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

Evolutionary Applications

Volumn 9, Issue 4, 2016, Pages 546-564

  Munshi South, Jason ^a   Zolnik, Christine P ^a   Harris, Stephen E ^b  

^a FORDHAM UNIVERSITY   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

DdRADSeq; Landscape genetics; Peromyscus; Population genomics; Rapid evolution; Single nucleotide polymorphism; Urbanization

Indexed keywords

EID: 84958601615     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12357     Document Type: Article

References (102)

1. Alexander, D. H., and K. Lange 2011. Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12:246.
2. Alexander, D. H., J. Novembre, and K. Lange 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19:1655-1664.
3. Andrews, S. 2010. FastQC: a quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
4. Austin, J. D., J. A. Gore, D. U. Greene, and C. Gotteland 2015. Conspicuous genetic structure belies recent dispersal in an endangered beach mouse (Peromyscus polionotus trissyllepsis). Conservation Genetics 16:915-928.
5. Balkenhol, N., and L. Waits 2009. Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Molecular Ecology 18:4151-4164.
6. Barley, A. J., P. J. Monnahan, R. C. Thomson, L. L. Grismer, and R. M. Brown 2015. Sun skink landscape genomics: assessing the roles of microevolutionary processes in shaping genetic and phenotypic diversity across a heterogeneous and fragmented landscape. Molecular Ecology 24:1696-1712.
7. Barnosky, A. D., E. A. Hadly, J. Bascompte, E. L. Berlow, J. H. Brown, M. Fortelius, W. M. Getz et al. 2012. Approaching a state shift in Earth's biosphere. Nature 486:52-58.
8. Barr, K. R., B. E. Kus, K. L. Preston, S. Howell, E. Perkins, and A. G. Vandergast 2015. Habitat fragmentation in coastal southern California disrupts genetic connectivity in the cactus wren (Campylorhynchus brunneicapillus). Molecular Ecology 24:2349-2363.
9. Barrett, R. D. H., and D. Schluter 2008. Adaptation from standing genetic variation. Trends in Ecology & Evolution 23:38-44.
10. Bedford, N. L., and H. E. Hoekstra 2015. Peromyscus mice as a model for studying natural variation. eLife 4:e06813.
11. Benítez-López, A., R. Alkemade, and P. A. Verweij 2010. The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biological Conservation 143:1307-1316.
12. Blair, R. B. 2001. Birds and Butterflies Along Urban Gradients in Two Ecoregions of the United States: is Urbanization Creating a Homogeneous Fauna? In J. L. Lockwood, and M. L. McKinney eds. Biotic Homogenization, pp. 33-56. Springer US, New York, NY.
13. Bradburd, G. 2014. BEDASSLE: Quantifies effects of geo/eco distance on genetic differentiation (version 1.5). https://cran.r-project.org/web/packages/BEDASSLE/index.html.
14. Bradburd, G. S., P. L. Ralph, and G. M. Coop 2013. Disentangling the effects of geographic and ecological isolation on genetic differentiation. Evolution 67:3258-3273.
15. Brunner, J. L., S. Duerr, F. Keesing, M. Killilea, H. Vuong, and R. S. Ostfeld 2013. An experimental test of competition among mice, chipmunks, and squirrels in deciduous forest fragments. PLoS One 8:e66798.
16. Burke, M. K., J. P. Dunham, P. Shahrestani, K. R. Thornton, M. R. Rose, and A. D. Long 2010. Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467:587-590.
17. Burnham, K. P., and D. R. Anderson . 2002. Model Selection and Multi-Model Inference: A Practical Information-Theoretic Approach. Springer, New York, NY.
18. Catchen, J., P. A. Hohenlohe, S. Bassham, A. Amores, and W. A. Cresko 2013. Stacks: an analysis tool set for population genomics. Molecular Ecology 22:3124-3140.
19. Chapman, J. R., S. Nakagawa, D. W. Coltman, J. Slate, and B. C. Sheldon 2009. A quantitative review of heterozygosity-fitness correlations in animal populations. Molecular Ecology 18:2746-2765.
20. Colosimo, P. F., K. E. Hosemann, S. Balabhadra, G. Jr Villarreal, M. Dickson, J. Grimwood, J. Schmutz et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928-1933.
21. Coop, G., J. K. Pickrell, J. Novembre, S. Kudaravalli, J. Li, D. Absher, R. M. Myers et al. 2009. The Role of Geography in Human Adaptation. PLoS Genetics 5:e1000500.
22. Cushman, S. A., and E. L. Landguth 2010. Spurious correlations and inference in landscape genetics. Molecular Ecology 19:3592-3602.
23. Danecek, P., A. Auton, G. Abecasis, C. A. Albers, E. Banks, M. A. DePristo, R. E. Handsaker et al. 2011. The variant call format and VCFtools. Bioinformatics 27:2156-2158.
24. Domingues, V. S., Y.-P. Poh, B. K. Peterson, P. S. Pennings, J. D. Jensen, and H. E. Hoekstra 2012. Evidence of adaptation from ancestral variation in young populations of beach mice. Evolution 66:3209-3223.
25. Donihue, C. M., and M. R. Lambert 2014. Adaptive evolution in urban ecosystems. Ambio 44:194-203.
26. Ellis, E. C., J. O. Kaplan, D. Q. Fuller, S. Vavrus, K. K. Goldewijk, and P. H. Verburg 2013. Used planet: a global history. Proceedings of the National Academy of Sciences 110:7978-7985.
27. Epps, C. W., J. D. Wehausen, V. C. Bleich, S. G. Torres, and J. S. Brashares 2007. Optimizing dispersal and corridor models using landscape genetics. Journal of Applied Ecology 44:714-724.
28. Etterson, J. R., and R. G. Shaw 2001. Constraint to adaptive evolution in response to global warming. Science 294:151-154.
29. Foll, M., and O. Gaggiotti 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180:977.
30. Franks, S. J., J. J. Weber, and S. N. Aitken 2014. Evolutionary and plastic responses to climate change in terrestrial plant populations. Evolutionary Applications 7:123-139.
31. Fuller, R. A., K. N. Irvine, P. Devine-Wright, P. H. Warren, and K. J. Gaston 2007. Psychological benefits of greenspace increase with biodiversity. Biology Letters 3:390-394.
32. Gibson, G., and I. Dworkin 2004. Uncovering cryptic genetic variation. Nature Reviews Genetics 5:681-690.
33. Goddard, M. A., A. J. Dougill, and T. G. Benton 2010. Scaling up from gardens: biodiversity conservation in urban environments. Trends in Ecology & Evolution 25:90-98.
34. Gortat, T., R. Rutkowski, A. Gryczyńska, A. Pieniaz˙ek, A. Kozakiewicz, and M. Kozakiewicz 2014. Anthropopressure gradients and the population genetic structure of Apodemus agrarius. Conservation Genetics 16:649-659.
35. Graves, T. A., P. Beier, and J. A. Royle 2013. Current approaches using genetic distances produce poor estimates of landscape resistance to interindividual dispersal. Molecular Ecology 22:3888-3903.
36. Groffman, P. M., J. Cavender-Bares, N. D. Bettez, J. M. Grove, S. J. Hall, J. B. Heffernan, S. E. Hobbie et al. 2014. Ecological homogenization of urban USA. Frontiers in Ecology and the Environment 12:74-81.
37. Haddad, N. M., L. A. Brudvig, J. Clobert, K. F. Davies, A. Gonzalez, R. D. Holt, T. E. Lovejoy et al. 2015. Habitat fragmentation and its lasting impact on Earth's ecosystems. Science Advances 1:e1500052.
38. Harris, S. E., J. Munshi-South, C. Obergfell, and R. O'Neill 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.
39. Harris, S. E., R. J. O'Neill, and J. Munshi-South 2015a. Transcriptome resources for the white-footed mouse (Peromyscus leucopus): new genomic tools for investigating ecologically divergent urban and rural populations. Molecular Ecology Resources 15:382-394.
40. Harris, S. E., A. T. Xue, D. Alvarado-Serrano, J. T. Boehm, T. Joseph, M. J. Hickerson, and J. Munshi-South 2015b. Urbanization shapes the demographic history of a city-dwelling native rodent. BioRxiv. doi:10.1101/032979 [Epub ahead of print].
41. Harrisson, K. A., A. Pavlova, M. Telonis-Scott, and P. Sunnucks 2014. Using genomics to characterize evolutionary potential for conservation of wild populations. Evolutionary Applications 7:1008-1025.
42. Harvey, M. G., and R. T. Brumfield 2015. Genomic variation in a widespread Neotropical bird (Xenops minutus) reveals divergence, population expansion, and gene flow. Molecular Phylogenetics and Evolution 83:305-316.
43. Heilig, G. K. 2011. World Urbanization Prospects: the 2011 Revision. United Nations, Department of Economic and Social Affairs (DESA), Population Division, Population Estimates and Projections Section, New York, NY.
44. Hobbs, R. J., S. Arico, J. Aronson, J. S. Baron, P. Bridgewater, V. A. Cramer, P. R. Epstein et al. 2006. Novel ecosystems: theoretical and management aspects of the new ecological world order. Global Ecology and Biogeography 15:1-7.
45. Hobbs, R. J., E. Higgs, and J. A. Harris 2009. Novel ecosystems: implications for conservation and restoration. Trends in Ecology & Evolution 24:599-605.
46. Hoffmann, A. A., and C. M. Sgrò 2011. Climate change and evolutionary adaptation. Nature 470:479-485.
47. Jha, S. 2015. Contemporary human-altered landscapes and oceanic barriers reduce bumble bee gene flow. Molecular Ecology 24:993-1006.
48. Jombart, T., and I. Ahmed 2011. Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070-3071.
49. Kenney-Hunt, J., A. Lewandowski, T. C. Glenn, J. L. Glenn, O. V. Tsyusko, R. J. O'Neill, J. Brown et al. 2014. A genetic map of Peromyscus with chromosomal assignment of linkage groups (a Peromyscus genetic map). Mammalian Genome 25:160-179.
50. Keyghobadi, N. 2007. The genetic implications of habitat fragmentation for animals. Canadian Journal of Zoology 85:1049-1064.
51. Kinnison, M., A. Hendry, and C. Stockwell 2007. Contemporary evolution meets conservation biology II: Impediments to integration and application. Ecological Research 22:947-954.
52. Kopelman, N. M., J. Mayzel, M. Jakobsson, N. A. Rosenberg, and I. Mayrose 2015. Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15:1179-1191.
53. Legendre, P., and M.-J. Fortin 2010. Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Molecular Ecology Resources 10:831-844.
54. Magle, S. B., V. M. Hunt, M. Vernon, and K. R. Crooks 2012. Urban wildlife research: past, present, and future. Biological Conservation 155:23-32.
55. Manichaikul, A., J. C. Mychaleckyj, S. S. Rich, K. Daly, M. Sale, and W.-M. Chen 2010. Robust relationship inference in genome-wide association studies. Bioinformatics 26:2867-2873.
56. Manthey, J. D., and R. G. Moyle 2015. Isolation by environment in White-breasted Nuthatches (Sitta carolinensis) of the Madrean Archipelago sky islands: a landscape genomics approach. Molecular Ecology 24:3628-3638.
57. Mazerolle, M. J. 2015. AICcmodavg: Model Selection and Multimodel Inference Based on (Q) AIC (c). R Package Version 2.0-3.
58. McKinney, M. L. 2002. Urbanization, biodiversity, and conservation. BioScience 52:883-890.
59. McRae, B. H. 2006. Isolation by resistance. Evolution 60:1551-1561.
60. McRae, B. H., and P. Beier 2007. Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences of the United States of America104:19885-19890.
61. Merilä, J., and A. P. Hendry 2014. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary Applications 7:1-14.
62. Meuwissen, T., B. Hayes, and M. Goddard 2013. Accelerating improvement of livestock with genomic selection. Annual Review of Animal Biosciences 1:221-237.
63. Monz, C. A., C. M. Pickering, and W. L. Hadwen 2013. Recent advances in recreation ecology and the implications of different relationships between recreation use and ecological impacts. Frontiers in Ecology and the Environment 11:441-446.
64. Mueller, J. C., J. Partecke, B. J. Hatchwell, K. J. Gaston, and K. L. Evans 2013. Candidate gene polymorphisms for behavioural adaptations during urbanization in blackbirds. Molecular Ecology 22:3629-3637.
65. Munshi-South, J. 2012. Urban landscape genetics: canopy cover predicts gene flow between white-footed mouse (Peromyscus leucopus) populations in New York City. Molecular Ecology 21:1360-1378.
66. Munshi-South, J., and K. Kharchenko 2010. Rapid, pervasive genetic differentiation of urban white-footed mouse (Peromyscus leucopus) populations in New York City. Molecular Ecology 19:4242-4254.
67. Munshi-South, J., and C. Nagy 2014. Urban park characteristics, genetic variation, and historical demography of white-footed mouse (Peromyscus leucopus) populations in New York City. PeerJ 2(March):e310.
68. Narum, S. R., C. A. Buerkle, J. W. Davey, M. R. Miller, and P. A. Hohenlohe 2013. Genotyping-by-sequencing in ecological and conservation genomics. Molecular Ecology 22:2841-2847.
69. Nowak, D. J., and E. J. Greenfield 2012. Tree and impervious cover change in U.S. cities. Urban Forestry & Urban Greening 11:21-30.
70. Oakley, C. G. 2013. Small effective size limits performance in a novel environment. Evolutionary Applications 6:823-831.
71. Orr, H. A. 2005. The genetic theory of adaptation: a brief history. Nature Reviews Genetics 6:119-127.
72. Ozer, F., H. Gellerman, and M. V. Ashley 2011. Genetic impacts of Anacapa deer mice reintroductions following rat eradication. Molecular Ecology 20:3525-3539.
73. Palumbi, S. 2001. Humans as the world's greatest evolutionary force. Science 293:1786-1790.
74. Pennings, P. S. 2012. Standing genetic variation and the evolution of drug resistance in HIV. PLoS Computational Biology 8:e1002527.
75. Peterson, B. K., J. N. Weber, E. H. Kay, H. S. Fisher, and H. E. Hoekstra 2012. Double digest RADseq: an inexpensive method for De Novo SNP discovery and genotyping in model and non-model species. PLoS One 7:e37135.
76. Prentis, P. J., J. R. Wilson, E. E. Dormontt, D. M. Richardson, and A. J. Lowe 2008. Adaptive evolution in invasive species. Trends in Plant Science 13:288-294.
77. Pritchard, J., M. Stephens, and P. Donnelly 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
78. Pritchard, J. K., J. K. Pickrell, and G. Coop 2010. The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Current Biology 20:R208-R215.
79. R Development Core Team. 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
80. Raj, A., M. Stephens, and J. K. Pritchard 2014. FastSTRUCTURE: variational Inference of Population Structure in Large SNP Data Sets. Genetics 197:573-589.
81. Ramalho, C. E., and R. J. Hobbs 2012. Time for a change: dynamic urban ecology. Trends in Ecology & Evolution 27:179-188.
82. Renaut, S., A. W. Nolte, S. M. Rogers, N. Derome, and L. Bernatchez 2011. SNP signatures of selection on standing genetic variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus spp.). Molecular Ecology 20:545-559.
83. Rivera-Ortíz, F. A., R. Aguilar, M. D. C. Arizmendi, M. Quesada, and K. Oyama 2014. Habitat fragmentation and genetic variability of tetrapod populations. Animal Conservation 18:249-258.
84. Rockman, M. V. 2008. Reverse engineering the genotype-phenotype map with natural genetic variation. Nature 456:738-744.
85. Ruddiman, W. F., E. C. Ellis, J. O. Kaplan, and D. Q. Fuller 2015. Defining the epoch we live in. Science 348:38-39.
86. Scarcelli, N., and P. X. Kover 2009. Standing genetic variation in FRIGIDA mediates experimental evolution of flowering time in Arabidopsis. Molecular Ecology 18:2039-2049.
87. Serieys, L. E. K., A. Lea, J. P. Pollinger, S. P. D. Riley, and R. K. Wayne 2015. Disease and freeways drive genetic change in urban bobcat populations. Evolutionary Applications 8:75-92.
88. Seto, K. C., B. Güneralp, and L. R. Hutyra 2012. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proceedings of the National Academy of Sciences 109:16083-16088.
89. Sexton, J. P., S. B. Hangartner, and A. A. Hoffmann 2014. Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution 68:1-15.
90. Shwartz, A., A. Turbé, R. Julliard, L. Simon, and A.-C. Prévot 2014. Outstanding challenges for urban conservation research and action. Global Environmental Change 28:39-49.
91. Steffen, W., P. J. Crutzen, and J. R. McNeill 2007. The Anthropocene: are humans now overwhelming the great forces of nature. Ambio 36:614-621.
92. Stockwell, C. A., A. P. Hendry, and M. T. Kinnison 2003. Contemporary evolution meets conservation biology. Trends in Ecology & Evolution 18:94-101.
93. Tanner, C. J., F. R. Adler, N. B. Grimm, P. M. Groffman, S. A. Levin, J. Munshi-South, D. E. Pataki et al. 2014. Urban ecology: advancing science and society. Frontiers in Ecology and the Environment 12:574-581.
94. Teotónio, H., I. M. Chelo, M. Bradić, M. R. Rose, and A. D. Long 2009. Experimental evolution reveals natural selection on standing genetic variation. Nature Genetics 41:251-257.
95. Väli, Ü., A. Einarsson, L. Waits, and H. Ellegren 2008. To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Molecular Ecology 17:3808-3817.
96. Vergnes, A., I. L. Viol, and P. Clergeau 2012. Green corridors in urban landscapes affect the arthropod communities of domestic gardens. Biological Conservation 145:171-178.
97. Vessey, S. H., and K. B. Vessey 2007. Linking behavior, life history and food supply with the population dynamics of white-footed mice (Peromyscus leucopus). Integrative Zoology 2:123-130.
98. Vitousek, P., H. Mooney, J. Lubchenco, and J. Melillo 1997. Human domination of Earth's ecosystems. Science 277:494-499.
99. Walsh, C. J., A. H. Roy, J. W. Feminella, P. D. Cottingham, P. M. Groffman, and R. P. II Morgan 2005. The urban stream syndrome: current knowledge and the search for a cure. Journal of the North American Benthological Society 24:706-723.
100. Wang, I. J., and G. S. Bradburd 2014. Isolation by environment. Molecular Ecology 23:5649-5662.
101. Xian, G., C. Homer, J. Demitz, J. Fry, N. Hossain, and J. Wickham 2011. Change of impervious surface area between 2001 and 2006 in the conterminous United States. Photogrammetric Engineering and Remote Sensing 77:758-762.
102. Zipperer, W. C., T. W. Foresman, S. P. Walker, and C. T. Daniel 2012. Ecological consequences of fragmentation and deforestation in an urban landscape: a case study. Urban Ecosystems 15:533-544.