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Contamination acts as a genotype-dependent barrier to gene flow, causing genetic erosion and fine-grained population subdivision in Mussels from the Strait of Istanbul

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Abstract

This study provides evidence of fine-grained genetic structuring in Mediterranean mussels (Mytilus galloprovincialis) from the Strait of Istanbul, caused by barriers to gene flow via contaminant-mediated selection. In this study, mitochondrial D-loop sequences were analyzed in mussels from 8 localities, all less than 30 kilometers apart, with differing contaminant loads. The results were: 1) Intra-population genetic differentiation (ΦST) between sites with high and low contaminant loads was high (up to 0.459), even at distances of only a few kilometers. 2) Genetic diversity was negatively correlated with the contaminant load (“genetic erosion”). 3) There was evidence of selection, based on haplotype frequencies and neutrality tests (Tajima’s D), with purifying selection at the most contaminated site and balancing selection at the least contaminated. 4) Genetic distance was not correlated with geographic distance (no isolation-by-distance), but was correlated with contaminant load at each site. 5) Population dendrograms and Bayesian estimators of migration indicated that gene flow between sites was affected by contamination. For the dendrograms of the sampling sites, the clades clustered according to contaminant load more than geographic distance. Overall, these results suggest that 1) contamination may serve as a genotype-dependent dispersal barrier (i.e., contamination may not affect total number of migrants, just the relative proportions of the haplotypes in the established immigrants), leading strong population differentiation over short distances, and 2) genetic erosion may occur by a combination of selection and altered patterns of haplotype-specific gene flow. These effects may be more pronounced in the Strait of Istanbul than in other locations because of the riverine nature and strong, uni-directional current of the strait.

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Acknowledgements

This paper is dedicated to the memory of Lee R. Shugart (December 23, 1931–September 20, 2021; Theodorakis et al. 2021). The authors would like to thank Southern Illinois University Edwardsville for funding a sabbatical project for C. Theodorakis; and Helmholz Zentrum, Istanbul Technical University, and Southern Illinois University Edwardsville for use of equipment and facilities; and the University of Illinois UIUC Core Sequencing Facility for a copy of Sequencher 5.0. The authors would also like to thank Dr. David Duvernell, SIUE (presently at University of Missouri Rolla), for assistance with and advice on genetic analyses, an anonymous Turkish youth for help in collecting samples from Site A, and an anonymous Turkish gentleman for assistance in collecting samples from Site C.

Funding

The work was supported, in part by the Genome Analysis Center (GAC) of the Helmholtz Zentrum München headed by Prof. Adamski, and by Southern Illinois University Edwardsville.

Author information

Authors and Affiliations

  1. Department of Environmental Sciences, Southern Illinois University Edwardsville, Edwardsville, IL, 62026-1099, USA

    Christopher W. Theodorakis

  2. Department of Biological Sciences, Southern Illinois University Edwardsville, Edwardsville, IL, 62026-1651, USA

    Christopher W. Theodorakis & Mary-Ann Meyer

  3. Faculty of Naval Architecture and Ocean Engineering, Istanbul Technical University, Maslak, Sarıyer, 34469, Istanbul, Turkey

    Oya Okay & Sevil Deniz Yakan

  4. Molecular EXposomics, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH), Ingolstädter Landstraße 1, 85764, Neuherberg, Germany

    Karl-Werner Schramm

  5. Department für Biowissenschaften, TUM, Wissenschaftszentrum Weihenstephan für Ernährung, Landnutzung und Umwelt, Weihenstephaner Steig 23, 85350, Freising, Germany

    Karl-Werner Schramm

Authors
  1. Christopher W. Theodorakis
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  2. Mary-Ann Meyer
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  3. Oya Okay
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  4. Sevil Deniz Yakan
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  5. Karl-Werner Schramm
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Contributions

CWT collected the mussels, conducted DNA extractions and sequencing reactions, analyzed some of the data, wrote most of the manuscript. M-AM analyzed much of the data, wrote some of the MS. OO assisted with the mussel collection and provided laboratory space and some supplies and reagents for dissection and DNA extraction. SDY assisted with the mussel collection and dissection and DNA extraction in the laboratory. K-WS provided laboratory space, supplies and reagents for DNA analysis, and funds for sequencing at the Helmholz core sequencing facility.

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Correspondence to Christopher W. Theodorakis.

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Theodorakis, C.W., Meyer, MA., Okay, O. et al. Contamination acts as a genotype-dependent barrier to gene flow, causing genetic erosion and fine-grained population subdivision in Mussels from the Strait of Istanbul. Ecotoxicology 33, 47–65 (2024). https://doi.org/10.1007/s10646-023-02725-9

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