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AMBIO

, Volume 44, Issue 3, pp 194–203 | Cite as

Adaptive evolution in urban ecosystems

  • Colin M. Donihue
  • Max R. LambertEmail author
Perspective
First Online:

Abstract

Urban ecologists have demonstrated that cities are functioning ecosystems. It follows then that species living in these contexts should participate in and experience the same suite of biological processes, including evolution, that have occupied scientists for centuries in more “natural” contexts. In fact, urban ecosystems with myriad novel contexts, pressures, and species rosters provide unprecedentedly potent evolutionary stimuli. Here, we present the case for studying adaptive evolution in urban settings. We then review and synthesize techniques into a coherent approach for studying adaptive evolution in urban settings that combines observations of phenotypic divergence, measurements of fitness benefits of novel genetically based phenotypes, and experimental manipulations of potential drivers of adaptation. We believe that studying evolution in urban contexts can provide insights into fundamental evolutionary biology questions on rate, direction, and repeatability of evolution, and may inform species and ecosystem service conservation efforts.

Keywords

Anthropocene Cities Ecosystem services Evolutionary ecology Experimental evolution Urbanization 
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Notes

Acknowledgments

We thank the School of Forestry and Environmental Studies for financial support and colleagues for informal discussions that influences our thinking. C. Stockwell and an anonymous reviewer made valuable contributions to the final draft.

References

  1. Alberti, M., J.M. Marzluff, E. Schulenberger, G. Bradley, C. Ryan, and C. Zumbrunnen. 2003. Integrating humans into ecology: Opportunities and challenges for studying urban ecosystems. BioScience 53: 1169–1179.CrossRefGoogle Scholar
  2. Angilletta Jr, M.J., R.S. Wilson, A.C. Niehaus, M.W. Sears, C.A. Navas, and P.L. Ribeiro. 2007. Urban physiology: Urban ants possess high heat tolerance. PLoS One 2(2): e258. doi: 10.1371/journal.pone.0000258.CrossRefGoogle Scholar
  3. Bjorklund, M., I. Ruiz, and J.C. Senar. 2010. Genetic differentiation in the urban habitat: The great tits (Parus major) of the parks of Barcelona city. Biological Journal of the Linnean Society 99: 9–19.CrossRefGoogle Scholar
  4. Blanquart, F., O. Kaltz, S.L. Nuismer, and S. Gandon. 2013. A practical guide to measuring local adaptation. Ecology Letters 16: 1195–1205.CrossRefGoogle Scholar
  5. Brady, S.P. 2012. Road to evolution? Local adaptation to road adjacency in an amphibian (Ambystoma maculatum). Scientific Reports 2: 235. doi: 10.1038/srep00235.CrossRefGoogle Scholar
  6. Burghardt, K.T., D.W. Tallamy, and W.G. Shriver. 2008. Impact of native plants on bird and butterfly biodiversity in suburban landscapes. Conservation Biology 23: 219–224.CrossRefGoogle Scholar
  7. Cheptou, P.O., O. Carrue, S. Rouifed, and A. Cantarel. 2008. Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proceedings of the National Academy of Sciences 105: 3796–3799.CrossRefGoogle Scholar
  8. Clarke, K.M., B.L. Fisher, and G. LeBuhn. 2008. The influence of urban park characteristics on ant (Hymenoptera, Formicidae) communities. Urban Ecosystems 11: 317–334.CrossRefGoogle Scholar
  9. Cothran, R.D., J.M. Brown, and R.A. Relyea. 2013. Proximity to agriculture is correlated with pesticide tolerance: Evidence for the evolution of amphibian resistance to modern pesticides. Evolutionary Applications 6: 832–841.CrossRefGoogle Scholar
  10. Danchin, E., L.A. Giraldeau, and F. Cezilly. 2008. Behavioural ecology. New York: Oxford University Press Inc.Google Scholar
  11. Endler, J.A. 1986. Natural selection in the wild. Princeton: Princeton University Press.Google Scholar
  12. Evans, K.L., K.J. Gaston, A.C. Frantz, M. Simeoni, S.P. Sharp, A. McGowan, D.A. Dawson, K. Walasz, et al. 2009. Independent colonization of multiple urban centres by a formerly forest specialist bird species. Proceedings of the Royal Society B 276: 2403–2410.CrossRefGoogle Scholar
  13. Faeth, S.H., P.S. Warren, E. Shochat, and W.A. Marussich. 2005. Trophic dynamics in urban communities. BioScience 55: 399–407.CrossRefGoogle Scholar
  14. Felson, A.J., E.E. Oldfield, and M.A. Bradford. 2013. Involving ecologists in shaping large-scale green infrastructure projects. BioScience 63: 882–890.CrossRefGoogle Scholar
  15. Garland Jr, T., and M.R. Rose. 2009. Experimental evolution. Berkeley: University of California Press.Google Scholar
  16. Grant, P.R., and B.R. Grant. 2002. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296: 707–711.CrossRefGoogle Scholar
  17. Grimm, N.B., S.H. Faeth, N.E. Golubiewski, C.L. Redman, J. Wu, X. Bai, and J.M. Briggs. 2008. Global change and the ecology of cities. Science 319: 756–760.CrossRefGoogle Scholar
  18. Groffman, P.M., J. Cavender-Bares, N.D. Bettez, J.M. Grove, S.J. Hall, J.B. Heffernan, S.E. Hobbie, K. Larson, et al. 2014. Ecological homogenization of urban USA. Frontiers in Ecology and the Environment 12: 74–81.CrossRefGoogle Scholar
  19. Hairston Jr, N.G., S.P. Ellner, M.A. Geber, T. Yoshida, and J.A. Fox. 2005. Rapid evolution and the convergence of ecological and evolutionary time. Ecology Letters 8: 1114–1127.CrossRefGoogle Scholar
  20. Harris, S.E., J. Munshi-South, C. Obergfell, and R. O’Neill. 2013. Signatures of rapid evolution in urban and rural transcriptomes of white-footed mice (Peromyscus leucopus) in the New York metropolitan area. PLoS One 8: e74938. doi: 10.1371/journal.pone.0074938.CrossRefGoogle Scholar
  21. Hendry, A.P., and M.T. Kinnison. 1999. The pace of modern life: Measuring rates of contemporary microevolution. Evolution 53: 1637–1653.CrossRefGoogle Scholar
  22. Hitchings, S.P., and T.J.C. Beebee. 1998. Loss of genetic diversity and fitness in common toad (Bufo bufo) populations isolated by inimical habitat. Journal of Evolutionary Biology 11: 269–283.Google Scholar
  23. Kareiva, P., and M. Marvier. 2012. What is conservation science? BioScience 62: 962–969.CrossRefGoogle Scholar
  24. Kettlewell, H.B.D. 1955. Selection experiments on industrial melanism in the Lepidoptera. Heredity 9: 323–342.CrossRefGoogle Scholar
  25. Kinzig, A.P., P. Warren, C. Martin, D. Hope, and M. Katti. 2005. The effects of human socioeconomic status and cultural characteristics on urban patterns of biodiversity. Ecology and Society 10: 23.Google Scholar
  26. Klerks, P.L., and J.S. Levinton. 1989. Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biological Bulletin 176: 135–141.CrossRefGoogle Scholar
  27. Knapp, S., L. Dinsmore, C. Fissore, S.E. Hobbie, I. Jakobsdottir, J. Kattge, J.Y. King, S. Klotz, et al. 2012. Phylogenetic and functional characteristics of household yard floras and their changes along an urbanization gradient. Ecology 93: S83–S98.CrossRefGoogle Scholar
  28. Lambert, M.R., S.N. Nielsen, A.N. Wright, R.C. Thomson, and H.B. Shaffer. 2013. Habitat features determine the basking distribution of introduced red-eared sliders and native western pond turtles. Chelonian Conservation and Biology 12: 192–199.CrossRefGoogle Scholar
  29. Lande, R., and S.J. Arnold. 1983. The measurement of selection on correlated characters. Evolution 37: 1210–1226.CrossRefGoogle Scholar
  30. Leinonen, T., R.J. Scott McCairns, R.B. O’Hara, and J. Merila. 2013. QST–FST comparisons: Evolutionary and ecological insights from genomic heterogeneity. Nature Reviews Genetics 14: 179–190.CrossRefGoogle Scholar
  31. Levinton, J.S., E. Suatoni, W. Wallace, R. Junkins, B. Kelaher, and B.J. Allen. 2003. Rapid loss of genetically based resistance to metals after the cleanup of a Superfund site. Proceedings of the National Academy of Sciences 100: 9889–9891.CrossRefGoogle Scholar
  32. Losos, J.B. 2009. Lizards in an evolutionary tree. Ecology and adaptive radiation of Anoles. Berkeley: University of California Press.Google Scholar
  33. Losos, J.B., K.I. Warheit, and T.W. Schoener. 1997. Adaptive differentiation following experimental island colonization in Anolis lizards. Nature 387: 70–73.CrossRefGoogle Scholar
  34. Loss, S.R., M.O. Ruiz, and J.D. Brawn. 2009. Relationships between avian diversity, neighborhood age, income, and environmental characteristics of an urban landscape. Biology Conservation 142: 2578–2585.CrossRefGoogle Scholar
  35. McKinney, M.L. 2008. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosystems 11: 161–176.CrossRefGoogle Scholar
  36. Merila, J., and A.P. Hendry. 2014. Climate change, adaptation, and phenotypic plasticity: The problem and the evidence. 2014. Evolutionary Applications 7: 1–14.CrossRefGoogle Scholar
  37. Millennium Ecosystem Assessment (MEA). 2005. Ecosystems and human well-being: Synthesis. Washington, DC: World Resources Institute.Google Scholar
  38. Mueller, J.C., J. Partecke, B.J. Hatchewell, K.J. Gaston, and K.L. Evans. 2013. Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Molecular Ecology 22: 3629–3637.CrossRefGoogle Scholar
  39. Munshi-South, J. 2012. Urban landscape genetics: canopy cover predicts gene flow between white-footed mouse (Peromyscus leucopus) populations in New York City. Molecular Ecology 21: 1360–1378.CrossRefGoogle Scholar
  40. Munshi-South, J., and K. Kharchenko. 2010. Rapid, pervasive genetic differentiation or urban white-footed mouse (Peromyscus leucopus) populations in New York City. Molecular Ecology 19: 4242–4254.CrossRefGoogle Scholar
  41. Munshi-South, J., Y. Zak, and E. Pehek. 2013. Conservation genetics of extremely isolated urban populations of the northern dusky salamander (Desmognathus fuscus) in New York City. Peer J 1: e64. doi: 10.7717/peerj.64.CrossRefGoogle Scholar
  42. Noel, S., M. Ouellet, P. Galois, and F.J. Lapointe. 2007. Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander. Conservation Genetics 8: 599–606.CrossRefGoogle Scholar
  43. Palkovacs, E.P., B.A. Wasserman, and M.T. Kinnison. 2011. Eco-evolutionary trophic dynamics: Loss of top predators drives trophic evolution and ecology of prey. PLoS One 6(4): e18879. doi: 10.1371/journal.pone.0018879.CrossRefGoogle Scholar
  44. Partecke, J., and E. Gwinner. 2007. Increased sedentariness in European blackbirds following urbanization: A consequence of local adaptation? Ecology 88: 882–890.CrossRefGoogle Scholar
  45. Partecke, J., I. Schwabl, and E. Gwinner. 2006. Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87: 1945–1952.CrossRefGoogle Scholar
  46. Post, D.M., and E.P. Palkovacs. 2009. Eco-evolutionary feedbacks in community and ecosystem ecology: Interactions between the ecological theatre and the evolutionary play. Philosophical Transactions of the Royal Society B 364: 1629–1640.CrossRefGoogle Scholar
  47. Rasanen, K.R., A. Laurila, and J. Merila. 2003. Geographic variation in acid stress tolerance of the moor frog, Rana arvalis. I. Local adaptation. Evolution 57: 352–362.CrossRefGoogle Scholar
  48. Rees, M., J.H. Roe, and A. Georges. 2009. Life in the suburbs: behavior: behavior and survival of a freshwater turtle in response to drought and urbanization. Biological Conservation 142: 3172–3181.CrossRefGoogle Scholar
  49. Reznick, D.A., H. Bryga, and J.A. Endler. 1990. Experimentally induced life-history evolution in a natural population. Nature 346: 357–359.CrossRefGoogle Scholar
  50. Schmitz, O.J. 2010. Resolving ecosystem complexity. Princeton: Princeton University Press.CrossRefGoogle Scholar
  51. Schochat, E. 2004. Credit or debit? Resource input changes population dynamics of city-slicker birds. Oikos 106: 622–626.CrossRefGoogle Scholar
  52. Schochat, E., P.S. Warren, S.H. Faeth, N.E. McIntyre, and D. Hope. 2006. From patterns to emerging processes in mechanistic urban ecology. Trends in Ecology & Evolution 21: 186–191.CrossRefGoogle Scholar
  53. Seto, K.C., R. Sanchez-Rodriguez, and M. Fragkias. 2010. The new geography of contemporary urbanization and the environment. Annual Review of Environmental Resources 35: 167–194.CrossRefGoogle Scholar
  54. Skinner, M.K. 2011. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenetics 6: 838–842.CrossRefGoogle Scholar
  55. Slabbekoorn, H., and M. Peet. 2003. Birds sing at a higher pitch in urban noise. Nature 424: 267.CrossRefGoogle Scholar
  56. Stearns, S.C. 1983. A natural experiment in life-history evolution: Field data on the introduction of mosquitofish (Gambusia affinis) to Hawaii. Nature 37: 601–617.Google Scholar
  57. Stearns, S.C., and R.F. Hoekstra. 2001. Evolution: an introduction. New York: Oxford University Press.Google Scholar
  58. Stockwell, C.A., A.P. Hendry, and M.T. Kinnison. 2003. Contemporary evolution meets conservation biology. Trends in Ecology & Evolution 18: 94–101.CrossRefGoogle Scholar
  59. Storz, J.F. 2005. Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology 14: 671–688.CrossRefGoogle Scholar
  60. Walsh, C.J., A.H. Roy, J.W. Feminella, P.D. Cottingham, P.M. Groffman, and R.P. Morgan II. 2005. The urban stream syndrome: Current knowledge and the search for a cure. Journal of the North American Benthological Society 24: 706–723.CrossRefGoogle Scholar
  61. Watkins, R., J. Palmer, and M. Kolokotroni. 2007. Increased temperature and intensification of the urban heat island: Implications for human comfort and urban design. Built Environment 33: 85–96.CrossRefGoogle Scholar
  62. West-Eberhard, M.J. 1989. Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics 20: 249–278.CrossRefGoogle Scholar
  63. Whitehead, A., D.A. Triant, D. Champlin, and D. Nacci. 2010. Comparative transcriptomics implicates mechanisms of evolved pollution tolerance in a killifish population. Molecular Ecology 19: 5186–5203.CrossRefGoogle Scholar
  64. Yeh, P.J. 2004. Rapid evolution in a sexually selected trait following population establishment in a novel habitat. Evolution 58: 166–174.CrossRefGoogle Scholar

Copyright information

© Royal Swedish Academy of Sciences 2014

Authors and Affiliations

  1. 1.School of Forestry and Environmental Studies, Greeley LaboratoryYale UniversityNew HavenUSA

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