Differences in sexual development in inbred and outbred zebrafish (Danio rerio) and implications for chemical testing

Aquatic Toxicology

Volumn 112-113, Issue , 2012, Pages 27-38

  Brown, A Ross ^a,b   Bickley, Lisa K ^b   Ryan, Thomas A ^a   Paull, Gregory C ^b   Hamilton, Patrick B ^b   Owen, Stewart F ^a   Sharpe, Alan D ^a   Tyler, Charles R ^b  

^a ASTRAZENECA   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Genetic variation; Inbreeding; Outbreeding; Phenotypic plasticity; Sexual development; Strain differences

Indexed keywords

DNA;

CHEMICAL POLLUTANT; CYPRINID; ECOTOXICOLOGY; GENETIC VARIATION; INBREEDING; PHENOTYPIC PLASTICITY; POLLUTION EXPOSURE; SEX RATIO; SEXUAL REPRODUCTION; TOXICITY TEST; WILD POPULATION;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY SIZE; CELL VIABILITY; CONTROLLED STUDY; ECOTOXICOLOGY; EMBRYO; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; FEMALE; FRY (FISH); GENETIC VARIABILITY; GERM CELL; GONAD DEVELOPMENT; HATCHING; HYBRID; INBREEDING; KARYOTYPE; MALE; NONHUMAN; OUTBREEDING; PHENOTYPIC VARIATION; PHYSICAL TOLERANCE; PRIORITY JOURNAL; REPRODUCTIVE TOXICITY; SEX DIFFERENCE; SEX DIFFERENTIATION; SEX RATIO; SEXUAL DEVELOPMENT; STRAIN DIFFERENCE; SURVIVAL RATE; ZEBRA FISH;

ANIMALS; BODY SIZE; BREEDING; FEMALE; GENETIC VARIATION; GONADS; INBREEDING; MALE; SEXUAL DEVELOPMENT; SPECIES SPECIFICITY; TIME FACTORS; TOXICITY TESTS; ZEBRAFISH;

ANIMALIA; DANIO RERIO;

EID: 84857131898     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2012.01.017     Document Type: Article

References (67)

1. Amos W., Wilmer J., Fullard K., Burg T.M., Croxall J.P., Bloch D., Coulson T. The influence of parental relatedness on reproductive success. Proc. R. Soc. Lond. B 2001, 268:2021-2027.
2. Anderson A.D., Weir B.S. A maximum-likelihood method for the estimation of pairwise relatedness in structured populations. Genetics 2007, 176:421-440.
3. Aparicio J.M., Ortego J., Cordero P.J. What should we weigh to estimate heterozygosity, alleles or loci?. Mol. Ecol. 2006, 15:4659-4665.
4. Armbruster P., Reed D.H. Inbreeding depression in benign and stressful environments. Heredity 2005, 95:235-242.
5. Baroiller J.F., D'Cotta H., Saillant E. Environmental effects on fish sex determination and differentiation. Sex. Dev. 2009, 3:118-135.
6. Bradley K.M., Breyer J.P., Melville D.B., Broman K.W., Knapik E.W., Smith J.R. An SNP-based linkage map for zebrafish reveals sex determination. Genes Genomes Genet. 2011, 1:3-11.
7. Bradshaw A.D. Evolutionary significance of phenotypic plasticity in plants. Adv. Genet. 1965, 13:115-155.
8. Brown A.R., Hosken D.J., Balloux F., Bickley L.K., LePage G., Owen S.F., Hetheridge M.J., Tyler C.R. Genetic variation, inbreeding and chemical exposure - combined effects in wildlife and critical considerations for ecotoxicology. Philos. Trans. R. Soc. B 2009, 364:3377-3390.
9. Brown A.R., Bickley L.K., LePage G., Hosken D.J., Paull G.C., Hamilton P.B., Owen S.F., Robinson J., Sharpe A.D., Tyler C.R. Are inbred laboratory zebrafish representative of outbred (wild) populations? - an ecotoxicology case study on an endocrine disrupting chemical. Environ. Sci. Technol. 2011, 45:4166-4172.
10. Brook B.W., Tonkyn D.W., O'Grady J.J., Frankham R. Contribution of inbreeding to extinction risk in threatened species. Conserv. Ecol. 2002, 6. art 16.
11. Bruford M.W., Hanotte O., Brookfield J.F.Y., Burke T. Multi-locus and single-locus DNA fingerprinting. Molecular Genetic Analysis of Populations: A Practical Approach 1998, IRL Press, Oxford. 2nd ed. A.R. Hoelzel (Ed.).
12. Charlesworth D., Willis J.H. The genetics of inbreeding depression. Nat. Rev. Genet. 2009, 10:783-796.
13. Charnov E.L., Bull J.J. When is sex environmentally determined?. Nature 1987, 266:829-830.
14. Chevalet C., Gillois M. Inbreeding depression and heterosis: expected means and variances among inbred lines and their crosses. Ann. Genet. Sel. Anim. 1978, 10:78-98.
15. 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, 42:5020-5025.
16. 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, 18:144-150.
17. Conover D.O., Kynard B.E. Environmental sex determination: interaction of temperature and genotype in a fish. Science 1981, 213:577-579.
18. Conover D.O., Heins S.W. Adaptive variation in environmental and genetic sex determination in a fish. Nature 1987, 326:496-498.
19. Crnokrak P., Roff D.A. Inbreeding depression in the wild. Heredity 1999, 83:260-270.
20. Delvin R.H., Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological and environmental influences. Aquaculture 2002, 208:191-364.
21. El Mousadik A., Petit R.J. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor. Appl. Genet. 1996, 92:832-839.
22. Evenden A.J., Depledge M.H. Genetic susceptibility in ecosystems: the challenge for ecotoxicology. Environ. Health Perspect. 1997, 105:849-854.
23. Falconer D.S., Mackay T.F.C. Introduction to Quantitative Genetics 1996, Longman, Harlow, UK. 4th ed.
24. Forbes V.E., Depledge M.H. Predicting population responses to pollutants: the significance of sex. Funct. Ecol. 1992, 6:376-381.
25. Godwin J., Luckenbach J.A., Borski R.J. Ecology meets endocrinology: environmental sex determination in fish. Evol. Dev. 2003, 5:40-49.
26. Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from , accessed 6/3/2011. http://www.unil.ch/izea/softwares/fstat.html.
27. Hoffman A.A., Parsons P.A. Evolutionary Genetics and Environmental Stress 1991, Oxford University Press, New York, USA.
28. Holbech H., Kinnberg K., Petersen G.I., Jackson P., Hylland K., Norrgren L., Bjerregaard P. Detection of endocrine disrupters: evaluation of a fish sexual development test (FSDT). Comp. Biochem. Physiol. C 2006, 144:57-66.
29. Lande R., Shannon S. The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 1996, 50:434-437.
30. Lawrence C., Ebersole J.P., Kesseli R.V. Rapid growth and out-crossing promote female development in zebrafish (Danio rerio). Environ. Biol. Fishes 2008, 81:239-246.
31. Lynch M. The genetic interpretation of inbreeding and outbreeding depression. Evolution 1991, 45:622-629.
32. Lynch M., Ritland K. Estimation of pairwise relatedness with molecular markers. Genetics 1999, 152:1753-1766.
33. Maack G., Segner H. Morphological development of the gonads in zebrafish. J. Fish Biol. 2003, 62:895-906.
34. Maack G., Segner H., Tyler C.R. Ontogeny of sexual differentiation in different strains of zebrafish (Danio rerio). Fish Physiol. Biochem. 2003, 28:125-128.
35. McCune A.R., Houle D., McMillan K., Annable R., Kondrashov A.S. Two classes of deleterious recessive alleles in a natural population of zebrafish, Danio rerio. Proc. R. Soc. Lond. B 2004, 271:2025-2033.
36. McClelland E.K., Naish K.A. What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conserv. Genet. 2007, 8:397-416.
37. Monson C.A., Sadler K.C. Inbreeding depression and outbreeding depression are evident in wild-type zebrafish lines. Zebrafish 2010, 7:189-197.
38. Mrakovcic M., Haley L.E. Inbreeding depression in the zebrafish Brachydanio rerio (Hamilton Buchanan). J. Fish Biol. 1979, 15:323-327.
39. NAS National Academy of Sciences Toxicity Testing in the 21st Century - A Vision and a Strategy 2007, National Academies Press, Washington, DC, http://www.nap.edu/catalog.phprecord_id=11970, accessed 6/3/2011.
40. Nei M. F-statistics and analysis of gene diversity in subdivided populations. Annal. Hum. Genet. Lond. 1977, 41:225-233.
41. Nowak C., Vogt C., Diogo J.B., Schwenk K. Genetic impoverishment in laboratory cultures of the test organism Chironomous riparius. Environ. Toxicol. Chem. 2007, 26:1018-1022.
42. OECD, 2011. OECD Guideline for Testing of Chemicals, Guideline 234: Fish, Sexual Development Test. Paris, France, adopted 28 July 2011.
43. Ospina-Alvarez N., Piferrer F. Temperature-dependent sex determination in fish revisted: prevalence, a single sex ratio response, pattern, and possible effects of climate change. PLoS ONE 2008, 3:e2837. (available online).
44. Park, S.D.E., 2001. Trypanotolerance in West African cattle and the population genetic effects of selection. Ph.D. Thesis. University of Dublin.
45. Parker G.A. The evolution of sexual size dimorphism in fish. J. Fish Biol. 1992, 41:1-20.
46. Paull G.C., Lange A., Henshaw A.C., Tyler C.R. Ontogeny of sexual development in the roach (Rutilus rutilus) and its interrelationships with growth and age. J. Morphol. 2008, 269:884-895.
47. Pigliucci M., Schlichting C.D., Jones C.S., Schwenk K. Developmental reaction norms: the interactions among allometry, ontogeny and plasticity. Plant Sp. Biol. 1996, 11:69-85.
48. Piron R.D. Spontaneous skeletal deformities in the Zebra Danio (Brachydanio rerio) bred for fish toxicity tests. J. Fish Biol. 1978, 13:79-83.
49. Rauch G.-J., Granato M., Haffter P. A polymorphic zebrafish line for genetic mapping using SSLPs on high-percentage agarose gels. Tech. Tips Online 1997, 2:148-150.
50. Reed D.H., Frankham R. Correlation between fitness and genetic diversity. Conserv. Biol. 2003, 17:230-237.
51. Reed D.H., Lowe E.H., Briscoe D.A., Frankham R. Fitness and adaptation in a novel environment: effect of inbreeding, prior environment, and lineage. Evolution 2003, 57:1822-1828.
52. Ritland K. Estimators for pairwise relatedness and inbreeding coefficients. Genet. Res. 1996, 67:175-186.
53. Rousset F. Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour. 2008, 8:103-106.
54. Shang E.H.H., Yu R.M.K., Wu R.S.S. Hypoxia affects sex differentiation and development, leading to a male-dominated population in zebrafish (Danio rerio). Environ. Sci. Technol. 2006, 40:3118-3122.
55. Slate J., David P., Dodds K.G., Veenvliet B.A., Glass B.C., Broad T.E., McEwan J.C. Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 2004, 93:255-265.
56. Smith-Gill S.J. Developmental plasticity: developmental conversion versus phenotypic modulation. Am. Zool. 1983, 23:47-55.
57. Snorrason S.S., Skúlason S. Adaptive speciation in northern freshwater fishes. Adaptive Speciation 2004, 210-228. Cambridge University Press, Cambridge. U. Dieckmann, M. Doebeli, J.A.J. Metz, D. Tautz (Eds.).
58. Spence R., Gerlach G., Lawrence C., Smith C. The behaviour and ecology of the zebrafish. Biol. Rev. 2008, 83:13-34.
59. Swindell W.R., Bouzat J.L. Selection and inbreeding depression: effects of inbreeding rate and inbreeding environment. Evolution 2006, 60:1014-1022.
60. Szulkin M., Bierne N., David P. Heterozygosity-fitness correlations: a time for reappraisal. Evolution 2010, 64:1202-1217.
61. Templeton A.R. Coadaptation and outbreeding depression. Conservation Biology: The Science of Scarcity and Diversity 1986, 105-116. Sinauer Associates Inc., Sunderland. M.E. Soule (Ed.).
62. Uchida D., Yamashita M., Kitano T., Iguchi T. An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp. Biochem. Physiol. Part A: Mol. Integr. Physiol. 2004, 137:11-20.
63. von Hofsten J., Olsson P.-E. Zebrafish sex determination and differentiation: Involvement of FTZ-F1 genes. Repro. Biol. Endocrinol. 2005, 3:63. (available on line http://www.rbej.com/content/3/1/63).
64. Wang J. Triadic IBD coefficients and applications to estimate pairwise relatedness. Genet. Res. 2007, 89:135-153.
65. Wang J. COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol. Ecol. Resour. 2010, 11:141-145.
66. Weir B.S., Cockerham C.C. Estimating F-statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
67. Whiteley A.R., Bhat A., Martine E.P., Mayden R.L., Arunahalam M., Uusi-Heikkila S., Ahmed A.T.A., Shrestha J., Clark M., Stemple D., Bernatchez L. Population genomics of wild and laboratory zebrafish (Danio rerio). Mol. Ecol. 2011, 20:4259-4276.