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Using Ancient DNA to Study the Origins and Dispersal of Ancestral Polynesian Chickens Across the Pacific

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Using Ancient DNA to Study the Origins and Dispersal of Ancestral Polynesian Chickens Across the Pacific Using ancient DNA to study the origins and dispersal of ancestral Polynesian chickens across the Pacific Vicki A. Thomsona, Ophélie Lebrasseurb, Jeremy J. Austina,c,1, Terry L. Huntd,e, David A. Burneyf, Tim Denhamg, Nicolas J. Rawlencea,h, Jamie R. Woodi, Jaime Gongoraj, Linus Girdland Flinkb,k, Anna Linderholmb, Keith Dobneyl, Greger Larsonb, and Alan Coopera,1 aAustralian Centre for Ancient DNA, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, SA 5005, Australia; bDurham Evolution and Ancient DNA, Department of Archaeology, and kSchool of Biological and Biomedical Sciences, Durham University, Durham DH1 3LE, United Kingdom; cSciences Department, Museum Victoria, Melbourne, VIC 3001, Australia; dClark Honors College and eDepartment of Anthropology, University of Oregon, Eugene, OR 97403; fNational Tropical Botanical Garden, Kalaheo, HI 96741; gSchool of Archaeology and Anthropology, ANU College of Arts and Social Sciences, The Australian National University, Canberra, ACT 0200, Australia; hAllan Wilson Centre for Molecular Ecology and Evolution, Department of Zoology, University of Otago, Dunedin 9016, New Zealand; iLandcare Research, Lincoln 7640, New Zealand; jFaculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia; and lDepartment of Archaeology, University of Aberdeen, Aberdeen AB24 3UF, Scotland Edited by David J. Meltzer, Southern Methodist University, Dallas, TX, and approved February 20, 2014 (received for review October 31, 2013) The human colonization of Remote Oceania remains one of the resolved, the precise details of this intensive migratory episode great feats of exploration in history, proceeding east from Asia remain unclear (6). across the vast expanse of the Pacific Ocean. Human commensal Human commensal and early domesticated species were wide- and domesticated species were widely transported as part of this ly, but not ubiquitously, dispersed as people colonized the Pacific. diaspora, possibly as far as South America. We sequenced mito- As a result, they provide an opportunity to study colonization chondrial control region DNA from 122 modern and 22 ancient events and subsequent movements for islands and regions where chicken specimens from Polynesia and Island Southeast Asia and they were successfully introduced, especially through the use of – used these together with Bayesian modeling methods to examine biomolecular techniques, including ancient DNA. In the Asia the human dispersal of chickens across this area. We show that Pacific region, the complex histories of Pacific island colo- specific techniques are essential to remove contaminating modern nizations have been investigated using the biological elements DNA from experiments, which appear to have impacted previous associated with these cultures, such as bottle gourds (7, 8), ANTHROPOLOGY sweet potatoes (9), pigs (10, 11), dogs (12), Pacific rats (13), studies of Pacific chickens. In contrast to previous reports, we find and chickens (14–17). However, studies of commensals and that all ancient specimens and a high proportion of the modern domesticates in the Pacific to date have provided limited res- chickens possess a group of unique, closely related haplotypes olution of dispersal routes, due to low amounts of genetic di- found only in the Pacific. This group of haplotypes appears to versity in many groups and overwriting of genetic signals by represent the authentic founding mitochondrial DNA chicken subsequent introductions, especially for cotransported species lineages transported across the Pacific, and allows the early like rats (10, 13, 18). dispersal of chickens across Micronesia and Polynesia to be Ancient and modern DNA from chickens provide an oppor- modeled. Importantly, chickens carrying this genetic signature tunity to study human-mediated dispersal across the Pacific due persist on several Pacific islands at high frequencies, suggesting to the extent of genetic and phenotypic diversity and the range of that the original Polynesian chicken lineages may still survive. archaeological material available. Although recent studies of No early South American chicken samples have been detected with the diagnostic Polynesian mtDNA haplotypes, arguing Significance against reports that chickens provide evidence of Polynesian contact with pre-European South America. Two modern speci- Ancient DNA sequences from chickens provide an opportunity mens from the Philippines carry haplotypes similar to the ancient to study their human-mediated dispersal across the Pacific due Pacific samples, providing clues about a potential homeland for to the significant genetic diversity and range of archaeological the Polynesian chicken. material available. We analyze ancient and modern material and reveal that previous studies have been impacted by con- Lapita | Pacific colonization | phylogeography | archaeology | migration tamination with modern chicken DNA and, that as a result, there is no evidence for Polynesian dispersal of chickens to pre- he colonization of the remote Pacific was one of the last great Columbian South America. We identify genetic markers of Thuman migrations, but despite the recent nature of the events, authentic ancient Polynesian chickens and use them to model the timing and routes remain an area of considerable debate. The early chicken dispersals across the Pacific. We find connections first colonization of Western Polynesia occurred around 3,250– between chickens in the Micronesian and Bismarck Islands, but 3,100 calendar years before present (cal B.P.) as part of the no evidence these were involved in dispersals further east. We eastward migration of Lapita pottery-bearing peoples (1). This also find clues about the origins of Polynesian chickens in migration occurred only a few hundred years after the emergence the Philippines. of this distinctive pottery tradition in the Bismarck Archipelago around 3,470–3,250 cal B.P., although its antecedents can be Author contributions: V.A.T., J.J.A., J.G., and A.C. designed research; V.A.T., O.L., N.J.R., traced to Island Southeast Asia (ISEA) (2–5). Following the initial J.R.W., L.G.F., and A.L. performed research; T.L.H., D.A.B., and K.D. contributed new reagents/analytic tools; V.A.T., J.J.A., and A.C. analyzed data; and V.A.T., J.J.A., T.D., G.L., movement into Western Polynesia, a prolonged 1,800-y hiatus, or and A.C. wrote the paper. “ ” pause, is apparent before further colonization (6), potentially The authors declare no conflict of interest. relating to the need to develop sailing technology essential for This article is a PNAS Direct Submission. crossing the vast ocean barrier to the east (between Samoa and Data deposition: The sequences reported in this paper have been deposited in the the Society Islands, 2,400 km; Fig. 1). The huge navigational GenBank database (accession nos. KJ000585–KJ000642). achievement of colonizing the remote East Polynesian triangle (an 1To whom correspondence may be addressed. E-mail: [email protected] or oceanic region roughly the size of North America) then occurred [email protected]. < rapidly ( 300 y) (6). Although the overall chronology of the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. eastern Pacific island colonization has recently been further 1073/pnas.1320412111/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1320412111 PNAS Early Edition | 1of6 Downloaded by guest on September 26, 2021 140o E 180o E 140o W 100o W 40o N 40o N Legend Haplogroup D Fig. 1. Map showing samples and localities mentioned in this Haplogroup E Near Remote Other haplogroups study. Samples from Vanuatu and Guam previously published Oceania Oceania 7 17 in Dancause et al. (26) are underlined, with haplogroup fre- 20o N 3500- Hawaii 20o N Philippines 4000BP(9) n=5 quencies of the chicken specimens indicated by pie charts (thick 23 Guam 2B outlines indicate ancient samples). Colors refer to haplotype/ 2A LCC 3450-3550BP(8) haplogroup: D haplogroup in red, E haplogroup in blue, and all 3 0 o o 1 5 0 other haplotypes are in black. Gray arrows represent move- North 1 9 Maluku Solomon Is. 28 ments inferred from archaeological data (49), whereas black Papua 12 Marquesas Papua Santa Cruz arrows represent routes tested in BayeSSC analysis (dashed 5 New Islands 31 4 6 arrows indicate movements tested in different scenarios, 20o S Guinea Vanuatu 20o S Society Is. 43 Niue 2 whereas solid arrows are constant across the different scenar- Western French Polynesia 7 Polynesia Tuamotos Gambier Is. Rapa Nui ios). 1, introduction of chickens within Near Oceania; 2, alter- 13 nate hypothesis proposed by (38); 3, introduction of chickens Eastern o o – 40 S Polynesia 40 S from New Guinea into Micronesia; 4 7, spread of chickens from Western Polynesia into, and within, Eastern Polynesia. Dashed line indicates demarcation between Near and Remote Oceania, 0 1,250 2,500 5,000 Kilometers Western Polynesia is defined by a dashed circle, and Eastern 140o E 180o E 140o W 100o W Polynesia is indicated by a gray shaded triangle. domestic chicken breeds have highlighted how the domestication Results process and subsequent breeding have resulted in a 70% loss The 61 WMG dataset (25) contained 363 single-nucleotide of nuclear genetic diversity (19), substantial phylogeographic polymorphisms (SNPs), of which 154 were potentially phyloge- structure remains within the mitochondrial (mtDNA) sequences netically informative, with 62 (17%) located in the rapidly of chickens worldwide
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