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 in gray squirrels. We show the prevalence of melanism in these mammals was positively associated with urbanization. Urban-rural clines in melanism were strongest in the largest cities with extensive forest cover and weakest or absent in cities with warm winter temperature, where thermal selection likely limits the prevalence of melanism. Our results demonstrate that novel traits can evolve in a highly repeatable manner among urban areas, modified by factors intrinsic to individual cities, including size, land cover, and climate.

Moving past the challenges and misconceptions in urban adaptation research

“…One approach to building a foundation of natural history information for urban organisms that have been successful in non‐urban environments (Fontaine et al, 2021 ; Sforzi et al, 2018 ) is to incorporate community‐sourced data collection into research. For example, Puckett et al ( 2020 ) used museum specimens to study changes in brown rat cranial shape over time, and Cosentino and Gibbs ( 2022 ) used community‐sourced data to demonstrate the parallel evolution of clines in melanic Eastern gray squirrels ( Sciurus carolinensis ). However, community‐sourced data is often limited as a result of socioeconomic biases of regions sampled or as a result of limited sampling of overlooked, camouflaged, or microscopic species that are less charismatic (Shirey et al, 2021 ).…”

“…In addition to a more quantitative assessment of urban environments, the global study of cities that vary in the intensity, age, and characteristics of urbanization will help shed light on the process of urban adaptation and aid in our ability to generalize findings. For example, Cosentino and Gibbs ( 2022 ) were able to disentangle selective agents contributing to parallel and non‐parallel clines in Eastern Gray Squirrel ( S. carolinensis ) melanic coat color associated with urbanization by comparing 43 North American cities that differed in size, age, and geographic location. In a global sample, Santangelo et al ( 2022 ) collected data on white clover ( Trifolium repens ) from over 160 cities worldwide to demonstrate that urbanization can lead to parallel adaptation despite considerable environmental variation among cities.…”

Moving past the challenges and misconceptions in urban adaptation research

“…In addition to a more quantitative assessment of urban environments, the global study of cities that vary in the intensity, age, and characteristics of urbanization will help shed light on the process of urban adaptation and aid in our ability to generalize findings. For example, Cosentino and Gibbs (2022) were able to disentangle selective agents contributing to parallel and non-parallel clines in Eastern Gray Squirrel (S. carolinensis ) melanic coat color associated with urbanization by comparing 43 North American cities that differed in size, age, and geographic location. In a global sample, Santangelo et al (2022) collected data on white clover (Trifolium repens ) from over 160 cities worldwide to demonstrate that urbanization can lead to parallel adaptation despite considerable environmental variation among cities.…”

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

“…2020; Santangelo et al . 2020a; Cosentino & Gibbs 2022), and in particular adaptation to anthropogenically mediated environmental change (Mueller et al . 2013; Donihue & Lambert 2014; Alberti et al .…”

“…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 et al 2020b). An increasing number of studies are treating global urbanization as a large-scale unplanned experiment, as a way to study parallel evolution (Perrier et al 2020;Santangelo et al 2020a;Cosentino & Gibbs 2022), and in particular adaptation to anthropogenically mediated environmental change (Mueller et al 2013;Donihue & Lambert 2014;Alberti et al 2016;Winchell et al 2016). The majority of studies of adaptation to urbanization treat urban areas as either homogeneous environments, contrasting urban versus nonurban areas (Winchell et al 2016;Theodorou et al 2018;Szulkin et al 2020a), or as continuous gradients of environmental change (Santangelo et al 2020b).…”