Signatures of positive selection and local adaptation to urbanization in white‐footed mice (Peromyscus leucopus)

Abstract

Urbanization significantly alters natural ecosystems and has accelerated globally. Urban wildlife populations are often highly fragmented by human infrastructure, and isolated populations may adapt in response to local urban pressures. However, relatively few studies have identified genomic signatures of adaptation in urban animals. We used a landscape genomics approach to examine signatures of selection in urban populations of white-footed mice (Peromyscus leucopus) in New York City. We analyzed 154,770 SNPs identified from transcriptome data from 48 P. leucopus individuals from three urban and three rural populations, and used outlier tests to identify evidence of urban adaptation. We accounted for demography by simulating a neutral SNP dataset under an inferred demographic history as a null model for outlier analysis. We also tested whether candidate genes were associated with environmental variables related to urbanization. In total, we detected 381 outlier loci and after stringent filtering, identified and annotated 19 candidate loci. Many of the candidate genes were involved in metabolic processes, and have well-established roles in metabolizing lipids and carbohydrates. Our results indicate that white-footed mice in NYC are adapting at the biomolecular level to local selective pressures in urban habitats. Annotation of outlier loci suggest selection is acting on metabolic pathways in urban populations, likely related to novel diets in cities that differ from diets in less disturbed areas.

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

“…Although urbanization can homogenize a multispecies wildlife community, urban gradients can lead to population subdivision within a species due to reduced gene flow across urban barriers and divergent selection pressures between rural and urban conspecifics (Johnson & Munshi-South, 2017;Santangelo, Ruth Rivkin, & Johnson, 2018). Urban barriers include buildings, freeways, and densely populated areas (such as city centers), with divergent selection pressures including varied noise and light pollution, diet, and disease and toxicant exposure between urban and rural environments (Brans, Stoks, & De Meester, 2018;Harris & Munshi-South, 2017;Isaksson, 2015;Ouyang et al, 2017;Sih, Ferrari, & Harris, 2011). The possibility for urban-rural gradients facilitating divergence has created a need for more research dedicated to assessing the evolutionary changes associated with urbanization (Alberti, 2015;Donihue & Lambert, 2015;Santangelo et al, 2018).…”

“…In some cases, urban areas may even serve as "theaters for evolution," where novel selective pressures drive rapid adaptation (Littleford-Colquhoun, Clemente, Whiting, Ortiz-Barrientos, & Frère, 2017). For example, signatures of urban adaptation have been reported for genes associated with lipid and carbohydrate metabolism (Harris & Munshi-South, 2017), harm avoidance behavior (Mueller, Partecke, Hatchwell, Gaston, & Evans, 2013), and toxicant exposure (Reid et al, 2016). Thus, adaptation is a potent force that can influence divergence in rural-urban conspecifics during initial colonization and longer-term persistence.…”

“…However, through use of neutral microsatellites, it could only assess neutral genetic structure without considering potential adaptive differences. For example, Zurich foxes may have different selection pressures associated with anthropogenic food availability (Contesse, Hegglin, Gloor, Bontadina, & Deplazes, 2004), which could influence selection on metabolic pathways (Harris & Munshi-South, 2017). City foxes may also 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).…”

Multivariate phenotypic divergence along an urbanization gradient

“…While we can make informed predictions about how particular traits might respond to urbanization from work in other systems, understanding how cities are driving phenotypic evolution requires quantifying divergence in many traits that simultaneously influence fitness. Studies suggest that natural selection drives genome-wide divergence along urbanization gradients (Harris & Munshi-South, 2017;Theodorou et al, 2018), indicating that the targets of natural selection in urban environments can be multifarious. Nevertheless, it is presently unclear to what extent populations exhibit multivariate phenotypic divergence along urbanization gradients and what suites of traits are most often favored as populations become more urbanized.…”

Genetic Adaptation in New York City Rats

“…Although no study to date has examined the genomic signatures of selection in urban rats, studies of another rodent in New York City, the white-footed mouse ( Peromyscus leucopus ), provide hypotheses on the traits subject to selection in urban rodents. Namely, immune response, detoxification of exogenous compounds, spermatogenesis, and metabolism genes were over-represented among putatively-selected exomic regions [25, 26, 27]. These findings may suggest that some genetic adaptations in urban rodents have arisen in response to increased disease pressure in dense urban settings, increased exposure to pollutants and shifts to novel diets.…”