{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,9,28]],"date-time":"2025-09-28T15:28:28Z","timestamp":1759073308550},"reference-count":43,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,12,16]],"date-time":"2019-12-16T00:00:00Z","timestamp":1576454400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,12,16]],"date-time":"2019-12-16T00:00:00Z","timestamp":1576454400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Chemical contamination may cause genetic erosion in natural populations by wiping out the most sensitive genotypes. This is of upmost concern if the loss of genetic variability is irreversible due to contaminant-driven elimination of alleles, which may happen if tolerance is a recessive or incompletely dominant trait \u2013 the recessive tolerance inheritance (working-) hypothesis. Accordingly, this work investigated the tolerance inheritance to lethal levels of a metal-rich acid mine drainage (AMD) and to copper sulphate in a population of<jats:italic>Pelophylax perezi<\/jats:italic>. Time-to-death for each egg, after being exposed to 60% of a sample of acid mine drainage and to 9\u2009mg\/L Cu, was registered, and, for each egg mass, the median lethal time (LT<jats:sub>50<\/jats:sub>) and respective quartiles (LT<jats:sub>25<\/jats:sub>and LT<jats:sub>75<\/jats:sub>) were computed. Results suggested that genetically determined tolerance could be probably driven by incomplete dominance (with possible maternal effect influence), preliminarily supporting the initial hypothesis.<\/jats:p>","DOI":"10.1038\/s41598-019-55838-9","type":"journal-article","created":{"date-parts":[[2019,12,16]],"date-time":"2019-12-16T11:03:32Z","timestamp":1576494212000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Genetically inherited tolerance may unveil trait dominance patterns in an amphibian model"],"prefix":"10.1038","volume":"9","author":[{"given":"E.","family":"Fasola","sequence":"first","affiliation":[]},{"given":"R.","family":"Ribeiro","sequence":"additional","affiliation":[]},{"given":"I.","family":"Lopes","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2019,12,16]]},"reference":[{"issue":"5","key":"55838_CR1","doi-asserted-by":"publisher","first-page":"983","DOI":"10.1080\/1080-700291905783","volume":"8","author":"N Van Straalen","year":"2002","unstructured":"Van Straalen, N. & Timmermans, M. Genetic Variation in Toxicant-Stressed Populations: An Evaluation of the \u2018Genetic Erosion\u2019 Hypothesis. Human and Ecological Risk Assessment: An International Journal 8(5), 983\u20131002 (2002).","journal-title":"Human and Ecological Risk Assessment: An International Journal"},{"key":"55838_CR2","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1016\/j.envpol.2015.04.027","volume":"204","author":"E Fasola","year":"2015","unstructured":"Fasola, E., Ribeiro, R. & Lopes, I. Microevolution Due to Pollution in Amphibians: A Review on the Genetic Erosion Hypothesis. Environmental Pollution 204, 181\u201390 (2015).","journal-title":"Environmental Pollution"},{"issue":"5","key":"55838_CR3","doi-asserted-by":"publisher","first-page":"889","DOI":"10.1007\/s10646-013-1070-0","volume":"22","author":"R Ribeiro","year":"2013","unstructured":"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 22(5), 889\u201399 (2013).","journal-title":"Ecotoxicology"},{"issue":"2","key":"55838_CR4","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/S0166-445X(98)00039-3","volume":"42","author":"C Barata","year":"1998","unstructured":"Barata, C., Baird, D. & Markich, S. Influence of Genetic and Environmental Factors on the Tolerance of Daphnia Magna Straus to Essential and Non-Essential Metals. Aquatic Toxicology 42(2), 115\u201337 (1998).","journal-title":"Aquatic Toxicology"},{"key":"55838_CR5","doi-asserted-by":"crossref","unstructured":"Hoffmann, A. & Parsons, P. Evolutionary Genetics and Environmental Stress. Oxford, UK. Oxford University Press (1991).","DOI":"10.1093\/oso\/9780198577324.001.0001"},{"key":"55838_CR6","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1007\/BF00127250","volume":"84","author":"M Macnair","year":"1991","unstructured":"Macnair, M. Why the Evolution of Resistance to Anthropogenic Toxins Normally Involves Major Gene Changes: The Limits to Natural Selection. Genetica 84, 213\u2013219 (1991).","journal-title":"Genetica"},{"key":"55838_CR7","doi-asserted-by":"crossref","unstructured":"Macnair, M. The Evolution of Plants in Metal-Contaminated Environments. In Environmental Stress Adaptation and Evolution, by Bijlsma R. and Loeschcke V., ed. Birkhauser Verlag. Basel, Switzerland, 3\u201324 (1997).","DOI":"10.1007\/978-3-0348-8882-0_1"},{"issue":"5","key":"55838_CR8","first-page":"441","volume":"50","author":"A Haridi","year":"1974","unstructured":"Haridi, A. Linkage Studies on DDT and Dieldrin Resistance in Species A and Species B of the Anopheles gambiae Complex. Bulletin of the World Health Organization 50(5), 441\u201348 (1974).","journal-title":"Bulletin of the World Health Organization"},{"key":"55838_CR9","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1038\/nrg2339","volume":"9","author":"A Hoffmann","year":"2008","unstructured":"Hoffmann, A. & Willi, Y. Detecting Genetic Responses to Environmental Change. Nature Reviews Genetic 9, 431\u201332 (2008).","journal-title":"Nature Reviews Genetic"},{"key":"55838_CR10","unstructured":"Jagadeesan, R. et al. Inheritance of Resistance to Phosphine in the Rusty Grain Beetle, Cryptolestes ferrugineus (Stephens). In 11th International Working Conference on Stored Product Protection, 453\u201360 (2014)."},{"issue":"3","key":"55838_CR11","doi-asserted-by":"publisher","first-page":"703","DOI":"10.1093\/jee\/84.3.703","volume":"84","author":"Bruce E. Tabashnik","year":"1991","unstructured":"Tabashnik, B. Determining the Mode of Inheritance of Pesticide Resistance with Backcross Experiments. Journal of Economic Enthomology, 703\u201312 (1991).","journal-title":"Journal of Economic Entomology"},{"key":"55838_CR12","doi-asserted-by":"crossref","unstructured":"Lovell, B. & Kearns, C. Inheritance of DDT-Dehydrochlorinase in the House Fly. Journal of Economic Enthomology, 931\u201335 (1959).","DOI":"10.1093\/jee\/52.5.931"},{"key":"55838_CR13","first-page":"53","volume-title":"In The Genetic Consequences of Man Made Change.","author":"R Wood","year":"1981","unstructured":"Wood, R. Insecticide Resistance: Genes and Mechanisms. In The Genetic Consequences of Man Made Change. (pp. 53\u201396. Academic Press, London, UK, 1981)."},{"key":"55838_CR14","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/0022-474X(76)90025-4","volume":"12","author":"J Greaves","year":"1976","unstructured":"Greaves, J., Rennison, B. & Redfern, R. Resistance of the Ship Rat, Rattus rattus L., to Warfarin. Journal of stored products 12, 65\u201370 (1976).","journal-title":"Journal of stored products"},{"key":"55838_CR15","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1017\/S0022172400055078","volume":"76","author":"M Wallace","year":"1976","unstructured":"Wallace, M. & Mac Swiney, F. A Major Gene Controlling Warfarin Resistance in the House Mouse. Journal of Hygene. 76, 173\u201381 (1976).","journal-title":"Journal of Hygene."},{"issue":"1","key":"55838_CR16","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-14-7","volume":"14","author":"D Proestou","year":"2014","unstructured":"Proestou, D., Flight, P., Champlin, D. & Nacci, D. Targeted Approach to Identify Genetic Loci Associated with Evolved Dioxin Tolerance in Atlantic Killifish (Fundulus Heteroclitus). BMC Evolutionary Biology 14(1), 7 (2014).","journal-title":"BMC Evolutionary Biology"},{"key":"55838_CR17","doi-asserted-by":"publisher","first-page":"1322","DOI":"10.1126\/science.1197296","volume":"331","author":"I Wirgin","year":"2011","unstructured":"Wirgin, I. et al. Mechanistic Basis of Resistance to PCBs in Atlantic Tomcod from the Hudson River. Science 331, 1322\u20131325 (2011).","journal-title":"Science"},{"key":"55838_CR18","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1038\/hdy.1992.35","volume":"68","author":"H Schat","year":"1992","unstructured":"Schat, H. & Ten Bookum, W. Genetic Control of Copper Tolerance in Silene vulgaris. Heredity 68, 219\u2013229 (1992).","journal-title":"Heredity"},{"key":"55838_CR19","doi-asserted-by":"crossref","unstructured":"CBD. Convention on Biological Diversity, http:\/\/www.cbd.int\/ (2013).","DOI":"10.4324\/9781315071770"},{"key":"55838_CR20","doi-asserted-by":"publisher","first-page":"2105","DOI":"10.1016\/j.chemosphere.2006.12.024","volume":"67","author":"M Medina","year":"2007","unstructured":"Medina, M., Correa, J. & Barata, C. Micro-Evolution due to Pollution: Possible Consequences for Ecosystem Responses to Toxic Stress. Chemosphere 67, 2105\u201314 (2007).","journal-title":"Chemosphere"},{"key":"55838_CR21","first-page":"5","volume":"57","author":"A Blaustein","year":"2007","unstructured":"Blaustein, A. & Bancroft, B. Amphibian Population Declines: Evolutionary Considerations. BioScience 57, 5 (2007).","journal-title":"BioScience"},{"issue":"1","key":"55838_CR22","doi-asserted-by":"publisher","first-page":"47","DOI":"10.3390\/d2010047","volume":"2","author":"J O\u2019Brien","year":"2010","unstructured":"O\u2019Brien, J. & Allentoft, M. Global Amphibian Declines, Loss of Genetic Diversity and Fitness: A Review. Diversity 2(1), 47\u201371 (2010).","journal-title":"Diversity"},{"issue":"9","key":"55838_CR23","doi-asserted-by":"publisher","first-page":"1877","DOI":"10.1111\/j.1365-294X.2011.05061.x","volume":"20","author":"E Luquet","year":"2011","unstructured":"Luquet, E. et al. Heterozygosity-Fitness Correlations among Wild Populations of European Tree Frog (Hyla arborea) Detect Fixation Load. Molecular Ecology 20(9), 1877\u201387 (2011).","journal-title":"Molecular Ecology"},{"issue":"1","key":"55838_CR24","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1046\/j.1523-1739.2003.01236.x","volume":"17","author":"D Reed","year":"2003","unstructured":"Reed, D. & Frankham, R. Correlation between Fitness and Genetic Diversity. Conservation Biology 17(1), 230\u201337 (2003).","journal-title":"Conservation Biology"},{"key":"55838_CR25","doi-asserted-by":"crossref","unstructured":"Schmeller, D., Schregel, J. & Veith, M. The Importance of Heterozygosity in a Frog\u2019s Life. Naturwissenschaften, 360\u201366 (2007).","DOI":"10.1007\/s00114-006-0205-z"},{"issue":"6","key":"55838_CR26","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1002\/etc.5620150614","volume":"15","author":"S Roark","year":"1996","unstructured":"Roark, S. & Brown, K. Effects of Metal Contamination From Mine Tailings on Allozyme Distributions of Populations of Great Plains Fishes. Environmental Toxicology and Chemistry 15(6), 921\u201327 (1996).","journal-title":"Environmental Toxicology and Chemistry"},{"key":"55838_CR27","doi-asserted-by":"crossref","unstructured":"Parsons, P. Stress-Resistance Genotypes, Metabolic Efficiency and Interpreting Evolutionary Change. In Environmental Stress. Adaptation and Evolution, by Bijlsma R. & Loeschcke V., ed. Birkhauser Verlag. Basel, Switzerland, 291\u2013305 (1997).","DOI":"10.1007\/978-3-0348-8882-0_16"},{"issue":"3","key":"55838_CR28","first-page":"149","volume":"49","author":"W Adlassnig","year":"2013","unstructured":"Adlassnig, W. et al. Amphibians in Metal-Contaminated Habitats. Salamandra 49(3), 149\u201358 (2013).","journal-title":"Salamandra"},{"issue":"5","key":"55838_CR29","doi-asserted-by":"publisher","first-page":"838","DOI":"10.1007\/s10646-013-1079-4","volume":"22","author":"O Sobral","year":"2013","unstructured":"Sobral, O., Marin-Morales, M. & Ribeiro, R. Could Contaminant Induced Mutations Lead to a Genetic Diversity Overestimation? Ecotoxicology 22(5), 838\u201346 (2013).","journal-title":"Ecotoxicology"},{"issue":"1","key":"55838_CR30","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1007\/s00244-003-2143-5","volume":"46","author":"I Lopes","year":"2004","unstructured":"Lopes, I., Baird, D. & Ribeiro, R. Genetic Determination of Tolerance to Lethal and Sublethal Copper Concentrations in Field Populations of Daphnia longispina. Archives of Environmental Contamination and Toxicology 46(1), 43\u201351 (2004).","journal-title":"Archives of Environmental Contamination and Toxicology"},{"key":"55838_CR31","doi-asserted-by":"publisher","unstructured":"Bosch, J., et al. The IUCN Red List of Threatened Species., https:\/\/doi.org\/10.2305\/IUCN.UK.2009.RLTS.T58692A11812894.en.(2001).","DOI":"10.2305\/IUCN.UK.2009.RLTS.T58692A11812894.en"},{"key":"55838_CR32","unstructured":"Almeida, N. et al. Guia FAPAS Dos Anf\u00edbios e R\u00e9pteis de Portugal. Porto, Portugal (2001)."},{"key":"55838_CR33","unstructured":"Arnold, N., Ovenden, D. Reptiles and Amphibians of Britain and Europe. Collins, London, UK, 34\u201335 (2002)."},{"key":"55838_CR34","unstructured":"American Society for Testing and Materials International (ASTM) Standard Guide for Conducting the Frog Embryo Teratogenesis Assay - Xenopus (FETAX). 1439\u20131498 (2004)."},{"issue":"4","key":"55838_CR35","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1002\/jat.2550070403","volume":"7","author":"D Dawson","year":"1987","unstructured":"Dawson, D. & Bantle, J. Development of a reconstituted water medium and preliminary validation of the Frog Embryo Teratogenesis Assay\u2014Xenopus (FETAX). Journal of Applied Toxicology 7(4), 237\u2013244 (1987).","journal-title":"Journal of Applied Toxicology"},{"key":"55838_CR36","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1303\/aez.33.339","volume":"33","author":"M Sakuma","year":"1998","unstructured":"Sakuma, M. Probit Analysis of Preference Data. Applied Entomology and Zoology 33, 339\u2013347 (1998).","journal-title":"Applied Entomology and Zoology"},{"key":"55838_CR37","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1007\/s10646-011-0634-0","volume":"20","author":"M Vandegehuchte","year":"2011","unstructured":"Vandegehuchte, M. & Janssen, C. Epigenetics and its Implications for Ecotoxicology. Ecotoxicology 20, 607\u2013624 (2011).","journal-title":"Ecotoxicology"},{"issue":"1","key":"55838_CR38","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1007\/s00442-005-0177-2","volume":"146","author":"M Dziminski","year":"2005","unstructured":"Dziminski, M. & Alford, R. Patterns and Fitness Consequences of Intraclutch Variation in Egg Provisioning in Tropical Australian Frogs. Oecologia 146(1), 98\u2013109 (2005).","journal-title":"Oecologia"},{"issue":"4","key":"55838_CR39","doi-asserted-by":"publisher","first-page":"546","DOI":"10.1007\/s00442-004-1762-5","volume":"142","author":"K R\u00e4s\u00e4nen","year":"2005","unstructured":"R\u00e4s\u00e4nen, K., Laurila, A. & Meril\u00e4, J. Maternal Investment in Egg Size: Environment and Population-Specific Effects on Offspring Performance. Oecologia 142(4), 546\u201333 (2005).","journal-title":"Oecologia"},{"issue":"10","key":"55838_CR40","doi-asserted-by":"publisher","first-page":"2383","DOI":"10.1002\/etc.5620201034","volume":"20","author":"D Di Toro","year":"2001","unstructured":"Di Toro, D. et al. Biotic Ligand Model of the Acute Toxicity of Metals. 1. Technical Basis. Environmental Toxicology and Ehemistry 20(10), 2383\u201396 (2001).","journal-title":"Environmental Toxicology and Ehemistry"},{"issue":"1","key":"55838_CR41","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1007\/s00114-003-0491-7","volume":"91","author":"T Lod\u00e9","year":"2004","unstructured":"Lod\u00e9, T. & Lesbarr\u00e8res, D. Multiple Paternity in Rana Dalmatina, a Monogamous Territorial Breeding Anuran. Naturwissenschaften 91(1), 44\u201347 (2004).","journal-title":"Naturwissenschaften"},{"key":"55838_CR42","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1038\/nature02879","volume":"431","author":"D Vieites","year":"2004","unstructured":"Vieites, D. et al. Post-Mating Clutch Piracy in an Amphibian. Nature 431, 305\u2013308 (2004).","journal-title":"Nature"},{"key":"55838_CR43","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1111\/j.1095-8312.2005.00521.x","volume":"86","author":"T Lod\u00e9","year":"2005","unstructured":"Lod\u00e9, T., Holveck, M. & Lesbarreres, D. Asynchronous Arrival Pattern, Operational Sex Ratio and Occurrence of Multiple Paternities in a Territorial Breeding Anuran, Rana dalmatina. Biological Journal of the Linnean Society 86, 191\u2013200 (2005).","journal-title":"Biological Journal of the Linnean Society"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-55838-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-55838-9","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-55838-9.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,28]],"date-time":"2024-07-28T18:00:20Z","timestamp":1722189620000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-55838-9"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,12,16]]},"references-count":43,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["55838"],"URL":"https:\/\/doi.org\/10.1038\/s41598-019-55838-9","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,12,16]]},"assertion":[{"value":"7 June 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 November 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 December 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"19179"}}