Urbanization drives parallel adaptive clines in plant populations

Abstract

13Urban areas are a new and increasingly dominant feature of terrestrial landscapes that 14 dramatically alter environments. It is unclear whether wild populations can adapt to the 15 unique challenges presented by urbanization. To address this problem, we sampled the 16 frequency of a Mendelian-inherited trait-cyanogenesis-in white clover (Trifolium 17 repens L.) plants along urbanization gradients in four large cities. Cyanogenesis protects 18 plants from herbivores, but also reduces freezing tolerance. Plants evolved reduced 19 cyanogenesis with increasing proximity to the urban center in three of the four cities. In 20 an experiment, we demonstrate that gradients in herbivore pressure do not cause these 21 clines. Instead, urban areas experience relatively cold minimum winter ground 22 temperatures because of reduced snow cover within cities, which selects against 23 2 cyanogenesis. Together, our study demonstrates that wild populations exhibit parallel 24 adaptive evolution in response to urbanization, which likely facilitates the persistence of 25 these plants and promotes pollinator abundance and diversity. 26 27 Main Text 28 (hereafter Ac) and Li; Plants must have dominant alleles at both loci to produce HCN 47 . The two components are stored separately in cells to avoid self-48 toxicity, and form HCN when they are brought together following tissue damage. 49Previous research found that cyanogenesis is most frequent in populations at low latitudes 50 and elevations, where herbivory is often highest and temperatures are warmer (Daday 51 1954a). It has been hypothesized that herbivores select for cyanogenesis in these warm 52 environments (Hughes 1991; Kooyers and Olsen 2012). In cold climates, cyanogenesis is 53 selected against because freezing temperatures lyse cells and trigger HCN release, 54 causing self-toxicity in cyanogenic plants (Daday 1958;Hughes 1991). 55 Environmental change associated with urbanization may alter natural selection on 56 cyanogenesis. Whereas herbivores are not consistently affected by urbanization (Raupp et 57 al. 2010), air temperatures are generally warmer in urban areas relative to non-urban 58 areas (Landsberg 1981). This may cause urban populations to experience fewer freezing 59 events than non-urban populations during winter (Parris and Hazell 2005), and 60consequently weaken selection against cyanogenesis in cities. Thus, we predicted that 61 cyanogenesis would increase in frequency with increasing proximity to urban centers. We 62 surveyed 2379 plants from 121 populations of white clover along three 50-km transects 63 radiating outward from downtown Toronto, Canada (Fig. S1), and screened them for their 64 ability to produce HCN. To confirm that selection is acting on HCN, and not on Ac or Li 65 individually for unrelated functions, we also quantified the frequencies of the Ac and Li 66 alleles. 67 68 69 4 Results and Discussion 70We found consistent changes in the frequency of cyanogenesis along each transect, but 71 clines were in the opposite direction to our predi...

Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators

“…We surveyed older nonsenescing (i.e., still completely green) leaves to ensure enough time had passed for herbivore damage to accumulate and to provide leaf age standardized estimates of herbivory across plants. Visual estimates of percentage leaf area lost provide results consistent with those derived from image software analyses (Johnson, Bertrand, & Turcotte, ) and are sensitive enough to detect defence‐mediated differences in herbivore damage in this system (Thompson & Johnson, ; Thompson, Renaudin, & Johnson, ). We also quantified the amount of floral damage by visually estimating the amount of area removed on each of five randomly selected banner petals (i.e., standard petal) from the middle whorl of a single, randomly selected inflorescence per plant; the mean of these measurements was used as an estimate of plant‐level floral damage.…”

City life on fast lanes: Urbanization induces an evolutionary shift towards a faster lifestyle in the water flea Daphnia

“…Our study involved multiple genotypes isolated from a total of 13 populations along independent urbanization gradients in Flanders (Northern Belgium). The observation that the differentiation among rural and urban populations was highly repeatable, as illustrated by the population averages plotted in Figure , indicates that the observed evolutionary changes are a general response to urbanization in this species in the study region (see also Johnson, Thompson, & Saini, ; Thompson, Renaudin, & Johnson, ; Tüzün et al., ). Our results on local adaptation at short spatial scales (Richardson, Urban, Bolnick, & Skelly, ) are in line with previous studies providing evidence for adaptive genetic trait change to other anthropogenic disturbances in water fleas over short time‐scales (months to a few years) and spatial distances (Geerts et al., ; Hairston, Ellner, Geber, Yoshida, & Fox, ; Jansen et al., ; Zhang, Jansen, De Meester, & Stoks, ), and with our earlier results on the evolution of a higher thermal tolerance in city populations (Brans, Jansen, et al., ).…”

“…As an increasing number of studies report genetic adaptation to urbanization in organisms ranging from plants (Cheptou et al., ; Johnson et al., ; Thompson et al., ) over insects (Diamond et al., ; Tüzün et al., ) to birds (Atwell et al., ; Mueller, Partecke, Hatchwell, Gaston, & Evans, ), understanding and predicting how populations and species respond to regional and local increases in urbanization will require insights on evolutionary trait change. For all eight studied traits, trait changes that result from adaptation to urbanized settings are in the same direction as the plasticity‐mediated responses to temperature increase (Figure a).…”

Moving past the challenges and misconceptions in urban adaptation research

“…Inclusion of local communities in urban and non-urban systems alike can improve the success of methodological approaches via the incorporation of local knowledge (Uprety et al 2012, Camacho et al 2021) and will help improve researcher outcomes in terms of safety, access, and study continuity (e.g., continued or repeated access, reduced vandalism). There are several examples where integrated approaches have been used to build a more comprehensive picture of urban adaptation: research onAnolis lizards has incorporated behavioral, phenotypic, experimental, and genomic analyses to understand adaptation to thermal and structural habitats (Winchell et al 2016, Aviles-Rodriguez et al 2019, Campbell-Staton et al 2020; work on white clover (Trifolium repens ) has involved the global community in sampling efforts complemented with experimental, phenotypic, and whole genome sequencing analyses to test for parallelism (Thompson et al 2016, Santangelo et al 2020b; research on Galapagos finches (Geospiza spp.) has employed morphometrics and behavioral approaches to understand how access to human foods alter historical patterns of diet-based selection on beak shape (De León et al 2011; and a combination of reciprocal transplants, phenotypic variation, and mate choice experiments in Tungara frogs (Engystomops pustulosus ) has revealed adaptive sexual selection (Halfwerk et al 2019).…”