Parentage outcomes in response to estrogen exposure are modified by social grouping in zebrafish

Environmental Science and Technology

Volumn 43, Issue 21, 2009, Pages 8400-8405

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

^a UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLEAN WATERS; ENDOCRINE DISRUPTING CHEMICALS; ETHINYLESTRADIOL; GENETIC DIVERSITY; LARGE GROUPS; NONLETHAL; REPRODUCTIVE OUTPUT; REPRODUCTIVE SUCCESS; SHORT-TERM EXPOSURE; SIGNIFICANT IMPACTS; SOCIAL GROUPS; ZEBRAFISH;

DNA MINISATELLITE; ESTROGEN; ETHINYLESTRADIOL;

ADULT; BEHAVIORAL RESPONSE; CYPRINID; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; GENETIC VARIATION; GROUP BEHAVIOR; PARENTAGE; POLLUTION EFFECT; POLLUTION EXPOSURE; REPRODUCTIVE PRODUCTIVITY;

ARTICLE; CONTROLLED STUDY; FEMALE; FEMINIZATION; GENETIC VARIABILITY; MALE; NONHUMAN; PARENTHOOD; PATERNITY; SEX DIFFERENCE; WATER ANALYSIS; WATER SAMPLING; ZEBRA FISH;

ANIMALS; CELL SURVIVAL; EMBRYO, NONMAMMALIAN; ETHINYL ESTRADIOL; FEMALE; MALE; OVUM; REPRODUCTION; SOCIAL BEHAVIOR; TIME FACTORS; ZEBRAFISH;

DANIO RERIO;

EID: 70350786681     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es902302u     Document Type: Article

References (51)

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. (Pubitemid 28389719)
2. Trudeau, V.; Tyler, C. Endocrine disruption. Gen. Comp. Endocr. 2007, 153 (1-3), 13.
3. Nakada, N.; Nyunoya, H.; Nakamura, M.; Hara, A.; Iguchi, T.; Takada, H. Identification of estrogenic compounds in waste-water effluent. Environ. Toxicol. Chem. 2004, 23 (12), 2807-2815. (Pubitemid 39603322)
4. Sarmah, A. K.; Northcott, G. L.; Leusch, F. D. L.; Tremblay, L. A. Asurvey of endocrine disrupting chemicals (EDCs) in municipal sewage and animal waste effluents in the Waikato region of New Zealand. Sci. Total Environ. 2006, 355 (1-3), 135-144.
5. 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. Sci. Total Environ. 1999, 228 (1), 87.
6. Liney, K.; Hagger, J.; Tyler, C.; Depledge, M.; Galloway, T.; Jobling, S. Health effects in fish of long-term exposure to effluents from wastewater treatment works. Environ. Health Perspect. 2006, 114 (Supplement 1), 81-89.
7. Liney, K. E.; Jobling, S.; Shears, J. A.; Simpson, P.; Tyler, C. R. Assessing the sensitivity of different life stages for sexual disruption in roach (Rutilus rutilus) exposed to effluents from wastewater treatment works. Environ. Health Perspect. 2005, 113 (10), 1299-1307.
8. Rodgers-Gray, T. P.; Jobling, S.; Kelly, C.; Morris, S.; Brighty, G.; Waldock, M. J.; Sumpter, J. P.; Tyler, C. R. Exposure of juvenile roach (Rutilus rutilus) to treated sewage effluent induces dose-dependent and persistent disruption in gonadal duct development. Environ. Sci. Technol. 2001, 35 (3), 462-470.
9. Jobling, S.; Beresford, N.; Nolan, M.; Rodgers-Gray, T.; Brighty, G. C.; Sumpter, J. P.; Tyler, C. R. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol. Reprod. 2002, 66 (2), 272-281.
10. Jobling, S.; Coey, S.; Whitmore, J. G.; Kime, D. E.; Van Look, K. J. W.; McAllister, B. G.; Beresford, N.; Henshaw, A. C.; Brighty, G.; Tyler, C. R.; Sumpter, J. P. Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol. Reprod. 2002, 67 (2), 515-524.
11. Jobling, S.; Tyler, C. R. Endocrine disruption in wild freshwater fish. Pure. Appl. Chem. 2003, 75 (11-12), 2219-2234.
12. Servos, M. R.; Bennie, D. T.; Burnison, B. K.; Jurkovic, A.; McInnis, R.; Neheli, T.; Schnell, A.; Seto, P.; Smyth, S. A.; Ternes, T. A. Distribution of estrogens, 17β-estradiol and estrone, in Canadian municipal wastewater treatment plants. Sci. Total Environ. 2005, 336 (1-3), 155-170.
13. 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.
14. Andersen, L.; Holbech, H.; Gessbo, A.; Norrgren, L.; Petersen, G. I. Effects of exposure to 17R-ethinylestradiol during early development on sexual differentiation and induction of vitel-logenin in zebrafish (Danio rerio). Comp. Biochem. Phys. C 2003, 134 (3), 365-374.
15. Santos, E. M.; Paull, G. C.; Van Look, K. J. W.; Workman, V. L.; Holt, W. V.; van Aerle, 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.
16. Grist, E. P. M.; Wells, N. C.; Whitehouse, P.; Brighty, G.; Crane, M. Estimating the effects of 17α-ethinylestradiol on populations of the fathead minnow Pimephales promelas: Are conventional toxicological endpoints adequate? Environ. Sci. Technol. 2003, 37 (8), 1609-1616. (Pubitemid 36438162)
17. Lange, R.; Hutchinson, T. H.; Croudace, C. P.; Siegmund, F. Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fatheadminnow(Pimephales promelas). Environ. Toxicol. Chem. 2001, 20 (6), 1216-1227. (Pubitemid 32861474)
18. Scholz, S.; Gutzeit, H. O. 17α-Ethinylestradiol affects reproduction, sexual differentiation, and aromatase gene expression of the medaka (Oryzias latipes). Aquat. Toxicol. 2000, 50 (4), 363-373.
19. Balch, G.; Mackenzie, C.; Metcalfe, C. Alterations to gonadal development and reproductive success in Japanese Medaka (Oryzias latipes) exposed to 17α-ethinylestradiol. Environ. Toxicol. Chem. 2004, 23 (3), 782-791. (Pubitemid 38250358)
20. Katsu, Y.; Lange, A.; Urushitani, H.; Ichikawa, R.; Paull, 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. (Pubitemid 46713405)
21. 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 Persp. 2004, 112 (17), 1725-1733.
22. 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. Proc. Natl. Acad. Sci. U.S.A. 2007, 104 (21), 8897-8901.
23. Caswell, H. Matrix Population Models, 2nd ed.; Sinauer Associates, Inc.: Sunderland, MA ,2001.
24. Miller, D. H.; Ankley, G. T. Modeling impacts on populations: fathead minnow (Pimephales promelas) exposure to the endocrine disruptor 17β-trenbolone as a case study. Ecotox. Environ. Safe. 2004, 59 (1), 1-9.
25. Gutjahr-Gobell, R. E.; Zaroogian, G. E.; Horowitz, D. J. B.; Gleason, T. R.; Mills, L. J. Individual effects of estrogens on a marine fish, Cunner (Tautogolabrus adspersus), extrapolated to the population level. Ecotox. Environ. Safe. 2006, 63 (2), 244-252.
26. Larsen, M. G.; Hansen, K. B.; Henriksen, P. G.; Baatrup, E. Male zebrafish (Danio rerio) courtship behaviour resists the feminising effects of 17α-ethinyloestradiol: Morphological sexual characteristics do not. Aquat. Toxicol. 2008, 87 (4), 234-244.
27. Coe, T. S.; Hamilton, P. B.; Hodgson, D.; Paull, G. C.; Stevens, J. R.; Sumner, K.; Tyler, C. R. An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish. Environ. Sci. Technol. 2008, 42 (13), 5020-5025.
28. Martinovic, D.; Hogarth, W. T.; Jones, R. E.; Sorensen, P. W. Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows. Environ. Toxicol. Chem. 2007, 26 (2), 271-278.
29. 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. (Pubitemid 44065644)
30. Pyron, M. Female preferences and male-male interactions in zebrafish (Danio rerio). Can. J. Zool. 2003, 81 (1), 122-125. (Pubitemid 36631773)
31. Spence, R.; Smith, C. Male territoriality mediates density and sex ratio effects on oviposition in the zebrafish (Danio rerio). Anim. Behav. 2005, 69, 1317-1323. (Pubitemid 40793439)
32. 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.
33. Xu, H.; Yang, J.; Wang, Y.; Jiang, Q.; Chen, H.; Song, H. Exposure to 17α-ethynylestradiol impairs reproductive functions of both male and female zebrafish (Danio rerio). Aquat. Toxicol. 2008, 88 (1), 1-8.
34. Jobling, S.; Williams, R.; Johnson, A.; Taylor, A.; Gross-Sorokin, M.; Nolan, M.; Tyler, C. R.; Van Aerle, 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 Persp. 2006, 114 (S1), 32-39.
35. Coe, T. S.; Hamilton, P. B.; Griffiths, A. M.; Hodgson, D. J.; Wahab, M. A.; Tyler, C. R. Genetic variation in strains of zebrafish (Danio rerio) and the implications for ecotoxicology studies. Ecotoxicology 2009, 18 (1), 144-150.
36. Santos, E. M.; Workman, V. L.; Paull, 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. Paull, 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, 87 (2), 115-126.
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. (Pubitemid 30122905)
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. Krop, E. J. M.; Matsui, E. C.; Sharrow, S. D.; Stone, M. J.; Gerber, P.; van der Zee, J. S.; Chapman, M. D.; Aalberse, R. C. Recombinant major urinary proteins of the mouse in specific IgE and IgG testing. Int. Arch. Allergy Appl. Immunol. 2007, 144, 296-304.
42. Bruford, M. W.; Hanotte, O.; Brookfield, J. F. Y.; Burke, T. Multilocus and Single-Locus DNA Finger printing. In Molecular Genetic Analysis of Populations: A Practical Approach, 2nd ed.; Hoelzel, A. R., Ed. IRL Press: Oxford, 1998.
43. 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
44. Crawley, M. J. The R Book. John Wiley and Sons, Ltd: Hoboken, NJ, 2007.
45. Ihaka, R.; Gentlemen, R. R. A language for data analysis and graphics. J. Comput. Graph. Stat. 1996, 5 (3), 299-314.
46. Crawley, M. J., Statistics: An Introduction Using R. John Wiley and Sons, Ltd: Hoboken, NJ, 2007.
47. Van den Belt, K.; Verheyen, R.; Witters, H. Effects of 17α-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. (Pubitemid 36677575)
48. Colman, J. R.; Baldwin, D.; Johnson, L. L.; Scholz, N. L. Effects of the synthetic estrogen, 17α-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat. Toxicol. 2009, 91 (4), 346-354.
49. Gurney, W. S. C. Modeling the demographic effects of endocrine disruptors. Environ. Health Persp. 2006, 114 (S1), 122-126.
50. Delaney, M.; Follet, C.; Ryan, N.; Hanney, N.; Lusk-Yablick, J.; Gerlach, G. Social interaction and distribution of female zebrafish (Danio rerio) in a large aquarium. Biol. Bull. 2002, 203 (2), 240-241. (Pubitemid 35255474)
51. Darrow, K. O.; Harris, W. A. Characterization and development of courtship in zebrafish (Danio rerio). Zebrafish 2004, 1 (1), 40-45.