Environmental Science and Pollution Research

, Volume 20, Issue 11, pp 7666–7679 | Cite as

Evidence of population genetic effects in Peromyscus melanophrys chronically exposed to mine tailings in Morelos, Mexico

  • Patricia Mussali-Galante
  • Efraín Tovar-Sánchez
  • Mahara Valverde
  • Leticia Valencia-Cuevas
  • E. Rojas
Research Article


Effects of environmental chemical pollution can be observed at all levels of biological organization. At the population level, genetic structure and diversity may be affected by exposure to metal contamination. This study was conducted in Huautla, Morelos, Mexico in a mining district where the main contaminants are lead and arsenic. Peromyscus melanophrys is a small mammal species that inhabits Huautla mine tailings and has been considered as a sentinel species. Metal bioaccumulation levels were examined by inductively coupled plasma mass spectrometry and genetic analyses were performed using eight microsatellite loci in 100 P. melanophrys individuals from 3 mine tailings and 2 control sites. The effect of metal bioaccumulation levels on genetic parameters (population and individual genetic diversity, genetic structure) was analyzed. We found a tissue concentration gradient for each metal and for the bioaccumulation index. The highest values of genetic differentiation (Fst and Rst) and the lowest number of migrants per generation (Nm) were registered among the exposed populations. Genetic distance analyses showed that the most polluted population was the most genetically distant among the five populations examined. Moreover, a negative and significant relationship was detected between genetic diversity (expected heterozygosity and internal relatedness) and each metal concentration and for the bioaccumulation index in P. melanophrys. This study highlights that metal stress is a major factor affecting the distribution and genetic diversity levels of P. melanophrys populations living inside mine tailings. We suggest the use of genetic population changes at micro-geographical scales as a population level biomarker.


Small mammals Peromyscus melanophrys Metals Mine tailings Genetic diversity Genetic structure Bioaccumulation 



This study was supported by a scolarship to P.M.G. (102684) by the National Council of Science and Technology (CONACyT).This paper constitutes a partial fulfillment of the Graduate Program in Biological Sciences of the National Autonomous University of México (UNAM). The authors thank the “Posgrado en Ciencias Biológicas, Universidad Nacional Autónoma de México (UNAM). We also thank Edith Rivas, Guillermo Sánchez, Evodio Rendon Alquicira, Guadalupe Rangel Altamirano and Laura Márquez for their technical assistance.


  1. Amos W, Worthington W, Fullard K, Burger TM, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc Lond B 68:2021–2027CrossRefGoogle Scholar
  2. Antolin MF, Van Horne B, Berger MD, Holloway AK, Roach JL, Weeks RD (2001) Effective population size and genetic structure of a Piute ground squirrel (Spermophilus mollis) population. Can J Zool 79:26–34Google Scholar
  3. Arif I, Khan H (2009) Molecular markers for biodiversity analysis of wildlife animals: a brief review. Animal Biodiv Conserv 32:9–17Google Scholar
  4. Belfiore N, Anderson S (1998) Genetic patterns as a tool for monitoring and assessment of environmental impacts: the example of genetic ecotoxicology. Environ Monit Assess 51:465–479CrossRefGoogle Scholar
  5. Belfiore N, Anderson S (2001) Effects of contaminants on genetic patterns in aquatic organisms: a review. Mutat Res 489:97–122CrossRefGoogle Scholar
  6. Bengtsson G, Nordström S, Rundgren S (1983) Population density and tissue metal concentration of lumbricids in forest soils near a brass mill. Environ Pollut A 30:87–108CrossRefGoogle Scholar
  7. Benton M, Malott M, Trybula J, Dean D, Guttman S (2002) Genetic effects of mercury contamination on aquatic snail populations: allozyme genotypes and DNA strand breakage. Environ Toxicol Chem 21:584–589CrossRefGoogle 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 24:2898–2907CrossRefGoogle Scholar
  9. Bernard A (2008) Biomarkers of metal toxicity in population studies: research potential and interpretation issues. J Toxicol Environ Health Part A 71:1259–1265CrossRefGoogle Scholar
  10. Berthier K, Galan M, Foltete JC, Charbonnel N, Cosson JF (2005) Genetic structure of the cyclic fossorial water voles (Arvicola terrestris): landscape and demographic influences. Mol Ecol 14:2861–2871CrossRefGoogle Scholar
  11. Berthier K, Charbonnel N, Galan M, Cosson JF (2006) Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Mol Ecol 15:2665–2676CrossRefGoogle Scholar
  12. Bervoets L, Blust R (2003) Metal concentrations in water, sediment and gudgeon (Gobio gobio) from a pollution gradient: relationship with fish condition factor. Environ Pollut 126:9–19CrossRefGoogle Scholar
  13. Bickham JW (2011) The four cornerstones of evolutionary toxicology. Ecotoxicology 20:497–502CrossRefGoogle Scholar
  14. Bickham J, Smolen M (1994) Somatic and heritable effects of environmental genotoxins and the emergence of evolutionary toxicology. Environ Health Persp 102:25–28CrossRefGoogle Scholar
  15. Bickham J, Sandhu S, Hebert P, Chikhi L, Athwal R (2000) Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat Res 463:33–51CrossRefGoogle Scholar
  16. Bourret V, Couture P, Campbell P, Bernatchez L (2008) Evolutionary ecotoxicology of wild yellow perch (Percha flavescens) populations chronically exposed to a polymetallic gradient. Aquat Toxicol 86:76–90CrossRefGoogle Scholar
  17. Brooks S, Lyon B, Goodsir F, Bignell J, Thain J (2009) Biomarker responses in mussels, an integrated approach to biological effects measurements. J Toxicol Env Health A 72:196–208CrossRefGoogle Scholar
  18. Brown AR, Hosken DJ, Balloux F, Bickley LK, LePage G, Owen SF, Hetheridge MJ, Tyler CR (2009) Genetic variation, inbreeding and chemical exposure–combined effects in wildlife and critical considerations for ecotoxicology. Phil Trans R Soc B 364:3377–3390CrossRefGoogle Scholar
  19. Burger J (1995) Heavy metal and selenium levels in feathers of herring gulls (Larus argentatus): differences due to year, gender, and age at Captree, Long Island. Environ Monit Assess 38:37–50CrossRefGoogle Scholar
  20. Burger J, Gochfeld M (1996) Heavy metal and selenium levels in Franklin’s gull (Larus pipixcan): parents and their eggs. Arch Environ Contam Toxicol 30:487–491CrossRefGoogle Scholar
  21. Cadena M (2003) Efecto de la perturbación y estacionalidad en la comunidad de roedores en una salva baja caducifolia en Morelos, México. Dissertation. Universidad de las Américas de Puebla.Google Scholar
  22. Carleton MD, Musser GG (2005) Order Rodentia. In: Wilson DE, Reeder DM (eds) Mammal species of the world a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore, pp 894–1531Google Scholar
  23. Chirhart S, Honeycutt R, Greenbaum I (2000) Microsatellite markers for the deer mouse Peromyscus maniculatus. Mol Ecol 9:1661–1686CrossRefGoogle Scholar
  24. Chirhart S, Honeycutt R, Greenbaum I (2005) Microsatellite variation and evolution in the Peromyscus maniculatus species group. Molec Phylogenet Evol 34:408–415CrossRefGoogle Scholar
  25. Coues E (1874) Synopsis of the Muridae in North America. Proc Acad Nat Sci Phila 3:173–196Google Scholar
  26. Dauwe T, Janssens E, Kempenaers B, Eens M (2004) The effect of heavy metal exposure on egg size, eggshell thickness and the number of spermatozoa in blue tit Parus caeruleus eggs. Environ Pollut 129:125–129CrossRefGoogle Scholar
  27. Deng J, Liao B, Ye M, Deng D, Lan C, Shu W (2007) The effects of heavy metal pollution on genetic diversity in zinc/cadmium hyperaccumulator Sedum alfredii populations. Plant Soil 297:83–92CrossRefGoogle Scholar
  28. Dmowski K, Kozakiewicz M, Kozakiewicz A (1995) Ecological effects of heavy metal pollution (Pb, Cd, Zn) on small mammal populations and communities. B Pol Acad Biol Sci 43:1–10Google Scholar
  29. Dorado O, Maldonado B, Arias D, Sorani V, Ramírez R, Leyva E (2005) Programa de conservación y manejo Reserva de la Biosfera Sierra de Huautla. Comisión Nacional de Áreas Naturales. Protegidas, MéxicoGoogle Scholar
  30. EPA Environmental Protection Agency (2000). Innovative remediation technologies: Field scale demonstration projects in North AmericaGoogle Scholar
  31. Erry BV, Macnair MR, Meharg AA, Shore RF (2000) Arsenic contamination in wood mice (Apodemus sylvaticus) and bank voles (Clethrionomys glareolus) on abandoned mine sites in southwest Britain. Environ Pollut 110:179–187CrossRefGoogle Scholar
  32. 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 131:479–491Google Scholar
  33. Folkeson L, Nyholm HEI, Tyler G (1990) Influence of acidity and other soil properties on metal concentrations in forest plants and animals. Sci Total Environ 96:211–233CrossRefGoogle Scholar
  34. Fratini S, Zane L, Ragionieri L, Vannini M, Cannicc S (2008) Relationship between heavy metal accumulation and genetic variability decrease in the intertidial crab Pachygrapsus marmoratus (Decapoda; Grapsidae). Estuar Coast Shelf S 79:679–686CrossRefGoogle Scholar
  35. Gardeström J, Dahl U, Kotsalainen O, Maxson A, Elfwing T, Grahn M, Bengtsson B, Breitholtz M (2008) Evidence of population genetic effects of long-term exposure to contaminated sediments: a multi-endpoint study with copepods. Aquat Toxicol 86:426–436CrossRefGoogle Scholar
  36. Gardner-Santana LC, Norris DE, Fornadel CM, Hinson ER, Klein SL, Glass GE (2009) Comensal ecology, urban landscapes and their influence on the genetic characteristics of city-dwelling Norway rats (Rattus norvegicus). Mol Ecol 18:2766–2778CrossRefGoogle Scholar
  37. Gauffre B, Estoup A, Bretagnolle V, Cosson F (2008) Spatial correlation structure of a small rodent in heterogeneous landscape. Mol Ecol 17:4619–4629CrossRefGoogle Scholar
  38. Hall ER (1981) The mammals of North America. John Wiley and Sons, New YorkGoogle Scholar
  39. Hebert PM, Murdoch-Luiker M (1996) Genetic effects of contaminant exposure-towards an assessment of impacts on animal populations. Sci Total Environ 191:23–58CrossRefGoogle Scholar
  40. INEGI (2004) Instituto Nacional de Estadística y Geografía. Información Geográfica del Estado de. Morelos, MéxicoGoogle Scholar
  41. INEGI (2009) Instituto Nacional de Estadística y Geografía. Información Geográfica del Estado de. Morelos, MéxicoGoogle Scholar
  42. Jiang ZF, HuangSZ HYL, Zhao JZ, Fu JJ (2011) Physiological response of Cu mine tailing remediation of Paulownia fortunei (Seem) Hemsl. Ecotoxicology dpoi:. doi: 10.1007/s10646-011-0836-5
  43. Kim S, Rodriguez M, Suh J, Song J (2003) Emergent effects of heavy metal pollution at a population level: Littorina brevicula a study case. Mar Pollut Bull 46:74–80CrossRefGoogle Scholar
  44. Klaper R, Rees CH, Drevnick P, Weber D, Sandheinrich M, Carvan M (2006) Gene expression changes related to endocrine function and decline in reproduction in fathead minnow (Pimephales promelas) after dietary methylmercury exposure. Environ Health Perspect 114:1337–1343CrossRefGoogle Scholar
  45. Lande R (1988) Genetics and demography in biological conservation. Science 241:455–1460CrossRefGoogle Scholar
  46. Laurinolli M, Bendell-Young L (1996) Copper, zinc, and cadmium concentrations in Peromyscus maniculatus sampled near an abandoned copper mine. Environ Contam Toxicol 30:481–486CrossRefGoogle Scholar
  47. Layne JN (1968) Ontogeny. In: King JA (ed) Biology of Peromyscus (Rodentia). The American Society of Mammalogists, Provo, Utah, pp 148–253, Publication number 2Google Scholar
  48. Lefèbvre C, Vernet P (1990) Microevolutionary processes on contaminated deposits. In: Shaw J (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press, Boca Raton, pp 285–300Google Scholar
  49. Levengood J, Heske E (2008) Heavy metal exposure, reproductive activity, and demographic patterns in white-footed mice (Peromyscus leucopus) inhabiting a contaminated wetland. Sci Total Environ 389:320–328CrossRefGoogle Scholar
  50. Lynch M, Conery J, Burger R (1995) Mutation accumulation and the extinction of small populations. Am Nat 146:489–518CrossRefGoogle Scholar
  51. Ma W, Denneman W, Faber J (1991) Hazardous exposure of ground-living small mammals to cadmium and lead in contaminated terrestrial ecosystems. Arch Environ Contam Toxicol 20:266–270CrossRefGoogle Scholar
  52. Maes GE, Raeymaekers JAM, Pampoulie C, Seynaeve A, Goemans G, Belpaire C, Volckaert FAM (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 73:99–114CrossRefGoogle Scholar
  53. Mares MA, Ernest KA (1995) Population and community ecology of small mammals in a gallery forest of central Brazil. J Mammal 76:750–768CrossRefGoogle Scholar
  54. Matson C, Lambert M, McDonald T, Autenrieth R, Donnelly K, Islamzadeh A, Politov D, Bickham J (2006) Evolutionary toxicology: population-level effects of chronic contaminant exposure on the marsh frogs (Rana ridibunda) of Azerbaijan. Environ Health Persp 114:547–552CrossRefGoogle Scholar
  55. Medina M, Correa J, Barata C (2007) Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere 67:2105–2114CrossRefGoogle Scholar
  56. Miller MP (2000) Tools for populations genetic analyses (TFPGA) 1.3: A window program for the analyses of allozyme and molecular population genetic data computer software distributed by author.Google Scholar
  57. Mills SL, Allendorf FW (1996) The one-migrant-per-generation rule in conservation and management. Coserv Biol 10:150–158Google Scholar
  58. Morales EO, Carrillo FC (2010) Plan municipal de desarrollo de Tlaquiltenango, Morelos. H. Ayuntamiento de Tlaquiltenango, Morelos. Accessed 19 September 2012
  59. Morgan AJ, Kille P, Sturzenbaum SR (2007) Microevolution and ecotoxicology of metals in invertebrates. Environ Sci Technol 41:1085–1096CrossRefGoogle Scholar
  60. Mossman CA, Waser PM (2001) Effects of habitat fragmentation on population genetic structure in the white-footed mouse (Peromyscus leucopus). Can J Zool 79:285–295Google Scholar
  61. Mullen L, Hirschmann R, Prince K, Glenn T, Dewey M, Hoekstra H (2006) Sixty polymorphic microsatellite markers for the old field mouse developed in Peromyscus polionotus and Peromyscus maniculatus. Mol Ecol Notes 6:36–40CrossRefGoogle Scholar
  62. Mussali-Galante P (2008) Estudio sobre la inducción de daño al ADN en sangre periférica de individuos expuestos a metales en al agua de bebida, en la población de Huautla, Morelos. Dissertation, Universidad Nacional Autónoma de MéxicoGoogle Scholar
  63. Nacci D, Hoffman GR (2008) Genetic variation in population-level ecological risk assessment. In: Barnthouse LW, Munns WR, Sorensen MT Jr (eds) Population-level ecological risk assessment. Taylor and Francis, New York, pp 93–112Google Scholar
  64. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590Google Scholar
  65. Page RDM (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358Google Scholar
  66. Pascoe GA, Blanchet RJ, Linder G, Lande R (1994) Bioavailability of metals and arsenic to small mammals at a mining waste-contaminated wetland. Genetics and demography in biological conservation. Science 241:455–1460Google Scholar
  67. Peakall DB (1992) Animal biomarkers as pollution indicators, Ecotoxicological Series No.1. Chapman & Hall, LondonCrossRefGoogle Scholar
  68. Peakall R, Lindenmayer D (2006) Genetic insights into population recovery following experimental perturbation in a fragmented landscape. Biol Conserv 132:520–532CrossRefGoogle Scholar
  69. Peakall R, Ruibal M, Lindmeyer D (2003) Spatial correlation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:118–295Google Scholar
  70. Phelps KL, McBee K (2009) Ecological characteristics of small mammal communities at a superfund site. Amer Midl Nat 161:57–68CrossRefGoogle Scholar
  71. Pra D, Rech-Frenke SI, Giulian R, Yoneama ML, Ferraz-Diaz J, Erdtmann B, Pegas-Henriques JA (2008) Genotoxicity and mutagenicity of iron and copper in mice. Biometals 21:289–297CrossRefGoogle Scholar
  72. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  73. Ricketts HJ, Morgan AJ, Spurgeon DJ, Kille P (2004) Measurement of annetocin gene expression: a new reproductive biomarker in earthworm ecotoxicology. Ecotox Environ Safety 57:4–10CrossRefGoogle Scholar
  74. Rogstad S, Keane B, Collier M (2003) Minisatellite DNA mutation rate in dandelions increases with leaf-tissue concentrations of Cr, Fe, Mn, and Ni. Environ Toxicol Chem 22:2093–2099CrossRefGoogle Scholar
  75. Rzedowski J (2006) Vegetación de México. Fondo de Cultura Económica, MexicoGoogle Scholar
  76. Sánchez CH, Romero MLA (1992) Mastofauna silvestre del ejido el Limón, municipio de Tepalcingo, Morelos. Univ Cienc Tec 2:87–95Google Scholar
  77. Scheirs J, Coan A, Covaci A, Beernaert J, Kayawe M, Caturla M, Wolf H, Baert P, Van Oostveldt P, Verhagen R, Blust R, Coen W (2006) Genotoxicity in wood mice (Apodemus sylvaticus) along a pollution gradient: exposure age and gender-related effects. Environ Toxicol Chem 25:2154–2162CrossRefGoogle Scholar
  78. Secretaría de Economía (2011) Panorama minero del Estado de Morelos. Servicio Geológico Mexicano, serie panorama minero de los estados, MexicoGoogle Scholar
  79. Sheffield SR, Sawicka-Kapusta K, Cohen JB, Rattner BA (2001) Rodentia and Lagomorpha. In: Shore RF, Rattner BA (eds) Ecotoxicology of wild mammals. John Wiley and Sons, New York, pp 215–314Google Scholar
  80. Shore RF, Douben PE (1994) Predicting ecotoxicological impacts of environmental contaminants on terrestrial small mammals. Rev Environ Contam T 134:49–89CrossRefGoogle Scholar
  81. Shugart L, Theodorakis C (1998) New trends in biological monitoring: application of biomarkers to genetic ecotoxicology. Biotherapy 11:119–127CrossRefGoogle Scholar
  82. Smith PN, Cobba GP, Harper FM, Adair BM, McMurry ST (2002) Comparison of white-footed mice and rice rats as biomonitors of polychlorinated biphenyl and metal contamination. Environ Pollut 119:261–268CrossRefGoogle Scholar
  83. Sneath PHA, Sokal RR (1973) Numerical taxonomy. The principles and practice of numerical classification. WH Freeman, San Francisco, 573 pGoogle Scholar
  84. Sommer S (2003) Effects of habitat fragmentation and changes of dispersal behavior after a recent population decline on the genetic variability of noncoding and coding DNA of a monogamous Malagasy rodent. Mol Ecol 12:2845–2851CrossRefGoogle Scholar
  85. Staton J, Schizas N, Chandler G, Coull B, Quattro J (2001) Ecotoxicology and population genetics: the emergence of “phylogeographic and evolutionary ecotoxicology”. Ecotoxicology 10:217–222CrossRefGoogle Scholar
  86. Statsoft (2000) Statistica for Windows, v. 5.1. Computer program manual. Tulsa, StatSoft IncGoogle Scholar
  87. Stockley P, Searle JB, Macdonald DW, Jones CS (1993) Female multiple mating behavior in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond B 254:173–179CrossRefGoogle Scholar
  88. Swofford DL, Olsen GJ (1990) Phylogeny reconstruction. In: Moritz C, Hillis DM (eds) Molecular systematics. Sinauer Associated Inc, Massachusetts, pp 411–501Google Scholar
  89. Theodorakis C (2001) Integration of genotoxic and population genetic endpoints in biomonitoring and risk assessment. Ecotoxicology 10:245–256CrossRefGoogle Scholar
  90. Tovar-Sánchez E, Cervantes LT, Martínez C, Rojas E, Valverde M, Ortiz-Hernández ML, Mussali-Galante P (2012) Comparison of two wild rodent species as sentinels of environmental contamination by mine tailings. Environ Sci Pollut Res 19:1677–1686CrossRefGoogle Scholar
  91. Ungherese G, Mengoni A, Somigli S, Baroni D, Focardi S, Ugolini A (2010) Relationship between heavy metals pollution and genetic diversity in Mediterranean population of the sandhopper Talitrus saltator (Montagu) (Crustaceae, Amphipoda). Environ Pollut 158:1638–1643CrossRefGoogle Scholar
  92. Valavanidis A, Vlachogianni T (2010) Metal pollution in ecosystems: ecotoxicology studies and risk assessment in the marine environment. Sci Adv Environ Toxicol Ecotox Issues.
  93. Van de Zande L, Van Apeldoorn RC, Blijdenstein AF, De Jong D, Van Delden W, Bijlsma R (2000) Microsatellite analysis of population structure and genetic differentiation within and between population of the root vole, Microtus oeconomus in the Netherlands. Mol Ecol 9:1651–1656CrossRefGoogle Scholar
  94. Van Straalen N (1999) Genetic biodiversity in toxicant-stressed populations. Prog Environ Sci 1:195–201Google Scholar
  95. Van Straalen N, Timmermans M (2002) Genetic variation in toxicant-stressed populations: an evaluation of the “genetic erosion” hypothesis. Hum Ecol Risk Assess 8:983–1002CrossRefGoogle Scholar
  96. Vargas V (2010) Estructura genética del roedor Baiomys musculus (Muridae) en la selva seca caducifolia en el estado de Morelos. Dissertation. Universidad Autónoma del Estado de MorelosGoogle Scholar
  97. Volke ST, Velasco TA, De la Rosa PA, Solórzano OG (2004) Evaluación de tecnologías de remediación para suelos contaminados con metales. Etapa I. Secretaría de Medio Ambiente y Recursos Naturales, MexicoGoogle Scholar
  98. Volke ST, Velasco TA, De la Rosa PA, Solórzano OG (2005) Evaluación de tecnologías de remediación para suelos contaminados con metales. Etapa II. Secretaría de Medio Ambiente y Recursos Naturales, MexicoGoogle Scholar
  99. Vucetich LM, Vucetich JA, Cleckner LB, Gorski PR, Peterson RO (2001) Mercury concentrations in deer mouse (Peromyscus maniculatus) tissues from Isle Royale National Park. Environ Pollut 114:11–38CrossRefGoogle Scholar
  100. Weber JN, Peters M, Tsyusko O, Linnen C, Hagen C, Schable N, Tuberville T, Mckee A, Lance S, Jones K, Fisher H, Dewey M, Hoekstra H, Glenn C (2010) Five hundred microsatellite loci for Peromyscus. Conserv Genet 11:1243–1246CrossRefGoogle Scholar
  101. Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer Associated Inc, MassachusettsGoogle Scholar
  102. Werre F, Ortiz-Hernández L (2000) Monografía geologica-minera del estado de Morelos. Consejo de Recursos Minerales, MexicoGoogle Scholar
  103. WHO World Health Organization (2007) Health risks of heavy metals from long range transboundary air pollution. WHO Regional Office for Europe, CopenhagenGoogle Scholar
  104. Yap CK, Tan SG, Ismail A, Omar H (2004) Allozyme polymorphisms and heavy metal levels in the green-lipped mussel Perna viridis (Linnaeus) collected from contaminated and uncontaminated sites in Malaysia. Environ Inter 30:39–46CrossRefGoogle Scholar
  105. Yap CK, Chua BH, Teh CH, Tan SG, Ismail A (2007) Primers of RAPD markers and heavy metal concentrations in Perna viridis (L.), collected from metal-contaminated and uncontaminated coastal waters: are they correlated with each other? Russian J Genet 43:544–550CrossRefGoogle Scholar
  106. Yap CK, Chong CM, Tan SG (2011) Allozyme polymorphism in the horseshoe crabs Carcinoscorpius rotundicauda collected from polluted intertidal area in Peninsular Malaysia. Environ Monit Assess 174:389–400CrossRefGoogle Scholar
  107. Yeh FC, Yang R, Boyle T (1999) PopGene Ver. 1.31. University of Alberta, CanadaGoogle Scholar
  108. Zar J (2010) Biostatistical analysis. Prentice-Hall, New-JerseyGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  • Patricia Mussali-Galante
    • 1
  • Efraín Tovar-Sánchez
    • 2
  • Mahara Valverde
    • 1
  • Leticia Valencia-Cuevas
    • 2
  • E. Rojas
    • 1
  1. 1.Departamento de Medicina Genómica y Toxicología Ambiental, Instituto de Investigaciones BiomédicasUniversidad Nacional Autónoma de MéxicoMéxicoMexico
  2. 2.Departamento de Sistemática y Evolución, Centro de Investigación en Biodiversidad y ConservaciónUniversidad Autónoma del Estado de MorelosMorelosMexico

Personalised recommendations