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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. 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 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 near neutrality in the city. Our findings demonstrate that selection outside the city can be sufficient to maintain urban-rural clines, and 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, highlighting the complex and sometimes protective role of urban landscapes in evolutionary processes. 

ABSTRACT Cities impose unique selection pressures on wildlife and generate clines in phenotypic traits along urban–rural gradients. Roads are a widespread feature of human‐dominated landscapes and are known to cause direct wildlife mortality; however, whether they act as a selective force influencing phenotypic trait variation along urban–rural gradients remains unclear. This study tested the hypothesis that roads influence natural selection of coat color in the eastern gray squirrel (Sciurus carolinensis), a species with two distinct coat colors: a gray morph that is common in all areas and a melanic morph more prevalent in urban areas than in rural ones. Vehicular collisions are a significant cause of mortality in eastern gray squirrels, with the melanic morph more visually conspicuous on roads and more easily detected and avoided by drivers than the gray morph. Standardized road cruise surveys along an urbanization gradient in Syracuse, New York, USA, revealed that the prevalence of melanism among living squirrels in Syracuse was negatively related to distance from the city center, whereas there was no urban–rural cline in melanism among road‐killed individuals, with the melanic morph underrepresented among road‐killed squirrels by up to 30% along the urbanization gradient. An examination of the prevalence of each color morph on and off road surfaces in a range‐wide compilation of > 100,000 photographs ofS. carolinensisalso indicated that the melanic morph was underrepresented among road‐killed squirrels imaged. Our study highlights vehicular collisions as an important source of natural selection on phenotypic traits, suggesting a potential role in shaping patterns of urban evolution and contributing to the maintenance of urban–rural clines. 

Abstract Phenotypic differences between urban and rural populations are well‐documented, but the evolutionary processes driving trait variation along urbanization gradients are often unclear. We combined spatial data on abundance, trait variation, and measurements of fitness to understand cline structure and test for natural selection on heritable coat color morphs (melanic, gray) of eastern gray squirrels (Sciurus carolinensis) along an urbanization gradient. Population surveys using remote cameras and visual counts at 76 sites along the urbanization gradient revealed a significant cline in melanism, decreasing from 48% in the city center to <5% in rural woodlands. Among 76 squirrels translocated to test for phenotypic selection, survival was lower for the melanic than gray morph in rural woodlands, whereas there was no difference in survival between color morphs in the city. These results suggest the urban–rural cline in melanism is explained by natural selection favoring the gray morph in rural woodlands combined with relaxed selection in the city. Our study illustrates how trait variation between urban and rural populations can emerge from selection primarily in rural populations rather than adaptation to novel features of the urban environment. 

Abstract Urbanization is the dominant trend of global land use change. The replicated nature of environmental change associated with urbanization should drive parallel evolution, yet insight into the repeatability of evolutionary processes in urban areas has been limited by a lack of multi-city studies. Here we leverage community science data on coat color in > 60,000 eastern gray squirrels (Sciurus carolinensis) across 43 North American cities to test for parallel clines in melanism, a genetically based trait associated with thermoregulation and crypsis. We show the prevalence of melanism was positively associated with urbanization as measured by impervious cover. Urban–rural clines in melanism were strongest in the largest cities with extensive forest cover and weakest or absent in cities with warmer winter temperatures, where thermal selection likely limits the prevalence of melanism. Our results suggest that novel traits can evolve in a highly repeatable manner among urban areas, modified by factors intrinsic to individual cities, including their size, land cover, and climate. 

Abstract Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest‐dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation‐by‐distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas.