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Effects of urban-induced mutations on ecology, evolution and health

Nature Ecology & Evolution (2024)Cite this article

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Abstract

Increasing evidence suggests that urbanization is associated with higher mutation rates, which can affect the health and evolution of organisms that inhabit cities. Elevated pollution levels in urban areas can induce DNA damage, leading to de novo mutations. Studies on mutations induced by urban pollution are most prevalent in humans and microorganisms, whereas studies of non-human eukaryotes are rare, even though increased mutation rates have the potential to affect organisms and their populations in contemporary time. Our Perspective explores how higher mutation rates in urban environments could impact the fitness, ecology and evolution of populations. Most mutations will be neutral or deleterious, and higher mutation rates associated with elevated pollution in urban populations can increase the risk of cancer in humans and potentially other species. We highlight the potential for urban-driven increased deleterious mutational loads in some organisms, which could lead to a decline in population growth of a wide diversity of organisms. Although beneficial mutations are expected to be rare, we argue that higher mutation rates in urban areas could influence adaptive evolution, especially in organisms with short generation times. Finally, we explore avenues for future research to better understand the effects of urban-induced mutations on the fitness, ecology and evolution of city-dwelling organisms.

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Fig. 1: Global concentrations and composition of mutagenic and carcinogenic pollutants.
Fig. 2: The potential for elevated mutation rates in cities to affect the evolution of a population relative to a fitness optimum.
Fig. 3: Potential biosentinel species for studying urban-associated mutations.

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Acknowledgements

The ideas for this Perspective were developed over several workshops and meetings, including the Urban Eco-Evo Research Coordination Network (NSF DEB-184063), the ‘Satellite Workshop on Urban Evolutionary and Ecological “Omics”’ funded by the Society of Molecular Biology and Evolution, and the Center for Biological Data Science at Virginia Commonwealth University. M.T.J.J. was supported by an NSERC Steacie Fellowship, a Canada Research Chair and an NSERC Discovery Grant. C.L.Y. was supported by a Canada Research Chair and, along with F.M., a Burroughs Wellcome Fund Innovations in Regulatory Sciences Award. D.N.A. was supported by a Plant Resilience Institute Fellowship from Michigan State University. E.J.C. was funded by NSF DBI-2109587 and the Living Earth Collaborative at Washington University in St. Louis. M.P.-R. (DEB-2332998) and W.B. (DEB-1754394) received funding from the National Science Foundation. C.G.L. was funded by ANID PIA/BASAL FB0002. J.G. was supported by grant PID2020-115874GB-I00 funded by MCIN/AEI/10.13039/501100011033 and by grant 2021 SGR 00417 funded by Departament de Recerca i Universitats, Generalitat de Catalunya. M.S. was supported by NCN Opus grant 2021/41/B/NZ8/04472.

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Authors and Affiliations

  1. Centre for Urban Environments, University of Toronto Mississauga, Mississauga, Ontario, Canada

    Marc T. J. Johnson, Irtaqa Arif, Rob W. Ness, Aude E. Caizergues & Madeleine Oman

  2. Department of Biology, University of Toronto Mississauga, Mississauga, Ontario, Canada

    Marc T. J. Johnson, Irtaqa Arif, Rob W. Ness, Aude E. Caizergues & Madeleine Oman

  3. Environmental Health Science and Research Bureau, Health Canada, Ottawa, Ontario, Canada

    Francesco Marchetti

  4. Department of Biology and Louis Calder Center, Fordham University, Armonk, NY, USA

    Jason Munshi-South

  5. Institute of Evolutionary Biology, Faculty of Biology, Biological and Chemical Research Centre, University of Warsaw, Warsaw, Poland

    Marta Szulkin

  6. Center for Biological Data Science, Virginia Commonwealth University, Richmond, VA, USA

    Brian C. Verrelli & Michael S. Rosenberg

  7. Department of Biology, University of Ottawa, Ottawa, Ontario, Canada

    Carole L. Yauk

  8. Department of Plant Biology, Department of Entomology, Plant Resilience Institute, Michigan State University, East Lansing, MI, USA

    Daniel N. Anstett

  9. Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA, USA

    Warren Booth

  10. Living Earth Collaborative, Washington University in St. Louis, St. Louis, MO, USA

    Elizabeth J. Carlen

  11. Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ, USA

    Anthony Dant

  12. Institute of Evolutionary Biology, CSIC, UPF, Barcelona, Spain

    Josefa González

  13. Departamento de Ciencias, Facultad de Artes Liberales, Universidad Adolfo Ibáñez, Santiago, Chile

    César González Lagos

  14. Center of Applied Ecology and Sustainability (CAPES), Santiago, Chile

    César González Lagos

  15. Department of Biology, Drexel University, Philadelphia, PA, USA

    Megan Phifer-Rixey

  16. School of Biological Sciences, University of California, San Diego, La Jolla, CA, USA

    Diana J. Rennison

  17. Department of Biology, New York University, New York, NY, USA

    Kristin M. Winchell

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  1. Marc T. J. Johnson
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Contributions

M.T.J.J. conceived and led the project. All authors (M.T.J.J., I.A., F.M., J.M.-S., R.W.N., M.S., B.C.V., C.L.Y., D.N.A., W.B., A.E.C., E.J.C., A.D., J.G., C.G.L., M.O., M.P.-R., D.J.R., M.S.R. and K.M.W.) contributed to brainstorming the ideas covered in the paper, and the original outline was written by the lead team members (F.M., J.M.-S., R.W.N., M.S., B.C.V. and C.L.Y.). I.A., M.T.J.J., F.M., J.M.-S., R.W.N., M.S., B.C.V., K.M.W. and C.L.Y. led the writing of specific sections and/or the preparation of the figures and tables. All remaining authors (D.N.A., W.B., A.E.C., E.J.C., A.D., J.G., C.G.L., M.O., M.P.-R., D.J.R., M.S.R. and K.M.W.) contributed to one or more sections, and all authors (M.T.J.J., I.A., F.M., J.M.-S., R.W.N., M.S., B.C.V., C.L.Y., D.N.A., W.B., A.E.C., E.J.C., A.D., J.G., C.G.L., M.O., M.P.-R., D.J.R., M.S.R. and K.M.W.) edited the final drafts of the paper.

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Correspondence to Marc T. J. Johnson.

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Johnson, M.T.J., Arif, I., Marchetti, F. et al. Effects of urban-induced mutations on ecology, evolution and health. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02401-z

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