Natural selection beyond city limits

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Abstract

Urbanization creates heterogeneous selective landscapes that cause the evolution of urban-rural clines in phenotypic traits. Although cities can introduce novel selection pressures, little attention has been paid to the role of selection outside the city in maintaining urban-rural clines. Here we integrate whole genome sequencing, demographic modeling, and complementary models of selection to test how natural selection in both urban and rural environments shapes the evolution of an urban-rural cline in coat color in eastern gray squirrels ( Sciurus carolinensis ). Coat color polymorphism in this species, which presents as either gray or melanic, is primarily determined by a 24-bp deletion in the melanocortin-1 receptor gene ( Mc1R ). Melanic squirrels are often more prevalent in urban environments but rare or absent in rural forests. Whole genome sequencing and demographic modeling revealed substantially greater urban-rural divergence at Mc1R than the genomic background, suggesting urban-rural clines in melanism are maintained by selection. We applied three separate approaches leveraging demographic and genomic data to estimate the selection coefficient against Mc1R alleles in each habitat, producing a surprising, yet consistent finding: strong selection against the melanic morph in the rural environment and neutrality or near neutrality in the city. Our findings demonstrate that selection outside the city can be sufficient to maintain urban-rural clines, and that urban environments can maintain genetic diversity that would otherwise be lost in rural landscapes. This study provides a rare opportunity to unravel both the spatial dynamics and the selective pressures shaping trait variation in a widespread vertebrate species that thrives across diverse landscapes, highlighting the complex and sometimes protective role of urban landscapes in evolutionary processes.

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