An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish

Environmental Science and Technology

Volumn 42, Issue 13, 2008, Pages 5020-5025

  Coe, Tobias S ^a   Hamilton, Patrick B ^a   Hodgson, David ^a   Paull, Gregory C ^a   Stevens, Jamie R ^a   Sumner, Katie ^a   Tyler, Charles R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOCRINE DISRUPTING CHEMICAL (EDC); ENDOCRINE DISRUPTION; ETHINYLESTRADIOL (EE2); POTENTIAL IMPACTS; REPRODUCTIVE FUNCTION; SEXUAL SELECTION; SOCIAL STRUCTURES;

FISH;

11 OXOTESTOSTERONE; ANDROGEN; ENDOCRINE DISRUPTOR; ETHINYLESTRADIOL; MICROSATELLITE DNA;

CONCENTRATION (COMPOSITION); CYPRINID; DOMINANCE; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; PATERNITY; REPRODUCTION; REPRODUCTIVE SUCCESS; SEX HORMONE; SEXUAL SELECTION; SOCIAL STRUCTURE; SPAWNING;

ANDROGEN BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREEDING; DNA DETERMINATION; ENVIRONMENTAL EXPOSURE; FEMALE; MATING SYSTEM; MOUSE; NONHUMAN; REPRODUCTIVE SUCCESS; REPRODUCTIVE TOXICITY; SEXUAL SELECTION; SPAWNING; ZEBRA FISH;

ANDROGENS; ANIMALS; DNA PRIMERS; ETHINYL ESTRADIOL; FEMALE; HIERARCHY, SOCIAL; MALE; MATING PREFERENCE, ANIMAL; MICROSATELLITE REPEATS; REPRODUCTION; TESTOSTERONE; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

DANIO RERIO;

ELEVATED PLASMA; ENDOCRINE DISRUPTING CHEMICALS; ENDOCRINE DISRUPTION; ENVIRONMENTAL ESTROGENS; ETHINYLESTRADIOL; GENETIC DIVERSITY; MATING SYSTEM; MICRO SATELLITE; POTENTIAL IMPACTS; REPRODUCTIVE FUNCTION; REPRODUCTIVE OUTPUT; REPRODUCTIVE SUCCESS; SEX HORMONES; SEXUAL SELECTION; SOCIAL STRUCTURE; ZEBRAFISH;

ENVIRONMENTAL ENGINEERING; ENVIRONMENTAL PROTECTION;

EID: 46849119184     PISSN: 0013936X     EISSN: None     Source Type: Journal    
DOI: 10.1021/es800277q     Document Type: Article

References (50)

1. Tyler, C. R.; Jobling, S.; Sumpter, J. P. Endocrine disruption in wildlife: a critical review of the evidence. Crit. Rev. Toxicol. 1998, 28 (4), 319-361.
2. Vos, J. G.; Dybing, E.; Greim, H. A.; Ladefoged, O.; Lambre, C.; Tarazona, J. V.; Brandt, I.; Vethaak, A. D. Health Effects of Endocrine-Disrupting Chemicals on Wildlife, with Special Reference to the European Situation. Crit. Rev. Toxicol. 2000, 30 (1), 71-133.
3. Hayes, T. B.; Collins, A.; Lee, M.; Mendoza, M.; Noriega, N.; Stuart, A. A.; Vonk, A. Hermaphroditic, demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. PNAS 2002, 99 (8), 5476-5480.
4. Oehlmann, J.; Schulte-Oehlmann, U.; Bachmann, J.; Oetken, M.; Lutz, I.; Kloas, W.; Ternes, T. A. Bisphenol A induces superfeminization in the ramshorn snail Marisa cornuarietis (Gastropoda: Prosobranchia) at environmentally relevant concentrations. Environ. Health Perspect. 2006, 114, 127-133.
5. Hirai, N.; Nanba, A.; Koshio, M.; Kondo, T.; Morita, M.; Tatarazako, N. Feminization of Japanese medaka (Oryzias latipes) exposed to 17 beta-estradiol: Effect of exposure period on spawning performance in sex-transformed females. Aquat. Toxicol. 2006, 79 (3), 288-295.
6. Pettersson, I.; Arukwe, A.; Lundstedt-Enkel, K.; Mortensen, A. S.; Berg, C. Persistent sex-reversal and oviducal agenesis in adult Xenopus (Silurana) tropicalis frogs following larval exposure to the environmental pollutant ethynylestradiol. Aquat. Toxicol. 2006, 79 (4), 356-365.
7. Robinson, C. D.; Brown, E.; Craft, J. A.; Davies, I. M.; Megginson, C.; Miller, C.; Moffat, C. F. Bioindicators and reproductive effects of prolonged 17β-oestradiol exposure in a marine fish, the sand goby (Pomatoschistus minutus). Aquat. Toxicol. 2007, 81, 397-408.
8. Scholz, S.; Gutzeit, H. O. 17-alpha-ethinylestradiol affects reproduction, sexual differentiation and aromatase gene expression ofthe medaka (Oryzias latipes). Aquat. Toxicol. 2000, 50 (4), 363-373.
9. Anway, M. D.; Cupp, A. S.; Uzumcu, M.; Skinner, M. K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 2005, 308 (5727), 1466-1469.
10. Corrieri, L.; Della Seta, D.; Canoine, V.; Fusani, L. Developmental exposure to xenoestrogen enhances spatial learning in male rats. Horm. Behav. 2007, 51 (5), 620-625.
11. Laessig, S. A.; Auger, A. P.; McCarthy, M. M.; Silbergeld, E. K. Effects of prenatal chlordecone on sexually differentiated behavior in adult rats. Neurotoxicol. Teratol. 2007, 29 (2), 255-263.
12. Della Seta, D.; Minder, I.; Belloni, V.; Aloisi, A. M.; Dessi-Fulgheri, F.; Farabollini, F. Pubertal exposure to estrogenic chemicals affects behavior in juvenile and adult male rats. Horm. Behav. 2006, 50 (2), 301-307.
13. Gray, M. A.; Teather, K. L.; Metcalfe, C. D. Reproductive success and behavior of Japanese medaka (Oryzias latipes) exposed to 4-tert-octylphenol. Environ. Toxicol. Chem. 1999, 18 (11), 2587-2594.
14. Bjerselius, R.; Lundstedt-Enkel, K.; Olsen, H.; Mayer, I.; Dimberg, K. Male goldfish reproductive behaviour and physiology are severely affected by exogenous exposure to 17[beta]-estradiol. Aquat. Toxicol. 2001, 53 (2), 139.
15. Doyle, C. J.; Lim, R. P. Sexual behavior and impregnation success of adult male mosquitofish following exposure to 17 beta-estradiol. Ecotoxicol. Environ. Safe. 2005, 61 (3), 392-397.
16. Nash, J. P.; Kime, D. E.; Van der Ven, L. T. M.; Wester, P. W.; Brion, F.; Maack, G.; Stahlschmidt-Allner, P.; Tyler, C. R. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ. Health Perspect. 2004, 112 (17), 1725-1733.
17. Fenske, M.; Maack, G.; Schafers, C.; Segner, H. An environmentally relevant concentration of estrogen induces arrest of male gonad development in zebrafish Danio rerio. Environ. Toxicol. Chem. 2005, 24 (5), 1088-1098.
18. Kidd, K. A.; Blanchfield, P. J.; Mills, K. H.; Palace, V. P.; Evans, R. E.; Lazorchak, J. M.; Flick, R. W. Collapse of a fish population after exposure to a synthetic estrogen. PNAS 2007, 104 (21), 8897-8901.
19. Grist, E. P. M.; Wells, N. C.; Whitehouse, P.; Brighty, G.; Crane, M. Estimating the effects of 17 alpha-ethinylestradiol on populations of the fathead minnow Pimephales promelas: Are conventional toxicological endpoints adequate? Environ. Sci. Technol. 2003, 37 (8), 1609-1616.
20. Caswell, H. Matrix Population Models, 2nd ed.; Sinauer Associates, 2001.
21. Hodgson, D. J.; Townley, S. Linking management changes to population dynamic responses: the transfer function of a projection matrix perturbation. J. Appl. Ecol. 2004, 41 (6), 1155-1161.
22. Lange, R.; Hutchinson, T. H.; Croudace, C. P.; Siegmund, F. Effects of the synthetic estrogen 17 alpha-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ. Toxicol. Chem. 2001, 20 (6), 1216-1227.
23. Meng, Y. B.; Lin, B. L.; Tominaga, M.; Nakanishi, J. Simulation ofthe population-level effects of 4-nonylphenol on wild Japanese medaka (Oryzias latipes). Ecol. Model. 2006, 197 (3-4), 350-360.
24. Miller, D. H.; Ankley, G. T. Modeling impacts on populations: fathead minnow (Pimephales promelas) exposure to the endocrine disrupter 17 beta-trenbolone as a case study. Ecotoxicol. Environ. Safe. 2004, 59 (1), 1-9.
25. Ankley, G. T.; Johnson, R. D. Small fish models for identifying and assessing the effects of endocrine-disrupting chemicals. Ilar J. 2004, 45 (4), 469-483.
26. Pyron, M. Female preferences and male-male interactions in zebrafish (Danio rerio). Can. J. Zool. 2003, 81 (1), 122-125.
27. Spence, R.; Smith, C. Mating preference of female zebrafish, Danio rerio, in relation to male dominance. Behav. Ecol. 2006, 17 (5), 779-783.
28. Pauli, G. C.; Van Look, K. J. W.; Santos, E. M.; Filby, A. L.; Gray, D. M.; Nash, J. P.; Tyler, C. R. Variability in measures of reproductive success in laboratory-kept colonies of zebrafish and implications for studies addressing population-level effects of environmental chemicals. Aquat. Toxicol. 2008, In Press, Corrected Proof.
29. Larsson, D. G. J.; Adolfsson-Erici, M.; Parkkonen, J.; Pettersson, M.; Berg, A. H.; Olsson, P. E.; Forlin, L. Ethinyloestradiol - an undesired fish contraceptive. Aquat. Toxicol. 1999, 45 (2-3), 91-97.
30. van Aerle, R.; Pounds, N.; Hutchinson, T. H.; Maddix, S.; Tyler, C. R. Window of sensitivity for the estrogenic effects of ethinylestradiol in early life-stages of fathead minnow Pimephales promelas. Ecotoxicology 2002, 11 (6), 423-434.
31. Hill, R. L.; Janz, D. M. Developmental estrogenic exposure in zebrafish (Danio rerio): I. Effects on sex ratio and breeding success. Aquat. Toxicol. 2003, 63 (4), 417-429.
32. Orn, S.; Holbech, H.; Madsen, T. H.; Norrgren, L.; Petersen, G. I. Gonad development and vitellogenin production in zebrafish (Danio rerio) exposed to ethinylestradiol and methyltestosterone. Aquat. Toxicol. 2003, 65 (4), 397-411.
33. Van den Belt, K.; Verheyen, R.; Witters, H. Effects of 17 alpha-ethynylestradiol in a partial life-cycle test with zebrafish (Danio rerio): effects on growth, gonads and female reproductive success. Sci. Total Environ. 2003, 309 (1-3), 127-137.
34. Katsu, Y.; Lange, A.; Urushitani, H.; Ichikawa, R.; Pauli, G. C.; Cahill, L. L.; Jobling, S.; Tyler, C. R.; Iguchi, T. Functional associations between two estrogen receptors, environmental estrogens, and sexual disruption in the Roach (Rutilus rutilus). Environ. Sci. Technol. 2007, 41 (9), 3368-3374.
35. Jobling, S.; Williams, R.; Johnson, A.; Taylor, A.; Gross-Sorokin, M.; Nolan, M.; Tyler, C. R.; Van Aerie, R.; Santos, E.; Brighty, G. Predicted exposures to steroid estrogens in U.K. rivers correlate with widespread sexual disruption in wild fish populations. Environ. Health Perspect. 2006, 114 (S1), 32-39.
36. Santos, E. M.; Workman, V. L.; Pauli, G. C.; Filby, A. L.; Van Look, K. J. W.; Kille, P.; Tyler, C. R. Molecular basis of sex and reproductive status in breeding zebrafish. Physiol. Genomics 2007, 30 (2), 111-122.
37. Pritchard, V. L.; Lawrence, J.; Butlin, R. K.; Krause, J. Shoal choice in zebrafish, Danio rerio: the influence of shoal size and activity. Anim. Behav. 2001, 62, 1085-1088.
38. Kelly, C. Analysis of steroids in environmental water samples using solid-phase extraction and ion-trap gas chromatography-mass spectrometry and gas chromatography-tandem mass spectrometry. J. Chromatogr. A 2000, 872, 309-314.
39. Borg, B.; Mayer, I. Androgens and behaviour in the three-spined stickleback. Behaviour 1995, 132, 1025-1035.
40. Scott, A. P.; Mackenzie, D. N.; Stacey, N. E. Endocrine changes during natural spawning of the white sucker Catostomus commersoni. II. Steroid hormones. Gen. Comp. Endocr. 1984, 56, 349-359.
41. Bruford, M. W.; Hanotte, O.; Brookfield, J. F. Y.; Burke, T. Multilocus and single-locus DNA fingerprinting. In Molecular Genetic Analysis of Populations: A practical approach, 2nd ed.; Hoelzel, A. R., Ed.; IRL Press: Oxford, 1998.
42. Danzmann, R. G. PROBMAX: A computer program for assigning unknown parentage in pedigree analysis from known genotypic pools of parents and progeny. J. Hered. 1997, 88 (4), 333-333.
43. Crawley, M. J. Statistics - An introduction using R; John Wiley and Sons, Ltd: New York, 2007.
44. Schafers, C.; Teigeler, M.; Wenzel, A.; Maack, G.; Fenske, M.; Segner, H. Concentration- and Time-dependent Effects of the Synthetic Estrogen, 17α-ethinylestradiol, on Reproductive Capabilities of the Zebrafish, Danio rerio. J. Toxicol. Environ. Health A 2007, 70, 768-779.
45. Santos, E. M.; Pauli, G. C.; Van Look, K. J. W.; Workman, V. L.; Holt, W. V.; van Aerie, R.; Kille, P.; Tyler, C. R. Gonadal transcriptome responses and physiological consequences of exposure to oestrogen in breeding zebrafish (Danio rerio). Aquat. Toxicol. 2007, 83 (2), 134.
46. Ternes, T. A.; Stumpf, M.; Mueller, J.; Haberer, K.; Wilken, R. D.; Servos, M. Behavior and occurrence of estrogens in municipal sewage treatment plants - I. Investigations in Germany, Canada and Brazil (vol 225, pg 81, 1999). Sci. Total Environ. 1999, 228 (1), 87-87.
47. Bell, A. M. Effects of an endocrine disrupter on courtship and aggressive behaviour of male three-spined stickleback, Gasterosteus aculeatus. Anim. Behav. 2001, 62, 775-780.
48. Brian, J. V.; Augley, J. J.; Braithwaite, V. A. Endocrine disrupting effects on the nesting behaviour of male three-spined stickleback Gasterosteus aculeatus L. J. Fish Biol. 2006, 68 (6), 1883-1890.
49. Spence, R.; Jordan, W. C.; Smith, C. Genetic analysis of male reproductive success in relation to density in the zebrafish, Danio rerio. Front. Zoo. 2006, 3, 5.
50. Cardwell, J. R.; Sorensen, P. W.; VanDerKraak, G. J.; Liley, N. R. Effect of dominance status on sex hormone levels in laboratory and wild-spawning male trout. Gen. Comp. Endocr. 1996, 101 (3), 333-341.