Conservation Genetics

, Volume 18, Issue 6, pp 1235–1245 | Cite as

Effects of emerging infectious diseases on host population genetics: a review

  • Donald T. McKnightEmail author
  • Lin Schwarzkopf
  • Ross A. Alford
  • Deborah S. Bower
  • Kyall R. Zenger
Review Article


Emerging infectious diseases threaten the survival of many species and populations by causing large declines and altering life history traits and population demographics. Therefore, it is imperative to understand how diseases impact wildlife populations so that effective management strategies can be planned. Many studies have focused on understanding the ecology of host/pathogen interactions, but it is equally important to understand the effects on host population genetic structure. In this review, we examined the literature on how infectious diseases influence host population genetic makeup, with a particular focus on whether or not they alter gene flow patterns, reduce genetic variability, and drive selection. Although the results were mixed, there was evidence for all of these outcomes. Diseases often fragmented populations into small, genetically distinct units with limited gene flow among them. In some cases, these isolated populations showed the genetic hallmarks of bottlenecks and inbreeding, but in other populations, there was sufficient gene flow or enough survivors to prevent genetic drift and inbreeding. Direct evidence of diseases acting as selective pressures in wild populations is somewhat limited, but there are several clear examples of it occurring. Also, several studies found that gene flow can impact the evolution of small populations either beneficially, by providing them with variation, or detrimentally, by swamping them with alleles that are not locally adaptive. Thus, differences in gene flow levels may explain why some species adapt while others do not. There are also intermediate cases, whereby some species may adapt to disease, but not at a rate that is meaningful for conservation purposes.


Adaptation Fragmentation Gene flow Genetic drift Population genetics 


Compliance with ethical standards

Conflict of interest

The authors affirm that they have no conflicts of interest to declare.


  1. Acevedo-Whitehouse K, Gullans F, Greig D, Amos W (2003) Inbreeding: disease susceptibility in California sea lions. Nature 422:6927CrossRefGoogle Scholar
  2. Addison JA, Hart MW (2004) Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites. Mar Biol 144:243–251. doi: 10.1007/s00227-003-1193-6 CrossRefGoogle Scholar
  3. Albert EM, Fernández-Beaskoetxea S, Godoy JA et al (2014) Genetic management of an amphibian population after a chytridiomycosis outbreak. Conserv Genet 16:103–111. doi: 10.1007/s10592-014-0644-6 CrossRefGoogle Scholar
  4. Alford RA, Bradfield KS, Richards SJ (2007) Global warming and amphibian losses. Nature 447:E3–E4. doi: 10.1038/nature05940 PubMedCrossRefGoogle Scholar
  5. Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190CrossRefGoogle Scholar
  6. Allentoft ME, O’Brien J (2010) Global amphibian declines, loss of genetic diversity and fitness: a review. Diversity 2:47–71. doi: 10.3390/d2010047 CrossRefGoogle Scholar
  7. Anderson PK, Cunningham AA, Patel NG et al (2004) Emerging infectious disease of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol Evol 19:535–544PubMedCrossRefGoogle Scholar
  8. Archie EA, Luikart G, Ezenwa VO (2009) Infecting epidemiology with genetics: A new frontier in disease ecology. Trends Ecol Evol 24:21–30PubMedCrossRefGoogle Scholar
  9. Atkinson CT, Woods KL, Dusek RJ et al (1995) Wildlife disease and conservation in Hawaii: pathogenicity of avian malaria (Plasmodium relictum) in experimentally infected iiwi (Vestiaria coccinea). Parasitology 111:S59–S69PubMedCrossRefGoogle Scholar
  10. Atkinson CT, Dusek RJ, Woods KL, Iko WM (2000) Pathogenicity of avian malaria in experimentally-infected Hawaii Amakihi. J Wildl Dis 36:197–201PubMedCrossRefGoogle Scholar
  11. Atkinson CT, Saili KS, Utzurrum RB, Jarvi SI (2013) Experimental evidence for evolved tolerance to avian malaria in a wild population of low elevation Hawai’i’amakihi (Hemignathus virens). Ecohealth 10:366–375PubMedCrossRefGoogle Scholar
  12. Bataille A, Cashins SD, Grogan L et al (2015) Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proc R Soc B 282:20143127–20143127. doi: 10.1098/rspb.2014.3127 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bengis RG, Kock RA, Fischer J (2002) Infectious animal diseases: the wildlife/livestock interface. Rev Sci Tech 21:53–66PubMedCrossRefGoogle Scholar
  14. Bennett AF (1998) Linkages in the landscape: the role of corridors and connectivity in wildlife conservation. World Conservation Union, Gland, SwitzerlandGoogle Scholar
  15. Benning TL, LaPointe D, Atkinson CT, Vitousek PM (2002) Interactions of climate change with biological invasions and land use in the Hawaiian islands: modeling the fate of endemic birds using a geographic information system. Proc Natl Acad Sci USA 99:14246–14249PubMedPubMedCentralCrossRefGoogle Scholar
  16. Berger L, Speare R, Daszak P et al (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci USA 95:9031–9036. doi: 10.1073/pnas.95.15.9031 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Biek R, Real LA (2010) The landscape genetics of infectious disease emergence and spread. Mol Ecol 19:3515–3531. doi: 10.1111/j.1365-294X.2010.04679.x PubMedPubMedCentralCrossRefGoogle Scholar
  18. Blanchong JA, Robinson SJ, Samuel MD, Foster JT (2016) Application of genetics and genomics to wildlife epidemiology. J Wildl Manage 80:593–608. doi: 10.1002/jwmg.1064 CrossRefGoogle Scholar
  19. Bonneaud C, Pérez-Tris J, Federici P et al (2006) Major histocompatibility alleles associated with local resistance to malaria in a passerine. Evol Int J org Evol 60:383–389CrossRefGoogle Scholar
  20. Bonneaud C, Balenger SL, Russell AF et al (2011) Rapid evolution of disease resistance is accompanied by functional changes in gene expression in a wild bird. Proc Natl Acad Sci USA 108:7866–7871. doi: 10.1073/pnas.1018580108 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bonneaud C, Balenger SL, Zhang J et al (2012) Innate immunity and the evolution of resistance to an emerging infectious disease in a wild bird. Mol Ecol 21:2628–2639. doi: 10.1111/j.1365-294X.2012.05551.x PubMedCrossRefGoogle Scholar
  22. Boots M, Hudson PJ, Sasaki A (2004) Large shifts in pathogen virulence related to host population structure. Science 303:824–844CrossRefGoogle Scholar
  23. Boots M, Best A, Miller MR, White A (2009) The role of ecological feedbacks in the evolution of host defence: what does theory tell us? Philos Trans R Soc Lond B 364:27–36. doi: 10.1098/rstb.2008.0160 CrossRefGoogle Scholar
  24. Bowne DR, Bowers M a (2004) Interpatch movements in spatially structured population: a literature review. Landsc Ecol 19:1–20. doi: 10.1023/B:LAND.0000018357.45262.b9 CrossRefGoogle Scholar
  25. Brüniche-Olsen A, Burridge CP, Austin JJ, Jones ME (2013) Disease induced changes in gene flow patterns among Tasmanian devil populations. Biol Conserv 165:69–78. doi: 10.1016/j.biocon.2013.05.014 CrossRefGoogle Scholar
  26. Brüniche-Olsen A, Austin JJ, Jones ME et al (2016) Detecting selection on temporal and spatial scales: a genomic time-series assessment of selective responses to devil facial tumor disease. PLoS ONE 11:1–15. doi: 10.1371/journal.pone.0147875 CrossRefGoogle Scholar
  27. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a free-living, island population. Evol Int J org Evol 53:1259–1267Google Scholar
  28. Couvet D (2002) Deleterious effects of restricted gene flow in fragmented populations. Conserv Biol 16:369–376. doi: 10.1046/j.1523-1739.2002.99518.x CrossRefGoogle Scholar
  29. Crooks KR, Sanjayan M (eds) (2006) Connectivity conservation. Conservation Biology 14. Cambridge University Press, CambridgeGoogle Scholar
  30. Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New YorkGoogle Scholar
  31. Daszak P, Berger L, Cunningham AA et al (1999) Emerging infectious diseases and amphibian population declines. Emerg Infect Dis 5:735–748. doi: 10.3201/eid0506.990601 PubMedPubMedCentralCrossRefGoogle Scholar
  32. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife–threats to biodiversity and human health. Science 287:443–449PubMedCrossRefGoogle Scholar
  33. Daszak P, Cunningham AA, Hyatt AD (2001) Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop 78:103–116PubMedCrossRefGoogle Scholar
  34. De Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126. doi: 10.1111/j.1461-0248.2004.00693.x CrossRefGoogle Scholar
  35. Dybdahl MF, Lively CM (1998) Host-parasite coevolution: evidence for rare advantage and time-lagged selection in a natural population. Evol Int J org Evol 52:1057–1066. doi: 10.2307/2411236 CrossRefGoogle Scholar
  36. Eggert LS, Terwilliger LA, Woodworth BL et al (2008) Genetic structure along an elevational gradient in Hawaiian honeycreepers reveals contrasting evolutionary responses to avian malaria. BMC Evol Biol 8:315. doi: 10.1186/1471-2148-8-315 PubMedPubMedCentralCrossRefGoogle Scholar
  37. Elderd BD, Dushoff J, Dwyer G (2008) Host-pathogen interactions, insect outbreaks, and natural selection for disease resistance. Am Nat 172:829–842PubMedCrossRefGoogle Scholar
  38. Epstein B, Jones M, Hamede R et al (2016) Rapid evolutionary response to a transmissible cancer in Tasmanian devils. Nat Commun 7:1–7. doi: 10.1038/ncomms12684 Google Scholar
  39. Fèvre EM, Bronsvoort BM de C, Hamilton KA, Cleaveland S (2006) Animal movements and the spread of infectious diseases. Trends Microbiol 14:125–131PubMedCrossRefGoogle Scholar
  40. Fisher MC, Henk DA, Briggs CJ et al (2013) Emergining fungal threats to animal, plant and ecosystem health. Nature 484:1–18. doi: 10.1038/nature10947.Emerging Google Scholar
  41. Foster JT, Woodworth BL, Eggert LE et al (2007) Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. Mol Ecol 16:4738–4746. doi: 10.1111/j.1365-294X.2007.03550.x PubMedCrossRefGoogle Scholar
  42. Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618. doi: 10.1111/mec.13139 PubMedCrossRefGoogle Scholar
  43. Frankham R, Ballou JD, Eldridge MDB et al (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475. doi: 10.1111/j.1523-1739.2011.01662.x PubMedCrossRefGoogle Scholar
  44. Frick WF, Pollock JF, Hicks AC et al (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329:679–682PubMedCrossRefGoogle Scholar
  45. Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496. doi: 10.1016/j.tree.2012.05.012 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Gandon S, Michalakis Y (2002) Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. J Evol Biol 15:451–462. doi: 10.1046/j.1420-9101.2002.00402.x CrossRefGoogle Scholar
  47. Gandon S, Capowiez Y, Dubois Y et al (1996) Local adaptation and gene-for-gene coevolution in a metapopulation model. Proc R Soc Lond B 263:1003–1009CrossRefGoogle Scholar
  48. García-Ramos G, Kirkpatrick M (1997) Genetic models of adaptation and gene flow in peripheral populations. Evol Int J Org Evol 51:21–28. doi: 10.1017/CBO9781107415324.004 CrossRefGoogle Scholar
  49. Gilpin ME, Soule ME (1986) Minimum viable populations: processes of species extinction. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 19–34Google Scholar
  50. Gortazar C, Ferroglio E, Höfle U et al (2007) Diseases shared between wildlife and livestock: a European perspective. Eur J Wildl Res 53:241–256CrossRefGoogle Scholar
  51. Green D, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Ann N Y Acad Sci 969:323–339PubMedCrossRefGoogle Scholar
  52. Hale KA, Briskie JV (2007) Decreased immunocompetence in a severely bottlenecked population of an endemic New Zealand bird. Anim Conserv 10:2–10CrossRefGoogle Scholar
  53. Harding KC, Harkonene T, Caswell H (2002) The 2002 European seal plague: epidemiology and population consequences. Ecol Lett 5:727–732CrossRefGoogle Scholar
  54. Harrison S, Bruna E (1999) Habitat fragmentation and large-scale conservation: what do we know for sure? Ecography 22:225–232CrossRefGoogle Scholar
  55. Harvell CD, Kim K, Burkholder JM et al (1999) Emerging marine diseases-climate links and anthropogenic factors. Science 285:1505–1510PubMedCrossRefGoogle Scholar
  56. Harvell CD, E MC, Ward JR et al (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162PubMedCrossRefGoogle Scholar
  57. Hawkins CE, Baars C, Hesterman H et al (2006) Emerging disease and population decline of an island endemic, the Tasmanian devil Sarcophilus harrisii. Biol Conserv 131:307–324CrossRefGoogle Scholar
  58. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162CrossRefGoogle Scholar
  59. Hitchings SP, Beebee TJC (1997) Genetic substructuring as a result of barriers to gene flow in urban Rana temporaria (common frog) populations: implications for biodiversity conservation. Heredity 79:117–127PubMedCrossRefGoogle Scholar
  60. Hoban SM, Gaggiotti OE, Bertorelle G, the ConGRESS Consortium (2013a) Sample Planning Optimization Tool for conservation and population Genetics (SPOTG): a software for choosing the appro- priate number of markers and samples. Method Ecol Evol 4:299–303CrossRefGoogle Scholar
  61. Hoban S, Gaggiotti OE, Bertorelle G (2013b) The number of markers and samples needed for detecting bottlenecks under realistic scenarios, with and without recovery: a simulation-based study. Mol Ecol 22:3444–3450PubMedCrossRefGoogle Scholar
  62. Hoban S, Kelley JL, Lotterhos KE et al (2016) Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat 188:000–000. doi: 10.1086/688018 CrossRefGoogle Scholar
  63. Hogg JT, Forbes SH, Steele BM, Luikart G (2006) Genetic rescue of an insular population of large mammals. Proc R Soc Lond B 273:1491–1499.CrossRefGoogle Scholar
  64. Holderegger R, Giulio MD (2010) The genetic effects of roads: a review of empirical evidence. Basic Appl Ecol 11:522–531. doi: 10.1016/j.baae.2010.06.006 CrossRefGoogle Scholar
  65. Hudson MA, Young RP, Jackso, JD et al (2016) Dynamics and genetics of a disease-driven species decline to near extinction: lessons for conservation. Sci Rep 6:srep30772.Google Scholar
  66. Hughes AR, Inouye BD, Johnson MTJ et al (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623PubMedCrossRefGoogle Scholar
  67. Hurtado P (2008) The potential impact of disease on the migratory structure of a partially migratory passerine population. Bull Math Biol 70:2264–2282PubMedCrossRefGoogle Scholar
  68. Jeffery KJM, Bangham CRM (2000) Do infectious diseases drive MHC diversity? Microbes Infect 2:133–1341CrossRefGoogle Scholar
  69. Johnson C, Johnson J, Vanderloo JP et al (2006) Prion protein polymorphisms in white-tailed deer influence susceptibility to chronic wasting disease. J Gen Virol 87:2109–2114PubMedCrossRefGoogle Scholar
  70. Johnson AJ, Pessier AP, Wellehan JFX et al (2008) Ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. J Wildl Dis 44:851–863PubMedCrossRefGoogle Scholar
  71. Jones ME, Cockburn A, Hamede R et al (2008) Life-histroy change in disease-ravaged Tasmanian devil popualtions. Proc Natl Acad Sci USA 105:10023–10027PubMedPubMedCentralCrossRefGoogle Scholar
  72. Karesh WB, Cook RA, Bennett EL, Newcomb J (2005) Wildlife trade and global disease emergence. Emerg Infect Dis 11:1000–1002PubMedPubMedCentralCrossRefGoogle Scholar
  73. Karlsson EK, Kwiatkowski DP, Sabeti PC (2014) Natural selection and infectious disease in human populations. Nat Rev Genet 15:379–393PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241. doi: 10.1111/j.1461-0248.2004.00684.x CrossRefGoogle Scholar
  75. Keane DP, Barr DJ, Bochsler PN et al (2008) Chronic wasting disease in a Wisconsin white-tailed deer farm. J Vet Diagn Investig 20:698–703CrossRefGoogle Scholar
  76. Keller I, Largiader CR (2003) Recent habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Proc R Soc Lond B 270:417–423CrossRefGoogle Scholar
  77. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. doi: 10.1016/S0169-5347(02)02489-8 CrossRefGoogle Scholar
  78. Keller LF, Jeffery KJ, Arcese P et al (2001) Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc R Soc Lond B 268:1387–1394CrossRefGoogle Scholar
  79. Kelly E, Phillips BL (2015) Targeted gene flow for conservation. Conserv Biol 30:259–267. doi: 10.1111/cobi.12623 PubMedCrossRefGoogle Scholar
  80. Kennedy S, Kuiken T, Jepson PD et al (2000) Mass die-off of Caspian seals caused by canine distemper virus. Emerg Infect Dis 6:637–639PubMedPubMedCentralCrossRefGoogle Scholar
  81. King KC, Lively CM (2012) Does genetic diversity limit disease spread in natural host populations. Heredity 190:199–203CrossRefGoogle Scholar
  82. Lachish S, McCallum H, Jones M (2008) Demography, disease and the devil: life-history changes in a disease-affected population of Tasmanian devils (Sarcophilus harrisii). J Anim Ecol 78:427–436PubMedCrossRefGoogle Scholar
  83. Lachish S, Miller KJ, Storfer A et al (2011) Evidence that disease-induced population decline changes genetic structure and alters dispersal patterns in the Tasmanian devil. Heredity 106:172–182. doi: 10.1038/hdy.2010.17 PubMedCrossRefGoogle Scholar
  84. Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158CrossRefGoogle Scholar
  85. Langdon JS, Humphrey JD (1987) Epizootic haematopoietic necrosis, a new viral disease in redfin perch, Perca fluviatilis L., in Australia. J Fish Dis 10:289–297CrossRefGoogle Scholar
  86. le Gouar PJ, Vallet D, David L et al (2009) How Ebola impacts genetics of western lowland gorilla populations. PLoS ONE. doi: 10.1371/journal.pone.0008375 PubMedPubMedCentralGoogle Scholar
  87. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189CrossRefGoogle Scholar
  88. Lesbarrères D, Primmer CR, Lodé T, Merilä J (2006) The effects of 20 years of highway presence on the genetic structure of Rana dalmatina populations. Ecoscience 13:531–538CrossRefGoogle Scholar
  89. Limborg NT, Helyar SJ, de Bruyn M et al (2012) Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol Ecol 21:3686–3703PubMedCrossRefGoogle Scholar
  90. Lips KR, Brem F, Brenes R et al (2006) Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci USA 103:3165–3170PubMedPubMedCentralCrossRefGoogle Scholar
  91. Lipscomb TP, Scott DP, Garber RL et al (2000) Common metastatic carcinoma of California sea lions (Zalophus californianus): evidence of genital origin and association with novel gammaherpesvirus. Vet Pathol 37:609–617PubMedCrossRefGoogle Scholar
  92. Longo A V, Savage AE, Hewson I, Zamudio KR (2015) Seasonal and ontogenetic variation of skin microbial communities and relationships to natural disease dynamics in declining amphibians. R Soc Open Sci 2:140377PubMedPubMedCentralCrossRefGoogle Scholar
  93. Lowry DB, Hoban S, Kelley JL et al (2016) Breaking RAD: An evaluation of the utility of restriction site associated DNA sequencing for genome scans of adaptation. Mol Ecol Resour 108:7866–7871. doi: 10.1111/1755-0998.12596 Google Scholar
  94. Mamaev LV, Denikina NN, Belikov SI et al (1995) Characterization of morbilliviruses isolated from Lake Baikal seals (Phoca sibirica). Vet Microbiol 44:349–379CrossRefGoogle Scholar
  95. May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B 219:281–313PubMedCrossRefGoogle Scholar
  96. McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379PubMedCrossRefGoogle Scholar
  97. Meagher S (1999) Genetic diversity and Capillaria hepatica (nematode) prevalence in Michigan deer mouse populations. Evolution 53:1318–1324PubMedCrossRefGoogle Scholar
  98. Melbourne BA, Hastings A (2008) Extinction risk depends strongly on factors contributing to stochasticity. Nature 454:100–103PubMedCrossRefGoogle Scholar
  99. Miller MW, Williams ES, McCarty CW et al (2000) Epizootiology of chronic wasting disease in free-ranging cervids in Colorado and Wyoming. J Wildl Dis 36:676–690PubMedCrossRefGoogle Scholar
  100. Minor ES, Urban DL (2008) A graph-theory framework for evaluating landscape connectivity and conservation planning. Conserv Biol 22:297–307PubMedCrossRefGoogle Scholar
  101. Morgan AD, Gandon S, Buckling A (2005) The effect of migration on local adaptation in a coevolving host–parasite system. Nature 437:253–256. doi: 10.1038/nature03913 PubMedCrossRefGoogle Scholar
  102. Morgan MJ, Hunter D, Pietsch R et al (2008) Assessment of genetic diversity in the critically endangered Australian corroboree frogs, Pseudophryne corroboree and Pseudophryne pengilleyi, identifies four evolutionarily significant units for conservation. Mol Ecol 17:3448–3463. doi: 10.1111/j.1365-294X.2008.03841.x PubMedGoogle Scholar
  103. Moritz C (1999) Conservation units and translocations: evolutionary processes. Hereditas 130:217–228CrossRefGoogle Scholar
  104. Murphy MA, Dezzani R, Pilliod DS, Storfer A (2010) Landscape genetics of high mountain frog metapopulations. Mol Ecol 19:3634–3649. doi: 10.1111/j.1365-294X.2010.04723.x PubMedCrossRefGoogle Scholar
  105. Nayfa MG, Zenger KR (2016) Unravelling the effects of gene flow and selection in highly connected populations of the silver-lip pearl oyster (Pinctada maxima). Mar Genom. doi: 10.1016/j.margen.2016.02.005 Google Scholar
  106. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evol Int J org Evol 29:1–10CrossRefGoogle Scholar
  107. O’Brien SJ, Everamnn JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 10:254–259CrossRefGoogle Scholar
  108. Pearman PB, Garner TWJ (2005) Susceptibility of Italian agile frog populations to an emerging strain of ranavirus parallels population genetic diversity. Ecol Lett 8:401–408CrossRefGoogle Scholar
  109. Peery MZ, Kirby R, Reid BN et al (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418. doi: 10.1111/j.1365-294X.2012.05635.x PubMedCrossRefGoogle Scholar
  110. Pounds JA, Bustamante MR, Coloma LA et al (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167. doi: 10.1038/nature04246 PubMedCrossRefGoogle Scholar
  111. Queney G, Ferrand N, Marchandeau S et al (2000) Absence of a genetic bottleneck in a wild rabbit (Oryctolagus cuniculus) population exposed to a severe viral epizootic. Mol Ecol 9:1253–1264. doi: 10.1046/j.1365-294X.2000.01003.x PubMedCrossRefGoogle Scholar
  112. Rachowicz LJ, Knapp RA, Morgan JAT et al (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671–1683PubMedCrossRefGoogle Scholar
  113. Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544CrossRefGoogle Scholar
  114. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  115. Robinson SJ, Samuel MD, Johnson CJ et al (2012) Emerging prion disease drives host selection in a wildlife population. Ecol Appl 22:1050–1059PubMedCrossRefGoogle Scholar
  116. Savage AE, Zamudio KR (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proc Natl Acad Sci USA 108:16705–16710.PubMedPubMedCentralCrossRefGoogle Scholar
  117. Savage AE, Zamudio KR (2016) Adaptive tolerance to a pathogenic fungus drives major histocompatibility complex evolution in natural amphibian populations. Proc R Soc B 283:20153115. doi: 10.1098/rspb.2015.3115 PubMedPubMedCentralCrossRefGoogle Scholar
  118. Savage AE, Becker CG, Zamudio KR (2015) Linking genetic and environmental factors in amphibian disease risk. Evol Appl 8:560–572. doi: 10.1111/eva.12264 PubMedPubMedCentralCrossRefGoogle Scholar
  119. Schoville SD, Tustall TS, Vredenburg VT et al (2011) Conservation genetics of evolutionary lineages of the endangered mountain yellow-legged frog, Rana muscosa (Amphibia: Ranidae), in southern California. Biol Conserv 144:2031–2040. doi: 10.1016/j.biocon.2011.04.025 CrossRefGoogle Scholar
  120. Scott ME (1988) The impact of infection and disease on animal populations: implications for conservation biology. Conserv Biol 2:40–56CrossRefGoogle Scholar
  121. Seitz WRA (1990) The influence of land use on the genetic structure of populations of the common frog Rana temporaria. Biol Conserv 54:23–249Google Scholar
  122. Serieys LEK, Lea A, Pollinger JP et al (2015) Disease and freeways drive genetic change in urban bobcat populations. Evol Appl 8:75–92. doi: 10.1111/eva.12226 PubMedCrossRefGoogle Scholar
  123. Shaffer ML (1981) Minimum population sizes for species conservation. Bioscience 31:131–134CrossRefGoogle Scholar
  124. Shultz AJ, Baker AJ, Hill GE et al (2016) SNPs across time and space: population genomic signatures of founder events and epizootics in the House Finch (Haemorhous mexicanus). Ecol Evol 6:7475–7489. doi: 10.1002/ece3.2444 PubMedPubMedCentralCrossRefGoogle Scholar
  125. Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430CrossRefGoogle Scholar
  126. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792PubMedCrossRefGoogle Scholar
  127. Smith KF, Sax DF, Lafferty KD (2006) Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20:1349–1357. doi: 10.1111/j.1523-1739.2006.00524.x PubMedCrossRefGoogle Scholar
  128. Spiegel CS, Hart PJ, Woodworth BL et al (2006) Distribution and abundance of forest birds in low-altitude habitat on Hawai’i Island: evidence for range expansion of native species. Bird Conserv Int 16:175–185.CrossRefGoogle Scholar
  129. Spielman D, Brook BW, Briscoe DA, Frankham R (2004) Does inbreeding and loss of genetic diversity decrease disease resistance? Conserv Genet 5:439–448CrossRefGoogle Scholar
  130. Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc Lond B 277:979–988.CrossRefGoogle Scholar
  131. Storfer (1999) Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87:173–180CrossRefGoogle Scholar
  132. Strand TM, Segelbacher G, Quintela M et al (2012) Can balancing selection on MHC loci counteract genetic drift in fragmented populations of black grouse. Ecol Evol 2:314–353CrossRefGoogle Scholar
  133. Talbi C, Lemey P, Suchard MA et al (2010) Phylodynamics and human-mediated dispersal of a zoonotic virus. PLoS Pathog 6:e1001166PubMedPubMedCentralCrossRefGoogle Scholar
  134. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496PubMedCrossRefGoogle Scholar
  135. Teacher AGF, Garner TWJ, Nichols RA (2009a) Evidence for directional selection at a novel major histocompatibility class I marker in wild common frogs (Rana temporaria) exposed to a viral pathogen (Ranavirus). PLoS ONE 4:e4616PubMedPubMedCentralCrossRefGoogle Scholar
  136. Teacher AGF, Garner TWJ, Nichols RA (2009b) Population genetic patterns suggest a behavioural change in wild common frogs (Rana temporaria) following disease outbreaks (Ranavirus). Mol Ecol 18:3163–3172. doi: 10.1111/j.1365-294X.2009.04263.x PubMedCrossRefGoogle Scholar
  137. Tompkins DM, Carver S, Jones ME et al (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends Parasitol 31:149–159PubMedCrossRefGoogle Scholar
  138. Traill LW, Brook BW, Frankham RR, Bradshaw CJA (2010) Pragmatic population viability targets in a rapidly changing world. Biol Conserv 143:28–34. doi: 10.1016/j.biocon.2009.09.001 CrossRefGoogle Scholar
  139. Trudeau KM, Britten HB, Restani M (2004) Sylvatic plague reduces genetic variability in black-tailed prairie dogs. J Wildl Dis 40:205–211. doi: 10.7589/0090-3558-40.2.205 PubMedCrossRefGoogle Scholar
  140. Tschirren B (2015) Borrelia burgdorferi sensu lato infection pressure shapes innate immune gene evolution in natural rodent populations across Europe. Biol Lett 11:20150263. doi: 10.1098/rsbl.2015.0263 PubMedPubMedCentralCrossRefGoogle Scholar
  141. Tschirren B, Andersson A, Scherman K, et al (2013) Polymorphisms at the innate immune receptor TLR2 are associated with Borrelia infection in a wild rodent population. Proc R Acad Sci B 280:20130364.Google Scholar
  142. Valsecchi E, Amos W, Raga J a et al (2004) The effects of inbreeding on moratlity during a morbillivirus outbreak in the Mediterranean striped dolphin (Stenella coeruleoalba). Anim Conserv 7:139–146CrossRefGoogle Scholar
  143. van Riper III C, van Riper SG, Goff ML, Laird M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecol Monogr 56:327–344CrossRefGoogle Scholar
  144. Vitalis R, Gautier M, Dawson KJ, Beaumont MA (2014) Detecting and measuring selection from gene frequency data. Genetics 196:799–817PubMedCrossRefGoogle Scholar
  145. Warner RE (1968) The role of introduced diseases in the extinction of the endemic Hawaiian avifauna. Condor 70:101–120CrossRefGoogle Scholar
  146. Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49. doi: 10.1016/j.tree.2014.10.009 PubMedCrossRefGoogle Scholar
  147. Whiteman NK, Matson KD, Bollmer JL, Parker PG (2006) Disease ecology in the Galapagos hawk (Buteo galapagoensis): host genetic diversity, parasite load and natural antibodies. Proc R Soc Lond B 273:797–804CrossRefGoogle Scholar
  148. Whitlock MC (2000) Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evol Int J Org Evol 54:1855–1861CrossRefGoogle Scholar
  149. Whittington RJ, Jones JB, Hine PM, Hyatt AD (1997) Epizootic mortality in the pilchard Sardinops sagax neopilchardus in Australia and New Zealand in 1995. I. Pathology and epizootiology. Dis Aquat Organ 28:1–16CrossRefGoogle Scholar
  150. Woodworth BL, Atkinson CT, LaPointe DA et al (2005) Host population persistence in the face of introduced vector-borne diseases: Hawaii Amakihi and avian malaria. Proc Natl Acad Sci USA 102:1531–1536PubMedPubMedCentralCrossRefGoogle Scholar
  151. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedPubMedCentralGoogle Scholar
  152. Zeisset I, Beebee TJC (2014) Drift rather than selection dominates MHC class II allelic diversity patterns at the biogeographical range scale in natterjack toads Bufo calamita. PLoS ONE 9:1–12. doi: 10.1371/journal.pone.0100176 CrossRefGoogle Scholar
  153. Zellmer AJ, Knowles LL (2009) Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence. Mol Ecol 18:3593–3602PubMedCrossRefGoogle Scholar
  154. Zenger KR, Richardson BJ, Vachot-Griffin AM (2003) A rapid population expansion retains genetic diversity within European rabbits in Australia. Mol Ecol 12:789–794. doi: 10.1046/j.1365-294X.2003.01759.x PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Donald T. McKnight
    • 1
    Email author
  • Lin Schwarzkopf
    • 1
  • Ross A. Alford
    • 1
  • Deborah S. Bower
    • 1
  • Kyall R. Zenger
    • 1
  1. 1.College of Science and EngineeringJames Cook UniversityTownsvilleAustralia

Personalised recommendations