Skip to main content
SpringerLink
Log in

Evolutionary toxicology: contaminant-induced genetic mutations in mosquitofish from Sumgayit, Azerbaijan

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

This study builds on a long-term program that has shown Sumgayit, Azerbaijan to contain wetlands with high levels of a diversity of chemical contaminants. Previous contaminant and biomarker studies of turtles and frogs showed a correlation between somatic chromosomal damage and chemical contaminants at Sumgayit. The objective of this study was to determine if a recently arrived species (mosquitofish) has genetic impacts similar to native species (marsh frogs) thus confirming the pattern is not the result of historical events such as glacial cycles, but is associated with recent chemical contamination. Nucleotide sequences of the mtDNA control region of invasive mosquitofish (Gambusia holbrooki) from Sumgayit were compared to mosquitofish from pristine sites in Europe and Azerbaijan and to native North American populations. Persistent heteroplasmy for a hyper-mutable simple sequence repeat and low haplotype and nucleotide diversities were observed in all invasive populations. However, Sumgayit possessed four de novo haplotypes and heteroplasmic conditions. All of the observed variable nucleotide positions were within or adjacent to a cytosine mononucleotide repeat. This repeat was within a conserved secondary structure; the region likely undergoes expansion and contraction at a rate sufficient to prevent fixation of the common 1/3 heteroplasmy. Whereas the 1/3 heteroplasmy appeared coincident with the establishment of mosquitofish in Europe, other forms of heteroplasmy resulted from contaminant-induced de novo mutations in Sumgayit. We conclude that Sumgayit is a mutational hotspot caused by legacy contaminants from chemical factories from the era of the Soviet Union.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ashley MV, Laipis PJ, Hauswirth WW (1989) Rapid segregation of heteroplasmic bovine mitochondria. Nucleic Acids Res 17:7325–7331

    Article  CAS  Google Scholar 

  • Baker RJ, Bickham AM, Bondarkov M, Gaschak SP, Matson CW, Rodgers BE, Wickliffe JK, Chesser RK (2001) Consequences of polluted environments on population structure: the bank vole (Clethrionomys glareolus) at Chornobyl. Ecotoxicology 10:211–216

    Article  CAS  Google Scholar 

  • Baker AR, Loughlin TR, Burkanov V, Matson CW, Trujillo RG, Calkins DG, Wickliffe JK, Bickham JW (2005) Variation of mitochondrial control region sequences of Steller sea lions, Eumetopias jubatus: the three-stock hypothesis. J Mammal 86:1075–1084

    Article  Google Scholar 

  • Beerli P (2003) MIGRATE: Documentation and program, part of LAMARC. Version 1.7.3. Revised July 2003. Available at http://evolution.genetics.washington.edu/lamarc.html

  • Bendall KE, Macauley VA, Baker JR, Sykes BC (1996) Heteroplasmic point mutations in the human mtDNA control region. Am J Hum Genet 59:1276–1287

    Google Scholar 

  • Bickham JW, Matson CW, Islamzadeh A, Rowe GT, Donnelly KC, Swartz CD, Rogers WJ, Autenrieth RL, McDonald TJ, Politov D, Wickliffe JK, Palatnikov G, Mekhtiev AA, Kasimov R (2003) Editorial: the unknown environmental tragedy in Sumgayit, Azerbaijan. Ecotoxicology 12:507–510

    Article  Google Scholar 

  • Brown DT, Samuels DC, Michael EM, Turnbull DM, Chinnery PF (2001) Random genetic drift determines the level of mutant mtDNA in human primary oocytes. Am J Hum Genet 68:533–536

    Google Scholar 

  • Caliani I, Porcelloni S, Mori G, Frenzilli G, Ferraro M, Marsili L, Casini S, Fossi MC (2009) Genotoxic effects of produced waters in mosquito fish (Gambusia affinis). Ecotoxicology 18:75–80

    Article  CAS  Google Scholar 

  • Dimauro S, Davidzon G (2005) Mitochondrial DNA and disease. Annals Med 37:222–232

    Article  CAS  Google Scholar 

  • Forster L, Forster P, Lutz-Bonengel S, Willkomm H, Brinkmann B (2002) Natural radioactivity and human mitochondrial DNA mutations. Proc Natl Acad Sci USA 99:13950–13954

    Article  CAS  Google Scholar 

  • Howell N (1999) Human mitochondrial disease: answering questions and questioning answers. Int Rev Cytol 186:49–116

    Article  CAS  Google Scholar 

  • Howell N, Bogolin Smejkal C (2000) Persistent heteroplasmy of a mutation in the human mtDNA control region: hypermutation as an apparent consequence of simple-repeat expansion/contraction. Amer J Hum Evol 66:1589–1598

    CAS  Google Scholar 

  • Krumholz LA (1948) Reproduction in the Western Mosquitofish, Gambusia affinis (Baird & Girard), and its use in mosquito control. Ecol Monogr 18:1–43

    Article  Google Scholar 

  • Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770

    Article  CAS  Google Scholar 

  • Lightowers RN, Chinnery PF, Turnbull DM, Howell N (1997) Mammalian mitochondrial genetics: heredity, heteroplasmy and disease. Trends Genet 13:450–455

    Article  Google Scholar 

  • Lopez JV, Cevario S, O’Brien SJ (1996) Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (numt) in the nuclear genome. Genomics 33:229–246

    Article  CAS  Google Scholar 

  • Maniatis TE, Fristch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Publications, New York

    Google Scholar 

  • Matson CW, Rodgers BE, Chesser RK, Baker RJ (2000) Genetic diversity of Clethrionomys glareolus populations from highly contaminated sites in the Chornobyl region, Ukraine. Environ Toxicol Chem 8:2130–2135

    Google Scholar 

  • Matson CW, Palatnikov G, Islamzadeh A, McDonald TJ, Autenrieth RL, Donnelly KC, Bickham JW (2005a) Chromosomal damage in two species of aquatic turtles (Emys orbicularis and Mauremys caspica) inhabiting contaminated sites in Azerbaijan. Ecotoxicology 14:1–13

    Article  Google Scholar 

  • Matson CW, Palatnikov G, McDonald TJ, Autenrieth RL, Donnelly KC, Anderson TA, Canas JE, Islamzadeh A, Bickham JW (2005b) Patterns of genotoxicity and contaminant exposure: Evidence of genomic instability in the marsh frogs (Rana ridibunda) of Sumgayit, Azerbaijan. Environ Toxicol Chem 24:2055–2064

    Article  CAS  Google Scholar 

  • Matson CW, Lambert MM, McDonald TJ, Autenrieth RL, Donnelly KC, Islamzadeh A, Politov DI, Bickham JW (2006) Evolutionary toxicology and population genetic effects of chronic contaminant exposure on marsh frogs (Rana ridibunda) in Sumgayit, Azerbaijan. Environ Health Perspect 114:547–552

    Article  CAS  Google Scholar 

  • Matson CW, Gillespie AM, McCarthy C, McDonald TJ, Bickham JW, Sullivan R, Donnelly KC (2009) Wildlife toxicology: biomarkers of genotoxic exposures at a hazardous waste site. Ecotoxicology 18:886–898

    Article  CAS  Google Scholar 

  • Matsuhashi T, Masuda R, Mano T, Yoshida MC (1999) Microevolution of the mitochondrial DNA control region in the Japanese brown bear (Ursus arctos) Population. Mol Biol Evol 16:676–684

    CAS  Google Scholar 

  • Overstreet RM, Hawkins WE, Deardorff TL (1996) The western mosquitofish as an environmental sentinel: parasites and histological lesions. In: Servos MR, Munkittrick KR, Carey JH, Van Der Kraak GJ (eds) Environmental fate and effects of pulp and paper mill effluents. St. Lucie Press, Delray Beach, FL, pp 495–510

    Google Scholar 

  • Pakendorf B, Stoneking M (2005) Mitochondrial DNA and human evolution. Annu Rev Genomics Hum Genet 6:165–183

    Article  CAS  Google Scholar 

  • Pereira F, Soares P, Carneiro J, Pereira L, Richards MB, Samuels DC, Amorim A (2008) Evidence for variable selective pressures at a large secondary structure of the human mitochondrial DNA control region. Mol Biol Evol 25:2759–2770

    Article  CAS  Google Scholar 

  • Poulton J, Marchington DR (2002) Segregation of mitochondrial DNA (mtDNA) in human oocytes and in animal models of mtDNA disease: clinical implications. Reproduction 123:751–755

    Article  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN, version 2.000: a software for population genetics data analysis, Genetics and Biometry Laboratory, University of Geneva, Switzerland

  • Shoffner JM, Lott MT, Lezza AMS, Seibel P, Ballinger SW, Wallace DC (1990) Myoclonic Epilepsy and Ragged-Red Fiber Disease (MERRF) is associated with a mitochondrial DNA tRNALys mutation. Cell 61:931–937

    Article  CAS  Google Scholar 

  • Smith MW, Smith MH, Chesser RK (1983) Biochemical genetics of mosquitofish. I. Environmental correlates, temporal and spatial heterogeneity of allele frequencies within a river drainage. Copeia 1983:182–193

    Article  Google Scholar 

  • Stearns SC (1983) A natural experiment in life-history evolution: field data on the introduction of mosquitofish (Gambusia affinis) to Hawaii. Evolution 37:601–617

    Article  Google Scholar 

  • Swartz CD, Donnelly KC, Islamzadeh A, Rowe GT, Rogers WJ, Palatnikov GM, Kasimov R, McDonald TJ, Wickliffe JK, Bickham JW (2003) Chemical contaminants and their effects in fish and wildlife from the industrial zone of Sumgayit, Republic of Azerbaijan. Ecotoxicology 12:511–523

    Article  Google Scholar 

  • Theodorakis CW, Bickham JW (2004) Molecular characterization of contaminant-indicative RAPD markers. Ecotoxicology 13:303–309

    Article  CAS  Google Scholar 

  • Theodorakis CW, Shugart LR (1997) Genetic ecotoxicology II: population genetic structure in radionuclide-contaminated mosquitofish (Gambusia affinis). Ecotoxicology 6:335–354

    Article  CAS  Google Scholar 

  • Theodorakis CW, Shugart LR (1998) Genetic ecotoxicology III: the relationship between DNA strand breaks and genotype in mosquitofish exposed to radiation. Ecotoxicology 7:227–236

    Article  CAS  Google Scholar 

  • Theodorakis CW, Blaylock BG, Shugart LR (1996) Genetic ecotoxicology I.: DNA integrity and reproduction in mosquitofish exposed in situ to radionuclides. Ecotoxicology 5:1–14

    Article  Google Scholar 

  • Theodorakis CW, Bickham JW, Elbl T, Shugart LR, Chesser RK (1998) Genetics of radionuclide-contaminated mosquitofish populations and homology between Gambusia affinis and G. holbrooki. Environ Toxicol Chem stry 17:1992–1998

    CAS  Google Scholar 

  • Theodorakis CW, Elbl T, Shugart LR (1999) Genetic ecotoxicology IV: survival and DNA strand breakage is dependant on genotype in radionuclide-exposed mosquitofish. Aquat Toxicol 45:275–291

    Article  Google Scholar 

  • Theodorakis CW, Bickham JW, Lamb T, Medica PA, Lyne TB (2001) Integration of genotoxicity and population genetic analyses in kangaroo rats (Dipodomys merriami) exposed to radionuclide contamination at the Nevada test site, USA. Environ Toxicol Chem 20:317–326

    Google Scholar 

  • Triant DA, DeWoody JA (2007) The occurence, detection, and avoidance of mitochonrial DNA translocations in mammalian systematics and phylogeography. J Mammal 88:908–920

    Article  Google Scholar 

  • Tully LA, Parsons TJ, Steighner RJ, Holland MM, Marino MA, Prenger VL (2000) A sensitive denaturing gradient-gel electrophoresis assay reveals a high frequency of heteroplasmy in hypervariable region 1 of the human mtDNA control region. Am J Hum Genet 67:432–443

    Google Scholar 

  • Vidal O, Garcia-Berthou E, Tedesco PA, Garcia-Martin J-L (2010) Origin and genetic diversity of mosquitofish (Gambusia holbrooki) introduced to Europe. Biol Invasions 12:841–851

    Article  Google Scholar 

  • Wallace DC, Brown MD, Lott MT (1999) Mitochondrial DNA variation in human evolution and disease. Gene 238:211–230

    Article  CAS  Google Scholar 

  • Welcomme RL (1988) International introductions of inland aquatic species. FAO Fish Tech Pap 294:318

    Google Scholar 

  • Wooten MC, Scribner KT, Smith MH (1988) Genetic variability and systematics of Gambusia in the Southeastern United States. Copeia 1988:283–298

    Article  Google Scholar 

  • Zsurka G, Csordas A (2008) MitoWheel 1.2. http://mitowheel.org/mitowheel.html

  • Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank A. A. Mekhtiev, G. Palatnikov, R. Kasimov, G. Kuliev and E. Askerov for logistical support and assistance in Azerbaijan. We thank the members of the MS advisory committee of B.P.R. for their advice and thoughtful review of the thesis: A. DeWoody, K. Nichols, and M. Zanis. We thank the following people for help in obtaining specimens: M. A. Pinto, I. Caliani, M. C. Fossi, V. Caputo, and E. Olmo. This article is modified from the MS thesis of B. P. R. Partial funding was provided by the National Institute of Environmental Health Sciences, Superfund Basic Research Programs grant ES04917, by a grant from the Lilly Endowment, Inc. awarded through Purdue University Center for the Environment at Discovery Park, and by the Department of Forestry and Natural Resources, Purdue University. This article is dedicated to the memory of the late K.C. Donnelly in recognition of his unfailing support for the study of human health, ecotoxicology, and the environmental crisis in Sumgayit. His kindness, energy, leadership and friendship are sorely missed.

Author information

Authors and Affiliations

  1. Department of Forestry and Natural Resources, Purdue University, West Lafayette, IN, USA

    Brian P. Rinner & John W. Bickham

  2. Center for the Environment, Purdue University, West Lafayette, IN, USA

    Brian P. Rinner & John W. Bickham

  3. Center for the Environmental Implications of NanoTechnology (CEINT), Duke University, Durham, NC, USA

    Cole W. Matson

  4. Sumgayit Centre for Environmental Rehabilitation, Sumgayit, Azerbaijan

    Arif Islamzadeh

  5. School of Rural Public Health, Texas A&M University, College Station, TX, USA

    Thomas J. McDonald

  6. Department of Veterinary Anatomy and Public Health, Texas A&M University, College Station, TX, USA

    Kirby C. Donnelly

Authors
  1. Brian P. Rinner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cole W. Matson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arif Islamzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Thomas J. McDonald
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kirby C. Donnelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John W. Bickham
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John W. Bickham.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rinner, B.P., Matson, C.W., Islamzadeh, A. et al. Evolutionary toxicology: contaminant-induced genetic mutations in mosquitofish from Sumgayit, Azerbaijan. Ecotoxicology 20, 365–376 (2011). https://doi.org/10.1007/s10646-010-0587-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-010-0587-8

Keywords

Search

Navigation