Molecular detection of hybridization between sympatric kangaroo species in south-eastern Australia

Heredity

Volumn 104, Issue 5, 2010, Pages 502-512

  Neaves, L E ^a   Zenger, K R ^b   Cooper, D W ^c   Eldridge, M D B ^d  

^a MACQUARIE UNIVERSITY   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d AUSTRALIAN MUSEUM   (Australia)

Author keywords

Introgressive hybridization; Kangaroos; Microsatellite; Mitochondrial DNA

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

CAPTIVITY; GENETIC MARKER; HYBRIDIZATION; INTROGRESSION; MARSUPIAL; MITOCHONDRIAL DNA; MOLECULAR ANALYSIS; MORPHOLOGY; POPULATION DENSITY; SYMPATRY; WILD POPULATION;

ANIMAL; ARTICLE; CHIMERA; CROSS BREEDING; GENE LOCUS; GENETICS; MARSUPIAL; SPECIES DIFFERENCE;

ANIMALS; CHIMERA; CROSSES, GENETIC; DNA, MITOCHONDRIAL; GENETIC LOCI; MACROPODIDAE; MICROSATELLITE REPEATS; SPECIES SPECIFICITY;

AUSTRALIA;

MACROPODIDAE; MACROPUS FULIGINOSUS; MACROPUS GIGANTEUS; MAMMALIA; METATHERIA; VERTEBRATA;

EID: 77951498215     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2009.137     Document Type: Article

References (77)

1. Anderson EC, Thompson EA (2002). A model-based method for identifying species hybrids using multilocus genetic data. Genetics 160: 1217-1229.
2. Arnold GW, Steven DE, Grassia A (1990). Associations between individuals and classes in groups of different size in a population of western grey kangaroos, Macropus fuliginosus. Aust Wildl Res 17: 551-562.
3. Arnold GW, Steven DE, Grassia A, Weeldenburg J (1992). Home-range size and fidelity of western grey kangaroos (Macropus fuliginosus) living in Remnants of Wandoo Woodland and Adjacent Farmland. Wildl Res 19: 137-143. (Pubitemid 23400826)
4. Barton NH (2001). The role of hybridization in evolution. Mol Ecol 10: 551-568.
5. Bee CA, Close RL (1993). Mitochondrial DNA analysis of introgression between adjacent taxa of rock-wallabies Petrogale species (Marsupialia: Macropodidae). Genet Res 61: 21-37.
6. Briscoe DA, Calaby JH, Close RL, Maynes GM, Murtagh CE, Sharman GB (1982). Isolation, introgression and genetic variation in rock wallabies. In: Groves RH and Ride WDL (eds). Species at Risk: Research in Australia. Australian Academy of Science: Canberra. pp 73-87.
7. Caughley G, Grigg GC, Smith L (1985). The effect of drought on kangaroo populations. J Wildl Manage 49: 679-685.
8. Caughley G, Brown B, Dostine P, Grice D (1984). The grey kangaroo overlap zone. Aust J Wildl Res 11: 1-10.
9. Chilton NB, Beveridge I, Hoste H, Gasser RB (1997). Evidence for hybridisation between Paramacropostrongylus iugalis and P. typicus (Nematoda: Strongyloidea) in grey kangaroos, Macropus fuliginosus and M. giganteus, in a zone of sympatry in eastern Australia. Int J Parasitol 31: 599-602.
10. Close RL, Lowry PS (1990). Hybrids in marsupial research. Aust J Zool 37: 259-267.
11. Coulson G (1990). Habitat separation in the grey kangaroos Macropus giganteus Shaw and Macropus fuliginosus Desmarest Marsupialia Macropodidae in Grampians National Park Western Victoria Australia. Aust Mammal 13: 33-40.
12. Coulson G (1999). Monospecific and heterospecific grouping and feeding behavior in grey kangaroos and red-necked wallabies. J Mammal 80: 270-282.
13. Coulson G, Coulson R (2001). A natural grey kangaroo hybrid? Aust Zool 31: 599-602.
14. Dobzhansky TH (1937). Genetics and the Origin of Species. Columbia University Press: New York.
15. Dowling TE, Secor CL (1997). The role of hybridization and introgression in the diversification of animals. Annu Rev Ecol Syst 28: 593-619.
16. Eldridge MDB, Close RL (1992). Taxonomy of Rock Wallabies, Petrogale (Marsupialia: Macropodidae). I. A Revision of the Eastern Petrogale with the Description of Three New Species. Aust J Zool 40: 605-625.
17. Eldridge MDB, Johnson PG, Close RL (1991). Chromosomal rearrangements in rock wallabies, Petrogale (Marsupialia: Macropodidae). IV. G-banding analysis of the Petrogale lateralis group. Aust J Zool 39: 621-627.
18. Eldridge MDB, Wilson ACC, Metcalfe CJ, Dollin AE, Bell JN, Johnson PM et al. (2001). Taxonomy of rock-wallabies, Petrogale (Marsupialia : Macropodidae). III. Molecular data confirms the species status of the purple-necked rockwallaby (Petrogale purpureicollis Le Souef). Aust J Zool 49: 323-343.
19. Ermakov O, Surin V, Titov S, Zborovsky S, Formozov N (2006). A search for Y-chromosomal species-specific markers and their use for hybridization analysis in ground squirrels (Spermophilus: Rodentia, sciuridae). Russ J Genet 42: 429-438.
20. Flamand JRB, Vankan D, Gairhe KP, Duong H, Barker JSF (2003). Genetic identification of wild Asian water buffalo in Nepal. Anim Conserv 6: 265-270.
21. Fumagalli L, Moritz C, Taberlet P, Friend JA (1999). Mitochondrial DNA sequence variation within the remnant populations of the endangered numbat (Marsupialia: Myrmecobiidae: Myrmecobius fasciatus). Mol Ecol 8: 1535-1549.
22. Goodman SJ, Barton NH, Swanson G, Abernethy K, Pemberton JM (1999). Introgression through rare hybridization: a genetic study of a hybrid zone between red and Sika Deer (Genus Cervus) in Argyll Scotland. Genetics 152: 355-371.
23. Goudet J (2000). FSTAT, a program for Windows (95 and above) to estimate and test gene diversities and Fixation indices (version 2.9.3). Available from http://www.unil.ch/popgen/ softwares/fstat.htm.
24. Hafner MS, Page RDM (1995). Molecular phylogenies and host parasite cospeciation: gophers and lice as a model system. Philos Trans R Soc Lond B Biol Sci 349: 77-83.
25. Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JW, Nadler SA (1994). Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265: 1087-1090.
26. Haldane JBS (1922). Sex ratio and unisexual sterility in hybrid animals. J Genet 12: 101-109.
27. Hawken RJ, Maccarone P, Toder R, Marshall Graves JA, Maddox JF (1999). Isolation and characterisation of marsupial IL5 genes. Immunogenetics 49: 942-948.
28. Hayman DL (1990). Marsupial cytogenetics. Aust J Zool 37: 331-349.
29. Hayman DL, Martin PG (1969). Cytogenetics of marsupials. In: Benirschke K (ed). Mammalian Cytogenetics. Spring-Verlag: New York. pp 191-217.
30. Higgins DG, Thompson JD, Gibson TJ (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-4680.
31. Kalinowski ST (2005). HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5: 187-189.
32. Kilpatrick CW (2002). Noncryogenic preservation of mammalian tissues for DNA extraction: an assessment of storage methods. Biochem Genet 40: 53-62.
33. Kingston J, Gwilliam J (2007). Hybridization between two sympatrically breeding species of fur seal at Iles Crozet revealed by genetic analysis. Conserv Genet 8: 1133-1145.
34. Kirsch JAW, Poole WE (1972). Taxonomy and distribution of the grey kangaroos, Macropus giganteus Shaw and Macropus fuliginosus (Desmarest), and their subspecies (Marsupialia: Macropodidae). Aust J Zool 20: 315-339.
35. Kovach WL (1999). MVSP-A Multivariate Statistical Package for Windows, Version 3.1. Kovach Computing Services: Pentraeth, Wales.
36. Kumar S, Tamura K, Nei M (2004). MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5: 150-163.
37. Kyle CJ, Davison A, Strobeck C (2003). Genetic structure of European pine martens (Martes martes), and evidence for introgression with M. Americana in England. Conserv Genet 4: 179-188.
38. Lancaster ML, Gemmell NJ, Negro S, Goldsworthy S, Sunnucks P (2006). Menage a trois on Macquarie Island: hybridization among three species of fur seal (Arctocephalus spp.) following historical population extinction. Mol Ecol 15: 3681-3692.
39. Lecis R, Pierpaoli M, Biro ZS, Szemethy L, Ragni B, Vercillo F et al. (2006). Bayesian analyses of admixture in wild and domestic cats (Felis silvestris) using linked microsatellite loci. Mol Ecol 15: 119-131.
40. Lu G, Basley DJ, Bernatchez L (2001). Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridisation between lineages of lake whitefish (Coregonus clupeaformis); relevance for speciation. Mol Ecol 10: 965-985.
41. Manel S, Gaggiotti OE, Waples RS (2005). Assignment methods: matching biological questions with appropriate techniques. TREE 20: 136-142.
42. Martinsen GD, Whitman TG, Turek RJ, Kiem P (2001). Hybrid populations selectively filter gene introgression between species. Evolution 55: 1325-1335.
43. Mayr E (1940). Speciation phenomena in birds. Am Nat 74: 249-278.
44. Mead RJ, Moulden DL, Twigg LE (1985). Significance of sulfhydryl compounds in the manifestation of fluoroacetate toxicity to the rat, brush-tailed possum, woylie and western grey kangaroo. Aust J Biol Sci 38: 139-149.
45. Melo-Ferreira J, Boursot P, Randi E, Kryukov A, Suchentrunk F, Ferrand N et al. (2007). The rise and fall of the mountain hare (Lepus timidus) during Pleistocene glaciations: expansion and retreat with hybridization in the Iberian Peninsula. Mol Ecol 16: 605-618.
46. Nielsen EE, Bach LA, Kotlick P (2006). HYBRIDLAB (version 1.0): a program for generating simulated hybrids from population samples. Mol Ecol Notes 6: 971-973.
47. Oliver AJ, King DR, Mead RJ (1979). Fluoro acetate tolerance a genetic marker in some Australian mammals. Aust J Zool 27: 363-372.
48. Park SDE (2001). Trypanotolerance in West African cattle and the population genetic effects of selection. PhD. thesis, University of Dublin.
49. Peakall R, Smouse PE (2006). GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288-295.
50. Pierpaoli M, Biro ZS, Herrmann M, Hupe K, Fernandes M, Ragni B et al. (2003). Genetic distinction of wildcat (Felis silvestris) populations in Europe, and hybridization with domestic cats in Hungary. Mol Ecol 12: 2585-2598.
51. Poole WE, Catling PC (1974). Reproduction in the two species of grey kangaroos, Macropus giganteus Shaw and M. fuliginosus (Desmarest) I. Sexual maturity and oestrus. Aust Wildl Res 22: 277-302.
52. Pritchard JK, Stephens M, Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155: 945-959.
53. Randi E, Lucchini V (2002). Detecting rare introgression of domestic dog genes into wild wolf (Canis lupus) populations by Bayesian admixture analyses of microsatellite variation. Conserv Genet 3: 29-43.
54. Raymond M, Rousset F (1995). GENEPOP: population genetics software for exact tests and ecumenicism. J Hered 86: 248-249. Available from http://kimura.univ-montp2.fr/Brousset/ Genepop.htm.
55. Rhymer JM, Simberloff D (1996). Extinction by hybridisation and introgression. Annu Rev Ecol Syst 27: 83-109.
56. Rice WR (1989). Analysing tables of statistical tests. Evolution 43: 223-225.
57. Robertson G (1986). The mortality of kangaroos in drought. Wildl Res 13: 349-354.
58. Salzburger W, Baric S, Sturmbauer C (2002). Speciation via introgressive hybridisation in East African cichlids? Mol Ecol 11: 619-625.
59. Schneider S, Roessli D, Excoffier L (2000). Arlequin: A Software for Population Genetics Data Analysis (Ver 2.000). Genetics and Biometry Lab, Department of Anthropology, University of Geneva.
60. Seehausen O (2004). Hybridization and adaptive radiation. TREE 19: 198-207.
61. Shepherd NC (1982). Extension of the known range of western grey kangaroos, Macropus fuliginosus, and eastern grey kangaroos, M. giganteus, in New South Wales. Aust Wildl Res 9: 389-391.
62. Sigg DP, Goldizen AW, Pople AR (2005). The importance of mating system in translocation programs: reproductive success of released male bridled nailtail wallabies. Biol Conserv 123: 289-300.
63. Slatkin M(1995). A measure of population subdivision based on microsatellite allele frequencies. Genetics 139: 457-462.
64. Smith PF, Konings A, Kornfield I (2003). Hybrid origin of a cichild population in Lake Malawi: implications for genetic variation and species diversity. Mol Ecol 12: 2497-2504.
65. Spencer PBS, Odorico DM, Jones SJ, Marsh HD, Miller DJ (1995). Highly variable microsatellites in isolated colonies of the rock-wallaby (Petrogale assimilis). Mol Ecol 4: 523-525.
66. Spiridonova L, Chelomina G, Tsuda K, Yonekawa H, Starikov V (2006). Genetic evidence of extensive introgression of short-tailed ground squirrel genes in a hybridization zone of Spermophilus major and S. erythrogenys, inferred from sequencing of the mtDNA cytochrome b gene. Russ J Genet 42: 802-809.
67. Sunnucks P, Wilson ACC, Beheregarary LB, Zenger KR, French J, Taylor AC (2000). SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Mol Ecol 9: 1699-1710.
68. Taylor AC, Sherwin WB, Wayne RK (1994). Genetic variation of microsatellite loci in a bottlenecked species: the northern hairy-nosed wombat Lasiorhinus krefftii. Mol Ecol 48: 245-247.
69. Thulin C-G, Fang M, Averianov AO (2006). Introgression from Lepus europaeus to L. timidus in Russia revealed by mitochondrial single nucleotide polymorphisms and nuclear microsatellites. Hereditas 143: 68-76.
70. Vaha J, Primmer CR (2005). Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15: 63-72.
71. Verardi A, Lucchini V, Randi E (2006). Detecting introgressive hybridization between free-ranging domestic dogs and wild wolves (Canis lupus) by admixture linkage disequilibrium analysis. Mol Ecol 15: 2845-2855.
72. Vila C, Walker C, Sundqvist AK, Flagstad O, Andersone Z, Casulli A et al. (2003). Combined use of maternal, paternal and bi-parental genetic markers for the identification of wolf-dog hybrids. Heredity 90: 17-24.
73. Ward TJ, Skow LC, Gallagher DS, Schnabel RD, Nall CA, Klolenda CE et al. (2001). Differential introgression of uniparentally inherited markers in bison populations with hybrid ancestry. Anim Genet 32: 89-91.
74. Weir BS, Cockerham CC (1984). Estimating F-statistics for the analysis of population structure. Evolution 38: 1358-1370.
75. Willis PM, Crespi BJ, Dill LM, Baird RW, Hanson MB (2004). Natural hybridization between Dall's porpoises (Phocoenoides dalli) and harbour porpoises (Phocoena phocoena). Can J Zool 82: 828-834.
76. Zenger KR, Cooper DW(2001a). Characterisation of 14 macropod microsatellite genetic markers. Anim Genet 32: 166-167.
77. Zenger KR, Cooper DW (2001b). A set of highly polymorphic microsatellite markers developed for the eastern grey kangaroo (Macropus giganteus). Mol Ecol Notes 1: 98-100.