Fine-scale genetic structure in Ethiopian wolves imposed by sociality, migration, and population bottlenecks

Conservation Genetics

Volumn 11, Issue 1, 2010, Pages 89-101

  Randall, Deborah A ^a,d   Pollinger, John P ^b   Argaw, Kifle ^c   Macdonald, David W ^a   Wayne, Robert K ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Ethiopian Wildlife Conservation Authority   (Ethiopia)

^d Frankfurt Zoological Society   (Ethiopia)

Author keywords

Canid conservation; Disease; Dispersal; Genetic drift; Microsatellites

Indexed keywords

AUTOCORRELATION; CANID; CONSERVATION GENETICS; DISEASE; DISPERSAL; GENETIC DRIFT; GENETIC STRUCTURE; POPULATION BOTTLENECK; POPULATION SIZE; SPECIES CONSERVATION;

BALE MOUNTAINS; ETHIOPIA;

CANIDAE; CANIS SIMENSIS;

EID: 74749105727     PISSN: 15660621     EISSN: 15729737     Source Type: Journal    
DOI: 10.1007/s10592-009-0005-z     Document Type: Article

References (89)

1. Aspi J, Roininen E, Ruokonen M, Kojola I, Vilà C (2006) Genetic diversity, population structure, effective population size and demographic history of the Finnish wolf population. Mol Ecol 15: 1561-1576.
2. Austin JD, Lougheed SC, Boag PT (2004) Controlling for the effects of history and nonequilibrium conditions in gene flow estimates in northern bullfrog (Rana catesbeiana) populations. Genetics 168: 1491-1506.
3. Beerli P, Felsenstein J (1999) Maximum likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152: 763-773.
4. Boutin-Ganache I, Raposo M, Raymond M, Deschepper CF (2001) M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31: 24-28.
5. Breen M, Jouquand S, Renier C et al (2001) Chromosome-specific single-locus FISH probes allow anchorage of an 1800-marker integrated radiation-hybrid/linkage map of the domestic dog genome to all chromosomes. Genome Res 11: 1784-1795.
6. Busch JD, Waser PM, DeWoody A (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16: 2450-2462.
7. Chao A (1984) Non-parametric estimation of the number of classes in a population. Scand J Stat 11: 265-270.
8. Chesser RK (1991a) Gene diversity and female philopatry. Genetics 127: 437-447.
9. Chesser RK (1991b) Influence of gene flow and breeding tactics on gene diversity within populations. Genetics 129: 573-583.
10. Ciofi C, Beaumont MA, Swingland IR, Bruford MW (1999) Genetic divergence and units for conservation in the Komodo dragon Veranus komodoensis. Proc R Soc Lond B 266: 2269-2274.
11. Clegg SM, Degnan SM, Kikkawa J et al (2002) Genetic consequences of sequential founder events by an island-colonizing bird. Proc Natl Acad Sci USA 99: 8127-8132.
12. Colwell RK (2005) EstimateS: statistical estimation of species richness and shared species from samples. Version 7. 5. User's Guide and application published at: http://purl.oclc.org/estimates.
13. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc Lond B 345: 101-118.
14. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent populations bottlenecks from allele frequency data. Genetics 144: 2001-2014.
15. Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York.
16. Di Rienzo A, Peterson AC, Garza JC et al (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91: 3166-3170.
17. Diniz-Filho J, Telles M (2002) Spatial autocorrelation analysis and the identification of operational units for conservation in continuous populations. Conserv Biol 16: 924-935.
18. El Mousadik A, Petit E (1996) High level of genetic differentiation for allelic richness among populations of the argan tree (Argania spinosa (L.) Skeels) endemic to Morroco. Theor Appl Genet 92: 832-839.
19. England P, Cornuet J, Berthier P, Tallmon D, Luikart G (2006) Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conserv Genet 7: 303-308.
20. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
21. Excoffier L, Novembre J, Schneider S (2000) SIMCOAL: a general coalescent program for the simulation of molecular data in interconnected populations with arbitrary demography. J Hered 91: 506-509.
22. Francisco LV, Langston AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7: 359-362.
23. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10: 305-318.
24. 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, Sunderland, MA, pp 13-34.
25. Goossens B, Chikhi L, Jalil MF et al (2005) Patterns of genetic diversity and migration in increasingly fragmented and declining orang-utan (Pongo pygmaeus) populations from Sabah, Malaysia. Mol Ecol 14: 441-456.
26. Gottelli D, Sillero-Zubiri C, Applebaum GD et al (1994) Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Mol Ecol 3: 301-312.
27. Gottelli D, Marino J, Sillero-Zubiri C, Funk SM (2004) The effect of the last glacial age on speciation and population genetic structure of the endangered Ethiopian wolf (Canis simensis). Mol Ecol 13: 2275-2286.
28. Goudet J (1995) FSTAT (Version 1. 2): a computer program to calculate F-statistics. J Hered 86: 485-486.
29. Goudet J, Raymond M, DeMeeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144: 1933-1940.
30. Haydon DT, Laurenson MK, Sillero-Zubiri C (2002) Integrating epidemiology into population viability analysis: managing the risk posed by rabies and canine distemper to the Ethiopian wolf. Conserv Biol 16: 1372-1383.
31. Haydon DT, Randall DA, Mathews L et al (2006) Low-coverage vaccination strategies for the conservation of endangered species. Nature 443: 692-695.
32. Hickerson MJ, Cunningham CW (2005) Contrasting Quaternary histories in an ecologically divergent sister pair of low-dispersing intertidal fish (Xiphister) revealed by multilocus DNA analysis. Evolution 59: 344-360.
33. Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38: 209-216.
34. Hooge PN, Eichenlaub B (2000) Animal movement extension to Arcview version 2.0. In Alaska Science Center-Biological Science Office, U. S. Geological Survey, Anchorage, AK, USA.
35. Jones ME, Paetkau D, Geffen E, Moritz C (2004) Genetic diversity and population structure of Tansmanian devils, the largest marsupial carnivore. Mol Ecol 13: 2197-2209.
36. Keller I, Largiadèr CR (2002) 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: 417-423.
37. Knobel D, Fooks AR, Brookes S et al (2008) Trapping and vaccination of endangered Ethiopian wolves to control an outbreak of rabies. J Appl Ecol 45: 109-116.
38. Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J Mammal 78: 320-335.
39. Laurenson K, Shiferaw F, Sillero-Zubiri C (1997) Disease, domestic dogs and the Ethiopian wolf: the current situation. In: Sillero-Zubiri C, Macdonald DW (eds) The Ethiopian wolf: status survey and conservation action plan. IUCN, Gland, Switzerland and Cambridge, UK, pp 32-40.
40. Laurenson MK, Sillero-Zubiri C, Thompson H et al (1998) Disease threats to endangered species: Ethiopian wolves, domestic dogs, and canine pathogens. Anim Conserv 1: 273-280.
41. Marino J (2003a) The spatial ecology of the Ethiopian wolf, Canis simensis. DPhil thesis, University of Oxford.
42. Marino J (2003b) Threatened Ethiopian wolves persist in small isolated Afroalpine enclaves. Oryx 37: 62-71.
43. Marino J, Sillero-Zubiri C, Macdonald DW (2006) Trends, dynamics and resilience of an Ethiopian wolf population. Anim Conserv 9: 49-58.
44. Marshall T, Slate J, Kruuk L, Pemberton J (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7: 639-655.
45. Maudet C, Miller C, Bassano B et al (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)]. Mol Ecol 11: 421-436.
46. McRae BH, Beier P, Dewald LE, Huynh LY, Keim P (2005) Habitat barriers limit gene flow and illuminate historical events in a wide-ranging carnivore, the American puma. Mol Ecol 14: 1965-1977.
47. Mellersh CS, Hitte C, Richman M et al (2000) An integrated linkage-radiation hybrid map of the canine genome. Mamm Genome 11: 120-130.
48. Moritz C (1995) Defining 'evolutionary significant units' for conservation. Trends Ecol Evol 9: 373-375.
49. Navidi W, Arnheim N, Waterman MS (1992) A multiple-tube approach for accurate genotyping of very small DNA samples by using PCR: statistical considerations. Am J Hum Genet 50: 347-359.
50. Neff MW, Broman KW, Mellersh CS et al (1999) A second-generation genetic linkage map of the domestic dog, Canis familiaris. Genetics 151: 803-820.
51. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York.
52. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29: 1-10.
53. O'Ryan C, Harley EH, Bruford MW et al (1998) Microsatellite analysis of genetic diversity in fragmented South African buffalo populations. Anim Conserv 1: 85-95.
54. Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16: 207-213.
55. Palstra FP, O'Connell F, Ruzzante DE (2007) Population structure and gene flow reversals in Atlantic salmon (Salmo salar) over contemporary and long-term temporal scales: effects of population size and life history. Mol Ecol 16: 4504-4522.
56. Pastor T, Garza JC, Allen P, Amos W, Aguilar A (2004) Low genetic variability in the highly endangered Mediterranean monk seal. J Hered 95: 291-300.
57. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
58. 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.
59. Pearse DE, Arndt AD, Velenzuela N et al (2006) Estimating population structure under nonequilibrium conditions in a conservation context: continent-wide population genetics of the giant Amazon river turtle, Podocnemis expansa (Chelonia; Podocnemididae). Mol Ecol 15: 985-1006.
60. Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size, Version 1. 3. In Queensland Government, Department of Primary Industries and Fisheries.
61. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90: 502-503.
62. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Genet 6: 847-859.
63. Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
64. Pruett CL, Winker K (2005) Northwestern song sparrow populations show genetic effects of sequential colonization. Mol Ecol 14: 1421-1434.
65. Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144: 383-387.
66. Randall DA, Williams SD, Kuzmin IV et al (2004) Rabies in endangered Ethiopian wolves. Emerg Infect Dis 10: 2214-2217.
67. Randall DA, Marino J, Haydon DT et al (2006) An integrated disease management strategy for the control of rabies in Ethiopian wolves. Biol Conserv 131: 151-162.
68. Randall DA, Pollinger JP, Wayne RK et al (2007) Inbreeding is reduced by female-biased dispersal and mating behavior in Ethiopian wolves. Behav Ecol 18: 579-589.
69. Rannala B, Hartigan JA (1996) Estimating gene flow in island populations. Genet Res 67: 147-158.
70. Raymond M, Rousset F (1995) GENEPOP (version 1. 2): population genetics software for exact tests and ecumenicism. J Hered 86: 248-249.
71. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43: 223-225.
72. Riley SPD, Pollinger JP, Sauvajot RM et al (2006) A southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15: 1733-1741.
73. Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN, version 2. 000: a software for population genetics analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland.
74. Scribner KT, Chesser RK (1993) Environmental and demographic correlates of spatial and seasonal genetic structure in the eastern cottontail (Sylvilagus floridanus). J Mammal 74: 1026-1045.
75. Sillero-Zubiri C, Gottelli D (1995a) Diet and feeding behavior of Ethiopian wolves (Canis simensis). J Mammal 76: 531-541.
76. Sillero-Zubiri C, Gottelli D (1995b) Spatial organization in the Ethiopian wolf Canis simensis: large packs and small stable home ranges. J Zool 237: 65-81.
77. Sillero-Zubiri C, Gottelli D, Macdonald DW (1996a) Male philopatry, extra-pack copulations and inbreeding avoidance in Ethiopian wolves (Canis simensis). Behav Ecol Sociobiol 38: 331-340.
78. Sillero-Zubiri C, King AA, Macdonald DW (1996b) Rabies and mortality in Ethiopian wolves (Canis simensis). J Wildl Dis 32: 80-86.
79. Sillero-Zubiri C, Marino J, Gottelli D, Macdonald DW (2004) Ethiopian wolves. In: Macdonald DW, Sillero-Zubiri C (eds) Biology and conservation of wild canids. Oxford University Press, Oxford, pp 311-322.
80. Storz JF (1999) Genetic consequences of mammalian social structure. J Mammal 80: 553-569.
81. Storz JF, Beaumont MA, Alberts SC (2002) Genetic evidence for a long-term population decline in a savannah-dwelling primate: inferences from a hierarchical Bayesian model. Mol Biol Evol 19: 1981-1990.
82. Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137: 1147-1155.
83. Taberlet P, Griffin AS, Goossens B et al (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 26: 3189-3194.
84. Turner TF, Wares JP, Gold JR (2002) Genetic effective size is three orders of magnitude smaller than adult census size in an abundant, estuarine-dependent marine fish (Sciaenops ocellatus). Genetics 162: 1329-1339.
85. Wayne RK, Koepfli KP (1996) Demographic and historical effects on genetic variation in carnivores. In: Gittleman JL (ed) Carnivore behavior, ecology, and evolution. Cornell University Press, Ithaca, pp 453-484.
86. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
87. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163: 1177-1191.
88. Wright S (1931) Evolution of Mendelian populations. Genetics 16: 97-159.
89. Wright S (1943) Isolation by distance. Genetics 28: 114-118.