Abstract

Cities are emerging as models for addressing the fundamental question of whether populations evolve in parallel to similar environments. Here, we examine the environmental factors that drive the evolution of parallel urban‐rural clines in a Mendelian trait—the cyanogenic antiherbivore defense of white clover (Trifolium repens). Previous work suggested urban‐rural gradients in frost and snow depth could drive the evolution of reduced hydrogen cyanide (HCN) frequencies in urban populations. Here, we sampled over 700 urban and rural clover populations across 16 cities along a latitudinal transect in eastern North America. In each population, we quantified changes in the frequency of genotypes that produce HCN, and in a subset of the cities we estimated the frequency of the alleles at the two genes (CYP79D15 and Li) that epistatically interact to produce HCN. We then tested the hypothesis that cold climatic conditions are necessary for the evolution of cyanogenesis clines by comparing the strength of clines among cities located along a latitudinal gradient of winter temperature and frost exposure. Overall, half of the cities exhibited urban‐rural clines in the frequency of HCN, whereby urban populations evolved lower HCN frequencies. Clines did not evolve in cities with the lowest temperatures and greatest snowfall, supporting the hypothesis that snow buffers plants against winter frost and constrains the formation of clines. By contrast, the strongest clines occurred in the warmest cities where snow and frost are rare, suggesting that alternative selective agents are maintaining clines in warmer cities. Some clines were driven by evolution at only CYP79D15, consistent with stronger and more consistent selection on this locus than on Li. Together, our results demonstrate that urban environments often select for similar phenotypes, but different selective agents and targets underlie the evolutionary response in different cities.

Highlights

  • The extent to which populations adapt in parallel to similar environmental conditions remains a fundamental problem in evolutionary biology (Losos 2017; Bolnick et al 2018)

  • Annual aridity index was not significant predictor of mean hydrogen cyanide (HCN) frequencies in our model (P = 0.36, Table S5) while soil moisture deficit was not included in any top models following model selection and averaging

  • Urbanization was associated with reduced HCN frequencies across cities, whereby the main effect of standardized distance from the urban center was positively associated with the aCC-BY-NC-ND 4.0 International license

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Summary

Introduction

The extent to which populations adapt in parallel to similar environmental conditions remains a fundamental problem in evolutionary biology (Losos 2017; Bolnick et al 2018). High levels of genetic and phenotypic parallelism suggest that adaptive evolution is constrained, increasing our confidence in predicting species’ responses to similar conditions (Losos 2011). Cities tend to share many biotic and abiotic environmental variables such as increased temperatures, elevated pollution, greater habitat fragmentation, and altered structure and composition of ecological communities (McKinney 2006), which can drive parallel adaptive evolution (Reid et al 2016; Winchell et al 2016; Yakub and Tiffin 2016; Kern and Langerhans 2018)

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