Evidence that disease-induced population decline changes genetic structure and alters dispersal patterns in the Tasmanian devil

Heredity

Volumn 106, Issue 1, 2011, Pages 172-182

  Lachish, S ^a,b   Miller, K J ^b   Storfer, A ^c   Goldizen, A W ^a   Jones, M E ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF TASMANIA   (Australia)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Disease; dispersal; genetic diversity; genetic structure; population decline; Tasmanian devil

Indexed keywords

DATA INTERPRETATION; DISEASE PREVALENCE; DISPERSAL; GENETIC DIFFERENTIATION; GENETIC MARKER; GENETIC STRUCTURE; INBREEDING; INFECTIOUS DISEASE; MARSUPIAL; POPULATION DECLINE; RELATEDNESS; SELECTION; TUMOR;

ANIMAL; ANIMAL DISEASE; ARTICLE; AUSTRALIA; FACE TUMOR; FEMALE; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; INBREEDING; MALE; MARSUPIAL; POPULATION DYNAMICS; SPECIES EXTINCTION;

ANIMALS; EXTINCTION, BIOLOGICAL; FACIAL NEOPLASMS; FEMALE; GENETIC MARKERS; GENETIC VARIATION; INBREEDING; MALE; MARSUPIALIA; POPULATION DYNAMICS; TASMANIA;

ANIMALIA; SARCOPHILUS HARRISII;

EID: 78650311082     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2010.17     Document Type: Article

References (77)

1. Allendorf FW (1986). Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5: 181-190.
2. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008). LOSITAN: a workbench to detect molecular adaptation based on a F-st-outlier method. BMC Bioinformatics 9: 5.
3. Beaumont MA, Nichols RA (1996). Evaluating loci for use in the genetic analysis of population structure. Proc R Soc Lond Ser B-Biol Sci 263: 1619-1626.
4. Bohonak AJ (1999). Dispersal, gene flow, and population structure. Q Rev Biol 74: 21-45.
5. Broquet T, Johnson CA, Petit E, Thompson I, Burel F, Fryxell JM (2006). Dispersal and genetic structure in the American marten, Martes americana. Mol Ecol 15: 1689-1697.
6. Busch JD, Waser PM, DeWoody JA (2009). The influence of density and sex on patterns of fine-scale genetic structure. Evolution 63: 2302-2314.
7. Carson HL (1990). Increased genetic variance after a population bottleneck. Trends Ecol Evol 5: 228-230.
8. Cornuet JM, Luikart G (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
9. Creel S (1998). Social Organisation and Effective Population Size in Carnivores. Behavioral Ecology and Conservation Biology. Oxford University Press: New York, USA.
10. de Castro F, Bolker B (2005). Mechanisms of disease-induced extinction. Ecol Lett 8: 117-126.
11. Donnelly CA, Woodroffe R, Cox DR, Bourne J, Gettinby G, Le Fevre AM et al. (2003). Impact of localized badger culling on tuberculosis incidence in British Cattle. Nature 426: 834-837.
12. Double MC, Peakall R, Beck NR, Cockburn A (2005). Dispersal, philopatry, and infidelity: dissecting local genetic structure in superb fairy-wrens (Malurus cyaneus). Evolution 59: 625-635.
13. England PR, Osler GHR, Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2003). Effects of intense versus diffuse population bottlenecks on microsatellite genetic diversity and evolutionary potential. Conservation Genetics 4: 595-604.
14. Farmer W (2006). Conservation genetics of the Tasmanian devil (Sarcophilus harrisii). BSc Honours thesis, University of Tasmania: Hobart.
15. Flagstad O, Walker CW, Vila C, Sundqvist AK, Fernholm B, Hufthammer AK et al. (2003). Two centuries of the Scandinavian wolf population: patterns of genetic variability and migration during an era of dramatic decline. Mol Ecol 12: 869-880.
16. Foster JT,Woodworth BL, Eggert LE, Hart PJ, Palmer D, Duffy DC et al. (2007). Genetic structure and evolved malaria resistance in Hawaiian honeycreepers. Mol Ecol 16: 4738-4746.
17. Frankham R (1995). Effective population size, adult population size ratios in wildlife-a review. Genet Res 66: 95-107.
18. Frankham R, Ballour JD, Briscoe DA (2002). Introduction to Conservation Genetics. Cambridge University Press: New York, USA617pp.
19. Garza JC, Williamson EG (2001). Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10: 305-318.
20. Gilpin ME, Soulé ME (1986). Minimum viable populations: processes of species extinction. In: Soulé ME (ed). Conservation Biology: The Science of Scarcity and Diversity. Sinauer Associates Inc: Sunderland, MA, USApp 19-34.
21. Goudet J (1995). FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86: 485-486.
22. Greenwood PJ (1980). Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28: 1140-1162.
23. Guo SW, Thompson EA (1992). Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48: 361-372.
24. Hailer F, Helander B, Folkestad AO, Ganusevich SA, Garstad S, Hauff P et al. (2006). Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2: 316-319.
25. Handley LJL, Perrin N (2007). Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16: 1559-1578.
26. Hawkins CE, Baars C, Hesterman H, Hocking GJ, Jones ME, Lazenby B et al. (2006). Emerging disease and population decline of an island endemic, the Tasmanian devil, Sarcophilus harrisii. Biol Conserv 131: 307-324.
27. Hood GM (2006). CSIRO. PopTools version 2.7.5. Available on the internet. *Url:http://www.cse.csiro.au/poptools.
28. Hosseini PR, Dhondt AA, Dobson AP (2006). Spatial spread of an emerging infectious disease: conjunctivitis in house finches. Ecology 87: 3037-3046.
29. Hudson PJ, Rizzoli AP, Grenfell BT, Heesterbeek H, Dobson A (2002). Ecology of Wildlife Diseases. Oxford University Press: New York, USA.
30. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL et al. (2008a). Global trends in emerging infectious diseases. Nature 451: 990-994.
31. Jones ME, Cockburn A, Hamede R, Hawkins C, Hesterman H, Lachish S et al. (2008b). Life-history change in diseaseravaged Tasmanian devil populations. Proc Natl Acad Sci USA 105: 10023-10027.
32. Jones ME, Jarman P, Lees C, Hesterman H, Hamede R, Mooney N et al. (2007). Conservation management of Tasmanian Devils in the context of an emerging, extinction-threatening disease: Devil Facial Tumor Disease. EcoHealth 4: 326-337.
33. Jones ME, Paetkau D, Geffen E, Moritz C (2003). Microsatellites for the Tasmanian devil (Sarcophilus laniarius). Mol Ecol Notes 3: 277-279.
34. Jones ME, Paetkau D, Geffen E, Moritz C (2004). Genetic diversity and population structure of Tasmanian devils, the largest marsupial carnivore. Mol Ecol 13: 2197-2209.
35. Knight ME, van Oppen MJH, Smith HL, Rico C, Hewitt GM, Turner GF (1999). Evidence for male-biased dispersal in Lake Malawi cichlids from microsatellites. Mol Ecol 8: 1521-1527.
36. Koenig WD, VanVuren D, Hooge PN (1996). Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends Ecol Evol 11: 514-517.
37. Lachish S, Jones M, McCallum H (2007). The impact of disease on the survival and population growth rate of the Tasmanian devil. J Animal Ecol 76: 926-936.
38. Lachish S, McCallum H, Jones ME (2009). Demography, disease and the devil: life-history changes in a disease-affected population of Tasmanian devils (Sarcophilus harrisii). J Animal Ecol 78: 427-436.
39. Lambin X, Aars J, Piertney SB (2001). Dispersal, intra-specific competition, kin competition and kin facilitation: a review of the empirical evidence. In: Clobert J, Danchin E, Dhondt AA and Nichols JD (eds). Dispersal. Oxford University Press: New York, USA.
40. Leblois R, Rousset F, Estoup A (2004). Influence of spatial and temporal heterogeneities on the estimation of demographic parameters in a continuous population using individual microsatellite data. Genetics 166: 1081-1092.
41. Luikart G, Cornuet JM (1998). Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12: 228-237.
42. Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998). Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7: 963-974.
43. Matthysen E (2005). Density-dependent dispersal in birds and mammals. Ecography 28: 403-416.
44. McCallum H, Jones ME, Hawkins C, Hamede RK, Lachish S, Sinn DL et al. (2009). Transmission dynamics of Tasmanian devil facial tumor disease may lead to disease-induced extinction. Ecology 90: 3379-3392.
45. McCallum H, Tompkins DM, Jones M, Lachish S, Marvanek S, Lazenby B et al. (2007). Distribution and impacts of Tasmanian devil facial tumor disease. EcoHealth 4: 318-325.
46. Nei M, Maruyama T, Chakraborty R (1975). The bottleneck effect and genetic variability in populations. Evolution 29: 1-10.
47. Nunn CL, Thrall PH, Stewart K, Harcourt AH (2008). Emerging infectious diseases and animal social systems. Evol Ecol 22: 519-543.
48. Otis DL, Burnham KP, White GC, Anderson DR (1978). Statistical inference from capture data on closed animal populations. Wildl Monogr 62: 135.
49. Peakall R, Ruibal M, Lindenmayer DB (2003). Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57: 1182-1195.
50. Peakall R, Smouse PE (2005). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
51. Pedersen AB, Jones KE, Nunn CL, Altizer S (2007). Infectious diseases and extinction risk in wild mammals. Conserv Biol 21: 1269-1279.
52. Pemberton D (1990). Social Organisation and Behaviour of the Tasmanian Devil, Sarcophilus harrisii. University of Tasmania: Hobart, Tasmania.
53. Pope LC, Butlin RK, Wilson GJ, Woodroffe R, Erven K, Conyers CM et al. (2007). Genetic evidence that culling increases badger movement: implications for the spread of bovine tuberculosis. Mol Ecol 16: 4919-4929.
54. Pusey AE (1987). Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2: 295-299.
55. Queney G, Ferrand N, Marchandeau S, Azevedo M, Mougel F, Branco M 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.
56. Raymond M, Rousset F (1995). GENEPOP (Version-1.2)- Population genetics software for exact tests and ecumencism. J Hered 86: 248-249.
57. Rice WR (1989). Analyzing tables of statistical tests. Evolution 43: 223-225.
58. Richardson BJ, Hayes RA, Wheeler SH, Yardin MR (2002). Social structures, genetic structures and dispersal strategies in Australian rabbit (Oryctolagus cuniculus) populations. Behav Ecol Sociobiol 51: 113-121.
59. Rousset F (1997). Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145: 1219-1228.
60. Rousset F (2000). Genetic differentiation between individuals. J Evol Biol 13: 58-62.
61. Siddle HV, Kreiss A, Eldridge MDB, Noonan E, Clarke CJ, Pyecroft S et al. (2007). Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial. Proc Natl Acad Sci USA 104: 16221-16226.
62. Slatkin M (1987). Gene flow and the geographic structure of natural populations. Science 236: 787-792.
63. Smith KF, Sax DF, Lafferty KD (2006). Evidence for the role of infectious disease in species extinction and endangerment. Conserv Biol 20: 1349-1357.
64. Smouse PE, Peakall R, Gonzales E (2008). A heterogeneity test for fine-scale genetic structure. Mol Ecol 17: 3389-3400.
65. Sommer S (2003). Effects of habitat fragmentation and changes of dispersal behaviour after a recent population decline on the genetic variability of non-coding and coding DNA of a monogamous Malagasy rodent. Mol Ecol 12: 2845-2851.
66. Storfer A (1999). Gene flow and endangered species translocations: a topic revisited. Biol Conserv 87: 173-180.
67. Stow AJ, Sunnock P, Briscoe DA, Gardner MG (2001). The impact of habitat fragmentation on dispersal of Cunningham's skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites. Mol Ecol 10: 867-878.
68. Teacher A, Garner TW, Nichols RA (2009). Population genetic patterns suggest a behavioural change in wild common frogs (Rana temporaria) following disease outbreaks (Ranavirus). Mol Ecol 18: 3163-3172.
69. Travis JMJ, Murrell DJ, Dytham C (1999). The evolution of density-dependent dispersal. Proc R Soc Lond Ser B-Biol Sci 266: 1837-1842.
70. Trudeau KM, Britten HB, Restani M (2004). Sylvatic plague reduces genetic variability in black-tailed prairie dogs. J Wildl Dis 40: 205-211.
71. Truett GE, Heeger P, Mynatt RL, Truett AA,Walker JA,Warman ML (2000). Preparation of PCR-Quality mouse genomic DNA with hot sodium hydroxide and Tris (Hot-SHOT). BioTechniques 29: 52-54.
72. Valsecchi E, Amos W, Raga JA, Podesta M, Sherwin W (2004). The effects of inbreeding on mortality during a morbillivirus outbreak in the Mediterranean striped dolphin (Stenella coeruleoalba). Anim Conserv 7: 139-146.
73. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004). MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4: 535-538.
74. Waples RS (1989). A generalised-approach for estimating effective population size from temporal changes in allele frequency. Genetics 121: 379-391.
75. Watts PC, Rousset F (2007). Compatible genetic and ecological estimates of dispersal rates in insect (Coenagion mercuriale: Odonata: Zygoptera) populations: analysis of 'neighbourhood size' using a more precise estimator. Mol Ecol 16: 737-751.
76. Weir BS, Cockerham CC (1984). Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
77. Wobeser G (2002). Disease management strategies for wildlife. Rev Sci Tech Off Int Epiz 21: 159-178.