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. 2016 Dec 28;283(1845):20162180.
doi: 10.1098/rspb.2016.2180.

Urbanization drives the evolution of parallel clines in plant populations

Ken A Thompson  1   2 , Marie Renaudin  3 , Marc T J Johnson  4   2
Affiliations

Urbanization drives the evolution of parallel clines in plant populations

Ken A Thompson et al. Proc Biol Sci. .

Abstract

Urban ecosystems are an increasingly dominant feature of terrestrial landscapes. While evidence that species can adapt to urban environments is accumulating, the mechanisms through which urbanization imposes natural selection on populations are poorly understood. The identification of adaptive phenotypic changes (i.e. clines) along urbanization gradients would facilitate our understanding of the selective factors driving adaptation in cities. Here, we test for phenotypic clines in urban ecosystems by sampling the frequency of a Mendelian-inherited trait-cyanogenesis-in white clover (Trifolium repens L.) populations along urbanization gradients in four cities. Cyanogenesis protects plants from herbivores, but reduces tolerance to freezing temperatures. We found that the frequency of cyanogenic plants within populations decreased towards the urban centre in three of four cities. A field experiment indicated that spatial variation in herbivory is unlikely to explain these clines. Rather, colder minimum winter ground temperatures in urban areas compared with non-urban areas, caused by reduced snow cover in cities, may select against cyanogenesis. In the city with no cline, high snow cover might protect plants from freezing damage in the city centre. Our study suggests that populations are adapting to urbanization gradients, but regional climatic patterns may ultimately determine whether adaptation occurs.

Keywords: adaptation; cyanogenesis; herbivory; natural selection; urban evolution; white clover.

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Figures

Figure 1.
Figure 1.
Urban populations of white clover, Trifolium repens, have evolved reduced cyanogenesis relative to non-urban populations in three cities. We observed parallel clines in cyanogenesis in: (a) Toronto (n populations = 121), (b) New York City (n = 48) and (c) Boston (n = 44), but not in (d) Montreal (n = 49). Each point represents the proportion of plants within a population that tested positive for cyanogenesis (mean n per population = 19.7 plants). Statistics were calculated using linear regression.
Figure 2.
Figure 2.
The benefits of cyanogenesis as a defence against herbivores do not explain the observed clines. Our field experiment revealed that cyanogenic plants (HCN+) received less leaf herbivory than acyanogenic plants (HCN−) (p = 0.004, ANOVA), but mean herbivory on both cyanotypes changed little within experimental populations (each n = 38) along an urbanization gradient in Toronto (HCN × distance interaction p = 0.29).
Figure 3.
Figure 3.
Urban ground temperatures were often colder than non-urban ground temperatures. (a) Analysis of daily relative urban coldness values (n = 59) reveals that it was often colder in Toronto during winter 2015 than in non-urban areas (curve is a 95% CI loess-smoothed surface). The inset shows the regression for the day circled in red. We hypothesized that relatively cold urban ground temperatures are caused by urban–rural snow depth gradients, and consistent with this expectation we found (b) a significant positive correlation between the daily relative urban coldness index value and regional snow depth on those days. (Online version in colour.)
Figure 4.
Figure 4.
Historical patterns in January–February snow cover and temperature across the four cities sampled in this study. (a) The NDSI decreased toward the urban centre of each city. The horizontal line at NDSI = 0.4 represents the threshold value for the presence of snow [35]. Montreal (top line) has high snow cover along the entire transect. (b) Montreal (MTL) has fewer days when temperatures are below 0°C and there is no snow cover (±1 s.e.), and (c) deeper snow cover (±1 s.e.) on days where temperatures are less than 0°C, than Toronto (TOR), New York City (NYC) and Boston (BST). Different letters represent significant differences at p < 0.05 (Tukey HSD). (Online version in colour.)
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