Evolution of life in urban environments

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Science  03 Nov 2017:
Vol. 358, Issue 6363, eaam8327
DOI: 10.1126/science.aam8327
  • A gradient in urbanization showing the skyline of Canada’s sixth largest city (Mississauga, Canada) on the horizon, and the Credit Valley and the University of Toronto Mississauga campus in the foreground.

  • Fig. 1 World map showing cities, the origin of human commensals, and the location of contemporary urban evolution studies.

    All cities with >300,000 people are shown. The approximate regions of origin of human commensals (Box 1) are shown as blue silhouettes. Urban evolution has been studied in the species and at the locations shown by black silhouettes. Only one location is shown when multiple cities were studied within a single species. The legend shows how variation in dot size and color correspond to human population sizes within cities. The species and locations shown are a representative subset of the studies in table S1.

  • Fig. 2 Diagram of a rural-urban gradient and predicted effects of urbanization on evolution.

    The central oval illustrates a gradient that includes woodlands, rural areas, suburbs, and a city. Park and woodland habitats become increasingly fragmented along the gradient. The river can be a natural barrier, whereas roads and buildings may represent anthropogenic barriers to gene flow. (Top) A landscape scenario leading to increases in genetic drift (top left oval) and decreased gene flow (top right oval). Here, organisms become increasingly isolated by impervious surfaces and other barriers, which increases genetic drift (top left) and restricts gene flow (top right) (darker red shading indicates unsuitable habitat). The top center figure shows the predicted evolutionary outcomes for genetic variation, gene flow, and genetic differentiation as fragmentation or resistance to dispersal increases. (Bottom) The predicted outcome of selection on allele frequencies at one locus that provides a fitness benefit in urban populations sampled along a gradient from the urban core to nonurban areas. Red and blue colors correspond to the relative frequency of two alleles at this locus. The lizard silhouettes depict hypothetical phenotypic adaptations (such as divergent body shape and size) along the same gradient (bottom). [Artistic rendering of the city was by B. Cohan.]

  • Fig. 3 Examples of how urbanization affects evolution.

    (A) Pollution from steel mills in industrial cities causes higher mutation rates in herring gull (Larus argentatus) as compared with nonindustrial cities or rural areas (mean ± 95% confidence interval) (30, 126). (B) Increased urbanization leads to more impervious surfaces, which is associated with stronger genetic drift and decreased genetic diversity in white-footed mice (P. leucopus) (37). (C) A major river, buildings, and woodlands increase resistance to gene flow in the common wall lizard (Podarcus muralis) (61), whereas urban vineyards and rocky substrates facilitate movement and decrease resistance to gene flow. The large white triangle in the top left contains no information about gene flow. (D) Clines in minimum winter temperatures from rural to urban areas select for genotypes with decreased chemical defenses in white clover (Trifolium repens) (36).

  • Table 1 Examples of evolution in noncommensal species in response to urbanization.

    Columns show species’ common and scientific names; the region of study (Africa, AF; Asia, AS; Europe, EU; North America, NA); the maximum number of cities examined in a single study; whether studies examined molecular genetic (G) or heritable phenotypic (P) evolutionary changes; and the mechanisms of evolution examined (mutation, U; genetic drift, D; gene flow, M; selection, S). A comprehensive list and description of species studied is included in table S1.

    Common nameScientific nameRegionNumber of citiesPhenotypic/
    DengueDengue virus type 4NA-GS, D (58)
    Holy hawksbeardCrepis sanctaEU1PS (39, 72, 73)
    Virginia pepperweedLepidium virginicumNA5G, PS, M (83)
    White cloverTrifolium repensNA4G, PS (36)
    Peppered mothBiston betulariaEU-G, PS (32, 69, 70, 127)
    KillifishFundulus heteroclitusNA4G, PS, D, M (33, 84, 128, 129)
    Amphibians and reptiles
    Crested anoleAnolis cristatellusNA3PS (82)
    Eastern water dragonIntellagama lesueuriiAU1G, PS, D, M (75)
    Red-backed salamanderPlethodon cinereusNA1GD, M (46, 130)
    Common wall lizardPodarcus muralisEU1GM (61)
    Fire salamanderSalamandra salamandraEU2GD, M (47, 131)
    House finchCarpodacus mexicanusNA1G, PS (71, 132)
    Dark-eyed juncoJunco hyemalisNA1PS, D (76, 81, 111, 133)
    Herring gullLarus argentatusNA6GU (30, 126)
    Common blackbirdTurdus merulaEU13P, GS, D, M (38, 51, 78, 134, 135)
    Striped field mouseApodemus agrariusEU1GD, M (43, 136)
    HumanHomo sapiensAF,AS,
    17GS (86)
    BobcatLynx rufusNA1GS, D, M (57)
    White-footed mousePeromyscus leucopusNA1GS, D, M (37, 65, 85, 112, 137, 138)
  • Table 2 Contemporary evolution of human commensals in urban environments.

    Columns show species’ common and scientific names, the evolutionary processes studied, and corresponding references

    Common nameScientific nameEvolutionary processesReferences
    German cockroachBlatella germanicaSelection: Sugar-baited pesticides impose selection that
    causes evolution of glucose aversion.
    Genetic drift: Pesticide treatment and founder events cause
    Gene flow: Genetic differentiation increases with spatial scale,
    being lowest within buildings, higher between buildings,
    and greatest between cities and continents.
    (93, 100, 139, 140)
    Bed bugCimex lectulariusSelection: Insecticide application drives evolution of resistance.
    Genetic drift: Population bottlenecks cause a loss of genetic
    diversity within populations.
    Gene flow: Limited dispersal contributes to high genetic
    differentiation between populations.
    (56, 94, 123, 141144)
    Northern house mosquitoCulex pipiens (molestus)Selection: Underground populations do not require a blood
    meal to lay eggs, lack a winter diapause and are reproductively
    isolated from aboveground populations.
    Genetic drift: Underground populations have less
    genetic diversity and are genetically differentiated from
    aboveground populations.
    (52, 53, 145, 146)
    Rock dove (aka “pigeon”)Columba liviaSelection: Darker morphs (with white rumps) exhibit lower
    predation to falcons, higher survival as young when exposed to
    lead, and greater defense against parasites.
    House mouseMus musculusGene flow: Populations exhibit patterns of early dispersal and
    population expansion, followed by patterns that mirror
    human migration and settlement patterns.
    Head and body licePediculus humanusSelection: Increased frequency of resistance to pesticides
    through time, which is related to mutations in
    the VSSC α-subunit gene.
    Norway ratRattus norvegicusSelection: Evolve resistance to warfarin pesticides through
    mutations in VKORCI.
    Genetic drift: Populations exhibit little evidence of inbreeding.
    Gene flow: There is moderate genetic differentiation
    and genetic clustering of populations, which is attributed to limited
    dispersal and natural barriers to gene flow.
    (92, 95, 98, 151, 152)
    Black ratRattus rattusGene flow: Populations exhibit substantial genetic clustering
    and patterns of dispersal and population expansion that reflect
    human dispersal and settlement.
  • Evolution of life in urban environments

    Marc T. J. Johnson and Jason Munshi-South

    Materials/Methods, Supplementary Text, Tables, Figures, and/or References

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    • Table S1 
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