Parallel evolution of urban–rural clines in melanism in a widespread mammal

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.

The effects of environmental heterogeneity within a city on the evolution of clines

“…Recently, urban areas have been shown to be a potent driver of evolutionary change, capable of affecting all principle mechanisms of evolution, including mutation, genetic drift, gene flow and natural selection (Johnson & Munshi‐South, 2017; Szulkin, Munshi‐South, et al, 2020). An increasing number of studies are treating global urbanization as a large‐scale unplanned experiment, as a way to study parallel evolution (Cosentino & Gibbs, 2022; Perrier et al, 2020; Santangelo, Miles, et al, 2020), and in particular adaptation to anthropogenically mediated environmental change (Alberti et al, 2016; Donihue & Lambert, 2014; Mueller et al, 2013; Winchell et al, 2016). The majority of studies of adaptation to urbanization treat urban areas as either homogeneous environments, contrasting urban versus non‐urban areas (Szulkin, Garroway, et al, 2020; Theodorou et al, 2018; Winchell et al, 2016), or as continuous gradients of environmental change (Santangelo, Thompson, et al, 2020).…”

“…

Global urbanization is causing dramatic changes to the physical environment and the biota living within cities (Grimm et al, 2008).Recently, urban areas have been shown to be a potent driver of evolutionary change, capable of affecting all principle mechanisms of evolution, including mutation, genetic drift, gene flow and natural selection (Johnson & Munshi-South, 2017;Szulkin, Munshi-South, et al, 2020). An increasing number of studies are treating global urbanization as a large-scale unplanned experiment, as a way to study parallel evolution (Cosentino & Gibbs, 2022;

…”

Colour scales with climate in North American ratsnakes: a test of the thermal melanism hypothesis using community science images

“…Using Google Images, Leighton et al [39] spearheaded the use of community-sourced images to study trait variation. More recently, studies have harnessed the abundance of iNaturalist community science images to examine intraspecific variation in traits like coloration [40][41][42][43], in addition to studying phenological trends [44][45][46][47] and predation rates [16]. Our study is the first to test range-wide colour and climate associations in North American ratsnakes, which is likely due to the challenges with documenting colour in these snakes.…”

Rural selection drives the evolution of an urban-rural cline in coat color in gray squirrels

“…Homozygotes for the deletion allele are black, whereas homozygotes for the recessive wild-type allele are gray. Melanics were the prevailing color morph in the northeastern United States prior to massive deforestation during European colonialism in the 18 th and 19 th centuries (e.g., Allen 1943, Schorger 1949, Robertson 1973), but today melanics are rare in rural forests and more common in urban areas, with urban-rural clines in melanism apparent across multiple cities (Cosentino and Gibbs 2022). These urban-rural clines are most evident in cities with relatively cold winter temperatures, where the deletion allele for melanism is likely maintained by selection for greater thermogenic capacity at cold temperature (Ducharme et al 1989).…”

“…First, we characterized spatial variation in the prevalence of melanism along the urbanization gradient. Previous studies documenting an urban-rural cline in this area were based on incidentally encountered squirrels via community science, which likely have spatial biases in sampling effort and detection of rare color morphs (Cosentino and Gibbs 2022). Here we used standardized surveys via remote cameras and visual counts and a novel hierarchical model that accounts for imperfect detection probability to test for an urban-rural cline.…”