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.
Highlights
Urbanization is increasing worldwide and broadly affecting wildlife across the growing rural–urban gradient (Knapp, Winter, & Klotz, 2017; Magle, Hunt, Vernon, & Crooks, 2012)
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
Can we identify evidence of selection at MHC‐linked markers or outlier SNPs associated with urban colonization?
Summary
Urbanization is increasing worldwide and broadly affecting wildlife across the growing rural–urban gradient (Knapp, Winter, & Klotz, 2017; Magle, Hunt, Vernon, & Crooks, 2012). A similar pattern emerged in urban bobcats following a severe mange outbreak exacerbated by anticoagulant rodenticide exposure (Serieys, Lea, Pollinger, Riley, & Wayne, 2015) In these and other systems, balancing selection maintained diversity at MHC genes (Ferrer‐Admetlla et al, 2008); perhaps due to the selective advantage immunogenetic variation confers against disease risk (DeCandia, Dobson, & vonHoldt, 2018; Spielman et al, 2004). City foxes may experience different disease pressures than rural foxes, as seen with the zoonotic cestode Echinococcus multilocularis transmission cycle within Zurich city foxes (Hofer et al, 2000; Otero‐Abad, Rüegg, Hegglin, Deplazes, & Torgerson, 2017) These variable selection pressures, combined with shifts in behavior to avoid human interactions (Gloor et al, 2001; Sih et al, 2011; Soulsbury, Baker, Iossa, & Harris, 2010), could facilitate strong pressures on city foxes not present in rural conspecifics and shape genetic differentiation between the subpopulations. Through examination of genome‐wide SNPs and MHC‐linked microsatellites, we addressed the following questions with a subset of the original Wandeler et al (2003) samples: 1. Do we observe subpopulation structure between urban and rural foxes in Zurich?
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