Evolutionary consequences of historical metal contamination for natural populations of Chironomus riparius (Diptera: Chironomidae)

Abstract

Populations inhabiting metal-impacted freshwater systems located nearby industrial and urban areas may be under intense selection. The present study aims to address two fundamental microevolutionary aspects of metal contamination in the midge Chironomus riparius (Meigen): Are populations inhabiting historically metal contaminated sites genetically adapted to metals? And, are populations from these sites genetically eroded? To answer these questions, C. riparius populations were sampled from three sites with well-known histories of metal contamination and three nearby-located references. Genetic adaptation to metals was investigated through acute and chronic exposures to cadmium (Cd), after rearing all populations for at least six generations under laboratory clean conditions. Genetic diversity was estimated based on the allelic variation of seven microsatellite markers. Results showed higher acute tolerance to Cd in populations originating from metal contaminated sites compared to their respective references and significant differences in two out of three pairwise comparisons. However, there was a mismatch between acute and chronic tolerance to Cd with results of the partial life-cycle tests suggesting fitness costs under control clean conditions in two metal-adapted populations. Despite no evidences of genetic erosion in populations sampled from metal contaminated sites, our results suggest genetically inherited tolerance to Cd in populations inhabiting historically contaminated sites. These findings lend support to the use of C. riparius as a model organism in evolutionary toxicology and highlight the importance of coupling measures of neutral genetic diversity with assessments of chemical tolerance of populations for a better understanding of contaminant-induced adaptation and evolutionary processes.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Adeyemi JA, Klerks PL (2013) Occurrence of copper acclimation in the least killifish Heterandria formosa, and associated biochemical and physiological mechanisms. Aquat Toxicol 130:51–57

    Article  Google Scholar 

  2. Agra AR, Guilhermino L, Soares AM, Barata C (2010) Genetic costs of tolerance to metals in Daphnia longispina populations historically exposed to a copper mine drainage. Environ Toxicol Chem 29:939–946

    CAS  Article  Google Scholar 

  3. Altshuler I, Demiri B, Xu S, Constantin A, Yan ND, Cristescu ME (2011) An integrated multi-disciplinary approach for studying multiple stressors in freshwater ecosystems: Daphnia as a model organism. Integr Comp Biol:icr103 51(4):623–633

  4. Armitage PD, Pinder L, Cranston P (2012) The chironomidae: biology and ecology of non-biting midges. Springer Science & Business Media, Dordrecht, Netherlands

  5. ASTM (1980) Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E-790-80. Philadelphia, USA

  6. Athrey N, Leberg PL, Klerks PL (2007) Laboratory culturing and selection for increased resistance to cadmium reduce genetic variation in the least killifish, Heterandria formosa. Environ Toxicol Chem 26:1916–1921

    CAS  Article  Google Scholar 

  7. Barata C, Baird DJ, Miñarro A, Soares AM (2000) Do genotype responses always converge from lethal to nonlethal toxicant exposure levels? Hypothesis tested using clones of Daphnia magna Straus. Environ Toxicol Chem 19:2314–2322

    CAS  Article  Google Scholar 

  8. Berckmoes V, Scheirs J, Jordaens K, Blust R, Backeljau T, Verhagen R (2005) Effects of environmental pollution on microsatellite DNA diversity in wood mouse (Apodemus sylvaticus) populations. Environ Toxicol Chem 24:2898–2907

    CAS  Article  Google Scholar 

  9. Bickham JW (2011) The four cornerstones of evolutionary toxicology. Ecotoxicology 20:497–502

    CAS  Article  Google Scholar 

  10. Campos D, Gravato C, Quintaneiro C, Soares AM, Pestana JL (2016) Responses of the aquatic midge Chironomus riparius to DEET exposure. Aquat Toxicol 172:80–85

    CAS  Article  Google Scholar 

  11. Coors A, Vanoverbeke J, De Bie T, De Meester L (2009) Land use, genetic diversity and toxicant tolerance in natural populations of Daphnia magna. Aquat Toxicol 95:71–79

    CAS  Article  Google Scholar 

  12. Costa C, Jesus-Rydin C (2001) Site investigation on heavy metals contaminated ground in Estarreja—Portugal. Eng Geol 60:39–47

    Article  Google Scholar 

  13. Costa D et al. (2012) Influence of adaptive evolution of cadmium tolerance on neutral and functional genetic variation in Orchesella cincta. Ecotoxicology 21:2078–2087

    CAS  Article  Google Scholar 

  14. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  Google Scholar 

  15. Farwell M, Drouillard KG, Heath DD, Pitcher TE (2012) Acclimation of life-history traits to experimental changes in environmental contaminant concentrations in brown bullhead (Ameiurus nebulosus). Environ Toxicol Chem 31:863–869

    CAS  Article  Google Scholar 

  16. Fasola E, Ribeiro R, Lopes I (2015) Microevolution due to pollution in amphibians: a review on the genetic erosion hypothesis. Environ Pollut 204:181–190

    CAS  Article  Google Scholar 

  17. Ferrington Jr LC (2008) Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. Hydrobiol 595:447–455

  18. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

  19. Frankham R (2005) Stress and adaptation in conservation genetics. J Evol Biol 18:750–755

    CAS  Article  Google Scholar 

  20. Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618

    Article  Google Scholar 

  21. Gall ML, Holmes SP, Dafforn KA, Johnston EL (2013) Differential tolerance to copper, but no evidence of population-level genetic differences in a widely-dispersing native barnacle. Ecotoxicology 22:929–937

    CAS  Article  Google Scholar 

  22. Geffard O, Geffard A, Chaumot A, Vollat B, Alvarez C, Tusseau‐Vuillemin MH, Garric J (2008) Effects of chronic dietary and waterborne cadmium exposures on the contamination level and reproduction of Daphnia magna. Environ Toxicol Chem 27:1128–1134

    CAS  Article  Google Scholar 

  23. Gonçalves EP, Boaventura RA, Mouvet C (1992) Sediments and aquatic mosses as pollution indicators for heavy metals in the Ave river basin (Portugal). Sci Total Environ 114:7–24

    Article  Google Scholar 

  24. Groenendijk D, Lücker SM, Plans M, Kraak MH, Admiraal W (2002) Dynamics of metal adaptation in riverine chironomids. Environ Pollut 117:101–109

    CAS  Article  Google Scholar 

  25. Groenendijk D, Postma JF, Kraak MH, Admiraal W (1998) Seasonal dynamics and larval drift of Chironomus riparius (Diptera) in a metal contaminated lowland river. Aquat Ecol 32:341–351

    CAS  Article  Google Scholar 

  26. Gusev O et al. (2014) Comparative genome sequencing reveals genomic signature of extreme desiccation tolerance in the anhydrobiotic midge. Nat Commun 5:1–9

  27. Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nat Rev Genet 9:421–432

    CAS  Article  Google Scholar 

  28. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statistics 6:65–70

  29. Inácio M, Pereira V, Pinto M (1998) Mercury contamination in sandy soils surrounding an industrial emission source (Estarreja, Portugal). Geoderma 85:325–339

    Article  Google Scholar 

  30. Irving EC, Baird DJ, Culp JM (2003) Ecotoxicological responses of the mayfly Baetis tricaudatus to dietary and waterborne cadmium: implications for toxicity testing. Environ Toxicol Chem 22:1058–1064

    CAS  Article  Google Scholar 

  31. Janssens TK, Roelofs D, Van Straalen NM (2009) Molecular mechanisms of heavy metal tolerance and evolution in invertebrates. Insect Sci 16:3–18

    CAS  Article  Google Scholar 

  32. Klerks P, Leberg P, Lance R, McMillin D, Means J (1997) Lack of development of pollutant-resistance or genetic differentiation in darter gobies (Gobionellus boleosoma) inhabiting a produced-water discharge site. Mar Environ Res 44:377–395

    CAS  Article  Google Scholar 

  33. Klerks P, Levinton J (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176:135–141

    CAS  Article  Google Scholar 

  34. Kliot A, Ghanim M (2012) Fitness costs associated with insecticide resistance. Pest Manag Sci 68:1431–1437

    CAS  Article  Google Scholar 

  35. Leonard EM, Pierce LM, Gillis PL, Wood CM, O’Donnell MJ (2009) Cadmium transport by the gut and Malpighian tubules of Chironomus riparius. Aquat Toxicol 92:179–186

    CAS  Article  Google Scholar 

  36. Leppänen MT, Postma JF, Groenendijk D, Kukkonen JV, Buckert-de Jong MC (1998) Feeding Activity of Midge Larvae (Chironomus riparius Meigen) in Metal-Polluted River Sediments. Ecotoxicol Environ Saf 41:251–257

    Article  Google Scholar 

  37. Lopes I, Baird D, Ribeiro R (2004) Genetic determination of tolerance to lethal and sublethal copper concentrations in field populations of Daphnia longispina. Arch Environ Contam Toxicol 46:43–51

    CAS  Article  Google Scholar 

  38. Lopes I, Baird DJ, Ribeiro R (2005) Genetically determined resistance to lethal levels of copper by Daphnia longispina: association with sublethal response and multiple/coresistance. Environ Toxicol Chem 24:1414–1419

    CAS  Article  Google Scholar 

  39. Lopes ML, Rodrigues AM, Quintino V (2014) Ecological effects of contaminated sediments following a decade of no industrial effluents emissions: the sediment quality triad approach. Mar Pollut Bull 87:117–130

    CAS  Article  Google Scholar 

  40. Maes G, Raeymaekers J, Pampoulie C, Seynaeve A, Goemans G, Belpaire C, Volckaert F (2005) 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 73:99–114

    CAS  Article  Google Scholar 

  41. Martins N, Bollinger C, Harper RM, Ribeiro R (2009) Effects of acid mine drainage on the genetic diversity and structure of a natural population of Daphnia longispina. Aquat Toxicol 92:104–112

    CAS  Article  Google Scholar 

  42. Martins V et al. (2011) The response of benthic foraminifera to pollution and environmental stress in Ria de Aveiro (N Portugal). J Iberian Geol 37:231–243

    Google Scholar 

  43. McMillan AM, Bagley MJ, Jackson SA, Nacci DE (2006) Genetic diversity and structure of an estuarine fish (Fundulus heteroclitus) indigenous to sites associated with a highly contaminated urban harbor. Ecotoxicology 15:539–548

    CAS  Article  Google Scholar 

  44. Medina MH, Correa JA, Barata C (2007) Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere 67:2105–2114

    CAS  Article  Google Scholar 

  45. Miller LM, Bartell SE, Schoenfuss HL (2012) Assessing the effects of historical exposure to endocrine-active compounds on reproductive health and genetic diversity in walleye, a native apex predator, in a large riverine system. Arch Environ Contam Toxicol 62:657–671

    CAS  Article  Google Scholar 

  46. Moe SJ, De Schamphelaere K, Clements WH, Sorensen MT, Van den Brink PJ, Liess M (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32:49–61

    CAS  Article  Google Scholar 

  47. Motulsky H, Christopoulos A (2004) Comparing models using the extra sum-of-squares F test. In: GraphPad Software, Inc. (ed) Fitting models to biological data using linear and nonlinear regression: a practical guide to curve fitting. Oxford University Press, Oxford, pp 138–142

  48. Nacci D et al. (1999) Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants. Marine Biol 134:9–17

    Article  Google Scholar 

  49. Nacci DE, Champlin D, Coiro L, McKinney R, Jayaraman S (2002) Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus. Environ Toxicol Chem 21:1525–1532

    CAS  Article  Google Scholar 

  50. Nair PMG, Park SY, Chung JW, Choi J (2013) Transcriptional regulation of glutathione biosynthesis genes, γ-glutamyl-cysteine ligase and glutathione synthetase in response to cadmium and nonylphenol in Chironomus riparius. Environ Toxicol Pharmacol 36:265–273

    CAS  Article  Google Scholar 

  51. Nowak C, Hankeln T, Schmidt ER, Schwenk K (2006) Development and localization of microsatellite markers for the sibling species Chironomus riparius and Chironomus piger (Diptera: Chironomidae). Mol Ecol Notes 6:915–917

    CAS  Article  Google Scholar 

  52. Nowak C, Vogt C, Pfenninger M, Schwenk K, Oehlmann J, Streit B, Oetken M (2009) Rapid genetic erosion in pollutant-exposed experimental chironomid populations. Environ Pollut 157:881–886

    CAS  Article  Google Scholar 

  53. OECD (2004a) Guideline for the testing of chemicals no 218. Sediment-water chironomid toxicity test using spiked sediment. Paris, France

  54. OECD (2004b) Test No. 219: Sediment-Water Chironomid Toxicity Using Spiked Water. OECD Publishing

  55. OECD (2011) Test No. 235: Chironomus sp., Acute Immobilisation Test. OECD Publishing

  56. Oppold A-M, Pedrosa JA, Bálint M, Diogo JB, Ilkova J, Pestana JL, Pfenninger M (2016) Support for the evolutionary speed hypothesis from intraspecific population genetic data in the non-biting midge Chironomus riparius. Proc R Soc B 283:2015–2413

    Article  Google Scholar 

  57. Paris JR, King RA, Stevens JR (2015) Human mining activity across the ages determines the genetic structure of modern brown trout (Salmo trutta L.) populations. Evol Appl 8:573–585

    Article  Google Scholar 

  58. Pauls SU et al. (2014) Integrating molecular tools into freshwater ecology: developments and opportunities. Freshw Biol 59:1559–1576

    Article  Google Scholar 

  59. Pauls SU, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946

    Article  Google Scholar 

  60. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  61. Pedrosa JAM et al. (2017) Investigating heritability of cadmium tolerance in Chironomus riparius natural populations: a physiological approach. Chemosphere 170:83–94

    CAS  Article  Google Scholar 

  62. Pedrosa JAM, Cocchiararo B, Verdelhos T, Soares AMVM, Pestana JLT, Nowak C (in press) Population genetic structure and hybridization patterns in the cryptic sister species Chironomus riparius and C. piger across differentially polluted freshwater systems. Ecotoxicology and Environmental Safety.

  63. Pfenninger M, Nowak C, Kley C, Steinke D, Streit B (2007) Utility of DNA taxonomy and barcoding for the inference of larval community structure in morphologically cryptic Chironomus (Diptera) species. Mol Ecol 16:1957–1968

    CAS  Article  Google Scholar 

  64. Postma J, Van Kleunen A, Admiraal W (1995) Alterations in life-history traits of Chironomus riparius (Diptera) obtained from metal contaminated rivers. Arch Environ Contam Toxicol 29:469–475

    CAS  Article  Google Scholar 

  65. Postma JF, VanNugteren P, De Jong MBB (1996) Increased cadmium excretion in metal‐adapted populations of the midge Chironomus riparius (Diptera). Environ Toxicol Chem 15:332–339

    CAS  Article  Google Scholar 

  66. Räsänen K, Kruuk L (2007) Maternal effects and evolution at ecological time‐scales. Functional Ecology 21:408–421

    Article  Google Scholar 

  67. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  68. Reis ARd, Parker A, Carter J, Ferreira MP (2005) Distribution of selected heavy metals in sediments of the Agueda River (central Portugal). J Environ Sci Health 40:305–316

    Article  Google Scholar 

  69. Ribeiro R, Baird DJ, Soares AM, Lopes I (2012) Contaminant driven genetic erosion: a case study with Daphnia longispina. Environ Toxicol Chem 31:977–982

    CAS  Article  Google Scholar 

  70. Ribeiro R, Lopes I (2013) Contaminant driven genetic erosion and associated hypotheses on alleles loss, reduced population growth rate and increased susceptibility to future stressors: an essay. Ecotoxicology 22:889–899

    CAS  Article  Google Scholar 

  71. Rodrigues AC, Gravato C, Quintaneiro C, Barata C, Soares AM, Pestana JL (2015) Sub-lethal toxicity of environmentally relevant concentrations of esfenvalerate to Chironomus riparius. Environ Pollut 207:273–279

    CAS  Article  Google Scholar 

  72. Salice CJ, Anderson TA, Roesijadi G (2010) Adaptive responses and latent costs of multigeneration cadmium exposure in parasite resistant and susceptible strains of a freshwater snail. Ecotoxicology 19:1466–1475

    CAS  Article  Google Scholar 

  73. Saro L, Lopes I, Martins N, Ribeiro R (2012) Testing hypotheses on the resistance to metals by Daphnia longispina: differential acclimation, endpoints association, and fitness costs. Environ Toxicol Chem 31:909–915

    CAS  Article  Google Scholar 

  74. Sibley PK, Ankley GT, Benoit DA (2001) Factors affecting reproduction and the importance of adult size on reproductive output of the midge Chironomus tentans. Environ Toxicol Chem 20:1296–1303

    CAS  Article  Google Scholar 

  75. Soares H, Boaventura R, Machado A, Da Silva JE (1999) Sediments as monitors of heavy metal contamination in the Ave river basin (Portugal): multivariate analysis of data. Environ Pollut 105:311–323

    CAS  Article  Google Scholar 

  76. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  Article  Google Scholar 

  77. Toušová Z, Kuta J, Hynek D, Adam V, Kizek R, Bláha L, Hilscherová K (2016) Metallothionein modulation in relation to cadmium bioaccumulation and age-dependent sensitivity of Chironomus riparius larvae. Environ Sci Pollut Res 23:10504–10513

    Article  Google Scholar 

  78. van Straalen NM, Timmermans MJ (2002) Genetic variation in toxicant-stressed populations: an evaluation of the “genetic erosion” hypothesis. Hum Ecol Risk Assess 8:983–1002

    Article  Google Scholar 

  79. Ward TJ, Robinson WE (2005) Evolution of cadmium resistance in Daphnia magna. Environ Toxicol Chem 24:2341–2349

    CAS  Article  Google Scholar 

  80. Whitehead A, Anderson SL, Kuivila KM, Roach JL, May B (2003) Genetic variation among interconnected populations of Catostomus occidentalis: implications for distinguishing impacts of contaminants from biogeographical structuring. Mol Ecol 12:2817–2833

    CAS  Article  Google Scholar 

  81. Wirgin I, Maceda L, Waldman J, Mayack DT (2015) Genetic variation and population structure of American mink Neovison vison from PCB-contaminated and non-contaminated locales in eastern North America. Ecotoxicology 24:1–15

  82. Xie L, Buchwalter DB (2011) Cadmium exposure route affects antioxidant responses in the mayfly Centroptilum triangulifer. Aquat Toxicol 105:199–205

    CAS  Article  Google Scholar 

  83. Xie L, Klerks PL (2003) Responses to selection for cadmium resistance in the least killifish, Heterandria formosa. Environ Toxicol Chem 22:313–320

    CAS  Article  Google Scholar 

  84. Xie L, Klerks PL (2004a) Changes in cadmium accumulation as a mechanism for cadmium resistance in the least killifish Heterandria formosa. Aquat Toxicol 66:73–81

    CAS  Article  Google Scholar 

  85. Xie L, Klerks PL (2004b) Fitness cost of resistance to cadmium in the least killifish (Heterandria formosa). Environ Toxicol Chem 23:1499–1503

    CAS  Article  Google Scholar 

  86. Xie L, Klerks PL (2004c) Metallothionein‐like protein in the least killifish Heterandria formosa and its role in cadmium resistance. Environ Toxicol Chem 23:173–177

    CAS  Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Portuguese Science Foundation (FCT) through CESAM: UID/AMB/50017/2013. We are thankful for the financial support of COMPETE program (Programa Operacional Fatores de Competitividade, FEDER component) and National funding through FCT- Fundação para a Ciência e Tecnologia within the research project MIDGE - Microevolutionary Dynamics and Genetic Erosion in pollution-affected Chironomus (Ref: PTDC/BIA-BEC/104125/2008). We are also thankful to FCT and POPH/FSE (Programa Operacional Potencial Humano/Fundo Social Europeu) for the post-doctoral fellowship of J. L. T. Pestana (SFRH/BPD/103897/2014), and the doctoral grants of Diana Campos (SFRH/BD/87370/2012) and João A. M. Pedrosa PhD grant (SFRH/BD/75606/2010).

Author information

Affiliations

Authors

Corresponding authors

Correspondence to João Pedrosa or João L. T. Pestana.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pedrosa, J., Campos, D., Cocchiararo, B. et al. Evolutionary consequences of historical metal contamination for natural populations of Chironomus riparius (Diptera: Chironomidae). Ecotoxicology 26, 534–546 (2017). https://doi.org/10.1007/s10646-017-1784-5

Download citation

Keywords

  • Cadmium
  • Freshwater
  • Metal adaptation
  • Genetic diversity
  • Invertebrates
  • Metal contamination