Mitochondrial DNA diversity of present-day Aboriginal Australians and implications for human evolution in Oceania

Journal of Human Genetics

Volumn 62, Issue 3, 2017, Pages 343-353

  Nagle, Nano ^a   Ballantyne, Kaye N ^b,c   Van Oven, Mannis ^c   Tyler Smith, Chris ^d   Xue, Yali ^d   Wilcox, Stephen ^e   Wilcox, Leah ^a   Turkalov, Rust ^e   Van Oorschot, Roland A H ^b   Van Holst Pellekaan, Sheila ^f,g   Schurr, Theodore G ^h   McAllister, Peter ⁱ   Williams, Lesley ^j   Kayser, Manfred ^c   John Mitchell, R ^a  

^a LA TROBE UNIVERSITY   (Australia)

^b Office of the Chief Forensic Scientist   (Australia)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^e Australian Genome Research Facility Ltd   (Australia)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

^g UNIVERSITY OF SYDNEY   (Australia)

^h UNIVERSITY OF PENNSYLVANIA   (United States)

ⁱ GRIFFITH UNIVERSITY   (Australia)

^j Community Elder and Cultural Advisor ^*  (Australia)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; AUSTRALIAN ABORIGINE; EVOLUTION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; INDIGENOUS AUSTRALIAN; MAJOR CLINICAL STUDY; MITOCHONDRIAL HAPLOGROUP; PACIFIC ISLANDS; SINGLE NUCLEOTIDE POLYMORPHISM; FEMALE; GENE FLOW; GENETIC VARIATION; GENETICS; HISTORY; MALE; OCEANIC ANCESTRY GROUP; PALEONTOLOGY; PHYLOGENY; PHYLOGEOGRAPHY; REPRODUCTIVE ISOLATION;

BIOLOGICAL EVOLUTION; DNA, MITOCHONDRIAL; FEMALE; GENE FLOW; GENETIC VARIATION; HAPLOTYPES; HISTORY, 21ST CENTURY; HISTORY, ANCIENT; HUMANS; MALE; OCEANIA; OCEANIC ANCESTRY GROUP; PALEONTOLOGY; PHYLOGENY; PHYLOGEOGRAPHY; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCTIVE ISOLATION;

EID: 85014016252     PISSN: 14345161     EISSN: 1435232X     Source Type: Journal    
DOI: 10.1038/jhg.2016.147     Document Type: Article

References (98)

1. Macaulay, V., Hill, C., Achilli, A., Rengo, C., Clarke, D., Meehan, W. et al. Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308, 1034-1036 (2005).
2. Oppenheimer, S. A single southern exit of modern humans from Africa: before or after Toba? Quat. Int. 258, 88-99 (2012).
3. Stringer, C. Palaeoanthropology. Coasting out of Africa. Nature 405, 24-25 27 (2000).
4. O'Connell, J. F. & Allen, J. The process, biotic impact, and global implications of the human colonization of Sahul about 47, 000 years ago. J. Archaeol. Sci. 56, 73-84 (2015).
5. Williams, A. N. A new population curve for prehistoric Australia. Proc. Biol. Sci. 280, 20130486 (2013).
6. Hudjashov, G., Kivisild, T., Underhill, P. A., Endicott, P., Sanchez, J. J., Lin, A. A. et al. Revealing the prehistoric settlement of Australia by Y chromosome and mtDNA analysis. Proc. Natl Acad. Sci. USA 104, 8726-8730 (2007).
7. Kayser, M., Brauer, S., Weiss, G., Schiefenhovel, W., Underhill, P. A. & Stoneking, M. Independent histories of human Y chromosomes from Melanesia and Australia. Am. J. Hum. Genet. 68, 173-190 (2001).
8. Pugach, I., Delfin, F., Gunnarsdottir, E., Kayser, M. & Stoneking, M. Genome-wide data substantiate Holocene gene flow from India to Australia. Proc. Natl Acad. Sci. USA 110, 1803-1808 (2013).
9. Huxley, T. H. On the geographical distribution of the chief modifications of mankind. J. Ethnol. Soc. Lond. 2, 404-412 (1870).
10. Bellwood, P. Man's Conquest of the Pacific: The Prehistory of Southeast Asia and Oceania (Collins, Auckland, New Zealand, 1978).
11. Birdsell, J. in Sunda and Sahul: Prehistoric Studies in Southeast Asia, Melanesia and Australia (eds Allen, J., Golson, J. & Jones, R.) 113-167 (Academic Press, London, UK, 1977).
12. O'Connell, J. F. & Allen, J. The restaurant at the end of the universe: mthe colonisation of Sahul. Aust. Archaeol. 74, 5-17 (2012).
13. Malaspinas, A. S., Westaway, M. C., Muller, C., Sousa, V. C., Lao, O., Alves, I. et al. A genomic history of Aboriginal Australia. Nature 538, 207-214 (2016).
14. van Holst Pellekaan, S. Genetic evidence for the colonization of Australia. Quat. Int. 285, 44-56 (2013).
15. Rasmussen, M., Guo, X., Wang, Y., Lohmueller, K. E., Rasmussen, S., Albrechtsen, A. et al. An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334, 94-98 (2011).
16. Reich, D., Patterson, N., Kircher, M., Delfin, F., Nandineni, M. R., Pugach, I. et al. Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am. J. Hum. Genet. 89, 516-528 (2011).
17. McEvoy, B. P., Lind, J. M., Wang, E. T., Moyzis, R. K., Visscher, P. M., van Holst Pellekaan, S. M. et al. Whole-genome genetic diversity in a sample of Australians with deep Aboriginal ancestry. Am. J. Hum. Genet. 87, 297-305 (2010).
18. Vandenberg, N., van Oorschot, R. A., Tyler-Smith, C. & Mitchell, R. J. Y-chromosomespecific microsatellite variation in Australian aboriginals. Hum. Biol. 71, 915-931 (1999).
19. Redd, A. J., Roberts-Thomson, J., Karafet, T., Bamshad, M., Jorde, L. B., Naidu, J. M. et al. Gene flow from the Indian subcontinent to Australia: evidence from the Y chromosome. Curr. Biol. 12, 673-677 (2002).
20. Karafet, T. M., Mendez, F. L., Sudoyo, H., Lansing, J. S. & Hammer, M. F. Improved phylogenetic resolution and rapid diversification of Y-chromosome haplogroup K-M526 in Southeast Asia. Eur. J. Hum. Genet. 23, 369-373 (2015).
21. van Holst Pellekaan, S., Frommer, M., Sved, J. & Boettcher, B. Mitochondrial control-region sequence variation in aboriginal Australians. Am. J. Hum. Genet. 62, 435-449 (1998).
22. van Holst Pellekaan, S. M., Ingman, M., Roberts-Thomson, J. & Harding, R. M. Mitochondrial genomics identifies major haplogroups in Aboriginal Australians. Am. J. Phys. Anthropol. 131, 282-294 (2006).
23. Redd, A. J. & Stoneking, M. Peopling of Sahul: mtDNA variation in aboriginal Australian and Papua New Guinean populations. Am. J. Hum. Genet. 65, 808-828 (1999).
24. Cann, R. L., Stoneking, M. & Wilson, A. C. Mitochondrial DNA and human evolution. Nature 325, 31-36 (1987).
25. Stoneking, M., Jorde, L. B., Bhatia, K. & Wilson, A. C. Geographic variation in human mitochondrial DNA from Papua New Guinea. Genetics 124, 717-733 (1990).
26. Vigilant, L., Stoneking, M., Harpending, H., Hawkes, K. & Wilson, A. C. African populations and the evolution of human mitochondrial DNA. Science 253, 1503-1507 (1991).
27. Lum, J. K., Rickards, O., Ching, C. & Cann, R. L. Polynesian mitochondrial DNAs reveal three deep maternal lineage clusters. Hum. Biol. 66, 567-590 (1994).
28. Betty, D. J., Chin-Atkins, A. N., Croft, L., Sraml, M. & Easteal, S. Multiple independent origins of the COII/tRNA(Lys) intergenic 9-bp mtDNA deletion in aboriginal Australians. Am. J. Hum. Genet. 58, 428-433 (1996).
29. Lum, J. K. & Cann, R. L. mtDNA lineage analyses: origins and migrations of Micronesians and Polynesians. Am. J. Phys. Anthropol. 113, 151-168 (2000).
30. Tommaseo-Ponzetta, M., Attimonelli, M., De Robertis, M., Tanzariello, F. & Saccone, C. Mitochondrial DNA variability of West New Guinea populations. Am. J. Phys. Anthropol. 117, 49-67 (2002).
31. Ingman, M. & Gyllensten, U. Mitochondrial genome variation and evolutionary history of Australian and New Guinean aborigines. Genome Res. 13, 1600-1606 (2003).
32. Ingman, M., Kaessmann, H., Paabo, S. & Gyllensten, U. Mitochondrial genome variation and the origin of modern humans. Nature 408, 708-713 (2000).
33. Huoponen, K., Schurr, T. G., Chen, Y. & Wallace, D. C. Mitochondrial DNA variation in an aboriginal Australian population: evidence for genetic isolation and regional differentiation. Hum. Immunol. 62, 954-969 (2001).
34. Underhill, P. A., Passarino, G., Lin, A. A., Shen, P., Mirazon Lahr, M., Foley, R. A. et al. The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann. Hum. Genet. 65, 43-62 (2001).
35. Kivisild, T., Shen, P., Wall, D. P., Do, B., Sung, R., Davis, K. et al. The role of selection in the evolution of human mitochondrial genomes. Genetics 172, 373-387 (2006).
36. Friedlaender, J. S., Friedlaender, F. R., Hodgson, J. A., Stoltz, M., Koki, G., Horvat, G. et al. Melanesian mtDNA complexity. PLoS ONE 2, e248 (2007).
37. Taylor, D., Nagle, N., Ballantyne, K. N., van Oorschot, R. A., Wilcox, S., Henry, J. et al. An investigation of admixture in an Australian Aboriginal Y-chromosome STR database. Forensic Sci. Int. Genet. 6, 532-538 (2012).
38. Presser, J. C., Stoneking, M. & Redd, A. J. Tasmanian aborigines and DNA. Pap. Proc. R. Soc. Tasmania 136, 35-38 (2002).
39. Nagle, N., Ballantyne, K. N., van Oven, M., Tyler-Smith, C., Xue, Y., Taylor, D. et al. Antiquity and diversity of aboriginal Australian Y-chromosomes. Am. J. Phys. Anthropol. 159, 367-381 (2016).
40. Bergstrom, A., Nagle, N., Chen, Y., McCarthy, S., Pollard, M. O., Ayub, Q. et al. Deep roots for Aboriginal Australian Y chromosomes. Curr. Biol. 26, 809-813 (2016).
41. Ballantyne, K. N., van Oven, M., Ralf, A., Stoneking, M., Mitchell, R. J., van Oorschot, R. A. et al. MtDNA SNP multiplexes for efficient inference of matrilineal genetic ancestry within Oceania. Forensic Sci. Int. Genet. 6, 425-436 (2012).
42. ABS. ABoS 2011 Estimates of Aboriginal and Torres Strait Islander Australians (Australian Bureau of Statistics (ABS), Canberra, 2011).
43. van Holst Pellekaan, S. M. Origins of the Australian and New Guinean Aborigines. Encyclopedia of Life Sciences (John Wiley and Sons, Chichester, UK, 2008).
44. Behar, D. M., van Oven, M., Rosset, S., Metspalu, M., Loogvali, E. L., Silva, N. M. et al. A 'Copernican' reassessment of the human mitochondrial DNA tree from its root. Am. J. Hum. Genet. 90, 675-684 (2012).
45. Hiscock, P. The Archaeology of Ancient Australia (Routledge, Sydney, NSW, Australia, 2008).
46. Horton, D. R. Cartographer Aboriginal Australia Wall Map (Aboriginal Studies Press, Canberra, ACT, Australia, 1996).
47. Gomes, S. M., Bodner, M., Souto, L., Zimmermann, B., Huber, G., Strobl, C. et al. Human settlement history between Sunda and Sahul: A focus on East Timor (Timor-Leste) and the Pleistocenic mtDNA diversity. BMC Genomics. 16, 70 (2015).
48. de Vries, H. G., Collee, J. M., van Veldhuizen, M. H., Achterhof, L., Smit Sibinga, C. T., Scheffer, H. et al. Validation of the determination of deltaF508 mutations of the cystic fibrosis gene in over 11 000 mouthwashes. Hum. Genet. 97, 334-336 (1996).
49. Andrews, R. M., Kubacka, I., Chinnery, P. F., Lightowlers, R. N., Turnbull, D. M. & Howell, N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat. Genet. 23, 147 (1999).
50. Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H., Coulson, A. R., Drouin, J. et al. Sequence and organization of the human mitochondrial genome. Nature 290, 457-465 (1981).
51. Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729 (2013).
52. Kloss-Brandstatter, A., Pacher, D., Schonherr, S., Weissensteiner, H., Binna, R., Specht, G. et al. HaploGrep: A fast and reliable algorithm for automatic classification of mitochondrial DNA haplogroups. Hum. Mutat. 32, 25-32 (2011).
53. van Oven, M. & Kayser, M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum. Mutat. 30, E386-E394 (2009).
54. Bandelt, H. J., Forster, P. & Röhl, A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16, 37-48 (1999).
55. Excoffier, L. & Lischer, H. E. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564-567 (2010).
56. Nei, M. Molecular Evolutionary Genetics (Columbia Univ. Press, New York, NY, USA, 1987).
57. IBM. SPSS v.21.0 for Windows (IBM, Chicago IL, 2012).
58. Hill, C., Soares, P., Mormina, M., Macaulay, V., Clarke, D., Blumbach, P. B. et al. A mitochondrial stratigraphy for island southeast Asia. Am. J. Hum. Genet. 80, 29-43 (2007).
59. van Oven, M., Brauer, S., Choi, Y., Ensing, J., Schiefenhovel, W., Stoneking, M. et al. Human genetics of the Kula Ring: Y-chromosome and mitochondrial DNA variation in the Massim of Papua New Guinea. Eur. J. Hum. Genet. 22, 1393-1403 (2014).
60. Chen, Y.-S., Olckers, A., Schurr, T. G., Kogelnik, A. M., Huoponen, K. & Wallace, D. C. mtDNA variation in the South African Kung and Khwe and their genetic relationships to other African populations. Am. J. Hum. Genet. 66, 1362-1383 (2000).
61. Helgason, A., Hickey, E., Goodacre, S., Bosnes, V., Stefansson, K., Ward, R. et al. mtDNA and the islands of the North Atlantic: estimating the proportions of Norse and Gaelic ancestry. Am. J. Hum. Genet. 68, 723-737 (2001).
62. Forster, P., Harding, R., Torroni, A. & Bandelt, H. J. Origin and evolution of Native American mtDNA variation: A reappraisal. Am. J. Hum. Genet. 59, 935-945 (1996).
63. Soares, P., Ermini, L., Thomson, N., Mormina, M., Rito, T., Rohl, A. et al. Correcting for purifying selection: An improved human mitochondrial molecular clock. Am. J. Hum. Genet. 84, 740-759 (2009).
64. Merriwether, D. A., Hodgson, J. A., Friedlaender, F. R., Allaby, R., Cerchio, S., Koki, G. et al. Ancient mitochondrial M haplogroups identified in the Southwest Pacific. Proc. Natl Acad. Sci. USA 102, 13034-13039 (2005).
65. Pierson, M. J., Martinez-Arias, R., Holland, B. R., Gemmell, N. J., Hurles, M. E. & Penny, D. Deciphering past human population movements in Oceania: provably optimal trees of 127 mtDNA genomes. Mol. Biol. Evol. 23, 1966-1975 (2006).
66. Tennant-Kelly, C. Tribes on Cherbourg settlement, Queensland. Oceania 5, 461-473 (1935).
67. Radcliffe-Brown, A. R. Former numbers and distribution of Australian Aborigines. Off. Yearbook 23, 687-696 (1930).
68. Mishmar, D., Ruiz-Pesini, E., Golik, P., Macaulay, V., Clark, A. G., Hosseini, S. et al. Natural selection shaped regional mtDNA variation in humans. Proc. Natl Acad. Sci. USA 100, 171-176 (2003).
69. Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586-1591 (2007).
70. Fu, Q., Mittnik, A., Johnson, P. L., Bos, K., Lari, M., Bollongino, R. et al. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr. Biol. 23, 553-559 (2013).
71. Barker, G., Barton, H., Bird, M., Daly, P., Datan, I., Dykes, A. et al. The 'human revolution' in lowland tropical Southeast Asia: The antiquity and behavior of anatomically modern humans at Niah Cave (Sarawak, Borneo). J. Hum. Evol. 52, 243-261 (2007).
72. Demeter, F., Shackelford, L. L., Bacon, A. M., Duringer, P., Westaway, K., Sayavongkhamdy, T. et al. Anatomically modern human in Southeast Asia (Laos) by 46 ka. Proc. Natl Acad. Sci. USA 109, 14375-14380 (2012).
73. Kayser, M., Choi, Y., van Oven, M., Mona, S., Brauer, S., Trent, R. J. et al. The impact of the Austronesian expansion: evidence from mtDNA and Y chromosome diversity in the Admiralty Islands of Melanesia. Mol. Biol .Evol. 25, 1362-1374 (2008).
74. Chandrasekar, A., Kumar, S., Sreenath, J., Sarkar, B. N., Urade, B. P., Mallick, S. et al. Updating phylogeny of mitochondrial DNA macrohaplogroup m in India: dispersal of modern human in South Asian corridor. PLoS ONE 4, e7447 (2009).
75. Kumar, S., Ravuri, R. R., Koneru, P., Urade, B. P., Sarkar, B. N., Chandrasekar, A. et al. Reconstructing Indian-Australian phylogenetic link. BMC Evol. Biol. 9, 173 (2009).
76. Greer, S., Henry, R. & McIntyre-Tamwoy, S. Mainland magic: interpreting cultural influences across Cape York-Torres Strait. Quat. Int. 385, 69-78 (2015).
77. Tabbada, K. A., Trejaut, J., Loo, J. H., Chen, Y. M., Lin, M., Mirazon-Lahr, M. et al. Philippine mitochondrial DNA diversity: A populated viaduct between Taiwan and Indonesia? Mol. Biol. Evol. 27, 21-31 (2010).
78. Jones, R. Tasmanian archeology: establishing the sequences. Annu. Rev. Anthropol. 24, 423-446 (1995).
79. Delfin, F., Min-Shan Ko, A., Li, M., Gunnarsdottir, E. D., Tabbada, K. A., Salvador, J. M. et al. Complete mtDNA genomes of Filipino ethnolinguistic groups: A melting pot of recent and ancient lineages in the Asia-Pacific region. Eur. J. Hum. Genet. 22, 228-237 (2014).
80. Heyer, E., Georges, M., Pachner, M. & Endicott, P. Genetic diversity of four Filipino Negrito populations from Luzon: comparison of male and female effective population sizes and differential integration of immigrants into Aeta and Agta communities. Hum. Biol. 85, 189-208 (2013).
81. Friedlaender, J., Schurr, T., Gentz, F., Koki, G., Friedlaender, F., Horvat, G. et al. Expanding Southwest Pacific mitochondrial haplogroups P and Q. Mol. Biol. Evol. 22, 1506-1517 (2005).
82. Chappell, J. Sea level changes forced ice breakouts in the Last Glacial cycle: new results from coral terraces. Q. Sci. Rev. 21, 1229-1240 (2002).
83. Lambeck, K. & Chappell, J. Sea level change through the last glacial cycle. Science 292, 679-686 (2001).
84. Kayser, M., Brauer, S., Weiss, G., Schiefenhövel, W., Underhill, P., Shen, P. et al. Reduced Y-chromosome, but not mitochondrial DNA, diversity in human populations from West New Guinea. Am. J. .Genet. 72, 281-302 (2003).
85. Glover, I. C. & Presland, G. in Recent Advances in Indo-Pacific Prehistory (eds Misra, V. N. & Bellwood, P.) 185-195 (Oxford and IBH, New Delhi, India, 1985) .
86. Gollan, K. in Recent Advances in Indo-Pacific Prehistory (eds Misra, V. N. & Bellwoood, P.) 439-443 (Oxford and IBH, New Delhi, India, 1985) .
87. Dixon, R. M. W. The Languages of Australia (Cambridge University Press, New York, NY, 1980).
88. Brown, P. Palaeoanthropology: of humans, dogs and tiny tools. Nature 494, 316-317 (2013).
89. Reesink, G., Singer, R. & Dunn, M. Explaining the linguistic diversity of Sahul using population models. PLoS Biol. 7, e1000241 (2009).
90. Ardalan, A., Oskarsson, M., Natanaelsson, C., Wilton, A. N., Ahmadian, A. & Savolainen, P. Narrow genetic basis for the Australian dingo confirmed through analysis of paternal ancestry. Genetica 140, 65-73 (2012).
91. Crowther, M. S., Fillios, M., Colman, N. & Letnic, M. An updated description of the Australian dingo (Canis dingo Meyer, 1793). J. Zool. 293, 192-203 (2014).
92. Fillios, M. A. & Taçon, P. S. C. 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. 7, 782-792 (2016).
93. Oskarsson, M. C., Klutsch, C. F., Boonyaprakob, U., Wilton, A., Tanabe, Y. & Savolainen, P. Mitochondrial DNA data indicate an introduction through Mainland Southeast Asia for Australian dingoes and Polynesian domestic dogs. Proc. Biol. Sci. 279, 967-974 (2012).
94. Savolainen, P., Leitner, T., Wilton, A. N., Matisoo-Smith, E. & Lundeberg, J. A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA. Proc. Natl Acad. Sci. USA 101, 12387-12390 (2004).
95. Smith, B. P. & Litchfield, C. A. A review of the relationship between Indigenous Australians, Dingoes (Canis dingo) and domestic dogs (Canis familiaris). Anthrozoos 22, 111-128 (2009).
96. Milham, P. & Thompson, P. Relative antiquity of human occupation and extinct fauna at Madura Cave, southeastern Western Australia. Mankind 10, 175-180 (1976).
97. McBryde, I. Coast and Estuary: Archaeological Investigations on the North Coast of New South Wales at Wombah and Schnapper Point (Australian Institute of Aboriginal Studies, Canberra, 1982).
98. Mulvaney, D., Lawton, G., Twidaie, C., Macintosh, N., Mahoney, J. & Wakefield, N. Archaeological excavation of rock shelter no. 6 Fromm's Landing, South Australia. Proc. R. Soc. Vic. 77, 479-516 (1964).