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. Urban habitats often contain extremely high population densities of just a few urban """"""""adapters"""""""", leading to biological homogenization. Artificially high primary productivity, a more stable and abundant food supply, and release from trophic competition result in these abnormal population densities. Urban populations also experience enhanced intraspecific competition, disease, and environmental pollution. Wildlife may rapidly adapt to these local urban 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 informative variation indicative of local adaptation. We will use these new approaches to examine adaptation to urbanization among populations of the white-footed mouse (Peromyscus leucopus), in New York City. First, we will generate deep exome sequence for white-footed mice from urban and non-urban populations in NYC using 454 and ABI SOLiD next-generation sequencing. Gene identity will be established through alignment with annotated rat, mouse, and Peromyscus genomes. We will identify genomic regions, and ultimately individual coding sequences, that exhibit statistical signatures of selection in urban populations. A preliminary reference exome for urban P. leucopus has already been sequenced and annotated, and several candidate loci have been identified. Additional analyses will examine quantitative changes in gene expression levels in urban populations using the SOLiD exome data, and potential regulatory changes outside of protein-coding regions using a genome-wide RAD-Seq (restriction site associated DNA sequencing) approach. We will also use landscape genomic analyses to examine whether selection pressures from urbanization result in an """"""""evolutionary syndrome"""""""" of correlated change across the NYC metro area, or alternatively, adaptation to local urban conditions in individual populations. Statistical associations between landscape elements (e.g. soil pollution, population density, habitat type) and informative variants will be investigated using new spatial genomic techniques. As a further step in documenting the selection pressures influencing potentially adaptive genetic variants, we will establish long-term study sites in the NYC metro area to examine the fitness consequences of candidate genetic variants and lay the groundwork for future field experiments. Finally, we will build upon our substantial prior efforts to integrate urban evolutionary biology into courses at Baruch College and the NYC High School for Environmental Studies.

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 organisms in human-dominated environments.

Agency
National Institute of Health (NIH)
Institute
National Institute of General Medical Sciences (NIGMS)
Type
Academic Research Enhancement Awards (AREA) (R15)
Project #
1R15GM099055-01A1
Application #
8367359
Study Section
Special Emphasis Panel (ZRG1-GGG-H (90))
Program Officer
Eckstrand, Irene A
Project Start
2012-09-10
Project End
2013-08-31
Budget Start
2012-09-10
Budget End
2013-08-31
Support Year
1
Fiscal Year
2012
Total Cost
$108,239
Indirect Cost
$27,509
Name
Bernard M. Baruch College
Department
Other Basic Sciences
Type
Schools of Arts and Sciences
DUNS #
620127493
City
New York
State
NY
Country
United States
Zip Code
10010
Izuogu, Adaeze O; McNally, Kristin L; Harris, Stephen E et al. (2017) Interferon signaling in Peromyscus leucopus confers a potent and specific restriction to vector-borne flaviviruses. PLoS One 12:e0179781
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
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; 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:
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