Urban park characteristics, genetic variation, and historical demography of white-footed mouse (Peromyscus leucopus) populations in New York City

Abstract

Severe fragmentation is a typical fate of native remnant habitats in cities, and urban wildlife with limited dispersal ability are predicted to lose genetic variation in isolated urban patches. However, little information exists on the characteristics of urban green spaces required to conserve genetic variation. In this study, we examine whether isolation in New York City (NYC) parks results in genetic bottlenecks in white-footed mice (Peromyscus leucopus), and test the hypotheses that park size and time since isolation are associated with genetic variability using nonlinear regression and information-theoretic model selection. White-footed mice have previously been documented to exhibit male-biased dispersal, which may create disparities in genetic variation between males and females in urban parks. We use genotypes of 18 neutral microsatellite data and four different statistical tests to assess this prediction. Given that sex-biased dispersal may create disparities between population genetic patterns inferred from bi- vs. uni-parentally inherited markers, we also sequenced a 324 bp segment of the mitochondrial D-loop for independent inferences of historical demography in urban P. leucopus. We report that isolation in urban parks does not necessarily result in genetic bottlenecks; only three out of 14 populations in NYC parks exhibited a signature of a recent bottleneck at 18 neutral microsatellite loci. Mouse populations in larger urban parks, or parks that have been isolated for shorter periods of time, also do not generally contain greater genetic variation than populations in smaller parks. These results suggest that even small networks of green spaces may be sufficient to maintain the evolutionary potential of native species with certain characteristics. We also found that isolation in urban parks results in weak to nonexistent sex-biased dispersal in a species known to exhibit male-biased dispersal in less fragmented environments. In contrast to nuclear loci, mitochondrial D-loop haplotypes exhibited a mutational pattern of demographic expansion after a recent bottleneck or selective sweep. Estimates of the timing of this expansion suggest that it occurred concurrent with urbanization of NYC over the last few dozens to hundreds of years. Given the general non-neutrality of mtDNA in many systems and evidence of selection on related coding sequences in urban P. leucopus, we argue that the P. leucopus mitochondrial genome experienced recent negative selection against haplotypes not favored in isolated urban parks. In general, rapid adaptive evolution driven by urbanization, global climate change, and other human-caused factors is underappreciated by evolutionary biologists, but many more cases will likely be documented in the near future.

Trapped within the city: integrating demography, time since isolation and population‐specific traits to assess the genetic effects of urbanization

“…No€ el & Lapointe 2010; Munshi-South & Nagy 2014), no urban genetics studies have incorporated quantitative estimates of contemporary N e to characterize the genetic effects of urbanization. Additionally, the effects of time since isolation were only considered as a predictor of genetic diversity and differentiation in two studies (Delaney et al 2010;Munshi-South & Nagy 2014), though both showed contrasting results, illustrating the difficulties in accurately quantifying its effects.…”

“…To our knowledge, while a handful of studies on urban populations have examined evidence of past bottlenecks (e.g. Noël & Lapointe ; Munshi‐South & Nagy ), no urban genetics studies have incorporated quantitative estimates of contemporary N e to characterize the genetic effects of urbanization. Additionally, the effects of time since isolation were only considered as a predictor of genetic diversity and differentiation in two studies (Delaney et al .…”

Population genomics of the Anthropocene: urbanization is negatively associated with genome‐wide variation in white‐footed mouse populations

“…Previous microsatellite‐based analyses on this system showed substantial genetic structure between white‐footed mouse populations in NYC's forest fragments (Munshi‐South and Kharchenko ). Park area, age, or the extent of habitat within parks did not explain levels of genetic variation among these populations (Munshi‐South and Nagy ), but these studies focused exclusively on forest fragments within NYC that were highly isolated by surrounding urbanization. In a separate analysis, we identified SNPs from transcriptomes sequenced from urban and rural populations, and found that population structure was greater among the urban than the rural populations (Harris et al.…”

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

“…readily adapt to environmental change (Linnen et al, 2009;Mullen & Hoekstra, 2008;Munshi-South & Richardson, 2017;Natarajan et al, 2013;Storz, Runck, Moriyama, Weber, & Fago, 2010;Storz, Sabatino, & Hoffmann, 2007;Storz et al, 2009;Weber, Peterson, & Hoekstra, 2013), making them good subjects for the study of local adaptation. White-footed mice are one of the few native mammals that thrive in extremely small, fragmented urban forests in North America (Munshi-South & Nagy, 2014;Pergams & Lacy, 2008;Rogic, Tessier, Legendre, Lapointe, & Millien, 2013), and tend to be found at higher densities in urban vs. rural patches due to a thick understory providing abundant food resources and HARRIS AND MUNSHI-SOUTH | 6337 exclusion of major predators and competitors (Rytwinski & Fahrig, 2007). Increased density may also be due to limited P. leucopus dispersal between urban sites.…”