass, A. H. 1993 Sex steroid levels in Porichthys notatus, a fish with alternative reproductive tactics and a review of the hormonal bases for male dimorphism among teleost fishes. Horm. Behav. 27, 332-347. (doi:10.1006/hbeh.1993.1025)
4. Cichoń, M., Dubiec, A. & Chadzińska, M. 2001 The effect of elevated reproductive effort on humoral immune function in collared flycatcher females. Acta Oecol. 22, 71-76. (doi:10.1016/S1146-609X(00)01094-8)
5. Collazos, M. E., Barriga, C. & Ortega, E. 1994 Optimum conditions for the activation of the alternative complement pathway of a cyprinid fish (Tinca tinca L.). Seasonal variations in the titres. Fish Shellfish Immunol. 4, 499-506. (doi:10.1006/fsim.1994.1044)
6. Côté, I. M. & Hunte, W. 1989 Male and female mate choice in the redlip blenny: why bigger is better. Anim. Behav. 38, 78-88.
7. Deerenberg, C., Apanius, V., Daan, S. & Bos, N. 1997 Reproductive effort decreases antibody responsiveness. Proc. R. Soc. B 264, 1021-1029. (doi:10.1098/rspb.1997.0141)
8. Folstad, I. & Karter, A. J. 1992 Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139, 603-622. (doi:10.1086/285346)
9. Gross, M. 1984 Sunfish, Salmon, and the evolution of alternative reproductive strategies and tactics in fishes. In Fish reproduction: strategies and tactics (ed. R. Wooton & G. Potts), pp. 55-75. London: Academic Press.
10. Hirschenhauser, K., Taborsky, M., Oliveira, T., Canario, A. V. M. & Oliveira, R. F. 2004 A test of the 'challenge hypothesis' in cichlid fish: simulated partner and territory intruder experiments. Anim. Behav. 68, 741-750. (doi:10.1016/j.anbehav.2003.12.015)
11. Kime, D. E. & Manning, N. J. 1982 Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta. Gen. Comp. Endocrinol. 48, 222-231. (doi:10.1016/0016-6480(82)90020-X)
12. Kindler, P. M., Bahr, J. M. & Philipp, D. P. 1991 The effects of exogenous 11-ketotestosterone, testosterone, and cyproterone acetate on prespawning and parental care behaviors of male bluegill. Horm. Behav. 25, 410-423. (doi:10.1016/0018-506X(91)90011-6)
13. Knapp, R. 2004 Endocrine mediation of vertebrate male alternative reproductive tactics: the next generation of studies. Integr. Comp. Biol. 43, 658-668.
14. Kortet, R., Taskinen, J., Sinisalo, T. & Jokinen, I. 2003 Breeding-related seasonal changes in immunocompetence, health state and condition of the cyprinid fish, Rutilus rutilus, L. Biol. J. Linn. Soc. 78, 117-127. (doi:10.1046/j.1095-8312.2003.00136.x)
15. Leonard, J. B. K., Iwata, M. & Ueda, H. 2002 Seasonal changes of hormones and muscle enzymes in adult lacustrine masu (Oncorhynchus masou) and sockeye salmon (O. nerka). Fish Physiol. Biochem. 25, 153-163. (doi:10.1023/A:1020512105096)
16. Martin II, L. B., Scheuerlein, A. & Wikelski, M. 2003 Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc. R. Soc. B 270, 153-158. (doi:10.1098/rspb. 2002.2185)
17. Meseguer, J., Esteban, M. A. & Rodriguez, A. 2002 Are thrombocytes and platelets true phagocytes? Microsc. Res. Tech. 57, 491-497. (doi:10.1002/jemt.10102)
18. Norris, K. & Evans, M. R. 2000 Ecological immunity: life history trade-offs and immune defense in birds. Behav. Ecol. 11, 19-20. (doi:10.1093/beheco/11.1.19)
19. Oliveira, R. F. 2005 Neuroendocrine mechanisms of alternative reproductive tactics in fish. In Behaviour and physiology of fish, vol. 24 (ed. K. A. Sloman, R. W. Wilson & S. Balshine) New York: Elsevier.
20. Oliveira, R. F., Miranda, J. A., Carvalho, N., Gonçalves, E. J., Grober, M. S. & Santos, R. S. 2000 Male mating success in the Azorean rock-pool blenny: the effects of body size, male behaviour and nest characteristics. J. Fish Biol. 57, 1416-1428. (doi:10.1111/j.1095- 8649.2000.tb02221.x)
21. Oliveira, R. F., Canário, A. V. M. & Grober, M. S. 2001a Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (pisces: blenniidae). Horm. Behav. 40, 266-275. (doi:10.1006/hbeh.2001.1683)
22. Oliveira, R. F., Canário, A. V. M., Grober, M. S. & Santos, R. S. 2001b Endocrine correlates of male polymorphism and alternative reproductive tactics in the Azorean rockpool blenny. Parablennius sanguinolentus parvicornis. Gen. Comp. Endocrinol. 121, 278-288. (doi:10.1006/gcen.2001.7596)
23. Oliveira, R. F., Carneiro, L. A., Canário, A. V. M. & Grober, M. S. 2001c Effects of androgens on social behavior and morphology of alternative reproductive males of the Azorean rock-pool blenny. Horm. Behav. 39, 157-166. (doi:10.1006/hbeh.2001.1643)
24. Oliveira, R. F., Carvalho, N., Miranda, J. A., Gonçalves, E. J., Grober, M. S. & Santos, R. S. 2002a The relationship between the presence of satellite males and nest-holders' mating success in the Azorean rock-pool blenny Parablennius sanguinolentus parvicornis. Ethology 108, 223-235. (doi:10.1046/j.1439-0310.2002.00776.x)
25. Oliveira, R. F., Hirschenhauser, K., Carneiro, L. & Canário, A. V. M. 2002b Social modulation of androgen levels in male teleost fish. Comp. Biochem. Physiol. B 132, 203-215. (doi:10.1016/S1096- 4959(01)00523-1)
26. Oliveira, R. F., Ros, A. F. H. & Gonçalves, D. M. 2005 Intrasexual variation in male reproduction in teleost fish: a comparative approach. Horm. Behav. 48, 430-439. (doi:10.1016/j.yhbeh.2005.06. 002)
27. Páll, M. K., Mayer, I. & Borg, B. 2002 Androgen and behavior in the male three-spined stickleback, Gasterosteus aculeatus. II. Castration and 11-ketoandrostenedione effects on courtship and parental care during the nesting cycle. Horm. Behav. 42, 337-344. (doi:10.1006/hbeh.2002.1820)
28. Rhen, T. & Crews, D. 2002 Variation in reproductive behaviour within a sex: neural systems and endocrine activation. J. Neuroendocrinol. 14, 517-531. (doi:10.1046/j.1365-2826.2002.00820.x)
29. Roberts, M. L., Buchanan, K. L. & Evans, M. R. 2004 Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim. Behav. 68, 227-239. (doi:10.1016/j.anbehav.2004.05.001)
30. Robertson, O. H. & Wexter, B. C. 1960 Histological changes in the organs and tissues of migrating and spawning pacific salmon (genus Oncorhynchus). Endocrinology 66, 222-239.
31. Robertson, O. H., Krupp, M. A., Favour, C. B., Hane, S. & Thomas, S. F. 1961 Physiological changes occurring in the blood of the pacific salmon (Oncorhynchus tshawytcha) accompanying sexual maturation and spawning. Endocrinology 68, 733-746.
32. Ros, A. F. H., Bruintjes, R., Santos, R. S., Canario, A. V. M.& Oliveira, R. F. 2004 The role of androgens in the trade-off between territorial and parental behavior in the Azorean rock-pool blenny, Parablennius parvicornis. Horm. Behav. 46, 491-497. (doi:10.1016/j.yhbeh.2004.04. 007)
33. Salek, S. J., Sullivan, C. V. & Godwin, J. 2001 Courtship behavior of male white perch, Morone americana: evidence for control by androgens. Comp. Biochem. Physiol. 130A, 731-740.
34. Santos, R. S. 1985 Parentais e satélites: tácticas alternativas de acasalamento nos machos de Blennius sanguinolentus Pallas (Pisces: Blenniidae). Arquipélago, Sér. Ciênc. Natur. 6, 119-146.
35. Santos, R. S. 1995 Anatomy and histology of secondary sexual characters gonads and liver of the rock-pool blenny, Parablennius sanguinolentus parvicornis (Piscus: Blenniidae) of the Azores. Arquipélago, Life Mar. Sci. 13A, 21-38.
36. Santos, R. S. & Almada, V. 1988 Intraspecific variations in reproductive tactics in males of the rocky intertidal fish Blennius sanguinolentus in Azores. In Behavioral adaptation to intertidal life (ed. G. Chellazzi & M. Vannini), pp. 421-447. New York: Plenum Press.
37. Santos, R. S. & Barreiros, J. P. 1993 The ethogram of Parablennius sanguinolentus parvicornis (Pisces: Blenniidae) of the Azores. Arquipélago, Life Mar. Sci. 11A, 73-90.
38. Santos, R. S. & Nash, R. D. M. 1996 Seasonal variations of injuries suffered by individuals of the Azorean rock-pool blenny (Parablennius sanguinolentus parvicornis). Copeia 1, 219-261.
39. Santos, R. S., Nash, R. D. M. & Hawkins, S. J. 1994 Fish assemblages on intertidal shores of the island of Faial, Azores. Arquipélago, Life Mar. Sci. 12, 87-100.
40. Santos, R. S., Nash, R. D. M. & Hawkins, S. J. 1995 Age, growth and sex ratio of the Azorean rock-pool blenny, Parablennius sanguinolentus parvicornis. J. Mar. Biol. Assoc. UK 75, 751-754.
41. Scaggiante, M., Grober, M. S., Lorenzi, V. & Rasotto, M. B. 2004 Changes along the male reproductive axis in response to social context in a gonochoristic gobiid, Zosterisessor ophiocephalus (Teleostei, Gobiidae), with alternative mating tactics. Horm. Behav. 46, 607-617. (doi:10.1016/j.yhbeh.2004.06.016)
42. Scott, A. P. & Vermeirssen, E. L. M. 1994 Production of conjugated steroids by teleost gonads and their role as pheromones. In Perspectives in comparative endocrinology (ed. K. G. Davey, R. E. Peter & S. S. Tobe), pp. 645-654. Ottawa: National Research Council of Canada.
43. Scott, A. P., MacKenzie, D. S. & Stacey, N. E. 1984 Endocrine changes during natural spawning in the white sucker, Catostomus commersoni. II. Steroid hormones. Gen. Comp. Endocrinol. 56, 349-359. (doi:10.1016/0016-6480(84)90077-7)
44. Semsar, K. & Godwin, J. 2003 Social influences on the arginine vasotocin system are independent of gonads in a sex-changing fish. J. Neurosci. 23, 4386-3493.
45. Sheldon, B. C. & Verhulst, S. 1996 Ecological immunity: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321. (doi:10.1016/0169-5347(96)10039-2)
46. Skarstein, F. & Folstad, I. 1996 Sexual dimorphism and the immunocompetence handicap: an observational approach using arctic charr. Oikos 76, 359-367.
47. Slater, C. H. & Schreck, C. B. 1993 Testosterone alters the immune response of Chinook salmon (Oncorhynchus tshawytcha). Gen. Comp. Endocrinol. 89, 291-298. (doi:10.1006/gcen.1993.1035)
48. Slater, C. H. & Schreck, C. B. 1997 Physiological levels of testosterone kill salmonid leucocytes, in vitro. Gen. Comp. Endocrinol. 106, 113-119. (doi:10.1006/gcen.1996.6858)
49. Slater, C. H. & Schreck, C. B. 1998 Season and physiological parameters modulate salmonid leucocyte androgen receptor affinity and abundance. Fish Shellfish Immunol. 8, 379-391. (doi:10.1006/fsim.1998.0150)
50. Slater, C. H., Fitzpatrick, M. S. & Schreck, C. B. 1995a Androgens and immunocompetence in salmonids: specific binding of and reduced immunocompetence of salmonid lymphocytes exposed to natural and synthetic androgens. Aquaculture 136, 363-370. (doi:10.1016/0044-8486(95) 01062-9)
51. Slater, C. H., Fitzpatrick, M. S. & Schreck, C. B. 1995b Characterization of an androgen receptor in salmonid lymphocytes: possible link to androgen induced immunosuppression. Gen. Comp. Endocrinol. 100, 218-225. (doi:10.1006/gcen.1995.1151)
52. Taborsky, M. 1994 Sneakers, satellites, and helpers: parasitic and cooperative behaviour in fish reproduction. Adv. Study Behav. 23, 1-100.
53. Taborsky, M. 1997 Bourgeois and parasitic tactics: do we need collective, functional terms for alternative reproductive behaviours? Behav. Ecol. Sociobiol. 41, 361-362. (doi:10.1007/s002650050396)
54. Taborsky, M. 1998 Sperm competition in fish: 'bourgeois' males and parasitic spawning. Trends Ecol. Evol. 13, 222-227. (doi:10.1016/S0169-5347(97)01318-9)
55. Taborsky, M. 2001 The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. J. Hered. 92, 100-110. (doi:10.1093/jhered/92.2.100)
56. Uglem, I., Galloway, T. F., Rosenqvist, G. & Folstad, I. 2001 Male dimorphism, sperm traits and immunology in the corkwing wrasse (Symphodus melops L.). Behav. Ecol. Sociobiol. 50, 511-518. (doi:10.1007/s002650100392)
57. Uglem, I., Mayer, I. & Rosenqvist, G. 2002 Variation in plasma steroids and reproductive traits in dimorphic males of corkwing wrasse (Symphodus melops L.). Horm. Behav. 41, 396-404. (doi:10.1006/hbeh.2002.1779)
58. Wedekind, C. & Folstad, I. 1994 Adaptive or nonadaptive immunosuppression by sex hormones? Am. Nat. 143, 936-938. (doi:10.1086/285641)
59. Weyts, F. A. A., Cohen, N., Flik, G. & Verburg-van-Kemenade, M. L. 1999 Interactions between the immune system and the hypothalamo-pituitary- interrenal axis in fish. Fish Shellfish Immunol. 9, 1-20. (doi:10.1006/fsim.1998.0170)
60. 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)