Disease and freeways drive genetic change in urban bobcat populations

Evolutionary Applications

Volumn 8, Issue 1, 2015, Pages 75-92

  Serieys, Laurel E K ^a   Lea, Amanda ^b   Pollinger, John P ^a   Riley, Seth P D ^c   Wayne, Robert K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b DUKE UNIVERSITY   (United States)

^c NATIONAL PARK SERVICE   (United States)

Author keywords

Balancing selection; Disease; Freeways; Immune linked loci; Major histocompatibility complex; Population structure; Toll like receptors; Urbanization

Indexed keywords

EID: 84921437115     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12226     Document Type: Article

References (111)

1. Acevedo-Whitehouse, K., T. R. Spraker, E. Lyons, S. R. Melin, F. Gulland, R. L. Delong, and W. Amos 2006. Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Molecular Ecology 15:1973-1982.
2. Aderem, A., and R. Ulevitch 2000. Toll-like receptors in the induction of the innate immune response. Nature 406:782-787.
3. Aguilar, A., G. Roemer, S. Debenham, M. Binns, D. Garcelon, and R. K. Wayne 2004. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proceedings of the National Academy of Sciences of the USA 101:3490-3494.
4. Antao, T., A. Lopes, R. J. Lopes, A. Beja-Pereira, and G. Luikart 2008. LOSITAN: a workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinformatics 9:323.
5. Areal, H., J. Abrantes, and P. J. Esteves 2011. Signatures of positive selection in Toll-like receptor (TLR) genes in mammals. BMC Evolutionary Biology 11:368.
6. de Assunção-Franco, M., D. J. Hoffman, J. Harwood, and W. Amos 2012. MHC genotype and near-deterministic mortality in grey seals. Scientific Reports 2:659.
7. Barreiro, L.B., M. Ben-Ali, H. Quach, G. Laval, E. Patin, J. K. Pickrell, C. Bouchier, et al. 2009. Evolutionary dynamics of Human Toll-Like receptors and their different contributions to host defense. PLOS Genetics 5:e1000562.
8. Beaumont, M. A., and R. A. Nichols 1996. Evaluating loci for use in the genetic analysis of population structure. Proceedings of the Royal Society of London B 263:1619-1626.
9. Beck, T. W., J. Menninger, W. J. Murphy, W. G. Nash, S. J. O'Brien, and N. Yuhki 2005. The feline major histocompatibility complex is rearranged by an inversion with a breakpoint in the distal class I region. Immunogenetics 56:702-709.
10. Beier, P., S. P. D. Riley, and R. Sauvajot 2010. Mountain Lions (Puma concolor). In S. Gehrt, S. P. D. Riley, and B. L. Cypher, eds. Urban Carnviores, pp. 141-155. John Hopkins University Press, Baltimore, MD.
11. Bernatchez, L., and C. Landry 2003. MHC studies in nonmodel vertebrates: what have we learned about natural selection in 15 years? Journal of Evolutionary Biology 16:363-677.
12. Berry, O., M. D. Tocher, and S. D. Sarre 2004. Can assignment tests measure dispersal? Molecular Ecology 13:551-561.
13. Black, W. C., C. F. Baer, M. F. Antolin, and N. M. DuTeau 2001. Population genomics: genome-wide sampling of insect populations. Annual Review of Entomology 46:441-469.
14. Bollmer, J. L., E. A. Ruder, J. A. Johnson, J. A. Eimes, and P. O. Dunn 2011. Drift and selection influence geographic variation at immune loci of prairie-chickens. Molecular Ecology 20:4695-4706.
15. Boutin-Ganache, I., M. Raposo, M. Raymond, and C. F. Deschepper 2001. M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. BioTechniques 31:24-28.
16. Bradley, C. A., and S. Altizer 2007. Urbanization and the ecology of wildlife diseases. Trends in Ecology & Evolution 22:95-102.
17. Brinkmann, B., M. Klintschar, F. Neuhuber, J. Hühne, and B. Rolf 1998. Mutation rate in human microsatellites: influence of the structure and length of the tandem repeat. The American Journal of Human Genetics 62:1408-1415.
18. Cammen, K., D. J. Hoffman, L. A. Knapp, J. Harwood, and W. Amos 2010. Geographic variation of the major histocompatibility complex in Eastern Atlantic grey seals (Halichoerus grypus). Molecular Ecology 20:740-752.
19. Carlsson, J. 2008. Effects of microsatellite null alleles on assignment testing. Journal of Heredity 99:616-623.
20. Chapuis, M., and A. Estoup 2007. Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24:621-631.
21. Coltman, D. W., J. G. Pilkington, J. A. Smith, and J. M. Pemberton 1999. Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evolution 53:1259-1267.
22. Cornuet, J. M., and G. Luikart 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001-2014.
23. Crawford, N. G. 2010. SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources 10:556-557.
24. Culver, M., P. W. Hedrick, K. Murphy, S. O'Brien, and M. J. Hornocker 2008. Estimation of the bottleneck size in Florida panthers. Animal Conservation 11:104-110.
25. Delaney, K. S., S. P. D. Riley, and R. N. Fisher 2010. A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS ONE 5:e12767.
26. Dlugosch, K. M., and I. M. Parker 2008. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Molecular Ecology 17:431-449.
27. Earl, D. A., and B. M. vonHoldt 2011. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4:359-361.
28. Epps, C. W., P. J. Palsbà ll, J. D. Wehausen, G. K. Roderick, R. R. Ramey II, and D. R. McCullough 2005. Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep. Ecology Letters 8:1029-1038.
29. Ernest, H. B., M. C. Penedo, B. P. May, M. Syvanen, and W. M. Boyce 2000. Molecular tracking of mountain lions in the Yosemite valley region in California: genetic analysis using microsatellites and faecal DNA. Molecular Ecology 9:433-441.
30. Espeleta, G. G., P. W. Hedrick, and S. T. Kalinowski 2001. Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity 86:439-450.
31. Evanno, G., S. Regnaut, and J. Goudet 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14:2611-2620.
32. Faircloth, B. C. 2008. MSATCOMMANDER: detection of microsatellite repeat arrays and automated, locus-specific primer design. Molecular Ecology Resources 8:92-94.
33. Ferrer-Admetlla, A., E. Bosch, M. Sikora, T. Marquès-Bonet, A. Ramírez-Soriano, A. Muntasell, A. Navarro et al. 2008. Balancing selection is the main force shaping the evolution of innate immunity genes. Journal of Immunology 181:1315-1322.
34. Forman, R. T., and L. E. Alexander 1998. Roads and their major ecological effects. Annual Review of Ecology and Systematics 29:207-231.
35. Frankham, R. 2005. Genetics and extinction. Biological Conservation 126:131-140.
36. Froeschke, G., and S. Sommer 2005. MHC class II DRB variability and parasite load in the striped mouse (Rhabdomys pumilio) in the Southern Kalahari. Molecular Biology and Evolution 22:1254-1259.
37. Garza, J. C., and E. G. Williamson 2001. Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10:305-318.
38. Gibeau, M. L., A. P. Clevenger, S. Herrero, and J. Wierzchowski 2002. Grizzly bear response to human development and activities in the Bow River Watershed, Alberta, Canada. Biological Conservation 103:227-236.
39. Goudet, J. 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86:485-486.
40. Guillot, G., F. Mortier, and A. Estoup 2005. GENELAND: a computer package for landscape genetics. Molecular Ecology Notes 5:712-715.
41. Harrison, S., and A. Hastings 1996. Genetic and evolutionary consequences of metapopulation structure. Trends in Ecology & Evolution 11:180-183.
42. Hedrick, P. W. 2002. Pathogen resistance and genetic variation at MHC loci. Evolution 56:1902-1908.
43. Hedrick, P. 2005. Genetics of Populations, 3rd edn. Jones and Bartlett Publishers, Sudbury, MA.
44. Heller, R., and H. Siegismund 2009. Relationship between three measures of genetic differentiation GST, DEST and G'ST: how wrong have we been? Molecular Ecology 18:2080-2083.
45. Hill, A. 1998. The immunogenetics of human infectious diseases. Annual Review of Immunology 16:593-617.
46. Hitchings, S. P., and T. J. C. Beebee 1997. Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117-127.
47. Huang, L. Y., and R. N. Germain 1992. MHC class II interaction with CD4 mediated by a region analogous to the MHC class I binding site for CD8. Nature 356:796-798.
48. Iwasaki, A., and R. Medzhitov 2010. Regulation of adaptive immunity by the innate immune system. Science 327:291-295.
49. Jakobsson, M., and N. A. Rosenberg 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801-1806.
50. Janeway, C. A., and R. Medzhitov 2002. Innate immune recognition. Annual Review of Immunology 20:197-216.
51. Jepson, A., W. Banya, F. Sisay-Joof, M. Hassan-King, C. Nunes, S. Bennett, and H. Whittle 1997. Quantification of the relative contribution of major histocompatibility complex (MHC) and non-MHC genes to human immune responses to foreign antigens. Infection and Immunity 65:872-876.
52. Jost, L. 2008. GST and its relatives do not measure differentiation. Molecular Ecology 17:4015-4026.
53. Kaisho, T., and S. Akira 2006. Toll-like receptor function and signaling. Journal of Allergy and Clinical Immunology 117:979-987.
54. Kalinowski, S. T., A. P. Wagner, and M. L. Taper 2006. ml-relate: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes 6:576-579.
55. Keller, L. 2002. Inbreeding effects in wild populations. Trends in Ecology & Evolution 17:230-241.
56. Keyghobadi, N. 2007. The genetic implications of habitat fragmentation for animals. Canadian Journal of Zoology 85:1049-1064.
57. Kimura, M. 1985. The Neutral Theory of Molecular Evolution. Cambridge University Press, New York, NY.
58. Klein, J. 1986. Natural History of the Major Histocompatibility Complex. John Wiley & Sons, New York, NY.
59. Knick, S. T., J. D. Brittell, and S. J. Sweeney 1985. Population characteristics of bobcats in Washington State. The Journal of Wildlife Management 49:721-728.
60. Krebs, C. J. 1994. Ecology: The Experimental Analysis of Distribution and Abundance. Harper Collins, New York.
61. Lande, R. 1998. Anthropogenic, ecological and genetic factors in extinction and conservation. Researches on Population Ecology 40:259-269.
62. Lee, J. S., E. W. Ruell, E. E. Boydston, L. M. Lyren, R. S. Alonso, J. L. Troyer, K. R. Crooks et al. 2012. Gene flow and pathogen transmission among bobcats (Lynx rufus) in a fragmented urban landscape. Molecular Ecology 21:1617-1631.
63. LoGiudice, K. 2003. Trophically transmitted parasites and the conservation of small populations: raccoon roundworm and the imperiled Allegheny woodrat. Conservation Biology 17:258-266.
64. Månsson, A., M. Fransson, M. Adner, M. Benson, R. Uddman, S. Björnsson, and L. O. Cardell 2010. TLR3 in human eosinophils: functional effects and decreased expression during allergic rhinitis. International Archives of Allergy and Immunology 151:118-128.
65. Marshall, T. C., J. Slate, L. E. Kruuk, and J. M. Pemberton 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7:639-655.
66. Mousadik, A., and R. J. Petit 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theoretical and Applied Genetics 92:832-839.
67. 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.
68. Nei, M. 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
69. Nei, M., T. Maruyama, and R. Chakraborty 1975. The bottleneck effect and genetic variability in populations. Evolution 29:1-10.
70. Neuman, E., J. W. Huleatt, H. Vargas, E. E. Rupp, and R. M. Jack 1992. Regulation of MHC class I synthesis and expression by human neutrophils. Journal of Immunology 148:3520-3527.
71. Ng, S. 2004. Use of highway undercrossings by wildlife in southern California. Biological Conservation 115:499-507.
72. Oliver, M. K., and S. B. Piertney 2012. Selection maintains MHC diversity through a natural population bottleneck. Molecular Biology and Evolution 29:1713-1720.
73. van Oosterhout, C., and W. Hutchinson 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology 4:535-538.
74. Pannell, J. R., and B. Charlesworth 2000. Effects of metapopulation processes on measures of genetic diversity. Philosophical Transactions of the Royal Society of London B, Biological Sciences 355:1851-1864.
75. Peakall, R., and P. E. Smouse 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537-2539.
76. Peery, M.Z., R. Kirby, B. N. Reid, R. Stoelting, E. Douchet-Beer, S. Robinson, C. Vasquez-Carrillo, et al. 2012. Reliability of genetic bottleneck tests for detecting recent population declines. Molecular Ecology 21:3403-3418.
77. Piertney, S. B., and M. K. Oliver 2005. The evolutionary ecology of the major histocompatibility complex. Heredity 96:7-21.
78. Piry, S., G. Luikart, and J. M. Cornuet 1999. Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. Journal of Heredity 90:502-503.
79. Pontius, J. U., J. C. Mullikin, D. R. Smith, K. Lindblad-Toh, S. Gnerre, M. Clamp, J. Chang et al. 2007. Initial sequence and comparative analysis of the cat genome. Genome Research 17:1675-1689.
80. Potter, N. S., and C. V. Harding 2001. Neutrophils process exogenous bacteria via an alternate Class I MHC processing pathway for presentation of peptides to T lymphocytes. Journal of Immunology 167:2538-2546.
81. Pritchard, J. K., M. Stephens, and P. Donnelly 2000. Inference of population structure using multilocus genotype data. Genetics 155:945-959.
82. R Development Core Team. 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. www.R-project.org/ (accessed on 1 December 2012).
83. Raymond, M., and F. Rousset 1995. GENEPOP (Version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86:248-249.
84. Rice, W. 1989. Analyzing tables of statistical tests. Evolution 43:223.
85. Rienzo, A. D. 1994. Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the USA 91:3166-3170.
86. Riley, S. P. D., R. M. Sauvajot, T. K. Fuller, E. C. York, D. A. Kamradt, C. Bromley, and R. K. Wayne 2003. Effects of urbanization and habitat fragmentation on bobcats and coyotes in southern California. Conservation Biology 17:566-576.
87. Riley, S. P. D., J. P. Pollinger, R. M. Sauvajot, E. C. York, C. Bromley, T. K. Fuller, and R. K. Wayne 2006. A southern California freeway is a physical and social barrier to gene flow in carnivores. Molecular Ecology 15:1733-1741.
88. Riley, S. P. D., C. Bromley, R. Poppenga, F. A. Uzal, L. Whited, and R. M. Sauvajot 2007. Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban southern California. Journal of Wildlife Management 71:1874-1884.
89. Riley, S., E. E. Boydston, K. R. Crooks, and L. M. Lyren 2010. Bobcats (Lynx rufus). In S. D. Gehrt, S. P. D. Riley, and B. L. Cypher, eds. Urban Carnivores, pp. 121-138. Johns Hopkins University Press, Baltimore, MD.
90. Riley, S. P. D., L. E. K. Serieys, and J. Moriarty 2014. Infectious disease and contaminants in urban wildlife: unforeseen and often overlooked threats. In R. A. McCleery, C. Moorman, and N. Peterson, eds. Urban Wildlife Science: Theory and Practice. Springer, New York, NY (in press).
91. Roach, J. C., G. Glusman, L. Rowen, A. Kaur, M. K. Purcell, K. D. Smith, L. E. Hood et al. 2005. The evolution of vertebrate Toll-like receptors. Proceedings of the National Academy of Sciences of the USA 102:9577-9582.
92. Roelke, M. E., J. S. Martenson, and S. J. O'Brien 1993. The consequences of demographic reduction and genetic depletion in the endangered Florida panther. Current Biology 3:340-350.
93. Sabroe, I., E. C. Jones, L. R. Usher, M. K. B. Whyte, and S. K. Dower 2002. Toll-Like Receptor (TLR)2 and TLR4 in human peripheral blood granulocytes: a critical role for monocytes in leukocyte lipopolysaccharide responses. The Journal of Immunology 168:4701-4710.
94. Saccheri, I., M. Kuussaari, M. Kankare, and P. Vikman 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392:491-494.
95. Savage, A. E., and K. R. Zamudio 2011. MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences of the USA 108:16705-16710.
96. Schaschl, H., F. Suchentrunk, D. L. Morris, H. Ben Slimen, S. Smith, and W. Arnold 2012. Sex-specific selection for MHC variability in Alpine chamois. BMC Evolutionary Biology 12:20.
97. Scheierup, M. H., X. Vekemans, and D. Charlesworth 2000. The effect of subdivision on variation at multi-allelic loci under balancing selection. Genetical Research 76:51-62.
98. Schoonmaker, C., and S. P. D. Riley 2011. Wildlife use of crossings and nearby areas along I-405 before, during, and after freeway widening: pre-construction report. Caltrans District 7:1-28.
99. Schröder, N. W., and R. R. Schumann 2005. Single nucleotide polymorphisms of Toll-like receptors and susceptibility to infectious disease. The Lancet Infectious Diseases 5:156-164.
100. Serieys, L. E. K., J. Foley, S. Owens, L. Woods, E. Boydston, L. Lyren, R. Poppenga et al. 2013. Serum chemistry, hematologic and post-mortem findings in bobcats (Lynx rufus) with notoedric mange. Journal of Parasitology 99:989-996.
101. Slatkin, M. 1977. Gene flow and genetic drift in a species subject to frequent local extinctions. Theoretical Population Biology 12:253-262.
102. Spielman, D., B. W. Brook, and R. Frankham 2004. Most species are not driven to extinction before genetic factors impact them. Proceedings of the National Academy of Sciences of the USA 101:15261-15264.
103. Temple, D. L., M. J. Chamberlain, and L. M. Conner 2010. Spatial ecology, survival and cause-specific mortality of gray roxes (Urocyon cinereoargenteus) in a longleaf pine ecosystem. The American Midland Naturalist 163:413-422.
104. Tschirren, B., M. Andersson, K. Scherman, H. Westerdahl, and L. Råberg 2011. Contrasting patterns of diversity and population differentiation at the innate immune gene Toll-like Receptor 2 (TLR2) in two sympatric rodent species. Evolution 66:720-731.
105. Wade, M., and D. McCauley 1988. Extinction and recolonization: their effects on the genetic differentiation of local populations. Evolution 42:995-1005.
106. Walton, S. F. 2010. The immunology of susceptibility and resistance to scabies. Parasite Immunology 32:532-540.
107. Waples, R. S. 2006. A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conservation Genetics 7:167-184.
108. Waples, R. S., and C. Do 2008. LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources 8:753-756.
109. Westerdahl, H., B. Hansson, S. Bensch, and D. Hasselquist 2004. Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? Journal of Evolutionary Biology 17:485-492.
110. Whittaker, D., A. Dapper, and M. Peterson 2012. Maintenance of MHC Class IIB diversity in a recently established songbird population. Journal of Avian Biology 43:109-118.
111. Williamson-Natesan, E. G. 2005. Comparison of methods for detecting bottlenecks from microsatellite loci. Conservation Genetics 6:396-399.