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Evidence of micro-evolution in Crocidura russula from two abandoned heavy metal mines: potential use of Cytb, CYP1A1, and p53 as gene biomarkers

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Abstract

Heavy metals accumulated in the environment due to the mining industry may impact on the health of exposed wild animals with consequences at the population level via survival and selection of the most resistant individuals. The detection and quantification of shifts in gene frequencies or in the genetic structure in populations inhabiting polluted sites may be used as early indicators of environmental stress and reveal potential ‘candidate gene biomarkers’ for environmental health assessment. We had previously observed that specimens of the Greater white-toothed shrew (Crocidura russula) from two heavy metal mines in Southern Portugal (the Aljustrel and the Preguiça mines) carried physiological alterations compared to shrews from an unpolluted site. Here, we further investigated whether these populations showed genetic differences in genes relevant for physiological homeostasis and/or that are associated with pathways altered in animals living under chronic exposure to pollution, and which could be used as biomarkers. We analysed the mitochondrial cytochrome b (Cytb) gene and intronic and/or exonic regions of four nuclear genes: CYP1A1, LCAT, PRPF31, and p53. We observed (1) population differences in allele frequencies, types of variation, and diversity parameters in the Cytb, CYP1A1, and p53 genes; (2) purifying selection of Cytb in the mine populations; (3) genetic differentiation of the two mine populations from the reference by the p53 gene. Adding to our previous observations with Mus spretus, we provide unequivocal evidence of a population effect exerted by the contaminated environment of the mines on the local species of small mammals.

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Data availability

Sequence data have been deposited in GenBank with accession numbers MZ962272-MZ962313. Additional information on sequence data is available from the figshare repository, at https://doi.org/10.6084/m9.figshare.16553997.

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Acknowledgements

The authors would like to acknowledge the helpful comments from an anonymous reviewer. We are also grateful to Vítor Sousa and Octávio S. Paulo for helping in data analyses.

Author contributions

ASQ and MLM conceived and designed the study. Material preparation, experimental work, and statistical analysis were performed by ASQ and AFD. The first draft of the paper was written by ASQ and all authors commented on previous versions of the paper. All authors read and approved the final paper.

Funding

By Fundação para a Ciência e a Tecnologia/Ministério da Ciência, Tecnologia e Ensino Superior (FCT/MCTES) to CESAM (UIDP/50017/2020+UIDB/50017/2020), through national funds. By national funds (OE), through FCT, in the scope of the framework contract foreseen in the numbers 4, 5, and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19, to ASQ.

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Correspondence to Ana Sofia Quina.

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The authors declare no competing interests.

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All samples used in this study were from a pre-existing collection, and were previously documented and published. The sacrifice of wild animals for the purpose of taking samples was performed under strict accordance with ethical directive 86/609/EEC on the protection of animals used for scientific purposes.

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Quina, A.S., Durão, A.F. & Mathias, M.d.L. Evidence of micro-evolution in Crocidura russula from two abandoned heavy metal mines: potential use of Cytb, CYP1A1, and p53 as gene biomarkers. Ecotoxicology 30, 1969–1982 (2021). https://doi.org/10.1007/s10646-021-02472-9

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  • DOI: https://doi.org/10.1007/s10646-021-02472-9

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