Advertisement

Geographic hot spots of dingo genetic ancestry in southeastern Australia despite hybridisation with domestic dogs

  • Kylie M. CairnsEmail author
  • Bradley J. Nesbitt
  • Shawn W. Laffan
  • Mike Letnic
  • Mathew S. Crowther
Research Article

Abstract

Hybridisation resulting from human-driven shifts in species ranges is a global conservation concern. In Australia, hybridisation between dingoes (Canis dingo) and domestic dogs (Canis familiaris) has been identified as an extinction threat to the dingo, and is thought to be particularly widespread in south-eastern Australia. Here, we investigated the extent of hybridisation between dingoes and dogs in a sample of 783 wild-caught canids from eastern New South Wales, using an established 23-microsatellite test. We then mapped the distribution of these samples and identified three areas that are geographic hotspots of high dingo genetic ancestry using geospatial analysis. Between 9 and 23% of the wild canids that we sampled were classified as only having or likely to have only dingo ancestry. Only 0.6% of the wild canids we sampled were classified as having no dingo ancestry. Introgression from domestic dogs into the southeastern dingo gene pool has been extensive, with 76–88% of sampled dingoes carrying some dog ancestry. Spatial analyses revealed several geographic hotspots of high dingo genetic ancestry within north-eastern New South Wales (NSW) where there was a higher than expected prevalence of dingoes with no domestic dog ancestry. A key finding of our study is the observation of several regions where dingoes were largely free of admixture from dogs. There is an ongoing need for evidence-based strategies to reduce human-driven hybridisation by identifying and maintaining natural barriers to reproduction or limiting opportunities for wild-domesticate hybridisation. Globally, legislators and land managers may need to consider less restrictive species definitions to conserve endangered or ecologically significant taxa.

Keywords

Introgression Canis familiaris Canis dingo Admixture Microsatellites Spatial analysis 

Notes

Acknowledgements

The authors acknowledge the contributions of A/Prof Alan Wilton (UNSW) who passed away in 2011, before this manuscript was completed and written. Special thanks to the 23 Dingo/wild dog DNA research project investigators who sourced DNA sample material during the 16 year project period including Brad Nesbitt (principal investigator), Michael Dodkin, Geoffrey James, Bernard Whitehead, Dave McFarlane, Andrew McDougal, David Jenkins, Peter Ellem, and James Baldwin. Thanks to the many collaborators from NSW National Parks and Wildlife Service, Rural Lands Protection Boards, Livestock Health & Pest Authorities, and NSW Department of Primary Industries who provided wild canid DNA samples for analysis. DNA genotyping carried out as part of this research were principally funded by the NSW National Parks and Wildlife Service.

Compliance with ethical standards

Conflict of interest

KMC is a scientific advisor to the Australian Dingo Foundation, New Guinea Highland Wild Dog Foundation and New Guinea Signing Dog Conservation Society. No other interests declared.

Supplementary material

10592_2019_1230_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1212 kb)
10592_2019_1230_MOESM2_ESM.xlsx (130 kb)
Supplementary material 2 (XLSX 129 kb)
10592_2019_1230_MOESM3_ESM.pdf (113 kb)
Supplementary material 3 (PDF 113 kb)
10592_2019_1230_MOESM4_ESM.pdf (1.3 mb)
Supplementary material 4 (PDF 1347 kb)
10592_2019_1230_MOESM5_ESM.xlsx (72 kb)
Supplementary material 5 (XLSX 71 kb)
10592_2019_1230_MOESM6_ESM.pdf (268 kb)
Supplementary material 6 (PDF 267 kb)
10592_2019_1230_MOESM7_ESM.pdf (114 kb)
Supplementary material 7 (PDF 114 kb)
10592_2019_1230_MOESM8_ESM.pdf (568 kb)
Supplementary material 8 (PDF 567 kb)

References

  1. Adams JR, Leonard JA, Waits LP (2003) Widespread occurrence of a domestic dog mitochondrial DNA haplotype in southeastern US coyotes. Mol Ecol 12:541–546PubMedCrossRefPubMedCentralGoogle Scholar
  2. Allen BL, Allen LR, Ballard G, Jackson SM, Fleming PJS (2017) A roadmap to meaningful dingo conservation. Canid Biol Conserv 20:45–56Google Scholar
  3. Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622CrossRefGoogle Scholar
  4. Anderson TM, vonHoldt BM, Candille SI, Musiani M, Greco C, Stahler DR, Smith DW, Padhukasahasram B, Randi E, Leonard JA, Bustamante CD, Ostrander EA, Tang H, Wayne RK, Barsh GS (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323:1339–1343PubMedPubMedCentralCrossRefGoogle Scholar
  5. Benson JF, Patterson BR (2013) Inter-specific territoriality in a Canis hybrid zone: spatial segregation between wolves, coyotes, and hybrids. Oecologia 173:1539–1550PubMedCrossRefPubMedCentralGoogle Scholar
  6. Bohling JH (2016) Strategies to address the conservation threats posed by hybridization and genetic introgression. Biol Conserv 203:321–327CrossRefGoogle Scholar
  7. Bohling JH, Waits LP (2011) Assessing the prevalence of hybridization between sympatric Canis species surrounding the red wolf (Canis rufus) recovery area in North Carolina. Mol Ecol 20:2142–2156PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bohling JH, Waits LP (2015) Factors influencing red wolf–coyote hybridization in eastern North Carolina, USA. Biol Conserv 184:108–116CrossRefGoogle Scholar
  9. Bruce E, Albright L, Sheehan S, Blewitt M (2014) Distribution patterns of migrating humpback whales (Megaptera novaeangliae) in Jervis Bay, Australia: a spatial analysis using geographical citizen science data. Appl Geogr 54:83–95CrossRefGoogle Scholar
  10. Cahill JA, Stirling I, Kistler L, Salamzade R, Ersmark E, Fulton TL, Stiller M, Green RE, Shapiro B (2015) Genomic evidence of geographically widespread effect of gene flow from polar bears into brown bears. Mol Ecol 24:1205–1217PubMedPubMedCentralCrossRefGoogle Scholar
  11. Cairns KM, Wilton AN (2016) New insights on the history of canids in Oceania based on mitochondrial and nuclear data. Genetica 144:553–565PubMedCrossRefPubMedCentralGoogle Scholar
  12. Cairns KM, Wilton AN, Ballard JWO (2011) The identification of dingoes in a background of hybrids. In: Urbano KV (ed) Advances in genetics research. Nova Science Publishers, New York, pp 309–327Google Scholar
  13. Cairns KM, Brown SK, Sacks BN, Ballard JWO (2017) Conservation implications for dingoes from the maternal and paternal genome: multiple populations, dog introgression and demography. Ecol Evol 7:9787–9807PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cairns KM, Shannon LM, Koler-Matznick J, Ballard JWO, Boyko AR (2018) Elucidating biogeographical patterns in Australian native canids using genome wide SNPs. PLoS ONE 13:e0198754PubMedPubMedCentralCrossRefGoogle Scholar
  15. Canestrelli D, Bisconti R, Chiocchio A, Maiorano L, Zampiglia M, Nascetti G (2017) Climate change promotes hybridisation between deeply divergent species. PeerJ 5:e3072PubMedPubMedCentralCrossRefGoogle Scholar
  16. Chan WY, Hoffmann AA, van Oppen MJH (2019) Hybridization as a conservation management tool. Conserv Lett 12:e12652CrossRefGoogle Scholar
  17. Colman N (2015) Morphological variation and ecological interactions of Australia’s apex predator—the dingo (Canis dingo). Western Sydney UniversityGoogle Scholar
  18. Corbett LK (2001a) Conservation status of the dingo. In: Dickman CR, Lunney D (eds) A symposium on the dingo. Royal Zoological Society of New South Wales, Sydney, pp 10–19CrossRefGoogle Scholar
  19. Corbett LK (2001b) The Dingo in Australia and Asia. University of NSW Press, SydneyGoogle Scholar
  20. Corbett LK (2008) Canis lupus ssp. dingo. The IUCN Red List of Threatened Species, Version 2014.1Google Scholar
  21. Crowther MS, Fillios M, Colman N, Letnic M (2014) An updated description of the Australian dingo (Canis dingo Meyer, 1793). J Zool 293:192–203CrossRefGoogle Scholar
  22. Drake AG, Klingenberg CP (2010) Large-scale diversification of skull shape in domestic dogs: disparity and modularity. Am Nat 175:289–301PubMedCrossRefGoogle Scholar
  23. Elledge AE, Allen LR, Carlsson B-L, Leung LK-P (2008) An evaluation of genetic analyses, skull morphology and visual appearance for assessing dingo purity: implications for dingo conservation. Wildl Res 35:812–820CrossRefGoogle Scholar
  24. ESRI (2018) ArcGIS Release 10.6. Redlands, CAGoogle Scholar
  25. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  26. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567PubMedPubMedCentralGoogle Scholar
  27. Fitzpatrick BM, Ryan ME, Johnson JR, Corush J, Carter ET (2015) Hybridization and the species problem in conservation. Curr Zool 61:206–216CrossRefGoogle Scholar
  28. Francisco LV, Langsten AA, Mellersh CS, Neal CL, Ostrander EA (1996) A class of highly polymorphic tetranucleotide repeats for canine genetic mapping. Mamm Genome 7:359–362PubMedCrossRefGoogle Scholar
  29. Fredholm M, Winterø AK (1995) Variation of short tandem repeats within and between species belonging to the Canidae family. Mamm Genome 6:11–18PubMedCrossRefGoogle Scholar
  30. Galov A, Fabbri E, Caniglia R, Arbanasić H, Lapalombella S, Florijančić T, Bošković I, Galaverni M, Randi E (2015) First evidence of hybridization between golden jackal (Canis aureus) and domestic dog (Canis familiaris) as revealed by genetic markers. R Soc Open Sci 2:150450PubMedPubMedCentralCrossRefGoogle Scholar
  31. Getis A, Ord JK (1992) The analysis of spatial association by use of distance statistics. Geogr Anal 24:189–206CrossRefGoogle Scholar
  32. Gottelli D, Sillero-zubiri C, Applebaum GD, Roy MS, Girman DJ, Garcia-moreno J, Ostrander EA, Wayne RK (1994) Molecular genetics of the most endangered canid: the Ethiopian wolf Canis simensis. Mol Ecol 3:301–312PubMedCrossRefPubMedCentralGoogle Scholar
  33. Halbert ND, Derr JN (2007) A comprehensive evaluation of cattle introgression into US Federal Bison Herds. J Hered 98:1–12PubMedCrossRefPubMedCentralGoogle Scholar
  34. Heppenheimer E, Cosio DS, Brzeski KE, Caudill D, Van Why K, Chamberlain MJ, Hinton JW, vonHoldt B (2018) Demographic history influences spatial patterns of genetic diversity in recently expanded coyote (Canis latrans) populations. Heredity 120:183–195PubMedCrossRefPubMedCentralGoogle Scholar
  35. Hertwig ST, Schweizer M, Stepanow S, Jungnickel A, Böhle UR, Fischer MS (2009) Regionally high rates of hybridization and introgression in German wildcat populations (Felis silvestris, Carnivora, Felidae). J Zool Syst Evol Res 47:283–297CrossRefGoogle Scholar
  36. Hindrikson M, Männil P, Ozolins J, Krzywinski A, Saarma U (2012) Bucking the trend in wolf-dog hybridization: first evidence from Europe of hybridization between female dogs and male wolves. PLoS ONE 7:e46465PubMedPubMedCentralCrossRefGoogle Scholar
  37. Hinton JW, Gittleman JL, Manen FT, Chamberlain MJ (2018) Size-assortative choice and mate availability influences hybridization between red wolves (Canis rufus) and coyotes (Canis latrans). Ecol Evol 8:3927–3940PubMedPubMedCentralCrossRefGoogle Scholar
  38. Hinton JW, Heppenheimer E, West KM, Caudill D, Karlin ML, Kilgo JC, Mayer JJ, Miller KV, Walch M, vonHoldt B, Chamberlain MJ (2019) Geographic patterns in morphometric and genetic variation for coyote populations with emphasis on southeastern coyotes. Ecol Evol 9:3389–3404PubMedPubMedCentralCrossRefGoogle Scholar
  39. Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485PubMedCrossRefGoogle Scholar
  40. Holmes NG, Humphreys SJ, Binns MM, Holliman A, Curtis R, Mellersh CS, Sampson I (1993) Isolation and characterization of microsatellites from the canine genome. Anim Genet 24:289–292PubMedCrossRefPubMedCentralGoogle Scholar
  41. Holmes NG, Dickens HF, Parker HL, Binns MM, Mellersh CS, Sampson J (1995) Eighteen canine microsatellites. Anim Genet 26:132a–133aCrossRefGoogle Scholar
  42. Hulsegge I, Schoon M, Windig J, Neuteboom M, Hiemstra SJ, Schurink A (2019) Development of a genetic tool for determining breed purity of cattle. Livest Sci 223:60–67CrossRefGoogle Scholar
  43. Janes JK, Miller JM, Dupuis JR, Malenfant RM, Gorrell JC, Cullingham CI, Andrew RL (2017) The K = 2 conundrum. Mol Ecol 26:3594–3602PubMedCrossRefPubMedCentralGoogle Scholar
  44. Jones FW (1921) The status of the dingo. R Soc South Aust 45:254–263Google Scholar
  45. Jones E (2009) Hybridisation between the dingo, Canis lupus dingo, and the domestic dog, Canis lupus familiaris, in Victoria: a critical review. Aust Mammal 31:1–7CrossRefGoogle Scholar
  46. Klütsch CFC, Seppälä EH, Fall T, Uhlén M, Hedhammar Å, Lohi H, Savolainen P (2011) Regional occurrence, high frequency but low diversity of mitochondrial DNA haplogroup d1 suggests a recent dog-wolf hybridization in Scandinavia. Anim Genet 42:100–103PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191PubMedPubMedCentralCrossRefGoogle Scholar
  48. Letnic M, Crowther MS (2012) Patterns in the abundance of kangaroo populations in arid Australia are consistent with the exploitation ecosystems hypothesis. Oikos 122:761–769CrossRefGoogle Scholar
  49. Letnic M, Baker L, Nesbitt B (2013) Ecologically functional landscapes and the role of dingoes as trophic regulators in south-eastern Australia and other habitats. Ecol Manag Restor 14:101–105CrossRefGoogle Scholar
  50. Maples Brian K, Gravel S, Kenny Eimear E, Bustamante Carlos D (2013) RFMix: a discriminative modeling approach for rapid and robust local-ancestry inference. Am J Hum Genet 93:278–288PubMedPubMedCentralCrossRefGoogle Scholar
  51. Mattucci F, Galaverni M, Lyons LA, Alves PC, Randi E, Velli E, Pagani L, Caniglia R (2019) Genomic approaches to identify hybrids and estimate admixture times in European wildcat populations. Sci Rep 9:11612PubMedPubMedCentralCrossRefGoogle Scholar
  52. Mellersh C, Holmes N, Binns M, Sampson J (1994) Dinucleotide repeat polymorphisms at four canine loci (LEI 003, LEI 007, LEI 008 and LEI 015). Anim Genet 25:125PubMedCrossRefPubMedCentralGoogle Scholar
  53. Mellersh CS, Langston AA, Acland GM, Fleming MA, Ray K, Wiegand NA, Francisco LV, Gibbs M, Aguirre GD, Ostrander EA (1997) A linkage map of the canine genome. Genomics 46:326–336PubMedCrossRefPubMedCentralGoogle Scholar
  54. Morell V (2016) Rethinking the North American wolf. Science 353:434PubMedCrossRefPubMedCentralGoogle Scholar
  55. Morris T, Letnic M (2017) Removal of an apex predator initiates a trophic cascade that extends from herbivores to vegetation and the soil nutrient pool. Proc R Soc B 284:20170111PubMedCrossRefPubMedCentralGoogle Scholar
  56. Muhlfeld CC, Kovach RP, Jones LA, Al-Chokhachy R, Boyer MC, Leary RF, Lowe WH, Luikart G, Allendorf FW (2014) Invasive hybridization in a threatened species is accelerated by climate change. Nat Clim Chang 4:620–624CrossRefGoogle Scholar
  57. Murphy SM, Adams JR, Cox JJ, Waits LP (2018) Substantial red wolf genetic ancestry persists in wild canids of southwestern Louisiana. Conserv Lett 12:e12621CrossRefGoogle Scholar
  58. Murray DL, Bastille-Rousseau G, Adams JR, Waits LP (2015) The challenges of Red Wolf conservation and the fate of an endangered species recovery program. Conserv Lett 8:338–344CrossRefGoogle Scholar
  59. Newsome AE, Corbett LK (1982) The identity of the dingo II. Hybridization with domestic dogs in captivity and in the wild. Aust J Zool 30(2):365CrossRefGoogle Scholar
  60. Newsome AE, Corbett LK (1985) The Identity of the Dingo III. The incidence of Dingoes, Dogs and Hybrids and their coat colours in remote and settled regions of Australia. Aust J Zool 33:363–373CrossRefGoogle Scholar
  61. Newsome AE, Corbett LK, Carpenter SM (1980) The identity of the dingo I. Morphological discriminants of dingo and dog skulls. Aust J Zool 28(4):615CrossRefGoogle Scholar
  62. OEH (2009) Predation and Hybridisation by Feral Dogs, Canis lupus familiaris—key threatening process listing. NSW Scientific Committee—final determination. NSW Office of Environment and Heritage https://www.environment.nsw.gov.au/determinations/feraldogsFD.htm. Accessed 04 Feb 2019
  63. Oliveira R, Randi E, Mattucci F, Kurushima JD, Lyons LA, Alves PC (2015) Toward a genome-wide approach for detecting hybrids: informative SNPs to detect introgression between domestic cats and European wildcats (Felis silvestris). Heredity 115:195–205PubMedPubMedCentralCrossRefGoogle Scholar
  64. Oskarsson MCR, Klütsch CFC, Boonyaprakob U, Wilton A, Tanabe Y, Savolainen P (2011) Mitochondrial DNA data indicate an introduction through Mainland Southeast Asia for Australian dingoes and Polynesian domestic dogs. Proc R Soc B 279:967–974PubMedCrossRefGoogle Scholar
  65. Ostrander EA, Sprague GF, Rine J (1993) Identification and characterization of dinucleotide repeat (CA)n markers for genetic mapping in dog. Genomics 16:207–213PubMedCrossRefGoogle Scholar
  66. Ostrander EA, Mapa FA, Yee M, Rine J (1995) One hundred and one new simple sequence repeat-based markers for the canine genome. Mamm Genome 6:192–195PubMedCrossRefGoogle Scholar
  67. Parr WCH, Wilson LAB, Wroe S, Colman NJ, Crowther MS, Letnic M (2016) Cranial shape and the modularity of hybridization in dingoes and dogs; hybridization does not spell the end for native morphology. Evol Biol 43:171–187CrossRefGoogle Scholar
  68. Primmer C, Mathews M (1993) Canine tetra-nucleotide repeat polymorphism at VIAS-D10 locus. Anim Genet 24:332PubMedCrossRefGoogle Scholar
  69. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945PubMedPubMedCentralGoogle Scholar
  70. Pritchard JK, Wen X, Falush D (2010) Documentation for structure software: version 2.3. University of Chicago, ChicagoGoogle Scholar
  71. Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83–109CrossRefGoogle Scholar
  72. Rosel PE, Wilcox LA, Sinclair C, Speakman TR, Tumlin MC, Litz JA, Zolman ES (2017) Genetic assignment to stock of stranded common bottlenose dolphins in southeastern Louisiana after the Deepwater Horizon oil spill. Endanger Species Res 33:221–234CrossRefGoogle Scholar
  73. Sacks BN, Brown SK, Stephens D, Pedersen NC, Wu J-T, Berry O (2013) Y chromosome analysis of dingoes and Southeast Asian village dogs suggests a Neolithic continental expansion from Southeast Asia followed by multiple Austronesian dispersals. Mol Biol Evol 13:1265–1275Google Scholar
  74. Sánchez-Guillén RA, Muñoz J, Rodríguez-Tapia G, Feria Arroyo TP, Córdoba-Aguilar A (2013) Climate-induced range shifts and possible hybridisation consequences in insects. PLoS ONE 8:e80531PubMedPubMedCentralCrossRefGoogle Scholar
  75. Schweizer RM, Durvasula A, Smith J, Vohr SH, Stahler DR, Galaverni M, Thalmann O, Smith DW, Randi E, Ostrander EA, Green RE, Lohmueller KE, Novembre J, Wayne RK (2018) Natural selection and origin of a melanistic allele in North American gray wolves. Mol Biol Evol 35:1190–1209PubMedPubMedCentralCrossRefGoogle Scholar
  76. Smith BP, Cairns KM, Adams JW, Newsome TM, Fillios M, Deaux EC, Parr WCH, Letnic M, Van Eeden LM, Appleby RG, Bradshaw CJA, Savolainen P, Ritchie EG, Nimmo DG, Archer-lean C, Greenville A, Dickman CR, Watson L, Moseby KE, Doherty TS, Wallach AD, Morrant DS, Crowther MS (2019) Taxonomic status of the Australian dingo: the case for Canis dingo Meyer, 1793. Zootaxa 4564:173–197CrossRefGoogle Scholar
  77. Smouse PE, Peakall R (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539PubMedPubMedCentralCrossRefGoogle Scholar
  78. Stephens D, Wilton AN, Fleming PJS, Berry O (2015) Death by sex in an Australian icon: a continent-wide survey reveals extensive hybridization between dingoes and domestic dogs. Mol Ecol 24:5643–5656PubMedCrossRefPubMedCentralGoogle Scholar
  79. Stephenson RL, Power MJ, Laffan SW, Suthers IM (2015) Tests of larval retention in a tidally energetic environment reveal the complexity of the spatial structure in herring populations. Fish Oceanogr 24:553–570CrossRefGoogle Scholar
  80. Steyer K, Tiesmeyer A, Muñoz-Fuentes V, Nowak C (2018) Low rates of hybridization between European wildcats and domestic cats in a human-dominated landscape. Ecol Evol 8(4):2290–2304PubMedPubMedCentralGoogle Scholar
  81. Stronen AV, Paquet PC (2013) Perspectives on the conservation of wild hybrids. Biol Conserv 167:390–395CrossRefGoogle Scholar
  82. Vaha J-P, Primmer C (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72PubMedCrossRefPubMedCentralGoogle Scholar
  83. van Wyk AM, Dalton DL, Hoban S, Bruford MW, Russo IRM, Birss C, Grobler P, van Vuuren BJ, Kotzé A (2017) Quantitative evaluation of hybridization and the impact on biodiversity conservation. Ecol Evol 7:320–330PubMedCrossRefPubMedCentralGoogle Scholar
  84. Vilà C, Wayne RK (1999) Hybridization between wolves and dogs. Conserv Biol 13:195–198CrossRefGoogle Scholar
  85. vonHoldt BM, Pollinger JP, Lohmueller KE, Han E, Parker HG, Quignon P, Degenhardt JD, Boyko AR, Earl DA, Auton A, Reynolds A, Bryc K, Brisbin A, Knowles JC, Mosher DS, Spady TC, Elkahloun A, Geffen E, Pilot M, Jedrzejewski W, Greco C, Randi E, Bannasch D, Wilton A, Shearman J, Musiani M, Cargill M, Jones PG, Qian Z, Huang W, Ding Z-L, Zhang Y-p, Bustamante CD, Ostrander EA, Novembre J, Wayne RK (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464:898–902PubMedPubMedCentralCrossRefGoogle Scholar
  86. vonHoldt B, Pollinger J, Earl D, Parker H, Ostrander E, Wayne R (2013) Identification of recent hybridization between gray wolves and domesticated dogs by SNP genotyping. Mamm Genome 24:80–88PubMedCrossRefPubMedCentralGoogle Scholar
  87. vonHoldt BM, Cahill JA, Fan Z, Gronau I, Robinson J, Pollinger JP, Shapiro B, Wall J, Wayne RK (2016) Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf. Sci Adv 2:e1501714PubMedPubMedCentralCrossRefGoogle Scholar
  88. vonHoldt BM, Brzeski KE, Wilcove DS, Rutledge LY (2018) Redefining the role of admixture and genomics in species conservation. Conserv Lett 11:e12371CrossRefGoogle Scholar
  89. Wallach AD, Ritchie EG, Read J, O’Neill AJ (2009) More than mere numbers: the impact of lethal control on the social stability of a top-order predator. PLoS ONE 4:e6861PubMedPubMedCentralCrossRefGoogle Scholar
  90. Wayne RK, Jenks SM (1991) Mitochondrial DNA analysis implying extensive hybridization of the endangered red wolf Canis rufus. Nature 351:565–568CrossRefGoogle Scholar
  91. Wilton A (2001) DNA methods of assessing Australian dingo purity. In: Dickman CR, Lunney D (eds) A Symposium on the dingo. Royal Zoological Society of New South Wales, Sydney, pp 49–55CrossRefGoogle Scholar
  92. Wilton AN, Steward DJ, Zafiris K (1999) Microsatellite variation in the Australian dingo. J Hered 90:108–111PubMedCrossRefPubMedCentralGoogle Scholar
  93. Zhang S-j, Wang G-D, Ma P, Zhang L-l, Yin T-T, Liu Y-h, Otecko NO, Wang M, Ma Y-p, Wang L, Mao B, Savolainen P, Zhang Y-p (2018) Genomic analysis of dingoes identifies genomic regions under reversible selection during domestication and feralization. bioRxiv, 472084Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Centre for Ecosystem Science, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.Evolution & Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  3. 3.School of Environmental and Rural ScienceUniversity of New EnglandArmidaleAustralia
  4. 4.School of Life and Environmental SciencesUniversity of SydneySydneyAustralia

Personalised recommendations