Differential Responses of Brain, Gonad and Muscle Steroid Levels to Changes in Social Status and Sex in a Sequential and Bidirectional Hermaphroditic Fish

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Lorenzi, Varenka ^a   Earley, Ryan L ^a   Grober, Matthew S ^a,b  

^a GEORGIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

11 OXOTESTOSTERONE; ESTRADIOL; TESTOSTERONE;

ANATOMICAL VARIATION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONCENTRATION (PARAMETERS); FEMALE; FISH; GONAD; HERMAPHRODITIC SPECIES; LYTHRYPNUS DALLI; MALE; MORPHOLOGY; MUSCLE; NONHUMAN; OUTCOME ASSESSMENT; SEX DIFFERENCE; SEX TRANSFORMATION; SOCIAL ENVIRONMENT; SOCIAL STATUS; TISSUE LEVEL;

ANIMALS; BRAIN; DISORDERS OF SEX DEVELOPMENT; FEMALE; FISHES; GONADAL STEROID HORMONES; GONADS; MALE; MUSCLES;

LYTHRYPNUS DALLI;

EID: 84870871353     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051158     Document Type: Article

References (56)

1. Nelson RJ (2005) An introduction to behavioral endocrinology. Sinauer Associate, Inc. Sunderland, MA.
2. Liley NR, Breton B, Fostier A, Tan ESP, (1986) Endocrine changes associated with spawning behavior and social stimuli in a wild population of rainbow trout (Salmo gairdneri): I. Males. Gen Comp Endocrinol 62: 145-156.
3. Oliveira RF, (2009) Social behavior in context: hormonal modulation of behavioral plasticity and social competence. Integrat Comp Biol 49: 423-440.
4. Oliveira RF, Hirschenhauser K, Carneiro LA, Canário AVM, (2002) Social modulation of androgen levels in male teleost fish. Comparative Biochemistry and Physiology Part B: Biochem. Mol Biol 132: 203-215.
5. Wingfield JC, (1984) Environmental and endocrine control of reproduction in the song sparrow, Melospiza melodia: II. Agonistic interactions as environmental information stimulating secretion of testosterone. Gen Comp Endocrinol 56: 417-424.
6. Remage-Healey L, Bass AH, (2005) Rapid elevations in both steroid hormones and vocal signaling during playback challenge: a field experiment in Gulf toadfish. Horm Behav 47: 297-305.
7. Remage-Healey L, Bass AH, (2006) From social behavior to neural circuitry: steroid hormones rapidly modulate advertisement calling via a vocal pattern generator. Horm Behav 50: 432-441.
8. Elekonich MM, Wingfield JC, (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Emberizidae: Melospiza melodia). Ethology 106: 493-510.
9. Davis ES, Marler CA, (2003) The progesterone challenge: steroid hormone changes following a simulated territorial intrusion in female Peromyscus californicus. Horm Behav 44: 185-198.
10. Desjardins JK, Hazelden MR, Van der Kraak GJ, Balshine S, (2006) Male and female cooperatively breeding fish provide support for the "Challenge Hypothesis". Behav Ecol 17: 149-154.
11. Taves MD, Ma C, Heimovics SA, Saldanha CJ, Soma KK, (2011) Measurement of steroid concentrations in brain tissue: methodological considerations. Front Endocrinol 2: 1-13.
12. Andersson E, Borg B, Lambert JGD, (1988) Aromatase activity in brain and pituitary of immature and mature Atlantic salmon (Salmo salar L.) parr. Gen Comp Endocrinol 72: 394-401.
13. Pasmanik M, Callard GV, (1985) Aromatase and 5[alpha]-reductase in the teleost brain, spinal cord, and pituitary gland. Gen Comp Endocrinol 60: 244-251.
14. Mayer I, Borg B, Schulz RD, (1990) Seasonal changes in and effect of castration/androgen replacement on the plasma levels of five androgens in the male three-spined stickleback, Gasterosteus aculeatus L. Gen Comp Endocrinol. 79: 23-30.
15. Schulz R, Blum V, (1991) Extragonadal 17[beta]-hydroxysteroid dehydrogenase activity in rainbow trout. Gen Comp Endocrinol 82: 197-205.
16. Balthazart J, Ball GF, (2006) Is brain estradiol a hormone or a neurotransmitter? Trends Neurosci 29: 241-249.
17. Black MP, Balthazart J, Baillien M, Grober MS, (2005) Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex-changing fish, Lythrypnus dalli. Proc R Soc B-Biol Sci 272: 2435-2440.
18. Cornil CA, Ball GF, Balthazart J, (2006) Functional significance of the rapid regulation of brain estrogen action: Where do the estrogens come from? Brain Res 1126: 2-26.
19. Remage-Healey L, Bass AH, (2006b) A rapid neuromodulatory role for steroid hormones in the control of reproductive behavior. Brain Res 1126: 27-35.
20. Schmidt KL, Pradhan DS, Shah AH, Charlier TD, Chin EH, et al. (2008) Neurosteroids, immunosteroids, and the balkanization of endocrinology. Gen Comp Endocrinol 157: 266-274.
21. Woolley CS, (2007) Acute effects of estrogen on neuronal physiology. Annual Rev Pharmacol Toxicol 47: 657-680.
22. Remage-Healey L, Maidment NT, Schlinger BA, (2008) Forebrain steroid levels fluctuate rapidly during social interactions. Nature Neurosci 11: 1327-1334.
23. Schultz DR, Perez N, Tan CK, Mendez AJ, Capo TR, et al. (2005) Concurrent levels of 11-ketotestosterone in fish surface mucus, muscle tissue and blood. J App Ichthyol 21: 394-398.
24. Barnett L, Earley R, Ebert D, Cailliet G, (2009) Maturity, fecundity, and reproductive cycle of the spotted ratfish, Hydrolagus colliei. Mar Biol 156: 301-316.
25. Nakamura M, Hourigan TF, Yamauchi K, Nagahama Y, Grau EG, (1989) Histological and ultrastructural evidence for the role of gonadal steriod hormones in sex change in the protogynous wrasse Thalassoma duperrey. Environ Biol Fishes 24: 117-136.
26. Reavis RH, Grober MS, (1999) An integrative model of sex change: social, behavioural and neurochemical changes in Lythrypnus dalli (Pisces) Acta Ethol. 2: 51-60.
27. Rodgers EW, Earley RL, Grober MS, (2007) Social status determines sexual phenotype in the bi-directional sex changing bluebanded goby Lythrypnus dalli. J Fish Biol 70: 1660-1668.
28. Frisch A, (2004) Sex-change and gonadal steroids in sequentially-hermaphroditic teleost fish. Rev Fish Biol Fisheries 14: 481-499.
29. Kroon FJ, Liley NR, (2000) The role of steroid hormones in protogynous sex change in the blackeye goby, Coryphopterus nicholsii (Teleostei: Gobiidae) Gen Comp Endocrinol. 118: 273-283.
30. Kroon FJ, Munday PL, Pankhurst NW, (2003) Steroid hormone levels and bi-directional sex change in Gobiodon histrio. J Fish Biol 62: 153-167.
31. Bhandari RK, Alam MA, Higa M, Soyano K, Nakamura M, (2005) Evidence that estrogen regulates the sex change of honeycomb grouper (Epinephelus merra), a protogynous hermaphrodite fish. J. Exp. Zool. Part A-Comp Exp Biol 303A: 497-503.
32. Bhandari RK, Alam MA, Soyano K, Nakamura M, (2006) Induction of female-to-male sex change in the honeycomb grouper (Epinephelus merra) by 11-ketotestosterone treatments. Zool Sci 23: 65-69.
33. Cardwell JR, Liley NR, (1991) Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride. Gen Comp Endocrinol 81: 7-20.
34. Kobayashi M, Aida K, Stacey NE, (1991) Induction of testis development by implantation of 11-ketotestosterone in female goldfish. Zool Sci 8: 389-393.
35. Lone KP, Al-Ablani S, Al-Yaqout A, (2001) Steroid hormone profiles and correlative gonadal histological changes during natural sex reversal of sobaity kept in tanks and sea-cages. J Fish Biol 58: 305-324.
36. Ohta K, Mine T, Yamaguchi A, Matsuyama M, (2001) Steroidogenic Pathway to Estradiol-17β synthesis in the ovarian follicles of the protogynous wrasse, Pseudolabrus sieboldi. Zool Sci 18: 937-945.
37. Yeung WSB, Chan STH, (1987) A radioimmunoassay study of the plasma levels of sex steriods in the protandrous, sex-reversing fish Rhabdosargus sarba (Sparidae) Gen Comp Endocrinol. 66: 353-363.
38. Behrents KC (1983) The comparative ecology and interactions between two sympatric gobies (Lythrypnus dalli and Lythrypnus zebra) PhD Dissertation, University of Southern California.
39. Lorenzi V, Earley RL, Rodgers EW, Pepper DR, Grober MS, (2008) Diurnal patterns and sex differences in cortisol, 11-ketotestosterone, testosterone, and 17 beta-estradiol in the bluebanded goby (Lythrypnus dalli). Gen Comp Endocrinol 155: 438-446.
40. Newman AEM, Chin EH, Schmidt KL, Bond L, Wynne-Edwards KE, et al. (2008) Analysis of steroids in songbird plasma and brain by coupling solid phase extraction to radioimmunoassay. Gen Comp Endocrinol 155: 503-510.
41. Borg B (1994) Androgens in teleost fishes. Comp. Biochem. Physiol. 109C, 219-245.
42. Diotel N, Do Rego JL, Anglade I, Vaillant C, Pellegrini E, et al. (2011) The Brain of Teleost Fish, a Source, and a Target of Sexual Steroids. Frontiers in Neuroscience 5: 137.
43. Avvakumov GV, Zhuk NI, Strel'chyonok OA, (1986) Subcellular distribution and selectivity of the protein-binding component of the recognition system for sex-hormone-binding protein-estradiol complex in human decidual endometrium. Biochim. Biophys Acta Gen Sub 881: 489-498.
44. Caldwell JD, Shapiro RA, Jirikowski GF, Suleman F, (2007) Internalization of sex hormone-binding globulin into neurons and brain cells in vitro and in vivo. Neuroendocrinol 86: 84-93.
45. Neat FC, Mayer I, (1999) Plasma concentrations of sex steroids and fighting in male Tilapia zillii. J Fish Biol 54: 695-697.
46. Miguel-Queralt S, Avvakumov GV, Blázquez M, Piferrer F, Hammond GL, (2005) Sea bass (Dicentrarchus labrax) sex hormone binding globulin: molecular and biochemical properties and phylogenetic comparison of its orthologues in multiple fish species. Mol Cell Endocrinol 229: 21-29.
47. Miguel-Queralt S, Knowlton M, Avvakumov GV, Al-Nouno R, Kelly GM, et al. (2004) Molecular and functional characterization of sex hormone binding globulin in zebrafish. Endocrinol 145: 5221-5230.
48. Pasmanik M, Callard GV, (1986) Characteristics of a testosterone-estradiol binding globulin (TEBG) in goldfish serum. Biol Reprod 35: 838-845.
49. Godwin JR, Thomas P, (1993) Sex-change and steroid profiles in the protandrous anemonefish Amphiprion melanopus (Pomacentridae, Teleostei). Gen Comp Endocrinol 91: 144-157.
50. Carlisle SL, Marxer-Miller SK, Canario AVM, Oliveira RF, Carneiro L, et al. (2000) Effects of 11-ketotestosterone on genital papilla morphology in the sex changing fish Lythrypnus dalli. J Fish Biol 57: 445-456.
51. Cardwell JR, Liley NR, (1991) Androgen control of social status in males of a wild population of stoplight parrotfish, Sparisoma viride (Scaridae). Horm Behav 25: 1-18.
52. Li GL, Liu XC, Lin HR, (2007) Seasonal changes of serum sex steroids concentration and aromatase activity of gonad and brain in red-spotted grouper (Epinephelus akaara). Anim Reprod Sci 99: 156-166.
53. Saldanha CJ, Remage-Healey L, Schlinger BA (2011) Synaptocrine Signaling: Steroid Synthesis and Action at the Synapse. Endocr Rev doi: 10.1210/er.2011-0004.
54. Kamel F, Mock EJ, Wright WW, Frankel AI, (1975) Alterations in plasma concentrations of testosterone, LH, and prolactin associated with mating in the male rat. Horm Behav 6: 277-288.
55. Macrides F, Bartke A, Dalterio S, (1975) Strange females increase plasma testosterone levels in male mice. Science 189: 1104-1106.
56. Pinxten R, de Riddera E, Eensa M, (2003) Female presence affects male behavior and testosterone levels in the European starling (Sturnus vulgaris). Horm Behav 44: 103-109.