Urbanization represents one of the most pervasive forces of anthropogenic change over the last century. More than 50% of the human population now occupies urban areas, and most ecosystems will experience urbanization in the near future. Remnant urban habitat patches often contain extremely high population densities of just a few urban 'adapters' or 'exploiters', leading to biological homogenization. Urban adapters achieve high population densities due to artificially high primary productivity, less severe temperature fluctuations due to the 'heat island' effect, a more stable and abundant food supply from human supplementation, and release from trophic competition in urban environments. Isolated urban populations experiencing the ecological conditions described above may rapidly adapt to local conditions, but few studies have examined this possibility. The emerging field of population genomics uses computational approaches to identify statistical outliers among large numbers of loci that are under selection. Recently, the advent of 'next generation' sequencing has made it possible to generate millions of sequences relatively cheaply and quickly, thus vastly improving the power to detect single nucleotide polymorphisms (SNPs) indicative of local adaptation. We will use these new approaches to examine local adaptation to urbanization among isolated populations of an urban adapter in New York City, the white-footed mouse (Peromyscus leucopus). First, we will generate deep transcriptome sequence for white-footed mice from urban and non-urban populations using 454 pyrosequencing. Gene identity will be established through alignment with annotated rat, mouse, and Peromyscus genomes (Aim 1). We will then identify coding sequences that exhibit statistical signatures of selection at non-synonymous SNPs in urban populations. We will examine these regions in multiple populations to examine whether selection pressures from urbanization result in an 'evolutionary syndrome' of correlated change across the landscape (Aim 2). It is difficult to predict a priori which genes will be under selection, but loci that facilitate dealing with physiological stress from high intraspecific competition, disease, and chronic exposure to pollutants are likely examples. Next, we will examine additional genomic variation between urban vs. non-urban populations due to alternative splicing and differential expression. We will use RNA-seq methodology on the Illumina next-generation sequencing platform to identify alternative splice variants and quantify transcript abundance across populations (Aim 3).

Public Health Relevance

Mammalian species that thrive in urban environments experience higher population densities; enhanced exposure to disease and environmental pollutants; and greater competition for limited resources. Such conditions are predicted to exert substantial selective pressures; but few studies have examined adaptive evolutionary changes in urban populations. The population genomics approach in this study will develop a new mammalian model system (the white-footed mouse; Peromyscus leucopus) for understanding the evolutionary forces that are rapidly shaping the biology of urban organisms.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Academic Research Enhancement Awards (AREA) (R15)
Project #
7R15GM099055-02
Application #
8779865
Study Section
Special Emphasis Panel (ZRG1-GGG-H (90))
Program Officer
Eckstrand, Irene A
Project Start
2012-09-10
Project End
2015-08-31
Budget Start
2013-09-01
Budget End
2015-08-31
Support Year
2
Fiscal Year
2012
Total Cost
$184,364
Indirect Cost
$65,094
Name
Fordham University
Department
Biology
Type
Other Domestic Higher Education
DUNS #
071011019
City
Bronx
State
NY
Country
United States
Zip Code
10458
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Garcia-Elfring, A; Barrett, R D H; Combs, M et al. (2017) Admixture on the northern front: population genomics of range expansion in the white-footed mouse (Peromyscus leucopus) and secondary contact with the deer mouse (Peromyscus maniculatus). Heredity (Edinb) 119:447-458
Harris, Stephen E; Munshi-South, Jason (2017) Signatures of positive selection and local adaptation to urbanization in white-footed mice (Peromyscus leucopus). Mol Ecol 26:6336-6350
Munshi-South, Jason; Richardson, Jonathan L (2017) Peromyscus transcriptomics: Understanding adaptation and gene expression plasticity within and between species of deer mice. Semin Cell Dev Biol 61:131-139
Harris, Stephen E; Xue, Alexander T; Alvarado-Serrano, Diego et al. (2016) Urbanization shapes the demographic history of a native rodent (the white-footed mouse, Peromyscus leucopus) in New York City. Biol Lett 12:
Munshi-South, Jason; Zolnik, Christine P; Harris, Stephen E (2016) Population genomics of the Anthropocene: urbanization is negatively associated with genome-wide variation in white-footed mouse populations. Evol Appl 9:546-64
Harris, Stephen E; O'Neill, Rachel J; Munshi-South, Jason (2015) Transcriptome resources for the white-footed mouse (Peromyscus leucopus): new genomic tools for investigating ecologically divergent urban and rural populations. Mol Ecol Resour 15:382-94
Munshi-South, Jason; Nagy, Christopher (2014) Urban park characteristics, genetic variation, and historical demography of white-footed mouse (Peromyscus leucopus) populations in New York City. PeerJ 2:e310
Harris, Stephen E; Munshi-South, Jason; Obergfell, Craig et al. (2013) Signatures of rapid evolution in urban and rural transcriptomes of white-footed mice (Peromyscus leucopus) in the New York metropolitan area. PLoS One 8:e74938