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

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          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.

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          Most cited references72

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          DnaSP, DNA polymorphism analyses by the coalescent and other methods.

          DnaSP is a software package for the analysis of DNA polymorphism data. Present version introduces several new modules and features which, among other options allow: (1) handling big data sets (approximately 5 Mb per sequence); (2) conducting a large number of coalescent-based tests by Monte Carlo computer simulations; (3) extensive analyses of the genetic differentiation and gene flow among populations; (4) analysing the evolutionary pattern of preferred and unpreferred codons; (5) generating graphical outputs for an easy visualization of results. The software package, including complete documentation and examples, is freely available to academic users from: http://www.ub.es/dnasp
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            Gene flow and the geographic structure of natural populations.

            M Slatkin (1987)
            There is abundant geographic variation in both morphology and gene frequency in most species. The extent of geographic variation results from a balance of forces tending to produce local genetic differentiation and forces tending to produce genetic homogeneity. Mutation, genetic drift due to finite population size, and natural selection favoring adaptations to local environmental conditions will all lead to the genetic differentiation of local populations, and the movement of gametes, individuals, and even entire populations--collectively called gene flow--will oppose that differentiation. Gene flow may either constrain evolution by preventing adaptation to local conditions or promote evolution by spreading new genes and combinations of genes throughout a species' range. Several methods are available for estimating the amount of gene flow. Direct methods monitor ongoing gene flow, and indirect methods use spatial distributions of gene frequencies to infer past gene flow. Applications of these methods show that species differ widely in the gene flow that they experience. Of particular interest are those species for which direct methods indicate little current gene flow but indirect methods indicate much higher levels of gene flow in the recent past. Such species probably have undergone large-scale demographic changes relatively frequently.
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              Null Hypothesis Testing: Problems, Prevalence, and an Alternative

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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ
                PeerJ Inc. (San Francisco, USA )
                2167-8359
                13 March 2014
                2014
                : 2
                : e310
                Affiliations
                [1 ]Department of Biological Sciences and the Louis Calder Center—Biological Field Station, Fordham University , Armonk, NY, USA
                [2 ]Mianus River Gorge Preserve , Bedford, NY, USA
                Article
                310
                10.7717/peerj.310
                3961106
                55e4d50e-d750-49c0-b7b9-70728487906b
                © 2014 Munshi-South et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 23 December 2013
                : 25 February 2014
                Funding
                Funded by: National Science Foundation
                Award ID: DEB 0817259
                Funded by: National Institute of General Medical Sciences/National Institutes of Health
                Award ID: 1R15GM099055-01A1
                This work was funded by grants from the National Science Foundation (DEB 0817259) and National Institute of General Medical Sciences/National Institutes of Health (1R15GM099055-01A1) to Jason Munshi-South. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Conservation Biology
                Ecology
                Evolutionary Studies
                Genetics
                Zoology

                population genetics,genetic variation,mitochondrial dna,urban ecology,sex-biased dispersal,selective sweep,genetic bottleneck,historical demography,urban evolutionary biology,peromyscus leucopus

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