Evolutionary ecotoxicology of perfluoralkyl substances (PFASs) inferred from multigenerational exposure: A case study with Chironomus riparius (Diptera, Chironomidae)

Aquatic Toxicology

Volumn 156, Issue , 2014, Pages 41-51

  Stefani, F ^a   Rusconi, M ^a   Valsecchi, S ^a   Marziali, L ^a  

^a Water Research Institute National Research Council IRSA CNR   (Italy)

Author keywords

Chironomus riparius; Evolutionary toxicology; Microsatellites; Multigenerational test; PFASs

Indexed keywords

PERFLUBUTANE; PERFLUOROOCTANESULFONIC ACID; PERFLUOROOCTANOIC ACID; PERFLUOROBUTANE SULFONATE; SULFONIC ACID DERIVATIVE; UNCLASSIFIED DRUG; ALKANESULFONIC ACID; FLUOROCARBON; MICROSATELLITE DNA; OCTANOIC ACID DERIVATIVE; WATER POLLUTANT;

BAYESIAN ANALYSIS; CHEMICAL POLLUTANT; ECOTOXICOLOGY; FLY; GENETIC VARIATION; LARVA; LIFE HISTORY TRAIT; MUTAGENICITY; MUTATION; NUMERICAL MODEL; POPULATION DYNAMICS; POPULATION SIZE; SURFACTANT; EVOLUTIONARY BIOLOGY; TOXICITY;

ARTICLE; CHIRONOMUS RIPARIUS; CONTROLLED STUDY; DNA EXTRACTION; ECOTOXICOLOGY; EVOLUTIONARY HOMOLOGY; GENE FREQUENCY; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC PARAMETERS; GENETIC VARIABILITY; HETEROZYGOSITY; LARVA; MICROSATELLITE MARKER; MUTAGENICITY; MUTATION RATE; NONHUMAN; POPULATION GENETICS; PRIORITY JOURNAL; RISK ASSESSMENT; SEX RATIO; TOXICITY TESTING; BAYES THEOREM; CONCENTRATION (PARAMETERS); EVOLUTION; EVOLUTIONARY ECOTOXICOLOGY; EXPOSURE; GENE LOCUS; LIFE HISTORY; POPULATION SIZE; REPRODUCTION; SURVIVAL; ANIMAL; CHIRONOMIDAE; DRUG EFFECTS; GENETICS; LIFE CYCLE STAGE; TOXICITY; WATER POLLUTANT;

CHIRONOMIDAE; CHIRONOMUS RIPARIUS; DIPTERA;

ALKANESULFONIC ACIDS; ANIMALS; BIOLOGICAL EVOLUTION; CAPRYLATES; CHIRONOMIDAE; ECOTOXICOLOGY; FLUOROCARBONS; LARVA; LIFE CYCLE STAGES; MICROSATELLITE REPEATS; REPRODUCTION; SEX RATIO; TOXICITY TESTS; WATER POLLUTANTS, CHEMICAL;

EID: 84906337645     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2014.07.020     Document Type: Article

References (70)

1. Ankley G.T., Bennett R.S., Erickson R.J., Hoff D.J., Hornung M.W., Johnson R.D., Mount D.R., Nichols J.W., Russom C.L., Schmieder P.K., Serrrano J.A., Tietge J.E., Villeneuve D.L. Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ. Toxicol. Chem. 2010, 29:730-741. 10.1002/etc.34.
2. Athrey N.R.G., Leberg P.L., Klerks P.L. Laboratory culturing and selection for increased resistance to cadmium reduce genetic variation in the least killifish Heterandria formosa. Environ. Toxicol. Chem. 2007, 26:1916-1921. 10.1897/06-589r.1.
3. Avila V., Chavarrias D., Sanchez E., Manrique A., Lopez-Fanjul C., Garcia-Dorado A. Increase of the spontaneous mutation rate in a long-term experiment with Drosophila melanogaster. Genetics 2006, 173:267-277. 10.1534/genetics.106.056200.
4. Baer C.F. Does mutation rate depend on itself?. PLoS Biol. 2008, 6:233-235. 10.1371/journal.pbio.0060052.
5. Beaumont M.A., Zhang W.Y., Balding D.J. Approximate Bayesian computation in population genetics. Genetics 2002, 162:2025-2035.
6. Ben-Shlomo R., Shanas U. Genetic ecotoxicology of asbestos pollution in the house mouse Mus musculus domesticus. Environ. Sci. Pollut. Res. 2011, 18:1264-1269. 10.1007/s11356-011-0481-9.
7. Bertorelle G., Benazzo A., Mona S. ABC as a flexible framework to estimate demography over space and time: some cons, many pros. Mol. Ecol. 2010, 19:2609-2625. 10.1111/j.1365-294X. 2010.04690.x.
8. Bickham J.W. The four cornerstones of evolutionary toxicology. Ecotoxicology 2011, 20:497-502. 10.1007/s10646-011-0636-y.
9. Bickham J.W., Sandhu S., Hebert P.D.N., Chikhi L., Athwal R. Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat. Res.: Rev. Mutat. Res. 2000, 463:33-51. 10.1016/s1383-5742(00)00004-1.
10. Bickham J.W., Smolen M.J. Somatic and heritable effects of environmental genotoxins and the emergence of evolutionary toxicology. Environ. Health Perspect. 1994, 102:25-28.
11. Bourret V., Couture P., Campbell P.G.C., Bernatchez L. Evolutionary ecotoxicology of wild yellow perch (Perca flavescens) populations chronically exposed to a polymetallic gradient. Aquat. Toxicol. 2008, 86:76-90. 10.1016/j.aquatox.2007.10.003.
12. Cornuet J.-M., Pudlo P., Veyssier J., Dehne-Garcia A., Gautier M., Leblois R., Marin J.-M., Estoup A. DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism DNA sequence and microsatellite data. Bioinformatics 2014, 30:1187-1189.
13. Coutellec M.A., Barata C. An introduction to evolutionary processes in ecotoxicology. Ecotoxicology 2011, 20:493-496. 10.1007/s10646-011-0637-x.
14. de Arruda M.P., Goncalves E.C., Schneider M.P.C., da Silva A.L.D., Morielle-Versute E. An alternative genotyping method using dye-labeled universal primer to reduce unspecific amplifications. Mol. Biol. Rep. 2010, 37:2031-2036. 10.1007/s11033-009-9655-7.
15. de Voogt P. Perfluorinated alkylated substances. Reviews of Environmental Contamination and Toxicology 2010, Springer, New York.
16. Dearfield K.L., Cimino M.C., McCarroll N.E., Mauer I., Valcovic L.R. Genotoxicity risk assessment: a proposed classification strategy. Mutat. Res. 2002, 521:121-135. 10.1016/s1383-5718(02)00236-x.
17. Ding G.H., Peijnenburg W. Physicochemical properties and aquatic toxicity of poly- and perfluorinated compounds. Crit. Rev. Environ. Sci. Technol. 2013, 43:598-678. 10.1080/10643389.2011.627016.
18. Excoffier L., Lischer H.E.L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 2010, 10::564-567. 10.1111/j.1755-0998.2010.02847.x.
19. Giesy J.P., Kannan K. Global distribution of perfluorooctane sulfonate in wildlife. Environ. Sci. Technol. 2001, 35:1339-1342. 10.1021/es001834k.
20. Guillemaud T., Beaumont M.A., Ciosi M., Cornuet J.M., Estoup A. Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data. Heredity 2010, 104:88-99. 10.1038/hdy.2009.92.
21. Guo S.W., Thompson E.A. Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 1992, 48:361-372. 10.2307/2532296.
22. Hey J., Nielsen R. Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:2785-2790. 10.1073/pnas.0611164104.
23. Hoff P.T., Van Dongen W., Esmans E.L., Blust R., De Coen W.M. Evaluation of the toxicological effects of perfluorooctane sulfonic acid in the common carp (Cyprinus carpio). Aquat. Toxicol. 2003, 62:349-359. 10.1016/s0166-445x(02)00145-5.
24. Hoffmann A.A., Willi Y. Detecting genetic responses to environmental change. Nat. Rev. Genet. 2008, 9:421-432. 10.1038/nrg2339.
25. Hoke R.A., Bouchelle L.D., Ferrell B.D., Buck R.C. Comparative acute freshwater hazard assessment and preliminary PNEC development for eight fluorinated acids. Chemosphere 2012, 87:725-733. 10.1016/j.chemosphere.2011.12.066.
26. Hyne R.V., Maher W.A. Invertebrate biomarkers: links to toxicosis that predict population decline. Ecotoxicol. Environ. Saf. 2003, 54:366-374. 10.1016/s0147-6513(02)00119-7.
27. Ji K., Kim Y., Oh S., Ahn B., Jo H., Choi K. Toxicity of perfluorooctane sulfonic acid and perfluorooctanoic acid on freshwater macroinvertebrates (Daphnia magna and Moina macrocopa) and fish (Oryzias latipes). Environ. Toxicol. Chem. 2008, 27:2159-2168. 10.1897/07-523.1.
28. Kannan K. Perfluoroalkyl and polyfluoroalkyl substances: current and future perspectives. Environ. Chem. 2011, 8:333-338. 10.1071/en11053.
29. Kannan K., Corsolini S., Falandysz J., Fillmann G., Kumar K.S., Loganathan B.G., Mohd M.A., Olivero J., Van Wouwe N., Yang J.H., Aldous K.M. Perfluorooctanesulfonate and related fluorochemicals in human blood from several countries. Environ. Sci. Technol. 2004, 38:4489-4495. 10.1021/es0493446.
30. Kawamoto K., Oashi T., Oami K., Liu W., Jin Y.H., Saito N., Sato I., Tsuda S. Perfluorooctanoic acid (PFOA) but not perfluorooctane sulfonate (PFOS) showed DNA damage in comet assay on Paramecium caudatum. J. Toxicol. Sci. 2010, 35:835-841. 10.2131/jts.35.835.
31. Kuchma O., Vornam B., Finkeldey R. Mutation rates in Scots pine (Pinus sylvestris L.) from the Chernobyl exclusion zone evaluated with amplified fragment-length polymorphisms (AFLPs) and microsatellite markers. Mutat. Res. 2011, 725:29-35. http://dx.doi.org/10.1016/j.mrgentox.2011.07.003.
32. Lau C., Anitole K., Hodes C., Lai D., Pfahles-Hutchens A., Seed J. Perfluoroalkyl acids: a review of monitoring and toxicological findings. Toxicol. Sci. 2007, 99:366-394. 10.1093/toxsci/kfm128.
33. Liu C., Chang V.W.C., Gin K.Y.H., Nguyen V.T. Genotoxicity of perfluorinated chemicals (PFCs) to the green mussel (Perna viridis). Sci. Total Environ. 2014, 487:117-122. http://dx.doi.org/10.1016/j.scitotenv.2014.04.017.
34. MacDonald M.M., Warne A.L., Stock N.L., Mabury S.A., Solomon K.R., Sibley P.K. Toxicity of perfluorooctane sulfonic acid and perfluorooctanoic acid to Chironomus tentans. Environ. Toxicol. Chem. 2004, 23:2116-2123. 10.1897/03-449.
35. Matson C.W., Lambert M.M., McDonald T.J., Autenrieth R.L., Donnelly K.C., Islamzadeh A., Politov D.I., Bickham J.W. Evolutionary toxicology: population-level effects of chronic contaminant exposure on the marsh frogs (Rana ridibunda) of Azerbaijan. Environ. Health Perspect. 2006, 114:547-552. 10.1289/ehp.8404.
36. Muller L.A.H., Vangronsveld J., Colpaert J.V. Genetic structure of Suillus luteus populations in heavy metal polluted and nonpolluted habitats. Mol. Ecol. 2007, 16:4728-4737. 10.1111/j.1365-294X.2007.03549.x.
37. Müller R., Seeland A., Jagodzinski L.S., Diogo J.B., Nowak C., Oehlmann J. Simulated climate change conditions unveil the toxic potential of the fungicide pyrimethanil on the midge Chironomus riparius: a multigeneration experiment. Ecol. Evol. 2012, 2:196-210. 10.1002/ece3.71.
38. Narum S.R., Buerkle C.A., Davey J.W., Miller M.R., Hohenlohe P.A. Genotyping-by-sequencing in ecological and conservation genomics. Mol. Ecol. 2013, 22:2841-2847. 10.1111/mec.12350.
39. Nobels I., Dardenne F., De Coen W., Blust R. Application of a multiple endpoint bacterial reporter assay to evaluate toxicological relevant endpoints of perfluorinated compounds with different functional groups and varying chain length. Toxicol. In Vitro 2010, 24:1768-1774. 10.1016/j.tiv.2010.07.002.
40. Nowak C., Czeikowitz A., Vogt C., Oetken M., Streit B., Schwenk K. Variation in sensitivity to cadmium among genetically characterized laboratory strains of the midge Chironomus riparius. Chemosphere 2008, 71:1950-1956. 10.1016/j.chemosphere.2007.12.023.
41. Nowak C., Hankeln T., Schmidt E.R., Schwenk K. Development and localization of microsatellite markers for the sibling species Chironomus riparius and Chironomus piger (Diptera, Chironomidae). Mol. Ecol. Notes 2006, 6:915-917.
42. Nowak C., Jost D., Vogt C., Oetken M., Schwenk K., Oehlmann J. Consequences of inbreeding and reduced genetic variation on tolerance to cadmium stress in the midge Chironomus riparius. Aquat. Toxicol. 2007, 85:278-284. http://dx.doi.org/10.1016/j.aquatox.2007.04.015.
43. Nowak C., Vogt C., Diogo J.B., Schwenk K. Genetic impoverishment in laboratory cultures of the test organism Chironomus riparius. Environ. Toxicol. Chem. 2007, 26:1018-1022. 10.1897/06-349R.1.
44. Nowak C., Vogt C., Pfenninger M., Schwenk K., Oehlmann J., Streit B., Oetken M. Rapid genetic erosion in pollutant-exposed experimental chironomid populations. Environ. Pollut. 2009, 157:881-886. http://dx.doi.org/10.1016/j.envpol.2008.11.005.
45. OECD Chironomid toxicity test using spiked sediment; Guideline for Testing of Chemicals No. 218. Paris: Organisation for Economic Cooperation and Development 2004.
46. OECD Chironomid toxicity test using spiked water; Guideline for Testing of Chemicals No. 219. Paris: Organisation for Economic Cooperation and Development 2004.
47. OECD Sediment-Water Chironomid Life-Cycle Toxycity Test using spiked water or spiked sediment; Guideline for the Testing of Chemicals No. 233. Paris: Organisation for Economic Cooperation and Development 2010.
48. Polesello, S., Pagnotta, R., Rusconi, M., Zaghi, C., Valsecchi, S., Unpublished results. A comprehensive study of occurrence and sources of perfluorinated compounds in surface waters of Italy.
49. Ribeiro R., Lopes I. Contaminant driven genetic erosion and associated hypotheses on alleles loss, reduced population growth rate and increased susceptibility to future stressors: an essay. Ecotoxicology 2013, 22:889-899. 10.1007/s10646-013-1070-0.
50. Rinner B.P., Matson C.W., Islamzadeh A., McDonald T.J., Donnelly K.C., Bickham J.W. Evolutionary toxicology: contaminant-induced genetic mutations in mosquitofish from Sumgayit, Azerbaijan. Ecotoxicology 2011, 20:365-376. 10.1007/s10646-010-0587-8.
51. Rodea-Palomares I., Leganes F., Rosal R., Fernandez-Pinas F. Toxicological interactions of perfluorooctane sulfonic acid (PFOS) and perfluorooctanoic acid (PFOA) with selected pollutants. J. Hazard. Mater. 2012, 201:209-218. 10.1016/j.jhazmat.2011.11.061.
52. 23rd Annual Meeting of SETAC Europe "Building a better future: responsible innovation and environmental protection", Glasgow, Scotland 2013, M. Rusconi, C.P.B. Martins, L. Marziali, M. Mazzoni, S. Polesello, F. Rosignoli, F. Stefani, S. Valsecchi (Eds.).
53. 23rd Annual Meeting of SETAC Europe "Building a better future: responsible innovation and environmental protection, Glasgow, Scotland 2013, M. Rusconi, L. Marziali, M. Mazzoni, S. Polesello, F. Rosignoli, F. Stefani, S. Valsecchi (Eds.).
54. Schuelke M. An economic method for the fluorescent labelling of PCR fragments. Nat. Biotechnol. 2000, 18:233-234. 10.1038/72708.
55. Shi X.J., Du Y.B., Lam P.K.S., Wu R.S.S., Zhou B.S. Developmental toxicity and alteration of gene expression in zebrafish embryos exposed to PFOS. Toxicol. Appl. Pharmacol. 2008, 230:23-32. 10.1016/j.taap.2008.01.043.
56. Silva R.M., Pereira F., Carneiro J., Sobral O., Ribeiro R., Amorim A., Soares A.M.V.M., Lopes I. Microevolution in a natural population of daphnia longispina exposed to acid mine drainage. interdisciplinary studies on environmental chemistry. Biological Responses to Contaminants 2010, 213-218. Terrapub, Tokyo, Japan. N. Hamamura, S. Suzuki, S. Mendo, C.M. Barroso, H. Iwata, S. Tanabe (Eds.).
57. Sukumaran S., Grant A. Effects of genotoxicity and its consequences at the population level in sexual and asexual Artemia assessed by analysis of inter-simple sequence repeats (ISSR). Mut. Res. 2013, 757:8-14. http://dx.doi.org/10.1016/j.mrgentox.2013.03.015.
58. Theodorakis C.W., Lee K.L., Adams S.M., Law C.B. Evidence of altered gene flow, mutation rate, and genetic diversity in redbreast sunfish from a pulp-mill-contaminated river. Environ. Sci. Technol. 2006, 40:377-386. 10.1021/es052095g.
59. Valsecchi S., Marziali L., Mazzoni M., Polesello S., Rusconi M., Stefani F. Bioaccumulation of perfluorinated alkyl acids in two benthic invertebrates: Lumbriculus variegatus and Chironomus riparius. 5th International Workshop on Per- and Polyfluorinated Alkyl Substances - PFAS1 2013, Helsingor, Copenaghen, Denmark.
60. 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. 10.1111/j.1471-8286.2004.00684.x.
61. van Straalen N.M., Janssens T.K.S., Roelofs D. Micro-evolution of toxicant tolerance: from single genes to the genome's tangled bank. Ecotoxicology 2011, 20:574-579. 10.1007/s10646-011-0631-3.
62. 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. 10.1080/1080-700291905783.
63. Vandegehuchte M.B., De Coninck D., Vandenbrouck T., De Coen W.M., Janssen C.R. Gene transcription profiles, global DNA methylation and potential transgenerational epigenetic effects related to Zn exposure history in Daphnia magna. Environ. Pollut. 2010, 158:3323-3329. 10.1016/j.envpol.2010.07.023.
64. Vandegehuchte M.B., Vandenbrouck T., De Coninck D., De Coen W.M., Janssen C.R. Gene transcription and higher-level effects of multigenerational Zn exposure in Daphnia magna. Chemosphere 2010, 80:1014-1020. 10.1016/j.chemosphere.2010.05.032.
65. Vogt C., Belz D., Galluba S., Nowak C., Oetken M., Oehlmann J. Effects of cadmium and tributyltin on development and reproduction of the non-biting midge Chironomus riparius (Diptera) - baseline experiments for future multi-generation studies. J. Environ. Sci. Health A: Tox. Hazard. Subst. Environ. Eng. 2007, 42:1-9. 10.1080/10934520601015255.
66. Vogt C., Hess M., Nowak C., Diogo J.B., Oehlmann J., Oetken M. Effects of cadmium on life-cycle parameters in a multi-generation study with Chironomus riparius following a pre-exposure of populations to two different tributyltin concentrations for several generations. Ecotoxicology 2010, 19:1174-1182. 10.1007/s10646-010-0501-4.
67. Vogt C., Nowak C., Diogo J.B., Oetken M., Schwenk K., Oehlmann J. Multi-generation studies with Chironomus riparius - effects of low tributyltin concentrations on life history parameters and genetic diversity. Chemosphere 2007, 67:2192-2200. 10.1016/j.chemosphere.2006.12.025.
68. Vogt C., Pupp A., Nowak C., Jagodzinski L.S., Baumann J., Jost D., Oetken M., Oehlmann J. Interaction between genetic diversity and temperature stress on life-cycle parameters and genetic variability in midge Chironomus riparius populations. Clim. Res. 2007, 33:207-214. 10.3354/cr033207.
69. 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. 10.1046/j.1365-294X. 2003.01933.x.
70. Zheng X.M., Liu H.L., Shi W., Wei S., Giesy J.P., Yu H.X. Effects of perfluorinated compounds on development of zebrafish embryos. Environ. Sci. Poll. Res. 2012, 19:2498-2505. 10.1007/s11356-012-0977-y.