Urban colonization through multiple genetic lenses: The city‐fox phenomenon revisited

Abstract

Urbanization is driving environmental change on a global scale, creating novel environments for wildlife to colonize. Through a combination of stochastic and selective processes, urbanization is also driving evolutionary change. For instance, difficulty in traversing human‐modified landscapes may isolate newly established populations from rural sources, while novel selective pressures, such as altered disease risk, toxicant exposure, and light pollution, may further diverge populations through local adaptation. Assessing the evolutionary consequences of urban colonization and the processes underlying them is a principle aim of urban evolutionary ecology. In the present study, we revisited the genetic effects of urbanization on red foxes ( Vulpes vulpes ) that colonized Zurich, Switzerland. Through use of genome‐wide single nucleotide polymorphisms and microsatellite markers linked to the major histocompatibility complex (MHC), we expanded upon a previous neutral microsatellite study to assess population structure, characterize patterns of genetic diversity, and detect outliers associated with urbanization. Our results indicated the presence of one large evolutionary cluster, with substructure evident between geographic sampling areas. In urban foxes, we observed patterns of neutral and functional diversity consistent with founder events and reported increased differentiation between populations separated by natural and anthropogenic barriers. We additionally reported evidence of selection acting on MHC‐linked markers and identified outlier loci with putative gene functions related to energy metabolism, behavior, and immunity. We concluded that demographic processes primarily drove patterns of diversity, with outlier tests providing preliminary evidence of possible urban adaptation. This study contributes to our overall understanding of urban colonization ecology and emphasizes the value of combining datasets when examining evolutionary change in an increasingly urban world.

Beyond the landscape: Resistance modelling infers physical and behavioural gene flow barriers to a mobile carnivore across a metropolitan area

“…While a founder effect may have created an initial reduction in genetic diversity among urban foxes, impermeable border fortifications could have limited gene flow and thus artificially maintained genetic differentiation between urban and rural foxes. However, genetic exchange between urban and rural foxes must also have remained sufficiently low in the ensuing 30 years to maintain genetic structure (with generation time being 2–3 years, DeCandia et al, ). Based on F ST values ( F ST ≥ 0.027), Wandeler et al () detected genetic differentiation between urban and rural foxes for the then recently (15 years) established fox population within Zurich.…”

“…However, assignment tests provided evidence for ongoing urban‐rural gene flow. A recent re‐analysis of the same data set identified only one evolutionary cluster (DeCandia et al, ). Further research in other metropolitan areas might help to clarify whether the urban island is a general phenomenon or a specificity of Berlin.…”

Biologia Futura: adaptive changes in urban populations

“…Many of the identified candidate genes have functions related to the metabolism and transport of lipids and carbohydrates, suggesting that selection acts on metabolic pathways in mice due to their novel diets in cities (Harris and Munshi-South 2017). Similar studies in other species indicate positive selection on candidate genes linked to various functions that may be involved in urban adaptations, including metabolism, detoxification, oxidative stress, heat tolerance, immunity, morphology, and behaviour (Reid et al 2016;Ravinet et al 2018;Theodorou et al 2018;DeCandia et al 2019).…”

Spatiotemporal spread of sarcoptic mange in the red fox (Vulpes vulpes) in Switzerland over more than 60 years: lessons learnt from comparative analysis of multiple surveillance tools

“…Demographic bottlenecks and population separations may lead to a decrease of genetic diversity [77]. This may limit the adaptive potential of populations to pathogens [78, 79] and, in turn, influence disease dynamics and increase vulnerability to diseases [80, 81]. The fox population collapse (already denominated as “rabies pit” [56]) in the Plateau and the Jura may have impaired, on the one hand, the transmission of S. scabiei due to the reduced density and therefore contacts among foxes and, on the other hand, removed diseased and also resistant individuals, disrupting the long-term host-parasite adaptation and generating a susceptible “naïve-like” population.…”