Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Subjects

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.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

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.

Data availability

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

References

  1. Gould, S. J. Wonderful Life: The Burgess Shale and the Nature of History (W.W. Norton & Co., 1990).

  2. Johnson, M. T. & Munshi-South, J. Evolution of life in urban environments. Science 358, eaam8327 (2017).

    Article  Google Scholar 

  3. Fernández-Juricic, E. Bird community composition patterns in urban parks of Madrid: the role of age, size and isolation. Ecol. Res. 15, 373–383 (2000).

    Article  Google Scholar 

  4. Munshi-South, J. Urban landscape genetics: canopy cover predicts gene flow between white-footed mouse (Peromyscus leucopus) populations in New York City. Mol. Ecol. 21, 1360–1378 (2012).

    Article  Google Scholar 

  5. Beninde, J. et al. Cityscape genetics: structural versus functional connectivity of an urban lizard population. Mol. Ecol. 25, 4984–5000 (2016).

    Article  Google Scholar 

  6. Miranda, A. C., Schielzeth, H., Sonntag, T. & Partecke, J. Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity? Glob. Change Biol. 19, 2634–2644 (2013).

    Article  Google Scholar 

  7. van Dongen, W. F. D., Robinson, R. W., Weston, M. A., Mulder, R. A. & Guay, P. Variation at the DRD4 locus is associated with wariness and local site selection in urban black swans. BMC Evol. Biol. 15, 253 (2015).

    Article  Google Scholar 

  8. Badyaev, A. V., Young, R. L., Oh, K. P. & Addison, C. Evolution on a local scale: developmental, functional, and genetic bases of divergence in bill form and associated song structure between adjecent habitats. Evolution 62, 1951–1964 (2008).

    Article  Google Scholar 

  9. Winchell, K. M., Reynolds, R. G., Prado-Irwin, S. R., Puente-Rolón, A. R. & Revell, L. J. Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution 70, 1009–1022 (2016).

    Article  Google Scholar 

  10. Brans, K. I. et al. Eco-evolutionary dynamics in urbanized landscapes: evolution, species sorting and the change in zooplankton body size along urbanization gradients. Philos. Trans. R. Soc. B 372, 20160030 (2016).

    Article  Google Scholar 

  11. Diamond, S. E., Chick, L., Perez, A. B. E., Strickler, S. A. & Martin, R. A. Rapid evolution of ant thermal tolerance across an urban-rural temperature cline. Biol. J. Linn. Soc. 121, 248–257 (2017).

    Article  Google Scholar 

  12. Harris, S. E. & Munshi-South, J. Signatures of positive selection and local adaptation to urbanization in white-footed mice (Peromyscus leucopus). Mol. Ecol. 26, 6336–6350 (2017).

    Article  CAS  Google Scholar 

  13. Huey, RaymondB. & Webster, P. T. Thermal biology of Anolis lizards in a complex fauna: the christatellus group on Puerto Rico. Ecology 57, 985–994 (1976).

    Article  Google Scholar 

  14. Huey, R. B. Behavioral thermoregulation in lizards: importance of associated costs. Science 184, 1001–1002 (1974).

    Article  Google Scholar 

  15. Winchell, K. M., Maayan, I., Fredette, J. R. & Revell, L. J. Linking locomotor performance to morphological shifts in urban lizards. Proc. R. Soc. B 285, 20180229 (2018).

    Article  Google Scholar 

  16. Oke, T. City size and the urban heat island. Atmos. Environ. 7, 769–779 (1973).

    Article  Google Scholar 

  17. Angiletta, M. J. et al. Urban physiology: city ants possess high heat tolerance. PLoS ONE 2, e258 (2007).

    Article  Google Scholar 

  18. Diamond, S. E. et al. Evolution of thermal tolerance and its fitness consequences: parallel and non-parallel responses to urban heat islands across three cities. Proc. R. Soc. B 285, 20180036 (2018).

    Article  Google Scholar 

  19. Cowles, R. & Bogert, C. A. Preliminary study of the thermal requirements of desert reptiles. Bull. Am. Mus. Nat. Hist. 83, 265–296 (1944).

    Google Scholar 

  20. Cho, H. Y. et al. Assembly of multi-tRNA synthetase complex via heterotetrameric glutathione transferase-homology domains. J. Biol. Chem. 290, 29313–29328 (2015).

    Article  CAS  Google Scholar 

  21. Anderson, L. L., Mao, X., Scott, B. A. & Crowder, C. M. Survival from hypoxia in C. elegans by inactivation of aminoacyl-tRNA synthetases. Science 323, 630–634 (2009).

    Article  CAS  Google Scholar 

  22. Yachdav, G. et al. PredictProtein—an open resource for online prediction of protein structural and functional features. Nucleic Acids Res. 42, 337–343 (2014).

    Article  Google Scholar 

  23. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).

    Article  Google Scholar 

  24. Langfelder, P. & Horvath, S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinform. 9, 559 (2008).

    Article  Google Scholar 

  25. Levis, N. A. & Pfennig, D. W. Evaluating ‘plasticity-first’ evolution in nature: key criteria and empirical approaches. Trends Ecol. Evol. 31, 563–574 (2016).

    Article  Google Scholar 

  26. Muñoz, M. M. et al. Evolutionary stasis and lability in thermal physiology in a group of tropical lizards. Proc. R. Soc. B 281, 20132433 (2014).

    Article  Google Scholar 

  27. Homer, C. G. et al. Completion of the 2011 National Land Cover Database for the conterminous United States representing a decade of land cover change information. Photogramm. Eng. Remote Sensing 81, 345–354 (2015).

    Google Scholar 

  28. Fick, S. E. & Hijmans, R. J. Worldclim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).

  29. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  Google Scholar 

  30. Alföldi, J. et al. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477, 587–591 (2011).

    Article  Google Scholar 

  31. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

    Article  Google Scholar 

  32. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

    Article  CAS  Google Scholar 

  33. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).

    Article  CAS  Google Scholar 

  34. Yates, A. et al. Ensembl 2016. Nucleic Acids Res. 44, D710–D716 (2016).

  35. McKenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

    Article  CAS  Google Scholar 

  36. Jombart, T. & Ahmed, I. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27, 3070–3071 (2011).

    Article  CAS  Google Scholar 

  37. Alexander, D. H., Novembre, J. & Lange, K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655–1664 (2009).

    Article  CAS  Google Scholar 

  38. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156–2158 (2011).

    Article  CAS  Google Scholar 

  39. Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A. & Cresko, W. A. Stacks: an analysis tool set for population genomics. Mol. Ecol. 22, 3124–3140 (2013).

    Article  Google Scholar 

  40. Weir, B. S. Genetic Data Analysis II: Methods for Discrete Population Genetic Data (Sinauer Associates, 1996).

  41. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300 (1995).

    Google Scholar 

Download references

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

Authors
  1. Shane C. Campbell-Staton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristin M. Winchell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolas C. Rochette
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jason Fredette
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Inbar Maayan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rena M. Schweizer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Julian Catchen
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

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

Reporting Summary

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-020-1131-8

This article is cited by

Search

Advanced search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research