Genetica

, Volume 144, Issue 5, pp 553–565 | Cite as

New insights on the history of canids in Oceania based on mitochondrial and nuclear data

Article

Abstract

How and when dingoes arrived in Oceania poses a fascinating question for scientists with interest in the historical movements of humans and dogs. The dingo holds a unique position as top terrestrial predator of Australia and exists in a wild state. In the first geographical survey of genetic diversity in the dingo using whole mitochondrial genomes, we analysed 16,428 bp in 25 individuals from five separate populations. We also investigated 13 nuclear loci to compare with the mitochondrial population history patterns. Phylogenetic analyses based upon mitochondrial DNA and nuclear DNA support the hypothesis that there are at least two distinct populations of dingo, one of which occurs in the northwest and the other in the southeast of the continent. Conservative molecular dating based upon mitochondrial DNA suggest that the lineages split approximately 8300 years before present, likely outside Australia but within Oceania. The close relationship between dingoes and New Guinea Singing Dogs suggests that plausibly dingoes spread into Australia via the land bridge between Papua New Guinea and Australia although seafaring introductions cannot be rejected. The geographical distribution of these divergent lineages suggests there were multiple independent dingo immigrations. Importantly, the observation of multiple dingo populations suggests the need for revision of existing conservation and management programs that treat dingoes as a single homogeneous population.

Keywords

Australia Dingo Divergence estimates Mitochondrial DNA Neolithic Nuclear DNA Phylogeography Population genetics 

Supplementary material

10709_2016_9924_MOESM1_ESM.pdf (149 kb)
Supplementary material 1 (PDF 148 kb)
10709_2016_9924_MOESM2_ESM.docx (81 kb)
Supplementary material 2 (DOCX 80 kb)
10709_2016_9924_MOESM3_ESM.xlsx (45 kb)
Supplementary material 3 (XLSX 44 kb)

References

  1. Anderson TM et al (2009) Molecular and evolutionary history of melanism in North American gray wolves. Science 323:1339–1343. doi:10.1126/science.1165448 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ardalan A, Oskarsson M, Natanaelsson C, Wilton A, Ahmadian A, Savolainen P (2012) Narrow genetic basis for the Australian dingo confirmed through analysis of paternal ancestry. Genetica 140:65–73. doi:10.1007/s10709-012-9658-5 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arendt M, Cairns KM, Ballard JWO, Savolainen P, Axelsson E (2016) Diet adaptation in dog reflects spread of prehistoric agriculture. Heredity. doi:10.1038/hdy.2016.48 PubMedGoogle Scholar
  4. Bocquet-Appel J-P (2011) When the world’s population took off: the springboard of the neolithic demographic transition. Science 333:560–561. doi:10.1126/science.1208880 CrossRefPubMedGoogle Scholar
  5. Brown RP, Yang Z (2011) Rate variation and estimation of divergence times using strict and relaxed clocks. BMC Evol Biol 11:271CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cairns KM (2015) Population differentiation in the dingo: biogeography and molecular ecology of the Australian Native Dog using maternal, paternal and autosomal genetic markers. University of New South Wales, SydneyGoogle Scholar
  7. Carmichael LE, Nagy JA, Larter NC, Strobeck C (2001) Prey specialization may influence patterns of gene flow in wolves of the Canadian Northwest. Mol Ecol 10:2787–2798. doi:10.1046/j.0962-1083.2001.01408.x CrossRefPubMedGoogle Scholar
  8. Carthey AJR, Banks PB (2012) When does an alien become a native species? A vulnerable native mammal recognizes and responds to its long-term alien predator. PLoS ONE 7:e31804. doi:10.1371/journal.pone.0031804 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Corbett LK (1995) The dingo in Australia and Asia. University of NSW Press, SydneyGoogle Scholar
  10. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. http://www.nature.com/nmeth/journal/v9/n8/abs/nmeth.2109.html—supplementary-information
  11. David B et al (2013) A 28,000 year old excavated painted rock from Nawarla Gabarnmang, northern Australia. J Archaeol Sci 40:2493–2501. doi:10.1016/j.jas.2012.08.015 CrossRefGoogle Scholar
  12. Davis E (2001) Legislative issues relating to control of dingoes and other wild dogs in New South Wales. 1. Approaches to future management. In: Dickman CR, Lunney D (eds) A symposium on the Dingo. Royal Zoological Society of New South Wales, SydneyGoogle Scholar
  13. Diamond J (2002) Evolution, consequences and future of plant and animal domestication. Nature 418:700–707CrossRefPubMedGoogle Scholar
  14. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol. doi:10.1093/molbev/mss075 Google Scholar
  15. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. doi:10.1111/j.1365-294X.2005.02553.x CrossRefPubMedGoogle Scholar
  16. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows Mol. Ecol Res 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x CrossRefGoogle Scholar
  17. Fillios MA, Taçon PSC (2016) Who let the dogs in? A review of the recent genetic evidence for the introduction of the dingo to Australia and implications for the movement of people. J Archaeol Sci Rep. doi:10.1016/j.jasrep.2016.03.001 Google Scholar
  18. Fleming P, Corbett LK, Harden R, Thomson P (2001) Managing the impacts of dingoes and other wild dogs. Bureau of Rural Sciences, CanberraGoogle Scholar
  19. Frantz LAF et al (2016) Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science 352:1228–1231. doi:10.1126/science.aaf3161 CrossRefPubMedGoogle Scholar
  20. Freedman AH et al (2014) Genome sequencing highlights the dynamic early history of dogs. PLoS Genet 10:e1004016. doi:10.1371/journal.pgen.1004016 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Fu YX (1997) Statistical tests of neutrality of mutations against population growth. Hitchhiking Backgr Sel Genet 147:915–925Google Scholar
  22. Gibbons A (2001) The peopling of the Pacific. Science 291:1735–1737. doi:10.1126/science.291.5509.1735 CrossRefPubMedGoogle Scholar
  23. Gollan K (1984) The Australian dingo: in the shadow of man. In: Archer M, Clayton G (eds) Vertebrate zoogeography and evolution in Australasia. Hesperian Press, CarlisleGoogle Scholar
  24. Haak W et al (2010) Ancient DNA from european early neolithic farmers reveals their near eastern affinities. PLoS Biol 8:e1000536. doi:10.1371/journal.pbio.1000536 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ho SYW, Lanfear R, Bromham L, Phillips MJ, Soubrier J, Rodrigo AG, Cooper A (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101. doi:10.1111/j.1365-294X.2011.05178.x CrossRefPubMedGoogle Scholar
  26. Ho SYW, Larson G (2006) Molecular clocks: when times are a-changin’. Trends Genet 22:79–83CrossRefPubMedGoogle Scholar
  27. van Holst Pellekaan S (2013) Genetic evidence for the colonization of Australia. Quat Int 285:44–56. doi:10.1016/j.quaint.2011.04.014 CrossRefGoogle Scholar
  28. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332. doi:10.1111/j.1755-0998.2009.02591.x CrossRefGoogle Scholar
  29. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefPubMedGoogle Scholar
  30. Karafet TM et al (2005) Balinese Y-chromosome perspective on the peopling of Indonesia: genetic contributions from pre-neolithic hunter–gatherers, Austronesian farmers, and Indian traders. Hum Biol 77:93–114CrossRefPubMedGoogle Scholar
  31. Kennedy LJ, Angles JM, Barnes A, Carmichael LE, Radford AD, Ollier WER, Happ GM (2007) DLA-DRB1, DQA1, and DQB1 alleles and haplotypes in North American gray wolves. J Hered 98:491–499. doi:10.1093/jhered/esm051 CrossRefPubMedGoogle Scholar
  32. Kidwell SM, Flessa KW (1996) The quality of the fossil record: populations, species, and communities. Annu Rev Earth Planet Sci 24:433–464. doi:10.1146/annurev.earth.24.1.433 CrossRefGoogle Scholar
  33. Kingman JFC (1982) The coalescent. Stoch Proc Appl 13:235–248. doi:10.1016/0304-4149(82)90011-4 CrossRefGoogle Scholar
  34. Koler-Matznick J, Brisbin IL, Feinstein M, Bulmer S (2004) An updated description of the New Guinea singing dog (Canis hallstromi, Troughton 1957). J Zool 261:109–118. doi:10.1017/S0952836903004060 CrossRefGoogle Scholar
  35. Larson G et al (2007) Phylogeny and ancient DNA of Sus provides insights into neolithic expansion in Island Southeast Asia and Oceania. PNAS 104:4834–4839. doi:10.1073/pnas.0607753104 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Larson G et al (2010) Patterns of East Asian pig domestication, migration, and turnover revealed by modern and ancient DNA. PNAS 107:7686–7691. doi:10.1073/pnas.0912264107 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Letnic M, Greenville A, Denny E, Dickman CR, Tischler M, Gordon C, Koch F (2010) Does a top predator suppress the abundance of an invasive mesopredator at a continental scale? Global Ecol Biogeogr 20:343–353CrossRefGoogle Scholar
  38. Letnic M, Ritchie EG, Dickman CR (2012) Top predators as biodiversity regulators: the dingo Canis lupus dingo as a case study. Biol Rev 87:390–413. doi:10.1111/j.1469-185X.2011.00203.x CrossRefPubMedGoogle Scholar
  39. Librado P, Rozas J (2009) DNAsp v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  40. Macintosh NWG (1975) The origin of the dingo: an enigma. In: Fox MW (ed) The Wild Canids—their systematics, behavioural ecology and evolution. Behavioral Science. Van Nostrand Reinhold Company, New York, pp 87–106Google Scholar
  41. McEvoy BP, Lind JM, Wang ET, Moyzis RK, Visscher PM, van Holst Pellekaan SM, Wilton AN (2010) Whole-genome genetic diversity in a sample of Australians with deep aboriginal ancestry. Am J Hum Genet 87:297–305. doi:10.1016/j.ajhg.2010.07.008 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Milham P, Thompson P (1976) Relative antiquity of human occupation and extinct fauna at madura cave. Southeastern Western Australia Mankind 10:175–180. doi:10.1111/j.1835-9310.1976.tb01149.x Google Scholar
  43. Moseby KE, Neilly H, Read JL, Crisp HA (2012) Interactions between a top order predator and exotic mesopredators in the Australian rangelands. Int J Ecol. doi:10.1155/2012/250352 Google Scholar
  44. Musiani M et al (2007) Differentiation of tundra/taiga and boreal coniferous forest wolves, coat color and association with migratory caribou. Mol Ecol 16:4149CrossRefPubMedGoogle Scholar
  45. 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. doi:10.1098/rspb.2011.1395 PubMedPubMedCentralGoogle Scholar
  46. Pang J-F et al (2009) mtDNA data indicate a single origin for dogs south of Yangtze river, less than 16,300 years ago, from numerous wolves. Mol Biol Evol 26:2849–2864CrossRefPubMedPubMedCentralGoogle Scholar
  47. Rambaut A, Drummond A (2007) Tracer v1.5 edn. http://beast.bio.ed.ac.uk/Tracer
  48. Randall D, Pollinger J, Argaw K, Macdonald D, Wayne R (2010) Fine-scale genetic structure in Ethiopian wolves imposed by sociality, migration, and population bottlenecks. Cons Gen 11:89–101. doi:10.1007/s10592-009-0005-z CrossRefGoogle Scholar
  49. Ripple WJ et al (2014) Status and ecological effects of the world’s largest carnivores. Science 343. doi:10.1126/science.1241484
  50. Robin S et al (2009) Genetic diversity of canine olfactory receptors. BMC Genom. doi:10.1186/1471-2164-10-21 Google Scholar
  51. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  52. Sacks BN, Brown SK, Ernest HB (2004) Population structure of California coyotes corresponds to habitat-specific breaks and illuminates species history. Mol Ecol 13:1265–1275. doi:10.1111/j.1365-294X.2004.02110.x CrossRefPubMedGoogle Scholar
  53. 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 13:1265–1275. doi:10.1093/molbev/mst027 Google Scholar
  54. Savolainen P, Leitner T, Wilton AN, Matisoo-Smith E, Lundeberg J (2004) A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. PNAS 101:12387–12390CrossRefPubMedPubMedCentralGoogle Scholar
  55. Shannon LM et al (2015) Genetic structure in village dogs reveals a Central Asian domestication origin. PNAS 112:13639–13644. doi:10.1073/pnas.1516215112 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Skoglund P, Ersmark E, Palkopoulou E, Dalén L (2015) Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Curr Biol 25:1515–1519. doi:10.1016/j.cub.2015.04.019 CrossRefPubMedGoogle Scholar
  57. Stenseth NC et al (2004) Snow conditions may create an invisible barrier for lynx. PNAS 101:10632–10634CrossRefPubMedPubMedCentralGoogle Scholar
  58. Stephens D (2011) The molecular ecology of Australian wild dogs: hybridisation, gene flow and genetic structure at multiple geographic scales. PhD, University of Western AustraliaGoogle Scholar
  59. Tacher S, Quignon P, Rimbault M, Dreano S, Andre C, Galibert F (2005) Olfactory receptor sequence polymorphism within and between breeds of dogs. J Hered 96:812–816. doi:10.1093/jhered/esi113 CrossRefPubMedGoogle Scholar
  60. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  61. Tappen M (1994) Bone weathering in the tropical rain forest. J Archaeol Sci 21:667–673. doi:10.1006/jasc.1994.1066 CrossRefGoogle Scholar
  62. Thalmann O et al (2013) Complete mitochondrial genomes of ancient Canids suggest a European origin of domestic dogs. Science 342:871–874. doi:10.1126/science.1243650 CrossRefPubMedGoogle Scholar
  63. Thomson P, Rose K, Kok N (1992) The behavioural ecology of dingoes in north-western Australia. VI. Temporary extraterritorial movements and dispersal. Wildl Res 19:585–595. doi:10.1071/WR9920585 CrossRefGoogle Scholar
  64. Von Holdt BM et al (2010) Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464:898–902. doi:http://www.nature.com/nature/journal/vaop/ncurrent/suppinfo/nature08837_S1.html
  65. Wallach AD, Johnson CN, Ritchie EG, O’Neill AJ (2010) Predator control promotes invasive dominated ecological states. Ecol Lett 13:1008–1018. doi:10.1111/j.1461-0248.2010.01492.x PubMedGoogle Scholar
  66. Wang G et al (2013) The genomics of selection in dogs and the parallel evolution between dogs and humans. Nat Commun 4:1860. doi:10.1038/ncomms2814 CrossRefPubMedGoogle Scholar
  67. Wang G-D et al (2016) Out of southern East Asia: the natural history of domestic dogs across the world. Cell Res 26:21–33. doi:10.1038/cr.2015.147 CrossRefPubMedGoogle Scholar
  68. Wilton A (2001) DNA methods of assessing australian dingo purity. In: Dickman CR, Lunney D (eds) A Symposium on the Australian dingo. Royal Zoological Society of New South Wales, Sydney, pp 49–55CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.School of Biotechnology and Biomolecular SciencesUniversity of New South WalesSydneyAustralia

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