Interactive effects of inbreeding and endocrine disruption on reproduction in a model laboratory fish

Evolutionary Applications

Volumn 6, Issue 2, 2013, Pages 279-289

  Bickley, Lisa K ^a   Brown, Andrew R ^a,b   Hosken, David J ^a   Hamilton, Patrick B ^a   Le Page, Gareth ^a,b   Paull, Gregory C ^a   Owen, Stewart F ^b   Tyler, Charles R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

Author keywords

Ecotoxicology; Fitness; Fungicide; Reproduction; Zebrafish

Indexed keywords

EID: 84874029516     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/j.1752-4571.2012.00288.x     Document Type: Article

References (52)

1. Andreasen, J. K. 1985. Insecticide resistance in mosquitofish of the Lower Rio Grande Valley of Texas - an ecological hazard? Archives of Environmental Contamination and Toxicology 14:573-577.
2. Ankley, G. T., K. M. Jensen, M. D. Kahl, E. A. Makynen, L. S. Blake, K. J. Greene, R. D. Johnson et al. 2007. Ketoconazole in the fathead minnow (Pimephales promelas): reproductive toxicity and biological compensation. Environmental Toxicology and Chemistry 26:1214-1223.
3. Armbruster, P., and D. H. Reed 2005. Inbreeding depression in benign and stressful environments. Heredity 95:235-242.
4. Aulstad, D., and A. Kittelsen 1971. Abnormal body curvatures of rainbow trout (Salmo gairdneri) inbred fry. Journal of the Fisheries Research Board of Canada 28:1918-1920.
5. Bijlsma, R., J. Bundgaard, and W. F. Van Putten 1999. Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology 12:1125-1137.
6. Borg, B. 1994. Androgens in teleost fishes. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 109:219-245.
7. Brown, A. R., D. J. Hosken, F. Balloux, L. K. Bickley, G. LePage, S. F. Owen, M. J. Hetheridge et al. 2009. Genetic variation, inbreeding and chemical exposure - combined effects in wildlife and critical considerations for ecotoxicology. Philosophical Transactions of the Royal Society B 364:3377-3390.
8. Brown, A. R., L. K. Bickley, G. Le Page, D. J. Hosken, G. C. Paull, P. B. Hamilton, S. F. Owen et al. 2011. Are toxicological responses in laboratory (inbred) zebrafish representative of those in outbred (wild) populations? A case study with an endocrine disrupting chemical Environmental Science and Technology 45:4166-4172.
9. Bruford, M. W., O. Hanotte, J. F. Y. Brookfield, and T. Burke 1998. Multilocus and single-locus DNA fingerprinting. In A. R. Hoelzel ed. Molecular genetic analysis of populations: A practical approach, 2nd Edition, pp. 287-336. IRL Press, Oxford.
10. Bryan, G. W., P. E. Gibbs, L. G. Hummerstone, and G. R. Burt 1986. The decline of the gastropod Nucella lapillus around south-west England: evidence for the effect of tributyltin from antifouling paints. Journal of the Marine Biological Association of the United Kingdom 66:611-640.
11. Coe, T. S., P. B. Hamilton, D. Hodgson, G. C. Paull, J. R. Stevens, K. Sumner, and C. R. Tyler 2008. An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish. Environmental Science and Technology 42:5020-5025.
12. Coe, T., P. Hamilton, A. Griffiths, D. Hodgson, M. Wahab, and C. R. Tyler 2009. Genetic variation in strains of zebrafish (Danio rerio) and the implications for ecotoxicology studies. Ecotoxicology 18:144-150.
13. Debeljak, N., M. Fink, and D. Rozman 2003. Many facets of mammalian lanosterol 14[alpha]-demethylase from the evolutionarily conserved cytochrome P450 family CYP51. Archives of Biochemistry and Biophysics 409:159-171.
14. Drayton, J. M., R. N. C. Milner, J. Hunt, and M. D. Jennions 2010. Inbreeding and advertisement calling in the cricket Teleogryllus commodus: laboratory and field experiments. Evolution 64:3069-3083.
15. Falconer, D. S. 1989. Introduction to quantitative genetics. 3rd Edition. Longman, New York.
16. Franklin, I. R., and R. Frankham 1998. How large must populations be to retain evolutionary potential? Animal Conservation 1:69-73.
17. Frommen, J. G. L., D. B. Mazzi, and C. M. Theo 2008. Inbreeding depression affects fertilization success and survival but not breeding coloration in threespine sticklebacks. Behaviour 145:425-441.
18. Fry, D. M. 1995. Reproductive effects in birds exposed to pesticides and industrial chemicals. Environmental Health Perspectives 103(Suppl 7):165-171.
19. Gallardo, J. A., and R. Neira 2005. Environmental dependence of inbreeding depression in cultured Coho salmon (Oncorhynchus kisutch): aggressiveness, dominance and intraspecific competition. Heredity 95:449-456.
20. Harris, C. A., P. B. Hamilton, T. J. Runnalls, V. Vinciotti, A. Henshaw, D. Hodgson, T. S. Coe et al. 2011. The consequences of feminization in breeding groups of wild fish. Environmental Health Perspectives 119:306-311.
21. Höglund, J. 2009. Evolutionary Conservation Genetics. Oxford University Press, Oxford.
22. Hughes, K. A. 1995. The evolutionary genetics of male life-history characters in Drosophila melanogaster. Evolution 49:521-537.
23. Keller, L. F., and D. M. Waller 2002. Inbreeding effects in wild populations. Trends in Ecology and Evolution 17:230-241.
24. Kidd, K. A., P. J. Blanchfield, K. H. Mills, V. P. Palace, R. E. Evans, J. M. Lazorchak, and R. W. Flick 2007. Collapse of a fish population after exposure to a synthetic estrogen. Proceedings of the National Academy of Sciences USA 104:8897-8901.
25. Kincaid, H. L. 1976. Inbreeding in rainbow trout (Salmo gairdneri). Journal of the Fisheries Research Board of Canada 33:2420-2426.
26. Lepesheva, G. L., and M. R. Waterman 2004. CYP51 - the omnipotent P450. Molecular and Cellular Endocrinology 215:165-170.
27. Lupetti, A., R. Danesi, M. Campa, M. D. Tacca, and S. Kelly 2002. Molecular basis of resistance to azole antifungals. Trends in Molecular Medicine 8:76-81.
28. Meagher, S., D. J. Penn, and W. K. Potts 2000. Male-male competition magnifies inbreeding depression in wild house mice. Proceedings of the National Academy of Sciences USA 97:3324-3329.
29. Michalczyk, Å. U., O. Y. Martin, A. L. Millard, B. C. Emerson, and M. J. G. Gage 2010. Inbreeding depresses sperm competitiveness, but not fertilization or mating success in male Tribolium castaneum. Proceedings of the Royal Society B 277:3483-3491.
30. Mrakovčič, M., and L. E. Haley 1979. Inbreeding depression in the zebrafish Brachydanio rerio. Journal of Fish Biology 15:323-327.
31. Nacci, D., L. Coiro, D. Champlin, S. Jayaraman, R. McKinney, T. R. Gleason, W. R. Munns Jr. et al. 1999. Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Marine Biology 134:9-17.
32. National Academy of Sciences (NAS) 2007. Toxicity testing in the 21st century - A vision and a strategy. National Academies Press, Washington, DC.
33. Nowak, C., D. Jost, C. Vogt, M. Oetken, K. Schwenk, and J. Oehlmann 2007. Consequences of inbreeding and reduced genetic variation on tolerance to cadmium stress in the midge Chironomus riparius. Aquatic Toxicology 85:278-284.
34. Okada, K., J. D. Blount, M. D. Sharma, R. R. Snook, and D. J. Hosken 2011. Male attractiveness, fertility and susceptibility to oxidative stress are influenced by inbreeding in Drosophila simulans. Journal of Evolutionary Biology 24:363-371.
35. OSPAR 2005. OSPAR background document on clotrimazole. ISBN 1-904426-38-7 Publication Number: 2005/199. pp36. OSPAR Commission.
36. Paull, G. C., K. J. W. Van Look, E. M. Santos, A. L. Filby, D. M. Gray, J. P. Nash, and C. R. Tyler 2008. Variability in measures of reproductive success in laboratory-kept colonies of zebrafish and implications for studies addressing population-level effects of environmental chemicals. Aquatic Toxicology 87:115-126.
37. Piron, R. D. 1978. Spontaneous skeletal deformities in the zebra danio (Brachydanio rerio) bred for fish toxicity tests. Journal of Fish Biology 13:79-83.
38. Prokop, Z. M., J. E. Les, P. K. Banás, P. Koteja, and J. Radwan 2010. Low inbreeding depression in a sexual trait in the stalkeyed fly Teleopsis dalmanni. Evolutionary Ecology 24:827-837.
39. Roff, D. A. 1997. Evolutionary quantitative genetics. Chapman & Hall, London.
40. Saccheri, I., P. Brakefield, and R. Nichols 1996. Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana. Evolution 50:2000-2013.
41. Scott, A. P., D. S. MacKenzie, and N. E. Stacey 1984. Endocrine changes during natural spawning in the white sucker, Catostomus commersoni: II. Steroid hormones. General and Comparative Endocrinology 56:349-359.
42. Slate, J., L. E. B. Kruuk, T. C. Marshall, J. M. Pemberton, and T. H. Clutton-Brock 2000. Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proceedings of the Royal Society B 267:1657-1662.
43. Stockwell, C. A., A. P. Hendry, and M. T. Kinnison 2003. Contemporary evolution meets conservation biology. Trends in Ecology and Evolution 18:94-101.
44. Tyler, C. R., and R. Goodhead 2010. Impacts of hormone-disrupting chemicals in wildlife. In N. Maclean ed. Silent summer: The state of wildlife in Britain and Ireland, pp. 125-140. Cambridge University Press, Cambridge.
45. Whiteley, A. R., A. Bhat, E. P. Martins, R. L. Mayden, M. Arunachalam, S. Uusi-Heikkilä, A. T. A. Ahmed et al. 2011. Population genomics of wild and laboratory zebrafish (Danio rerio). Molecular Ecology 20:4259-4276.
46. Whitlock, M. C. 1995. Variance-induced peak shifts. Evolution 49:252-259.
47. Williams, L. M., and M. F. Oleksiak 2008. Signatures of selection in natural populations adapted to chronic pollution. BMC Evolutionary Biology 8:282.
48. Wirgin, I., N. K. Roy, M. Loftus, R. C. Chambers, D. G. Franks, and M. E. Hahn 2011. Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson river. Science 331:1322-1325.
49. Woods, P. E., J. D. Paulauskis, L. A. Weigt, M. A. Romano, and S. I. Guttman 1989. Genetic variation in laboratory and field populations of the midge, Chironomus tentans: implications for toxicology. Environmental Toxicology and Chemistry 8:1067-1074.
50. Zajitschek, S. R. K., and R. C. Brooks 2010. Inbreeding depression in male traits and preference for outbred males in Poecilia reticulate. Behavioural Ecology 21:884-891.
51. Zarn, J. A., B. J. Bruschweiler, and J. R. Schlatter 2003. Azole fungicides affect mammalian steroidogenesis by inhibiting sterol 14 alpha-demethylase and aromatase. Environmental Health Perspectives 111:255-261.
52. Zhang, W., Y. Ramamoorthy, T. Kilicarslan, H. Nolte, R. F. Tyndale, and E. M. Sellers 2002. Inhibition of cytochromes P450 by antifungal imidazole derivatives. Drug Metabolism and Disposition 30:314-318.