Abstract
Purpose of Review
Urbanization has the potential to jeopardize the sustainability of populations of organisms living within and dispersing across urban areas. Landscape genetics approaches offer a great promise for quantifying how urban features affect ecological and evolutionary processes for species living within and around cities. In this review, we assess the current state (2015–2020) of urban landscape genetics research, examining what types of urban features are quantified, what genetic measures are used, what species are studied, and in which geographic regions they are conducted. We then make recommendations for future research.
Recent Findings
We identified relatively few landscape genetic studies conducted within urban areas published in the last 5 years. We also found a publication bias towards certain taxa and geographic regions (mainly mammals studied in North America), based on results from relatively few molecular markers. These studies used varied measures of urbanization in their analysis, but the most common was urban land use/land cover measured at different resolutions, followed by buildings/development and transportation infrastructure (roads, railroads, and tramways). The results of these studies reflect previously conducted urban research findings that urban features may inhibit, facilitate, or have no correlation with gene flow, usually a product of which focal taxa is being studied, as well as what urban features are present/measured within variable cityscapes.
Summary
We urge future research to directly measure urban features and stress the need for explicitly sampling within and around urban areas to gain full understanding of whether urbanization impedes, facilitates, or does not affect genetic differentiation between populations. To facilitate the development of robust theory, we urge the formation of a global network of urban landscape geneticists to collaborate and sample diverse taxa, in varied global landscapes and climates, and analyze genome-wide datasets for more robust conclusions about gene flow and genetic diversity. We advocate for analyzing urban features at multiple scales to allow broad conclusions about the effects of urbanization across studies, taxa, and regions. Finally, we recommend that study designs include social, cultural, and economic differences in human land use, which have the potential to affect how species disperse, survive, and reproduce in urban areas. Taking these factors into account, we can make novel advances in understanding how complex urban landscapes shape contemporary evolution.
Similar content being viewed by others
References
Szulkin M, Garroway CJ, Corsini M, Kotarba AZ, Dominoni D. How to quantify urbanization when testing for urban evolution. In: Szulkin M, Munshi-South J, Charmantier A, editors. Urban Evolutionary Biology. 1st ed. Oxford: Oxford University Press; 2020. p. 13–32.
Hulme-Beaman A, Dobney K, Cucchi T, Searle JB. An ecological and evolutionary framework for commensalism in anthropogenic environments. Trends Ecol Evol [Internet]. 2016;31(8):633–45. https://doi.org/10.1016/j.tree.2016.05.001.
Des Roches S, Brans KI, Lambert MR, Rivkin LR, Savage AM, Schell CJ, et al. Socio-Eco-Evolutionary Dynamics in Cities. Evol Appl (under Revis). 2020.
Schell CJ, Dyson K, Fuentes TL, Des Roches S, Harris NC, Miller DS, et al. The ecological and evolutionary consequences of systemic racism in urban environments. Science (80- ) [Internet]. 2020;4497(August):eaay4497 Available from: https://www.sciencemag.org/lookup/doi/10.1126/science.aay4497.
Avolio M, Blanchette A, Sonti NF, Locke DH. Time is not money: income is more important than lifestage for explaining patterns of residential yard plant community structure and diversity in Baltimore. Front Ecol Evol. 2020;8(April):1–14.
Chamberlain DE, Henry DAW, Reynolds C, Caprio E, Amar A. The relationship between wealth and biodiversity: a test of the luxury effect on bird species richness in the developing world. Glob Chang Biol. 2019;25(9):3045–55.
Locke DH, Hall B, Grove JM, Pickett STA, Ogden LA, Aoki C, et al. Residential housing segregation and urban tree canopy in 37 US Cities. SocArXiv. 2020.
Holderegger R, Wagner HH, et al. Bioscience. 2008;58(3):199–207.
Beninde J, Feldmeier S, Werner M, Peroverde D, Schulte U, Hochkirch A, et al. Cityscape genetics: structural vs. functional connectivity of an urban lizard population. Mol Ecol. 2016;25(20):4984–5000.
LaPoint S, Balkenhol N, Hale J, Sadler J, van der Ree R. Ecological connectivity research in urban areas. Funct Ecol. 2015;29(7):868–78.
Rasmussen SL, Nielsen JL, Jones OR, Berg TB, Pertoldi C. Genetic structure of the European hedgehog (Erinaceus europaeus) in Denmark. PLoS One. 2020;15(1):1–21.
Jha S, Kremen C. Urban land use limits regional bumble bee gene flow. Mol Ecol. 2013;22(9):2483–95.
Balbi M, Ernoult A, Poli P, Madec L, Guiller A, Martin MC, et al. Functional connectivity in replicated urban landscapes in the land snail (Cornu aspersum). Mol Ecol. 2018;27(6):1357–70.
Braunisch V, Segelbacher G, Hirzel AH. Modelling functional landscape connectivity from genetic population structure: a new spatially explicit approach. Mol Ecol. 2010;19(17):3664–78.
Gutiérrez-Rodríguez J, Gonçalves J, Civantos E, Martínez-Solano I. Comparative landscape genetics of pond-breeding amphibians in Mediterranean temporal wetlands: the positive role of structural heterogeneity in promoting gene flow. Mol Ecol [Internet]. 2017; [cited 2017 Aug 23]; Available from: http://doi.wiley.com/10.1111/mec.14272.
Serieys LEK, Lea A, Pollinger JP, Riley SPD, Wayne RK. Disease and freeways drive genetic change in urban bobcat populations. Evol Appl. 2015;8(1):75–92.
Combs M, Puckett EE, Richardson J, Mims D, Munshi-South J. Spatial population genomics of the brown rat (Rattus norvegicus) in New York City. Mol Ecol. 2018;27(1):83–98.
Fusco NA, Pehek E, Munshi-South J. Urbanization reduces gene flow but not genetic diversity of stream salamander populations in the New York City metropolitan area. Evol Appl. 2020:0–2.
Carlen E, Munshi-South J. Widespread genetic connectivity of feral pigeons across the Northeastern megacity. Evol Appl. 2020;March:1–13.
Munshi-South J, Richardson JL. Landscape genetic approaches to understanding movement and gene flow in cities (Chapter 4). In: Urban Evolutionary Biology: Oxford University Press; 2020. p. 54–73.
Storfer A, Murphy MA, Spear SF, Holderegger R, Waits LP. Landscape genetics: where are we now? Mol Ecol. 2010;19(17):3496–514.
Zeller KA, McGarigal K, Whiteley AR. Estimating landscape resistance to movement: a review. Landsc Ecol [Internet]. 2012;27(6):777–97 [Cited 2014 Dec 5] Available from: http://link.springer.com/10.1007/s10980-012-9737-0.
Waits LP, Cushman SA, Spear SF. Applications of landscape genetics to connectivity research in terrestrial animals [Chapter 12]. In: Balkenhol N, Cushman SA, Storfer AT, Waits LP, editors. Landscape genetics: concepts, methods, applications: Wiley; 2016. p. 199–219.
Miles LS, Rivkin LR, Johnson MTJ, Munshi-South J, Verrelli BC. Gene flow and genetic drift in urban environments. Mol Ecol. 2019;28(18):4138–51.
Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, et al. Putting the “landscape” in landscape genetics. Heredity (Edinb). 2007;98(3):128–42.
Manel SS, Holderegger R. Ten years of landscape genetics. Trends Ecol Evol. 2013;28(10):614–21.
Richardson JL, Brady SP, Wang IJ, Spear SF. Navigating the pitfalls and promise of landscape genetics. Mol Ecol [Internet]. 2016 [cited 2016 Jan 12];25(4):n/a-n/a. Available from: http://doi.wiley.com/10.1111/mec.13527
Centeno-Cuadros A, Hulva P, Romportl D, Santoro S, Stříbná T, Shohami D, et al. Habitat use, but not gene flow, is influenced by human activities in two ecotypes of Egyptian fruit bat (Rousettus aegyptiacus). Mol Ecol. 2017;26(22):6224–37.
Parks LC, Wallin DO, Cushman SA, McRae BH. Landscape-level analysis of mountain goat population connectivity in Washington and southern British Columbia. Conserv Genet. 2015;16(5):1195–207.
Baudouin G, Bech N, Bagnères AG, Dedeine F. Spatial and genetic distribution of a north American termite, Reticulitermes flavipes. across the landscape of Paris. Urban Ecosyst. 2018;21(4):751–64.
Alvarado-Serrano DF, Van Etten ML, Chang SM, Baucom RS. The relative contribution of natural landscapes and human-mediated factors on the connectivity of a noxious invasive weed. Heredity (Edinb) [Internet]. 2019;122(1):29–40. https://doi.org/10.1038/s41437-018-0106-x.
Arredondo TM, Marchini GL, Cruzan MB. Evidence for human-mediated range expansion and gene flow in an invasive grass. Proc R Soc B Biol Sci. 2018;285:20181125.
Fountain-Jones NM, Craft ME, Funk WC, Kozakiewicz C, Trumbo DR, Boydston EE, et al. Urban landscapes can change virus gene flow and evolution in a fragmentation-sensitive carnivore. Mol Ecol. 2017;26(22):6487–98.
van Rees CB, Reed MJ, Wilson RE, Underwood JG, Sonsthagen SA. Landscape genetics identifies streams and drainage infrastructure as dispersal corridors for an endangered wetland bird. Int J Bus Innov Res. 2018;17(3):8328–43.
Sacks BN, Brazeal JL, Lewis JC. Landscape genetics of the nonnative red fox of California. Ecol Evol. 2016;6(14):4775–91.
Evans MJ, Rittenhouse TAG, Hawley JE, Rego PW, Eggert LS. Spatial genetic patterns indicate mechanism and consequences of large carnivore cohabitation within development. Ecol Evol. 2018;8(10):4815–29.
Homer C, Dewitz J, Yang L, Jin S, Danielson P, Xian G, et al. Completion of the 2011 National Land Cover Database for the conterminous United States-Representing a decade of land cover change information. Photogammetric Eng Remote Sens. 2015;81(5):345–54.
Homer C, Dewitz J, Jin S, Xian G, Costello C, Danielson P, et al. Conterminous United States land cover change patterns 2001–2016 from the 2016 National Land Cover Database. ISPRS J Photogramm Remote Sens. 2020;162(March):184–99.
Nunes de Lima MV. (2005) CORINE Land Cover updating for the year 2000. IMAGE2000 and CLC2000. Products and methods. EC, DG JRC. Institute for Environment and Sustainability.
Kimmig SE, Beninde J, Brandt M, Schleimer A, Kramer-Schadt S, Hofer H, et al. Beyond the landscape: resistance modelling infers physical and behavioural gene flow barriers to a mobile carnivore across a metropolitan area. Mol Ecol. 2020;29(3):466–84.
Adavodi R, Khosravi R, Cushman SA, Kaboli M. Topographical features and forest cover influence landscape connectivity and gene flow of the Caucasian pit viper, Gloydius caucasicus (Nikolsky, 1916), in Iran. Landsc Ecol [Internet]. 2019;34(11):2615–30. https://doi.org/10.1007/s10980-019-00908-6.
Roy CL, Gregory AJ. Landscape genetic evaluation of a tallgrass prairie corridor using the Greater Prairie-chicken (Tympanuchus cupido). Landsc Ecol [Internet]. 2019;34(6):1425–43. https://doi.org/10.1007/s10980-019-00862-3.
Sanderson EW, Jaiteh M, Levy MA, Redford KH, Wannebo AV, Woolmer G. The human footprint and the last of the wild. Bioscience. 2002;52(10):891–904.
Dupont L, Torres-Leguizamon M, Rene-Corail P, Mathieu J. Landscape features impact connectivity between soil populations: a comparative study of gene flow in earthworms. Mol Ecol. 2017;26(12):3128–40.
Cox K, Maes J, Van Calster H, Mergeay J. Effect of the landscape matrix on gene flow in a coastal amphibian metapopulation. Conserv Genet. 2017;18(6):1359–75.
Thatte P, Joshi A, Vaidyanathan S, Landguth E, Ramakrishnan U. Maintaining tiger connectivity and minimizing extinction into the next century: insights from landscape genetics and spatially-explicit simulations. Biol Conserv [Internet]. 2018;218(November 2017):181–91. https://doi.org/10.1016/j.biocon.2017.12.022.
Khosravi R, Hemami MR, Malekian M, Silva TL, Rezaei HR, Brito JC. Effect of landscape features on genetic structure of the goitered gazelle (Gazella subgutturosa) in Central Iran. Conserv Genet. 2018;19(2):323–36.
Amaral KE, Palace M, O’Brien KM, Fenderson LE, Kovach AI. Anthropogenic habitats facilitate dispersal of an early successional obligate: implications for restoration of an endangered ecosystem. PLoS One. 2016;11(3):1–21.
Mapelli FJ, Boston ESM, Fameli A, Gómez Fernández MJ, Kittlein MJ, Mirol PM. Fragmenting fragments: landscape genetics of a subterranean rodent (Mammalia, Ctenomyidae) living in a human-impacted wetland. Landsc Ecol. 2020:0123456789.
Braaker S, Kormann U, Bontadina F, Obrist MK. Prediction of genetic connectivity in urban ecosystems by combining detailed movement data, genetic data and multi-path modelling. Landsc Urban Plan [Internet]. 2017;160:107–14. https://doi.org/10.1016/j.landurbplan.2016.12.011.
Jo Y-S, Lee SR, Baccus JT, Jung J, Forstner MRJ. Environmental factors affecting population level genetic divergence of the striped field mouse (Apodemus agrarius) in South Korea. Ecol Res [Internet]. 2018;33(5):989–99. https://doi.org/10.1007/s11284-018-1613-1.
United Nations (2019) World urbanization prospects: the 2019 revision [Internet]. New York, United. 32 p. Available from: http://esa.un.org/unpd/wup/Highlights/WUP2014-Highlights.pdf
Tumas HR, Shamblin BM, Woodrey M, Nibbelink NP, Chandler R, Nairn C. Landscape genetics of the foundational salt marsh plant species black needlerush (Juncus roemerianus Scheele) across the northeastern Gulf of Mexico. Landsc Ecol [Internet]. 2018;0123456789(9):1557–73. https://doi.org/10.1007/s10980-018-0687-z.
Johnson MTJ, Munshi-South J. Evolution of life in urban environments. Science (80- ). 2017;358(6363):eaam8327.
Chapman AD (2009) Numbers of living species in Australia and the world [Internet]. Vol. 2nd, Report for the Australian Biological Resources Study. Available from: http://www.environment.gov.au/biodiversity/abrs/publications/other/species-numbers/2009/06-references.html
Alter EA, Tariq L, Creed JK, Megafu E. Evolutionary responses of marine organisms to urbanized seascapes. Evol Appl. 2020;2.
Kern EMA, Langerhans RB. Urbanization drives contemporary evolution in stream fish. Glob Chang Biol. May 2017;2018:3791–803.
Kotze J, Venn S, Niemela J, Spence J. Effects of Urbanization on the ecology and evolution of arthropods. Urban Ecol patterns, Process Appl. 2011:159–66.
Cushman SA, Max T, Meneses N, Evans LM, Ferrier S, Honchak B, et al. Landscape genetic connectivity in a riparian foundation tree is jointly driven by climatic gradients and river networks. Ecol Appl. 2014;24(5):1000–14.
Lawson Handley LJ, Estoup A, Evans DM, Thomas CE, Lombaert E, Facon B, et al. Ecological genetics of invasive alien species. BioControl. 2011;56(4):409–28.
Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet [Internet]. 2016;2:81–92. https://doi.org/10.1038/nrg.2015.28%5Cn10.1038/nrg.2015.28%5Cnhttp://www.nature.com/nrg/journal/vaop/ncurrent/abs/nrg.2015.28.html#supplementary-information.
Konzen ER, Imaculada Z (2020) Landscape genetics: from classic molecular markers to genomics. In: Molecular Medicine [Internet]. IntechOpen; 2020. Available from: https://www.intechopen.com/books/advanced-biometric-technologies/liveness-detection-in-biometrics
Allendorf FW. Genetics and the conservation of natural populations: allozymes to genomes. Mol Ecol. 2017;26(2):420–30.
Hand BK, Lowe WH, Kovach RP, Muhlfeld CC, Luikart G. Landscape community genomics: understanding eco-evolutionary processes in complex environments. Trends Ecol Evol [Internet]. 2015;30(3):161–8. https://doi.org/10.1016/j.tree.2015.01.005.
Freeland JR. Molecular Ecology. West Sussex: Wiley; 2005. p. 44–59.
McCartney-Melstad E, Vu JK, Shaffer HB. Genomic data recover previously undetectable fragmentation effects in an endangered amphibian. Mol Ecol. 2018;27(22):4430–43.
Moll RJ, Cepek JD, Lorch PD, Dennis PM, Tans E, Robison T, et al. What does urbanization actually mean? A framework for urban metrics in wildlife research. J Appl Ecol. 2019;56(5):1289–300.
Lean J, Hammer MP, Unmack PJ, Adams M, Beheregaray LB. Landscape genetics informs mesohabitat preference and conservation priorities for a surrogate indicator species in a highly fragmented river system. Heredity (Edinb) [Internet]. 2017;118:374–84 Available from: http://www.nature.com/doifinder/10.1038/hdy.2016.111.
Smith JG, Jennings MK, Boydston EE, Crooks KR, Ernest HB, Riley SPD, et al. Carnivore population structure across an urbanization gradient: a regional genetic analysis of bobcats in southern California. Landsc Ecol [Internet]. 2020;35(3):659–74. https://doi.org/10.1007/s10980-020-00971-4.
Homola JJ, Loftin CS, Kinnison MT. Landscape genetics reveals unique and shared effects of urbanization for two sympatric pool-breeding amphibians. Ecol Evol. 2019;9(20):11799–823.
Balkenhol N, Gugerli F, Cushman SA, Waits LP, Coulon A, Arntzen JW, et al. Identifying future research needs in landscape genetics: where to from here? Landsc Ecol. 2009;24(4):455–63.
Donihue CM, Lambert MR. Adaptive evolution in urban ecosystems. Ambio [Internet]. 2014;44:194–203 Available from: http://link.springer.com/article/10.1007/s13280-014-0547-2.
Lambert MR, Donihue CM. Urban biodiversity management using evolutionary tools. Nat Ecol Evol. 2020;4(7):903–10. https://doi.org/10.1038/s41559-020-1193-7.
Cushman SA, Landguth EL. Scale dependent inference in landscape genetics. Landsc Ecol. 2010;25(6):967–79.
Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James PMA, Rosenberg MS, et al. Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol. 2010;19:3565–75.
Acknowledgments
The authors would like to thank Dr. Kristen Winchell for helping to conceptualize the figure.
Funding
JM-S was funded by National Science Foundation grant DEB 1457523. EJC was funded by Fordham University’s Freedman Fellowship for Women in Science (2020–2021).
Author information
Authors and Affiliations
Contributions
The concept and design of this study were developed by all three authors. Nicole A. Fusco took the lead in writing the manuscript, with revisions contributed by Elizabeth J. Carlen and Jason Munshi-South. NAF developed the supplementary table. All three authors conceived of the design of the figure, but EJC took the lead in developing the final figure.
Corresponding author
Ethics declarations
Conflict of Interest
Nicole A. Fusco, Elizabeth J. Carlen, and Jason Munshi-South declare that they have no conflict of interest.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Urban Landscape Ecology
Supplementary Information
ESM 1
(DOCX 62 kb)
Rights and permissions
About this article
Cite this article
Fusco, N.A., Carlen, E.J. & Munshi-South, J. Urban Landscape Genetics: Are Biologists Keeping Up with the Pace of Urbanization?. Curr Landscape Ecol Rep 6, 35–45 (2021). https://doi.org/10.1007/s40823-021-00062-3
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40823-021-00062-3