Population bottlenecks, genetic diversity and breeding ability of the three-spined stickleback (Gasterosteus aculeatus) from three polluted English Rivers

Aquatic Toxicology

Volumn 142-143, Issue , 2013, Pages 264-271

  Santos, Eduarda M ^a   Hamilton, Patrick B ^a   Coe, Tobias S ^a   Ball, Jonathan S ^a   Cook, Alastair C ^b   Katsiadaki, Ioanna ^b   Tyler, Charles R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b CENTRE FOR ENVIRONMENT   (United Kingdom)

Author keywords

Fish populations; Mesocosm; Polluted rivers; Reproductive competitiveness

Indexed keywords

COMPETITION (ECOLOGY); FISH; FITNESS; GENETIC STRUCTURE; MESOCOSM; POLLUTION EFFECT; POLLUTION EXPOSURE; POPULATION DYNAMICS; POPULATION GENETICS; REPRODUCTIVE STATUS; RIVER POLLUTION;

ARTICLE; BOTTLENECK POPULATION; BREEDING; COMPETITIVE ABILITY; CONTAMINATED FISH; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEMALE; GASTEROSTEUS ACULEATUS; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; MALE; MICROSATELLITE MARKER; NONHUMAN; POPULATION GENETIC STRUCTURE; PRIORITY JOURNAL; REPRODUCTIVE FITNESS; REPRODUCTIVE HISTORY; RIVER ECOSYSTEM; WATER POLLUTION; WATER QUALITY;

AIRE RIVER; ENGLAND; TEES RIVER; UNITED KINGDOM;

FISH POPULATIONS; MESOCOSM; POLLUTED RIVERS; REPRODUCTIVE COMPETITIVENESS;

ANIMALS; BREEDING; ENGLAND; FEMALE; GENETIC VARIATION; MALE; POPULATION DYNAMICS; REPRODUCTION; RIVERS; SMEGMAMORPHA; WATER POLLUTANTS, CHEMICAL;

EID: 84884364450     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.08.008     Document Type: Article

References (61)

1. Allchin C.R., Law R.J., Morris S. Polybrominated diphenylethers in sediments and biota downstream of potential sources in the UK. Environ. Pollut. 1999, 105:197-207.
2. Antao T., Lopes A., Lopes R.J., Beja-Pereira A., Luikart G. LOSITAN: a workbench to detect molecular adaptation based on a F(st)-outlier method. BMC Bioinformatics 2008, 9:323.
3. Arkoosh M.R., Casillas E., Huffman P., Clemons E., Evered J., Stein J.E., Varanasi U. Increased susceptibility of juvenile chinook salmon from a contaminated estuary to Vibrio anguillarum. Trans. Am. Fish. Soc. 1998, 127:360-374.
4. Belfiore N.M., Anderson S.L. Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat. Res.-Rev. Mutat. Res. 2001, 489:97-122.
5. Blackburn M.A., Kirby S.J., Waldock M.J. Concentrations of alkyphenol polyethoxylates entering UK estuaries. Mar. Pollut. Bull. 1999, 38:109-118.
6. Blackburn M.A., Waldock M.J. Concentrations of alkylphenols in rivers and estuaries in England and Wales. Water Res. 1995, 29:1623-1629.
7. Brown A.R., Bickley L.K., Le Page G., Hosken D.J., Paull G.C., Hamilton P.B., Owen S.F., Robinson J., Sharpe A.D., Tyler C.R. Are toxicological responses in laboratory (inbred) zebrafish representative of those in outbred (wild) populations? - A case study with an endocrine disrupting chemical. Environ. Sci. Technol. 2011, 45:4166-4172.
8. Brown A.R., Hosken D.J., Balloux F.o., 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. Phil. Trans. Roy. Soc. B 2009, 364:3377-3390.
9. Bruford M.W., Hanotte O., Brookfield J.F.Y., Burke T. Multilocus and single-locus DNA fingerprinting. Molecular Genetic Analysis of Populations: A Practical Approach 1998, 287-336. IRL Press, Oxford.
10. Carriere Y., Deland J.P., Roff D.A., Vincent C. Life-history costs associated with the evolution of insecticide resistance. Proc. Roy. Soc. B: Biol. Sci. 1994, 258:35-40.
11. Coors A., Vanoverbeke J., De Bie T., De Meester L. Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquat. Toxicol. 2009, 95:71-79.
12. Cornuet J.M., Luikart G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 1996, 144:2001-2014.
13. Cowx I.G., Portocarrero-Aya M. Paradigm shifts in fish conservation: moving to the ecosystem services concept. J. Fish Biol. 2011, 79:1663-1680.
14. Dominguez-Dominguez O., Boto L., Alda F., De Leon G.P.P. Human impacts on drainages of the Mesa Central, Mexico, and its genetic effects on an endangered fish, Zoogoneticus quitzeoensis. Conserv. Biol. 2007, 21:168-180.
15. Durrant C.J., Stevens J.R., Hogstrand C., Bury N.R. The effect of metal pollution on the population genetic structure of brown trout (Salmo trutta L.) residing in the River Hayle, Cornwall, UK. Environ. Pollut. 2011, 159:3595.
16. Gardestrom J., Dahl U., Kotsalainen O., Maxson A., Elfwing T., Grahn M., Bengtsson B.-E., Breitholtz M. Evidence of population genetic effects of long-term exposure to contaminated sediments - a multi-endpoint study with copepods. Aquat. Toxicol. 2008, 86:426-436.
17. Goudet J. FSTAT (Version 1.2): a computer program to calculate F-statistics. J. Hered. 1995, 86:485-486.
18. Goudet, J., 2001. FSTAT, a program to estimate and test gene diversities and fixation indices. http://www2.unil.ch/popgen/softwares/fstat.htm.
19. Hamlin H.J., Guillette L.J. Birth defects in wildlife: the role of environmental contaminants as inducers of reproductive and developmental dysfunction. Syst. Biol. Reprod. Med. 2011, 56:113-121.
20. Harries J.E., Sheahan D.A., Jobling S., Matthiessen P., Neall M., Sumpter J.P., Taylor T., Zaman N. Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout. Environ. Toxicol. Chem. 1997, 16:534-542.
21. Harris C.A., Hamilton P.B., Runnalls T.J., Vinciotti V., Henshaw A., Hodgson D., Coe T.S., Jobling S., Tyler C.R., Sumpter J.P. The consequences of feminization in breeding groups of wild fish. Environ. Health Perspect. 2011, 119:306-311.
22. Heckel G., Zbinden M., Mazzi D., Kohler A., Reckeweg G., Bakker T.C.M., Largiader C.R. Microsatellite markers for the three-spined stickleback (Gasterosteus aculeatus L.) and their applicability in a freshwater and an anadromous population. Conserv. Genet. 2002, 3:79-81.
23. Hudson-Edwards K., Macklin M., Taylor M. Historic metal mining inputs to Tees river sediment. Sci. Total Environ. 1997, 194:437-445.
24. Jensen L.F., Hansen M.M., Carlsson J., Loeschcke V., Mensberg K.L.D. Spatial and temporal genetic differentiation and effective population size of brown trout (Salmo trutta, L.) in small Danish rivers. Conserv. Genet. 2005, 6:615-621.
25. 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, 67:515-524.
26. Jobling S., Nolan M., Tyler C.R., Brighty G., Sumpter J.P. Widespread sexual disruption in wild fish. Environ. Sci. Technol. 1998, 32:2498-2506.
27. Largiader C.R., Fries V., Kobler B., Bakker T.C.M. Isolation and characterization of microsatellite loci from the three-spined stickleback (Gasterosteus aculeatus L.). Mol. Ecol. 1999, 8:342-344.
28. Lind E.E., Grahn M. Directional genetic selection by pulp mill effluent on multiple natural populations of three-spined stickleback (Gasterosteus aculeatus). Ecotoxicology 2011, 20:503-512.
29. Luikart G., Allendorf F.W., Cornuet J.M., Sherwin W.B. Distortion of allele frequency distributions provides a test for recent population bottlenecks. J. Hered. 1998, 89:238-247.
30. Lye C.M., Frid C.L.J., Gill M.E., Cooper D.W., Jones D.M. Estrogenic alkylphenols in fish tissues, sediments, and waters from the UK Tyne and Tees estuaries. Environ. Sci. Technol. 1999, 33:1009-1014.
31. Maes G.E., Raeymaekers J.A.M., Pampoulie C., Seynaeve A., Goemans G., Belpaire C., Volckaert F.A.M. The catadromous European eel Anguilla anguilla (L.) as a model for freshwater evolutionary ecotoxicology: relationship between heavy metal bioaccumulation, condition and genetic variability. Aquat. Toxicol. 2005, 73:99-114.
32. Makinen H.S., Cano J.M., Merila J. Genetic relationships among marine and freshwater populations of the European three-spined stickleback (Gasterosteus aculeatus) revealed by microsatellites. Mol. Ecol. 2006, 15:1519-1534.
33. Makinen H.S., Cano M., Merila J. Identifying footprints of directional and balancing selection in marine and freshwater three-spined stickleback (Gasterosteus aculeatus) populations. Mol. Ecol. 2008, 17:3565-3582.
34. McMillan A.M., Bagley M.J., Jackson S.A., Nacci D.E. Genetic diversity and structure of an estuarine fish (Fundulus heteroclitus) indigenous to sites associated with a highly contaminated urban harbor. Ecotoxicology 2006, 15:539-548.
35. Meyer J.N., Di Giuliuo R.T. Heritable adaptation and fitness costs in killifish (Fundulus heteroclitus) inhabiting a polluted estuary. Ecol. Appl. 2003, 13:490-503.
36. Milinski M. The function of mate choice in sticklebacks: optimizing MHC genetics. J. Fish Biol. 2003, 63:1-16.
37. Murdoch M.H., Hebert P.D.N. Mitochondrial-DNA diversity of brown bullhead from contaminated and relatively pristine sites in the Great Lakes. Environ. Toxicol. Chem. 1994, 13:1281-1289.
38. Nunn A.D., Harvey J.P., Britton J.R., Frear P.A., Cowx I.G. Fish, climate and the Gulf Stream: the influence of abiotic factors on the recruitment success of cyprinid fishes in lowland rivers. Freshwater Biol. 2007, 52:1576-1586.
39. Oaks J.L., Gilbert M., Virani M.Z., Watson R.T., Meteyer C.U., Rideout B.A., Shivaprasad H.L., Ahmed S., Chaudhry M.J.I., Arshad M., Mahmood S., Ali A., Khan A.A. Diclofenac residues as the cause of vulture population decline in Pakistan. Nature 2004, 427:630-633.
40. Piry S., Luikart G., Cornuet J.M. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J. Hered. 1999, 90:502-503.
41. Postma J.F., Davids C. Tolerance induction and life-cycle changes in cadmium-exposed Chironomus riparius (Diptera) during consecutive generations. Ecotoxicol. Environ. Saf. 1995, 30:195-202.
42. Raymond M., Rousset F. Genepop (Version-1.2) - population-genetics software for exact tests and ecumenicism. J. Hered. 1995, 86:248-249.
43. Rice W.R. Analyzing tables of statistical tests. Evolution 1989, 43:223-225.
44. Roark S., Brown K. Effects of metal contamination from mine tailings on allozyme distributions of populations of great plains fishes. Environ. Toxicol. Chem. 1996, 15:921-927.
45. Roark S.A., Nacci D., Coiro L., Champlin D., Guttman S.I. Population genetic structure of a nonmigratory estuarine fish (Fundulus heteroclitus) across a strong gradient of polychlorinated biphenyl contamination. Environ. Toxicol. Chem. 2005, 24:717-725.
46. Rousset F. GENEPOP'007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol. Ecol. Resour. 2008, 8:103-106.
47. Sheahan D.A., Brighty G.C., Daniel M., Jobling S., Harries J.E., Hurst M.R., Kennedy J., Kirby S.J., Morris S., Routledge E.J., Sumpter J.P., Waldock M.J. Reduction in the estrogenic activity of a treated sewage effluent discharge to an English river as a result of a decrease in the concentration of industrially derived surfactants. Environ. Toxicol. Chem. 2002, 21:515-519.
48. Shikano T., Shimada Y., Herczeg G., Merila J. History vs. habitat type: explaining the genetic structure of European nine-spined stickleback (Pungitius pungitius) populations. Mol. Ecol. 2010, 19:1147-1161.
49. Shirley M.D.F., Sibly R.M. Genetic basis of a between-environment trade-off involving resistance to cadmium in Drosophila melanogaster. Evolution 1999, 53:826-836.
50. Tatara C.P., Mulvey M., Newman M.C. Genetic and demographic responses of mosquitofish (Gambusia holbrooki) populations exposed to mercury for multiple generations. Environ. Toxicol. Chem. 1999, 18:2840-2845.
51. van Aerle R., Nolan M., Jobling S., Christiansen L.B., Sumpter J.P., Tyler C.R. Sexual disruption in a second species of wild cyprinid fish (the gudgeon, Gobio gobio) in United Kingdom freshwaters. Environ. Toxicol. Chem. 2001, 20:2841-2847.
52. Van Oosterhout C., Hutchinson W.F., Wills D.P.M., Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 2004, 4:535-538.
53. van Straalen N.M., Timmermans M. Genetic variation in toxicant-stressed populations: an evaluation of the "genetic erosion" hypothesis. Hum Ecol. Risk Assess. 2002, 8:983-1002.
54. Whitehead A., Anderson S.L., Kuivila K.M., Roach J.L., May B. Genetic variation among interconnected populations of Catostomus occidentalis: implications for distinguishing impacts of contaminants from biogeographical structuring. Mol. Ecol. 2003, 12:2817-2833.
55. Williams A., Milner N., O'Keeffe N., Clarke A., Webb H. Environment Agency: River Tees Salmon Action Plan Review 2009.
56. Williams L.M., Oleksiak M.F. Signatures of selection in natural populations adapted to chronic pollution. BMC Evol. Biol. 2008, 8:282.
57. Williams L.M., Oleksiak M.F. Ecologically and evolutionarily important SNPs identified in natural populations. Mol. Biol. Evol. 2011, 28:1817-1826.
58. Williams R.J., Keller V.D.J., Johnson A.C., Young A.R., Holmes M.G.R., Wells C., Gross-Sorokin M., Benstead R. A national risk assessment for intersex in fish arising from steroid estrogens. Environ. Toxicol. Chem. 2009, 28:220-230.
59. Wirgin I., Roy N.K., Loftus M., Chambers R.C., Franks D.G., Hahn M.E. Mechanistic basis of resistance to PCBs in Atlantic tomcod from the Hudson River. Science 2011, 331:1322-1325.
60. Wirgin I., Waldman J.R. Resistance to contaminants in North American fish populations. Mutat. Res.-Fund. Mol. Mutagen. 2004, 552:73-100.
61. Wootton R.J. The Biology of Sticklebacks 1976, Academic Press, London and New York.