Signatures of Rapid Evolution in Urban and Rural Transcriptomes of White-Footed Mice (Peromyscus leucopus) in the New York Metropolitan Area

Abstract

Urbanization is a major cause of ecological degradation around the world, and human settlement in large cities is accelerating. New York City (NYC) is one of the oldest and most urbanized cities in North America, but still maintains 20% vegetation cover and substantial populations of some native wildlife. The white-footed mouse, Peromyscus leucopus , is a common resident of NYC’s forest fragments and an emerging model system for examining the evolutionary consequences of urbanization. In this study, we developed transcriptomic resources for urban P . leucopus to examine evolutionary changes in protein-coding regions for an exemplar “urban adapter.” We used Roche 454 GS FLX+ high throughput sequencing to derive transcriptomes from multiple tissues from individuals across both urban and rural populations. From these data, we identified 31,015 SNPs and several candidate genes potentially experiencing positive selection in urban populations of P . leucopus . These candidate genes are involved in xenobiotic metabolism, innate immune response, demethylation activity, and other important biological phenomena in novel urban environments. This study is one of the first to report candidate genes exhibiting signatures of directional selection in divergent urban ecosystems.

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

“…Our previous study investigated non-synonymous polymorphisms in pooled transcriptome samples and we reported evidence for positive selection in genes dealing with metabolism, immunity, and methylation in NYC white-footed mice (Harris et al 2013). This current study supports the phenotypic traits likely under selection in urban environments, identifying outlier genes that play major roles in metabolism, and to a lesser extent, immunity, but few outlier genes were identified in both the current and previous studies.…”

“…In brief, we randomly chose eight adult white-footed mice (equal numbers of males and females) from each of six sampling locations (N = 48 total) representative of urban and rural habitats and with minimal within-site genetic structure (Fig. 1) (Harris et al 2013, 2015). Three sampling sites were within NYC parks: Central Park in Manhattan (CP), New York Botanical Gardens in the Bronx (NYBG), and Flushing Meadows—Willow Lake in Queens (FM).…”

“…There is also substantial genetic structure between NYC parks as measured by microsatellites (Munshi-South & Kharchenko 2010), genome-wide SNPs (Munshi-South et al 2016) and demographic modeling (Harris et al 2016). We have also previously identified signatures of selection in urban populations of NYC white-footed mice (Harris et al 2013), though we used smaller datasets and more limited approaches than presented here.…”

Adaptive evolution in urban ecosystems

“…There is also evidence for repeated selection on the SERT gene, which regulates anxiety behavior (e.g., harm avoidance), in European blackbirds across a suite of cities (including Madrid, Berlin, and Prague; Mueller et al 2013). New York City mice also show genetic divergences at loci important for traits like immune response, metabolism, and spermatogenesis (Harris et al 2013). While the latter three studies have shown a genetic basis for a trait change in urban settings, none have determined whether these traits are indeed adaptive (i.e., if there is a reproductive or fitness benefit).…”

Urbanization shapes the demographic history of a native rodent (the white-footed mouse, Peromyscus leucopus ) in New York City

“…White-footed mice are abundant in small, fragmented urban forests [14][15][16] and exchange migrants only through vegetated corridors between isolated NYC parks [17]. Substantial genetic structure at microsatellite loci exists between NYC parks [8], and there is evidence of divergence and selection in genes underlying functional traits in urban populations [18].…”