Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Gridlock and beltways: the genetic context of urban invasions

Abstract

The rapid expansion of urban land across the globe presents new and numerous opportunities for invasive species to spread and flourish. Ecologists historically rejected urban ecosystems as important environments for ecology and evolution research but are beginning to recognize the importance of these systems in shaping the biology of invasion. Urbanization can aid the introduction, establishment, and spread of invaders, and these processes have substantial consequences on native species and ecosystems. Therefore, it is valuable to understand how urban areas influence populations at all stages in the invasion process. Population genetic tools are essential to explore the driving forces of invasive species dispersal, connectivity, and adaptation within cities. In this review, we synthesize current research about the influence of urban landscapes on invasion genetics dynamics. We conclude that urban areas are not only points of entry for many invasive species, they also facilitate population establishment, are pools for genetic diversity, and provide corridors for further spread both within and out of cities. We recommend the continued use of genetic studies to inform invasive species management and to understand the underlying ecological and evolutionary processes governing successful invasion.

This is a preview of subscription content, log in to check access.

Fig. 1

References

  1. Airoldi L, Turon X, Perkol-Finkel S, Rius M, Keller R (2015) Corridors for aliens but not for natives: effects of marine urban sprawl at a regional scale. Divers Distrib 21:755–768. https://doi.org/10.1111/ddi.12301

  2. Akhoundi M, Kengne P, Cannet A, Brengues C, Berenger JM, Izri A, Marty P, Simard F, Fontenille D, Delaunay P (2015) Spatial genetic structure and restricted gene flow in bed bugs (Cimex lectularius) populations in France. Infect Genet Evol 34:236–243. https://doi.org/10.1016/j.meegid.2015.06.028

  3. Alberti M (2005) The effects of urban patterns on ecosystem function. Int Reg Sci Rev 28:168–192. https://doi.org/10.1177/0160017605275160

  4. Allendorf FW, Berry O, Ryman N (2014) So long to genetic diversity, and thanks for all the fish. Mol Ecol 23:23–25. https://doi.org/10.1111/mec.12574

  5. Anastacio PM, Ribeiro F, Capinha C, Banha F, Gama M, Filipe AF, Rebelo R, Sousa R (2018) Non-native freshwater fauna in Portugal: a review. Sci Total Environ 650:1923–1934. https://doi.org/10.1016/j.scitotenv.2018.09.251

  6. Ariori C, Aiello-Lammens ME, Silander JA (2017) Plant invasion along an urban-to-rural gradient in northeast Connecticut. J Urban Ecol 3:1–13. https://doi.org/10.1093/jue/jux008

  7. Arredondo TM, Marchini GL, Cruzan MB (2018) Evidence for human-mediated range expansion and gene flow in an invasive grass. Proc Biol Sci 285:20181125. https://doi.org/10.1098/rspb.2018.1125

  8. Balbi M, Ernoult A, Poli P, Madec L, Guiller A, Martin MC, Nabucet J, Beaujouan V, Petit EJ (2018) Functional connectivity in replicated urban landscapes in the land snail (Cornu aspersum). Mol Ecol 27:1357–1370. https://doi.org/10.1111/mec.14521

  9. Balkenhol N, Cushman S, Storfer A, Waits L (2015) Landscape genetics : concepts, methods, applications. John Wiley & Sons Incorporated, Chicester, United Kingdom

  10. Baudouin G, Bech N, Bagnères A-G, Dedeine F (2018) Spatial and genetic distribution of a north American termite, Reticulitermes flavipes, across the landscape of Paris. Urban Ecosyst 21:751–764. https://doi.org/10.1007/s11252-018-0747-9

  11. Beaumont P (1978) Man’s impact on river systems: a world-wide view. Area 10:38–41

  12. Beninde J, Feldmeier S, Werner M, Peroverde D, Schulte U, Hochkirch A, Veith M (2016) Cityscape genetics: structural vs. functional connectivity of an urban lizard population. Mol Ecol 25:4984–5000. https://doi.org/10.1111/mec.13810

  13. Beninde J, Feldmeier S, Veith M, Hochkirch A (2018) Admixture of hybrid swarms of native and introduced lizards in cities is determined by the cityscape structure and invasion history. Proc Biol Sci. https://doi.org/10.1098/rspb.2018.0143

  14. Blackburn TM, Lockwood JL, Cassey P (2015) The influence of numbers on invasion success. Mol Ecol 24:1942–1953. https://doi.org/10.1111/mec.13075

  15. Bolger DT, Suarez AV, Crooks KR, Morrison SA, Case TJ (2000) Arthropods in urban habitat fragments in southern California: area, age, and edge effects. Ecol Appl 10:1230–1248. https://doi.org/10.1890/1051-0761(2000)010[1230:Aiuhfi]2.0.Co;2

  16. Boone MD, Semlitsch RD, Little EE, Doyle MC (2007) Multiple stressors in amphibian communities: effects of chemical contamination, bullfrogs, and fish. Ecol Appl 17:291–301. https://doi.org/10.1890/1051-0761(2007)017[0291:MSIACE]2.0.CO;2

  17. Brans KI, Govaert L, Engelen JM, Gianuca AT, Souffreau C, De Meester L (2017a) Eco-evolutionary dynamics in urbanized landscapes: evolution, species sorting and the change in zooplankton body size along urbanization gradients. Philos Trans R Soc Lond B Biol Sci. https://doi.org/10.1098/rstb.2016.0030

  18. Brans KI, Jansen M, Vanoverbeke J, Tuzun N, Stoks R, De Meester L (2017b) The heat is on: genetic adaptation to urbanization mediated by thermal tolerance and body size. Glob Chang Biol 23:5218–5227. https://doi.org/10.1111/gcb.13784

  19. Buckley YM, Anderson S, Catterall CP, Corlett RT, Engel T, Gosper CR, Nathan RAN, Richardson DM, Setter M, Speigel ORR, Vivian-Smith G, Voigt FA, Weir JES, Westcott DA (2006) Management of plant invasions mediated by frugivore interactions. J Appl Ecol 43:848–857. https://doi.org/10.1111/j.1365-2664.2006.01210.x

  20. Burford Reiskind MO, Labadie P, Bargielowski I, Lounibos LP, Reiskind MH (2018) Rapid evolution and the genomic consequences of selection against interspecific mating. Mol Ecol 27:3641–3654. https://doi.org/10.1111/mec.14821

  21. Burford Reiskind MO, Reed EMX, Elias A, Giacomini JJ, McNear AF, Nieuwsma J, Parker GA, Roberts RB, Rossie RE, Stephenson CN, Stevens JL, Williams BE (2019) The genomics of invasion: characterization of red lionfish (Pterois volitans) populations from the native and introduced ranges. Biol Invasions 21:2471–2483. https://doi.org/10.1007/s10530-019-01992-0

  22. Caprio MA, Tabashnik BE (1992) Gene flow accelerates local adaptation among finite populations: simulating the evolution of insecticide resistance. J Econ Entomol 85:611–620. https://doi.org/10.1093/jee/85.3.611

  23. Cavin JS, Kull CA (2017) Invasion ecology goes to town: from disdain to sympathy. Biol Invasions 19:3471–3487. https://doi.org/10.1007/s10530-017-1588-9

  24. Chang AL et al (2009) Tackling aquatic invasions: risks and opportunities for the aquarium fish industry. Biol Invasions 11:773–785. https://doi.org/10.1007/s10530-008-9292-4

  25. Chapple DG, Miller KA, Kraus F, Thompson MB (2013) Divergent introduction histories among invasive populations of the delicate skink (Lampropholis delicata): has the importance of genetic admixture in the success of biological invasions been overemphasized? Divers Distrib 19:134–146. https://doi.org/10.1111/j.1472-4642.2012.00919.x

  26. Cheptou PO, Carrue O, Rouifed S, Cantarel A (2008) Rapid evolution of seed dispersal in an urban environment in the weed Crepis sancta. Proc Natl Acad Sci USA 105:3796–3799. https://doi.org/10.1073/pnas.0708446105

  27. Christen DC, Matlack GR (2009) The habitat and conduit functions of roads in the spread of three invasive plant species. Biol Invasions 11:453–465. https://doi.org/10.1007/s10530-008-9262-x

  28. Colangelo P, Abiadh A, Aloise G, Amori G, Capizzi D, Vasa E, Annesi F, Castiglia R (2015) Mitochondrial phylogeography of the black rat supports a single invasion of the western Mediterranean basin. Biol Invasions 17:1859–1868. https://doi.org/10.1007/s10530-015-0842-2

  29. Collins PJ, Schlipalius DI (2018) Insecticide resistance. In: Athanassiou CG, Arthur FH (eds) Recent advances in stored product protection. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 169–182. https://doi.org/10.1007/978-3-662-56125-6_8

  30. Combs M, Puckett EE, Richardson J, Mims D, Munshi-South J (2018) Spatial population genomics of the brown rat (Rattus norvegicus) in New York City. Mol Ecol 27:83–98. https://doi.org/10.1111/mec.14437

  31. Cook E, Jahnke M, Kerckhof F, Minchin D, Faasse M, Boos K, Ashton G (2007) European expansion of the introduced amphipod Caprella mutica Schurin, 1935. Aquat Invasions 2:411–421. https://doi.org/10.3391/ai.2007.2.4.11

  32. Crissman JR, Booth W, Santangelo RG, Mukha DV, Vargo EL, Schal C (2010) Population genetic structure of the German cockroach (Blattodea: Blattellidae) in apartment buildings. J Med Entomol 47:553–564. https://doi.org/10.1093/jmedent/47.4.553

  33. Cristescu ME (2015) Genetic reconstructions of invasion history. Mol Ecol 24:2212–2225. https://doi.org/10.1111/mec.13117

  34. Da Silva AG, Eberhard JR, Wright TF, Avery ML, Russello MA (2010) Genetic evidence for high propagule pressure and long-distance dispersal in monk parakeet (Myiopsitta monachus) invasive populations. Mol Ecol 19:3336–3350. https://doi.org/10.1111/j.1365-294X.2010.04749.x

  35. Dalla Bona AC, Piccoli CF, Leandro AS, Kafka R, Twerdochilib AL, Navarro-Silva MA (2012) Genetic profile and molecular resistance of Aedes (Stegomyia) aegypti (Diptera: Culicidae) in Foz do Iguacu (Brazil), at the border with Argentina and Paraguay. Zoologia 29:520–548. https://doi.org/10.1590/S1984-46702012000600005

  36. Darling JA, Galil BS, Carvalho GR, Rius M, Viard F, Piraino S (2017) Recommendations for developing and applying genetic tools to assess and manage biological invasions in marine ecosystems. Mar Policy 85:56–64. https://doi.org/10.1016/j.marpol.2017.08.014

  37. De Kort H, Mergeay J, Jacquemyn H, Honnay O (2016) Transatlantic invasion routes and adaptive potential in North American populations of the invasive glossy buckthorn, Frangula alnus. Ann Bot 118:1089–1099. https://doi.org/10.1093/aob/mcw157

  38. Diamond SE, Chick L, Perez A, Strickler SA, Martin RA (2017) Rapid evolution of ant thermal tolerance across an urban-rural temperature cline. Biol J Linn Soc 121:248–257. https://doi.org/10.1093/biolinnean/blw047

  39. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449. https://doi.org/10.1111/j.1365-294X.2007.03538.x

  40. Dlugosch KM, Anderson SR, Braasch J, Cang FA, Gillette HD (2015) The devil is in the details: genetic variation in introduced populations and its contributions to invasion. Mol Ecol 24:2095–2111. https://doi.org/10.1111/mec.13183

  41. Drake JM, Lodge DM (2007) Rate of species introductions in the Great Lakes via ships’ ballast water and sediments. Can J Fish Aquat Sci 64:530–538. https://doi.org/10.1139/f07-029

  42. Duckworth RA, Badyaev AV (2007) Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci USA 104:15017–15022. https://doi.org/10.1073/pnas.0706174104

  43. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139. https://doi.org/10.1016/s0169-5347(98)01554-7

  44. Duncan RP (2016) How propagule size and environmental suitability jointly determine establishment success: a test using dung beetle introductions. Biol Invasions 18:985–996. https://doi.org/10.1007/s10530-016-1083-8

  45. Egizi A, Kiser J, Abadam C, Fonseca DM (2016) The hitchhiker’s guide to becoming invasive: exotic mosquitoes spread across a US state by human transport not autonomous flight. Mol Ecol 25:3033–3047. https://doi.org/10.1111/mec.13653

  46. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523. https://doi.org/10.1007/s10021-002-0151-3

  47. Eritja R, Palmer JRB, Roiz D, Sanpera-Calbet I, Bartumeus F (2017) Direct evidence of adult Aedes albopictus dispersal by car. Sci Rep 7:14399. https://doi.org/10.1038/s41598-017-12652-5

  48. Estoup A, Ravigné V, Hufbauer R, Vitalis R, Gautier M, Facon B (2016) Is there a genetic paradox of biological invasion? Annu Rev Ecol Evol Syst 47:51–72. https://doi.org/10.1146/annurev-ecolsys-121415-032116

  49. Facon B, David P (2006) Metapopulation dynamics and biological invasions: a spatially explicit model applied to a freshwater snail. Am Nat 168:769–783. https://doi.org/10.1086/508669

  50. Faulkner KT, Hurley BP, Robertson MP, Rouget M, Wilson JRU (2017) The balance of trade in alien species between South Africa and the rest of Africa. Bothalia 47:1–16. https://doi.org/10.4102/abc.v47i2.2157

  51. Firth LB, Knights AM, Bridger D, Evans AJ, Mieszkowska N, Moore PJ, O’Connor NE, Sheehan EV, Thompson RC, Hawkins SJ (2016) Ocean sprawl: challenges and opportunities for biodiversity management in a changing world. In: Hughes RN, Hughes DJ, Smith IP, Dale AC (eds) Oceanography and marine biology: an annual review. CRC Press, Boca Raton, pp 189–262. https://plymsea.ac.uk/id/eprint/7164

  52. Fischer ML, Salgado I, Beninde J, Klein R, Frantz AC, Heddergott M, Cullingham CI, Kyle CJ, Hochkirch A (2017) Multiple founder effects are followed by range expansion and admixture during the invasion process of the raccoon (Procyon lotor) in Europe. Divers Distrib 23:409–420. https://doi.org/10.1111/ddi.12538

  53. Francis RA, Chadwick MA (2012) What makes a species synurbic? Appl Geogr 32:514–521. https://doi.org/10.1016/j.apgeog.2011.06.013

  54. Francis RA, Lorimer J (2011) Urban reconciliation ecology: the potential of living roofs and walls. J Environ Manag 92:1429–1437. https://doi.org/10.1016/j.jenvman.2011.01.012

  55. Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385. https://doi.org/10.1038/sj.hdy.6800634

  56. Gaertner M, Wilson JRU, Cadotte MW, MacIvor JS, Zenni RD, Richardson DM (2017) Non-native species in urban environments: patterns, processes, impacts and challenges. Biol Invasions 19:3461–3469. https://doi.org/10.1007/s10530-017-1598-7

  57. Gardner-Santana LC, Norris DE, Fornadel CM, Hinson ER, Klein SL, Glass GE (2009) Commensal ecology, urban landscapes, and their influence on the genetic characteristics of city-dwelling Norway rats (Rattus norvegicus). Mol Ecol 18:2766–2778. https://doi.org/10.1111/j.1365-294X.2009.04232.x

  58. Garnas JR, Auger-Rozenberg MA, Roque A, Bertelsmeier C, Wingfield MJ, Saccaggi DL, Roy HE, Slippers B (2016) Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences. Biol Invasions 18:935–952. https://doi.org/10.1007/s10530-016-1082-9

  59. Gippet JMW, Mondy N, Diallo-Dudek J, Bellec A, Dumet A, Mistler L, Kaufmann B (2016) I’m not like everybody else: urbanization factors shaping spatial distribution of native and invasive ants are species-specific. Urban Ecosyst 20:157–169. https://doi.org/10.1007/s11252-016-0576-7

  60. Goddard MA, Dougill AJ, Benton TG (2010) Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol Evol 25:90–98. https://doi.org/10.1016/j.tree.2009.07.016

  61. Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib 11:549–558. https://doi.org/10.1111/j.1366-9516.2005.00195.x

  62. Gozlan RE, Britton JR, Cowx I, Copp GH (2010) Current knowledge on non-native freshwater fish introductions. J Fish Biol 76:751–786. https://doi.org/10.1111/j.1095-8649.2010.02566.x

  63. Groeneveld E, Belzile F, Lavoie C (2014) Sexual reproduction of Japanese knotweed (Fallopia japonica s.l.) at its northern distribution limit: new evidence of the effect of climate warming on an invasive species. Am J Bot 101:459–466. https://doi.org/10.3732/ajb.1300386

  64. Hanski I (1982) Dynamics of regional distribution: the core and satellite species hypothesis. Oikos 38:210–221. https://doi.org/10.2307/3544021

  65. Holmstrup M, Bindesbøl AM, Oostingh GJ, Duschl A, Scheil V, Köhler H-R, Loureiro S, Soares AMVM, Ferreira ALB, Kienle C, Gerhardt A, Laskowski R, Kramarz PE, Bayley M, Svendsen C, Spurgeon DJ (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Tot Environ 408:3746–3762. https://doi.org/10.1016/j.scitotenv.2009.10.067

  66. Hufbauer RA, Facon B, Ravigne V, Turgeon J, Roucaud J, Lee CE, Rey O, Estoup A (2012) Anthropogenically induced adaptation to invade (AIAI): contemporary adaptation to human-altered habitats within the native range can promote invasions. Evol Appl 5:89–101. https://doi.org/10.1111/j.1752-4571.2011.00211.x

  67. Hulme PE (2011) Addressing the threat to biodiversity from botanic gardens. Trends Ecol Evol 26:168–174. https://doi.org/10.1016/j.tree.2011.01.005

  68. Hulme PE, Pauchard A, Pyšek P, Vilà M, Alba C, Blackburn TM, Bullock JM, Chytrý M, Dawson W, Dunn AM, Essl F, Genovesi P, Maskell LC, Meyerson LA, Nuñez MA, Pergl J, Pescott OL, Pocock MJ, Richardson DM, Roy HE, Smart SM, Štajerová K, Stohlgren T, van Kleunen M, Winter M (2015) Challenging the view that invasive non-native plants are not a significant threat to the floristic diversity of Great Britain. Proc Natl Acad Sci USA 112:E2988–E2989. https://doi.org/10.1073/pnas.1506517112

  69. Hulme-Beaman A, Dobney K, Cucchi T, Searle JB (2016) An ecological and evolutionary framework for commensalism in anthropogenic environments. Trends Ecol Evol 31:633–645. https://doi.org/10.1016/j.tree.2016.05.001

  70. Ishii H, Ichinose G, Ohsugi Y, Iwasaki A (2016) Vegetation recovery after removal of invasive Trachycarpus fortunei in a fragmented urban shrine forest. Urban For Urban Gree 15:53–57. https://doi.org/10.1016/j.ufug.2015.11.008

  71. Javal M, Lombaert E, Tsykun T, Courtin C, Kerdelhué C, Prospero S, Roques A, Roux G (2019) Deciphering the worldwide invasion of the Asian long-horned beetle: a recurrent invasion process from the native area together with a bridgehead effect. Mol Ecol. https://doi.org/10.1111/mec.15030

  72. Jodoin Y, Lavoie C, Villeneuve P, Theriault M, Beaulieu J, Belzile F (2008) Highways as corridors and habitats for the invasive common reed Phragmites australis in Quebec, Canada. J Appl Ecol 45:459–466. https://doi.org/10.1111/j.1365-2664.2007.01362.x

  73. Johnson MTJ, Munshi-South J (2017) Evolution of life in urban environments. Science 358:eaam8327. https://doi.org/10.1126/science.aam8327

  74. Johnson LE, Padilla DK (1996) Geographic spread of exotic species: ecological lessons and opportunities from the invasion of the zebra mussel Dreissena polymorpha. Biol Conserv 78:23–33. https://doi.org/10.1016/0006-3207(96)00015-8

  75. Johnson PTJ, Olden JD, Vander Zanden MJ (2008) Dam invaders: impoundments facilitate biological invasions into freshwaters. Front Ecol Environ 6:357–363. https://doi.org/10.1890/070156

  76. Johnson MTJ, Prashad CM, Lavoignat M, Saini HS (2018) Contrasting the effects of natural selection, genetic drift and gene flow on urban evolution in white clover (Trifolium repens). Proc Biol Sci 285:20181019. https://doi.org/10.1098/rspb.2018.1019

  77. Kamdem C, Fouet C, Gamez S, White BJ (2017) Pollutants and insecticides drive local adaptation in African malaria mosquitoes. Mol Biol Evol 34:1261–1275. https://doi.org/10.1093/molbev/msx087

  78. Katsanevakis S, Zenetos A, Belchior C, Cardoso AC (2013) Invading European seas: assessing pathways of introduction of marine aliens. Ocean Coast Manag 76:64–74. https://doi.org/10.1016/j.ocecoaman.2013.02.024

  79. Kirichenko N, Augustin S, Kenis M (2018) Invasive leafminers on woody plants: a global review of pathways, impact, and management. J Pest Sci 92:93–106. https://doi.org/10.1007/s10340-018-1009-6

  80. Koch E, Clark JM, Cohen B, Meinking TL, Ryan WG, Stevenson A, Yetman R, Yoon KS (2016) Management of head louse infestations in the United States—a literature review. Pediatr Dermatol 33:466–472. https://doi.org/10.1111/pde.12982

  81. Kolbe JJ, Larson A, Losos JB, de Queiroz K (2008) Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species. Biol Lett 4:434–437. https://doi.org/10.1098/rsbl.2008.0205

  82. Kong F, Yin H, Nakagoshi N, Zong Y (2010) Urban green space network development for biodiversity conservation: identification based on graph theory and gravity modeling. Landsc Urban Plan 95:16–27. https://doi.org/10.1016/j.landurbplan.2009.11.001

  83. Kühn I, Wolf J, Schneider A (2017) Is there an urban effect in alien plant invasions? Biol Invasions 19:3505–3513. https://doi.org/10.1007/s10530-017-1591-1

  84. Kwik J, Kho ZY, Quek BS, Tan HH, Yeo D (2013) Urban stormwater ponds in Singapore: potential pathways for spread of alien freshwater fishes. BioInvasions Rec 2:239–245. https://doi.org/10.3391/bir.2013.2.3.11

  85. Lambdon PW, Pyšek P, Basnou C, Hejda M, Arianoutsou M, Essl F, Jarošík V, Pergl J, Winter M, Anastasiu P, Andripoulos P, Bazos I, Brundu G, Celesti-Grapow L, Chassot P, Delipetrou P, Josefsson M, Kark S, Klotz S, Kokkoris Y, Kühn I, Marchante H, Perglová I, Pino J, Vilà M, Zikos A, Roy D, Hulme PE (2008) Alien flora of Europe: species diversity, temporal trends, geographical patterns and research needs. Preslia 80:101–149

  86. Larson BMH (2005) The war of the roses: demilitarizing invasion biology. Front Ecol Environ 3:495–500. https://doi.org/10.1890/1540-9295(2005)003[0495:TWOTRD]2.0.CO;2

  87. Larson BMH (2007) An alien approach to invasive species: objectivity and society in invasion biology. Biol Invasions 9:947–956. https://doi.org/10.1007/s10530-007-9095-z

  88. Leniaud L, Pichon A, Uva P, Bagneres AG (2009) Unicoloniality in Reticulitermes urbis: a novel feature in a potentially invasive termite species. Bull Entomol Res 99:1–10. https://doi.org/10.1017/S0007485308006032

  89. Leprieur F, Beauchard O, Blanchet S, Oberdorff T, Brosse S (2008) Fish invasions in the world’s river systems: when natural processes are blurred by human activities. PLoS Biol 6:e28. https://doi.org/10.1371/journal.pbio.0060028

  90. Li F, Wang R, Paulussen J, Liu X (2005) Comprehensive concept planning of urban greening based on ecological principles: a case study in Beijing, China. Landsc Urban Plan 72:325–336. https://doi.org/10.1016/j.landurbplan.2004.04.002

  91. Li HS, Zou SJ, De Clercq P, Pang H (2018) Population admixture can enhance establishment success of the introduced biological control agent Cryptolaemus montrouzieri. BMC Evol Biol 18:36. https://doi.org/10.1186/s12862-018-1158-5

  92. Lindholm AK, Breden F, Alexander HJ, Chan WK, Thakurta SG, Brooks R (2005) Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia. Mol Ecol 14:3671–3682. https://doi.org/10.1111/j.1365-294X.2005.02697.x

  93. Linz GM, Homan HJ, Gaulker SM, Penry LB, Bleier WJ (2007) European starlings: a review of an invasive species with far-reaching impacts. In: Witmer GW, Pitt WC, Fagerstone KA (eds) Managing vertebrate invasive species. USDA/APHIS Wildlife Research Center Fort Collins, Colorado, pp 378–386

  94. Lockwood JL, Cassey P, Blackburn T (2005) The role of propagule pressure in explaining species invasions. Trends Ecol Evol 20:223–228. https://doi.org/10.1016/j.tree.2005.02.004

  95. Lovell ST, Taylor JR (2013) Supplying urban ecosystem services through multifunctional green infrastructure in the United States. Landsc Ecol 28:1447–1463. https://doi.org/10.1007/s10980-013-9912-y

  96. Luniak M (2004) Synurbization-adaptation of animal wildlife to urban development. In: Proceedings of the 4th international symposium on urban wildlife conservation, pp 50–55

  97. MacDougall AS, McCune JL, Eriksson O, Cousins SAO, Partel M, Firn J, Hierro JL (2018) The neolithic plant invasion hypothesis: the role of preadaptation and disturbance in grassland invasion. New Phytol 220:94–103. https://doi.org/10.1111/nph.15285

  98. Mangombi JB, Brouat C, Loiseau A, Banga O, Leroy EM, Bourgarel M, Duplantier JM (2016) Urban population genetics of the invasive black rats in Franceville, Gabon. J Zool 299:183–190. https://doi.org/10.1111/jzo.12334

  99. Mayer K, Haeuser E, Dawson W, Essl F, Kreft H, Pergl J, Pyšek P, Weigelt P, Winter M, Lenzner B, van Kleunen M (2017) Naturalization of ornamental plant species in public green spaces and private gardens. Biol Invasions 19:3613–3627. https://doi.org/10.1007/s10530-017-1594-y

  100. McDonnell MJ, Hahs AK (2015) Adaptation and adaptedness of organisms to urban environments. Annu Rev Ecol Evol Syst 46:261–280. https://doi.org/10.1146/annurev-ecolsys-112414-054258

  101. McGeoch MA, Genovesi P, Bellingham PJ, Costello MJ, McGrannachan C, Sheppard A (2016) Prioritizing species, pathways, and sites to achieve conservation targets for biological invasion. Biol Invasions 18:299–314. https://doi.org/10.1007/s10530-015-1013-1

  102. McIntyre NE, Knowles-Yánez K, Hope D (2000) Urban ecology as an interdisciplinary field: differences in the use of “urban” between the social and natural sciences. Urban Ecosyst 4:5–24. https://doi.org/10.1023/a:1009540018553

  103. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005

  104. Medley KA, Jenkins DG, Hoffman EA (2015) Human-aided and natural dispersal drive gene flow across the range of an invasive mosquito. Mol Ecol 24:284–295. https://doi.org/10.1111/mec.12925

  105. Menke SB, Guénard B, Sexton JO, Weiser MD, Dunn RR, Silverman J (2011) Urban areas may serve as habitat and corridors for dry-adapted, heat tolerant species; an example from ants. Urban Ecosyst 14:135–163. https://doi.org/10.1007/s11252-010-0150-7

  106. Merilä J, Björklund M, Baker AJ (1996) The successful founder: genetics of introduced Carduelis chloris (greenfinch) populations in New Zealand. Heredity 77:410. https://doi.org/10.1038/hdy.1996.161

  107. Milbau A, Stout JC (2008) Factors associated with alien plants transitioning from casual, to naturalized, to invasive. Conserv Biol 22:308–317. https://doi.org/10.1111/j.1523-1739.2007.00877.x

  108. Miles LS, Rivkin LR, Johnson MTJ, Munshi-South J, Verrelli BC (2019) Gene flow and genetic drift in urban environments. Mol Ecol. https://doi.org/10.1111/mec.15221

  109. Miller NJ, Sappington TW (2017) Role of dispersal in resistance evolution and spread. Curr Opin Insect Sci 21:68–74. https://doi.org/10.1016/j.cois.2017.04.005

  110. Miranda AC (2017) Mechanisms of behavioural change in urban animals: the role of microevolution and phenotypic plasticity. In: Murgui E, Hedblom M (eds) Ecology and conservation of birds in urban environments. Springer, Cham, pp 113–132

  111. Moles AT, Gruber MAM, Bonser SP (2008) A new framework for predicting invasive plant species. J Ecol 96:13–17. https://doi.org/10.1111/j.1365-2745.2007.01332.x

  112. Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492. https://doi.org/10.1890/070064

  113. Morais P, Reichard M (2018) Cryptic invasions: a review. Sci Tot Environ 613–614:1438–1448. https://doi.org/10.1016/j.scitotenv.2017.06.133

  114. Moricca S, Bracalini M, Croci F, Corsinovi S, Tiberi R, Ragazzi A, Panzavolta T (2018) Biotic factors affecting ecosystem services in urban and peri-urban forests in Italy: the role of introduced and impending pathogens and pests. Forests 9:65. https://doi.org/10.3390/f9020065

  115. Munns WR Jr (2006) Assessing risks to wildlife populations from multiple stressors: overview of the problem and research needs. Ecol Soc 11:23

  116. National Academies of Sciences Engineering, and Medicine (2016) Gene drives on the horizon: advancing science, navigating uncertainty, and aligning research with public values. The National Academies Press, Washington, DC. https://doi.org/10.17226/23405

  117. Ojaveer H, Galil BS, Carlton JT, ALleway H, Goulletquer P, Lehtiniemi M, Marchini A, Miller W, Occhipinti-Ambrogi A, Peharda M, Ruiz GM, Williams SL, Zaiko A (2018) Historical baselines in marine bioinvasions: implications for policy and management. PLoS ONE 13:e0202383. https://doi.org/10.1371/journal.pone.0202383

  118. Ożgo M, Bogucki Z (2011) Colonization, stability, and adaptation in a transplant experiment of the polymorphic land snail Cepaea nemoralis (Gastropoda: Pulmonata) at the edge of its geographical range. Biol J Linn Soc 104:462–470. https://doi.org/10.1111/j.1095-8312.2011.01732.x

  119. Padayachee AL, Irlich UM, Faulkner KT, Gaertner M, Procheş Ş, Wilson JRU, Rouget M (2017) How do invasive species travel to and through urban environments? Biol Invasions 19:3557–3570. https://doi.org/10.1007/s10530-017-1596-9

  120. Pauchard A, Aguayo M, Peña E, Urrutia R (2006) Multiple effects of urbanization on the biodiversity of developing countries: the case of a fast-growing metropolitan area (Concepción, Chile). Biol Conserv 127:272–281. https://doi.org/10.1016/j.biocon.2005.05.015

  121. Pickett ST, Cadenasso ML, Grove JM, Boone CG, Groffman PM, Irwin E, Kaushal SS, Marshall V, McGrath BP, Nilon CH, Pouyat RV, Szlavecz K, Troy A, Warren P (2011) Urban ecological systems: scientific foundations and a decade of progress. J Environ Manag 92:331–362. https://doi.org/10.1016/j.jenvman.2010.08.022

  122. Polsky C, Grove JM, Knudson C, Groffman PM, Bettez N, Cavender-Bares J, Hall SJ, Heffernan JB, Hobbie SE, Larson KL, Morse JL, Neill C, Nelson KC, Ogden LA, O’Neil-Dunne J, Pataki DE, Chowdhury RR, Steele MK (2014) Assessing the homogenization of urban land management with an application to US residential lawn care. Proc Natl Acad Sci USA 111:4432–4437. https://doi.org/10.1073/pnas.1323995111

  123. Prowse TAA, Cassey P, Ross JV, Pfitzner C, Wittmann TA, Thomas P (2017) Dodging silver bullets: good CRISPR gene-drive design is critical for eradicating exotic vertebrates. Proc Biol Sci. https://doi.org/10.1098/rspb.2017.0799

  124. Pyšek P (1995) On the terminology used in plant invasion studies. In: Pyšek P, Prach K, Rejmánek M, Wade M (eds) Plant invasions: general aspects and special problems. SPB Academic Publishing, Amsterdam, pp 71–81

  125. Pyšek P (1998) Is there a taxonomic pattern to plant invasions? Oikos 82:282–294. https://doi.org/10.2307/3546968

  126. Qiao H, Liu W, Zhang Y, Zhang YY, Li QQ (2019) Genetic admixture accelerates invasion via provisioning rapid adaptive evolution. Mol Ecol. https://doi.org/10.1111/mec.15192

  127. Quinn LD, Culley TM, Stewart JR (2012) Genetic comparison of introduced and native populations of Miscanthus sinensis (Poaceae), a potential bioenergy crop. Grassl Sci 58:101–111. https://doi.org/10.1111/j.1744-697X.2012.00248.x

  128. Richardson JL et al (2017) Using fine-scale spatial genetics of Norway rats to improve control efforts and reduce leptospirosis risk in urban slum environments. Evol Appl 10:323–337. https://doi.org/10.1111/eva.12449

  129. Riley CB, Herms DA, Gardiner MM (2018) Exotic trees contribute to urban forest diversity and ecosystem services in inner-city Cleveland, OH. Urban For Urban Green 29:367–376. https://doi.org/10.1016/j.ufug.2017.01.004

  130. Rollinson DP, Coleman JC, Downs CT (2015) Seasonal differences in foraging dynamics, habitat use and home range size of Wahlberg’s epauletted fruit bat in an urban environment. Afr Zool 48:340–350. https://doi.org/10.1080/15627020.2013.11407601

  131. Romero A, Potter MF, Potter DA, Haynes KF (2007) Insecticide resistance in the bed bug: a factor in the pest’s sudden resurgence? J Med Entomol 44:175–178. https://doi.org/10.1603/0022-2585(2007)44[175:Iritbb]2.0.Co;2

  132. Rosenfeld JA, Reeves D, Brugler MR, Narechania A, Simon S, Durrett R, Foox J, Shianna K, Schatz MC, Gandara J, Afshinnekoo E, Lam ET, Hastie AR, Chan S, Cao H, Saghbini M, Kentsis A, Planet PJ, Kholodovych V, Tessler M, Baker R, DeSalle R, Sorkin LN, Kolokontronis SO, Siddall ME, Amato G, Mason CE (2016) Genome assembly and geospatial phylogenomics of the bed bug Cimex lectularius. Nat Commun 7:10164. https://doi.org/10.1038/ncomms10164

  133. Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632. https://doi.org/10.1093/icb/37.6.621

  134. Russello MA, Avery ML, Wright TF (2008) Genetic evidence links invasive monk parakeet populations in the United States to the international pet trade. BMC Evol Biol 8:217. https://doi.org/10.1186/1471-2148-8-217

  135. Rutkowski R, Kosewska A, Ceryngier P, Szczepański S, Wawer W, Twardowska K, Twardowski J (2017) Genetic diversity of an invasive invertebrate in an urban environment, as exemplified by the harlequin ladybird Harmonia axyridis (Pallas, 1773). Ann Zool 67:759–772. https://doi.org/10.3161/00034541anz2017.67.4.011

  136. Salo P, Korpimaki E, Banks PB, Nordstrom M, Dickman CR (2007) Alien predators are more dangerous than native predators to prey populations. Proc Biol Sci 274:1237–1243. https://doi.org/10.1098/rspb.2006.0444

  137. Sasaki T, Ishii H, Morimoto Y (2018) Evaluating restoration success of a 40-year-old urban forest in reference to mature natural forest. Urban For Urban Green 32:123–132. https://doi.org/10.1016/j.ufug.2018.04.008

  138. Säumel I, Kowarik I (2010) Urban rivers as dispersal corridors for primarily wind-dispersed invasive tree species. Landsc Urban Plan 94:244–249. https://doi.org/10.1016/j.landurbplan.2009.10.009

  139. Schmidt TL, Filipovic I, Hoffmann AA, Rasic G (2018) Fine-scale landscape genomics helps explain the slow spatial spread of Wolbachia through the Aedes aegypti population in Cairns, Australia. Heredity 120:386–395. https://doi.org/10.1038/s41437-017-0039-9

  140. Schrieber K, Lachmuth S (2017) The genetic paradox of invasions revisited: the potential role of inbreeding x environment interactions in invasion success. Biol Rev Camb Philos Soc 92:939–952. https://doi.org/10.1111/brv.12263

  141. Seebens H, Blackburn TM, Dyer EE, Genovesi P, Hulme PE, Jeschke JM, Pagad S, Pyšek P, van Kleunen M, Winter M, Ansong M, Arianoutsou M, Bacher S, Blasius B, Brockerhoff EG, Brundu G, Capinha C, Causton CE, Celesti-Grapow L, Dawson W, Dullinger S, Economo EP, Fuentes N, Guénard B, Jäger H, Kartesz J, Kenis M, Kühn I, Lenzner B, Liebhold AM, Mosena A, Moser D, Nentwig W, Nishino M, Pearman D, Pergl J, Rabitsch W, Rojas-Sandoval J, Roques A, Rorke S, Rossinelli S, Roy HE, Scalera R, Schindler S, Štajerová K, Tokarska-Guzik B, Walker K, Ward DF, Yamanaka T, Essl F (2018) Global rise in emerging alien species results from increased accessibility of new source pools. Proc Natl Acad Sci USA 115:E2264–E2273. https://doi.org/10.1073/pnas.1719429115

  142. Seto KC, Guneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci USA 109:16083–16088. https://doi.org/10.1073/pnas.1211658109

  143. Sherpa S, Rioux D, Pougnet-Lagarde C, Despres L (2018) Genetic diversity and distribution differ between long-established and recently introduced populations in the invasive mosquito Aedes albopictus. Infect Genet Evol 58:145–156. https://doi.org/10.1016/j.meegid.2017.12.018

  144. Signorile AL, Wang J, Lurz PWW, Bertolino S, Carbone C, Reuman DC, Jeschke J (2014) Do founder size, genetic diversity and structure influence rates of expansion of North American grey squirrels in Europe? Divers Distrib 20:918–930. https://doi.org/10.1111/ddi.12222

  145. Simberloff D (2005) Non-native species DO threaten the natural environment! J Agric Environ Ethics 18:595–607. https://doi.org/10.1007/s10806-005-2851-0

  146. Terando AJ, Costanza J, Belyea C, Dunn RR, McKerrow A, Collazo JA (2014) The southern megalopolis: using the past to predict the future of urban sprawl in the Southeast US. PLoS ONE 9:e102261. https://doi.org/10.1371/journal.pone.0102261

  147. Thibault M, Masse F, Pujapujane A, Lannuzel G, Bordez L, Potter MA, Fogliani B, Vidal E, Brescia F (2018) “Liaisons dangereuses”: the invasive red-vented bulbul (Pycnonotus cafer), a disperser of exotic plant species in New Caledonia. Ecol Evol 8:9259–9269. https://doi.org/10.1002/ece3.4140

  148. Tingley R, García-Díaz P, Arantes CRR, Cassey P (2018) Integrating transport pressure data and species distribution models to estimate invasion risk for alien stowaways. Ecography 41:635–646. https://doi.org/10.1111/ecog.02841

  149. Triggs SJ, Green WQ (1989) Geographic patterns of genetic variation in brushtail possums Trichosurus vulpecula and implications for pest control. New Zeal J Ecol 12:1–16. https://www.jstor.org/stable/24053175

  150. Tufts DM, VanAcker MC, Fernandez MP, DeNicola A, Egizi A, Diuk-Wasser MA (2019) Distribution, host-seeking phenology, and host and habitat associations of Haemaphysalis longicornis ticks, Staten Island, New York, USA. Emerg Infect Dis 25:792–796. https://doi.org/10.3201/eid2504.181541

  151. United Nations Statistics Division (2017) Population density and urbanization. United Nations. https://unstats.un.org/UNSD/Demographic/sconcerns/densurb/densurbmethods.htm. Accessed 5 Jan 2019

  152. Useni Sikuzani Y, Sambiéni Kouagou R, Maréchal J, Ilunga wa Ilunga E, Malaisse F, Bogaert J, Munyemba Kankumbi F (2018) Changes in the spatial pattern and ecological functionalities of green spaces in Lubumbashi (the Democratic Republic of Congo) in relation with the degree of urbanization. Trop Conserv Sci 11:1940082918771325. https://doi.org/10.1177/1940082918771325

  153. Vangestel C, Mergeay J, Dawson DA, Vandomme V, Lens L (2011) Spatial heterogeneity in genetic relatedness among house sparrows along an urban-rural gradient as revealed by individual-based analysis. Mol Ecol 20:4643–4653. https://doi.org/10.1111/j.1365-294X.2011.05316.x

  154. Vargo EL, Crissman JR, Booth W, Santangelo RG, Mukha DV, Schal C (2014) Hierarchical genetic analysis of German cockroach (Blattella germanica) populations from within buildings to across continents. PLoS ONE 9:e102321. https://doi.org/10.1371/journal.pone.0102321

  155. Verhoeven KJ, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc Biol Sci 278:2–8. https://doi.org/10.1098/rspb.2010.1272

  156. Vila M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, PErgl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x

  157. Wagner NK, Ochocki BM, Crawford KM, Compagnoni A, Miller TE (2017) Genetic mixture of multiple source populations accelerates invasive range expansion. J Anim Ecol 86:21–34. https://doi.org/10.1111/1365-2656.12567

  158. Wang J-S, Hung C-M (2019) Barn swallow nest predation by a recent urban invader, the Taiwan whistling thrush—implications for the evolution of urban avian communities. Zool Stud 58:8. https://doi.org/10.6620/ZS.2019.58-01

  159. Wang Z, Baker AJ, Hill GE, Edwards SV (2003) Reconciling actual and inferred population histories in the house finch (Carpodacus mexicanus) by AFLP analysis. Evolution 57:2852–2864

  160. Webber BL, Raghu S, Edwards OR (2015) Opinion: is CRISPR-based gene drive a biocontrol silver bullet or global conservation threat? Proc Natl Acad Sci USA 112:10565–10567. https://doi.org/10.1073/pnas.1514258112

  161. Williams JL, Kendall BE, Levine JM (2016) Rapid evolution accelerates plant population spread in fragmented experimental landscapes. Science 353:482–485. https://doi.org/10.1126/science.aaf6268

  162. Williams JL, Hufbauer RA, Miller TEX (2019) How evolution modifies the variability of range expansion. Trends Ecol Evol. https://doi.org/10.1016/j.tree.2019.05.012

  163. Willson JD, Dorcas ME, Snow RW (2010) Identifying plausible scenarios for the establishment of invasive Burmese pythons (Python molurus) in southern Florida. Biol Invasions 13:1493–1504. https://doi.org/10.1007/s10530-010-9908-3

  164. Yanai Z, Dayan T, Mienis H, Gasith A (2017) The pet and horticultural trades as introduction and dispersal agents of non-indigenous freshwater molluscs. Manag Biol Invasions 8:523–532. https://doi.org/10.3391/mbi.2017.8.4.07

  165. Zefferman EP, McKinney ML, Cianciolo T, Fritz BI (2018) Knoxville’s urban wilderness: moving toward sustainable multifunctional management. Urban For Urban Green 29:357–366. https://doi.org/10.1016/j.ufug.2017.09.002

Download references

Acknowledgements

We thank M. Zuckerberg, M. H. Reiskind, and N. M. Haddad for comments on drafts of this manuscript. We also thank two anonymous reviewers for their comments that greatly improved this manuscript.

Author information

All authors conceived of the idea for the review. EMXR led the writing with significant contributions from MES and ASM. MOBR provided extensive editorial advice.

Correspondence to E. M. X. Reed.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Kendi Davies.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Reed, E.M.X., Serr, M.E., Maurer, A.S. et al. Gridlock and beltways: the genetic context of urban invasions. Oecologia (2020). https://doi.org/10.1007/s00442-020-04614-y

Download citation

Keywords

  • Synthesis
  • Population genetics
  • Landscape genetics
  • Invasive species
  • Urban ecosystems