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Parallel selection on thermal physiology facilitates repeated adaptation of city lizards to urban heat islands

Nature Ecology & Evolution volume 4, pages 652–658 (2020)Cite this article

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Abstract

Only recently have we begun to understand the ecological and evolutionary effects of urbanization on species, with studies revealing drastic impacts on community composition, gene flow, behaviour, morphology and physiology. However, our understanding of how adaptive evolution allows species to persist, and even thrive, in urban landscapes is still nascent. Here, we examine phenotypic, genomic and regulatory impacts of urbanization on a widespread lizard, the Puerto Rican crested anole (Anolis cristatellus). We find that urban lizards endure higher environmental temperatures and display greater heat tolerance than their forest counterparts. A single non-synonymous polymorphism within a protein synthesis gene (RARS) is associated with heat tolerance plasticity within urban heat islands and displays parallel signatures of selection in cities. Additionally, we identify groups of differentially expressed genes between habitats showing elevated genetic divergence in multiple urban–forest comparisons. These genes display evidence of adaptive regulatory evolution within cities and disproportionately cluster within regulatory modules associated with heat tolerance. This study provides evidence of temperature-mediated selection in urban heat islands with repeatable impacts on physiological evolution at multiple levels of biological hierarchy.

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Fig. 1: Urban lizards experience higher temperatures and display great heat tolerance than their forest counterparts.
Fig. 2: Chromosome 1 of the crested anole genome contains a region with significantly higher levels of genetic divergence than genome-wide average.
Fig. 3: A single non-synonymous variant within arginyl tRNA synthetase is associated with greater heat tolerance in urban habitats.
Fig. 4: Evidence of adaptive regulatory divergence between lizards in urban and forest habitats.

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Data availability

Sequence and metadata associated with this study have been deposited at NCBI under project no. PRJNA592594.

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Acknowledgements

We thank Z. Cheviron, N. Senner, M. Stager and J. Velotta for comments and insights that were valuable in the development of this project. We are grateful to the many people who helped in the laboratory, with animal care and in the field, in particular: K. Aviles-Rodriguez, E. Boates, D. Briggs, Q. Quach and K. Schliep.

Author information

Author notes

  1. These authors contributed equally: Shane C. Campbell-Staton, Kristin M. Winchell.

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA

    Shane C. Campbell-Staton & Nicolas C. Rochette

  2. Institute for Society and Genetics, University of California, Los Angeles, CA, USA

    Shane C. Campbell-Staton

  3. Biology Department, University of Massachusetts Boston, Boston, MA, USA

    Kristin M. Winchell & Jason Fredette

  4. Department of Biology, Washington University, St. Louis, MO, USA

    Kristin M. Winchell

  5. Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA

    Inbar Maayan

  6. Division of Biological Sciences, University of Montana, Missoula, MT, USA

    Rena M. Schweizer

  7. Department of Animal Biology, University of Illinois, Champaign-Urbana, IL, USA

    Julian Catchen

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  1. Shane C. Campbell-Staton
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Contributions

S.C.C.-S. and K.M.W. conceived the project design. S.C.C.-S., K.M.W., J.F. and I.M. performed thermal experiments. K.M.W. produced common garden data. S.C.C. and R.M.S. performed RNA-seq expression analyses. S.C.C.-S. and N.C.R. performed analyses of sequence data. S.C.C.-S., K.M.W., N.C.R., J.F., I.M., R.M.S. and J.C. participated in writing the manuscript.

Corresponding author

Correspondence to Shane C. Campbell-Staton.

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Supplementary Information

Supplemental methods, results, discussion, Figs. 1–20 and Tables 1–4.

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Campbell-Staton, S.C., Winchell, K.M., Rochette, N.C. et al. Parallel selection on thermal physiology facilitates repeated adaptation of city lizards to urban heat islands. Nat Ecol Evol 4, 652–658 (2020). https://doi.org/10.1038/s41559-020-1131-8

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