A Holistic Picture of Austronesian Migrations Revealed by Phylogeography of Pacific Paper Mulberry

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A Holistic Picture of Austronesian Migrations Revealed by Phylogeography of Pacific Paper Mulberry A holistic picture of Austronesian migrations revealed by phylogeography of Pacific paper mulberry Chi-Shan Chang (張至善)a,1, Hsiao-Lei Liu (劉筱蕾)b,1, Ximena Moncadac, Andrea Seelenfreundd, Daniela Seelenfreunde, and Kuo-Fang Chung (鍾國芳)b,2 aDepartment of Natural Resources and Environmental Studies, National Dong Hwa University, Shoufeng, Hualien 97401, Taiwan; bSchool of Forestry and Resource Conservation, National Taiwan University, Taipei 10617, Taiwan; cCentro de Estudios de Zonas Áridas (CEAZA), La Serena 1720170, Chile; dEscuela de Antropología, Facultad de Ciencias Sociales, Universidad Academia de Humanismo Cristiano, Santiago 7500828, Chile; and eDepartment of Biochemistry and Molecular Biology, Facultad de Ciencias Químicas y Farmacéuticas, Universidad de Chile, Santiago 8380494, Chile Edited by Patrick V. Kirch, University of California, Berkeley, CA, and approved September 10, 2015 (received for review February 15, 2015) The peopling of Remote Oceanic islands by Austronesian speakers Near Oceanic cultures had resulted in the “Innovation” of the Lapita is a fascinating and yet contentiouspartofhumanprehistory. cultural complex (2, 13). Linguistic, archaeological, and genetic studies have shown the Human migration entails complex skills of organization and complex nature of the process in which different components that cultural adaptations of migrants or colonizing groups (1, 3). Suc- helped to shape Lapita culture in Near Oceania each have their own cessful colonization to resource-poor islands in Remote Oceania unique history. Important evidence points to Taiwan as an Austro- involved conscious transport of a number of plant and animal nesian ancestral homeland with a more distant origin in South China, species critical for both the physical survival of the settlers and whereas alternative models favor South China to North Vietnam their cultural transmission (14). In the process of Austronesian or a Southeast Asian origin. We test these propositions by studying expansion into Oceania, a number of animals (e.g., chicken, pigs, phylogeography of paper mulberry, a common East Asian tree rats, and dogs) and plant species (e.g., bananas, breadfruit, taro, species introduced and clonally propagated since prehistoric times yam, paper mulberry, etc.), either domesticated or managed, were across the Pacific for making barkcloth, a practical and symbolic introduced over time from different source regions (3, 8, 15). component of Austronesian cultures. Using the hypervariable chlo- Although each of these species has been shown to have a different “ ” roplast ndhF-rpl32 sequences of 604 samples collected from East history (8), all these commensal species were totally dependent ANTHROPOLOGY Asia, Southeast Asia, and Oceanic islands (including 19 historical her- upon humans for dispersal across major water gaps (6, 8, 16). The barium specimens from Near and Remote Oceania), 48 haplotypes continued presence of these species as living populations far are detected and haplotype cp-17 is predominant in both Near and outside their native ranges represents legacies of the highly skilled Remote Oceania. Because cp-17 has an unambiguous Taiwanese seafaring and navigational abilities of the Austronesian voyagers. origin and cp-17–carrying Oceanic paper mulberries are clonally Given their close association to and dependence on humans propagated, our data concur with expectations of Taiwan as the for their dispersal, phylogeographic analyses of these commensal Austronesian homeland, providing circumstantial support for the species provide unique insights into the complexities of Austro- nesian expansion and migrations (6, 8, 17). This “commensal “outofTaiwan” hypothesis. Our data also provide insights into the dispersal of paper mulberry from South China “into North Taiwan,” the “out of South China–Indochina” expansion to New Significance Guinea, and the geographic origins of post-European introductions of paper mulberry into Oceania. Paper mulberry, a common East Asian tree used for paper making, is propagated across the Pacific for making barkcloth, Broussonetia papyrifera | commensal approach | a practical and symbolic component of Austronesian material DNA of herbarium specimens | out of Taiwan hypothesis | culture. Using chloroplast DNA sequences, we demonstrate a Voyaging Corridor Triple I tight genealogical link between its populations in South China and North Taiwan, and South Taiwan and Remote Oceania by he peopling of Remote Oceania by Austronesian speakers way of Sulawesi and New Guinea, presenting the first study, to T(hereafter Austronesians) concludes the last stage of Neo- our knowledge, of a commensal plant species transported to – Polynesia whose phylogeographic structure concurs with ex- lithic human expansion (1 3). Understanding from where, when, “ ” and how ancestral Austronesians bridged the unprecedentedly pectations of the out of Taiwan hypothesis of Austronesian expansion. As a commensal plant likely transported across the broad water gaps of the Pacific is a fascinating and yet conten- full range of Austronesian expansion from South China to East tious subject in anthropology (1–8). Linguistic, archaeological, Polynesia, paper mulberry may also be the most widely trans- and genetic studies have demonstrated the complex nature of the ported fiber crop in human prehistory. process, where different components that helped to shape Lapita – culture in Near Oceania each have their own unique history (1 3). Author contributions: C.-S.C., A.S., D.S., and K.-F.C. designed research; A.S. and K.-F.C. Important evidence points to Taiwan as an Austronesian ancestral contributed new reagents/analytic tools; C.-S.C. collected plant materials in China, Sulawesi, homelandwithamoredistantorigininSouthChina(SChina) and Hawaii; H.-L.L. collected molecular data and collected plant materials in Taiwan and – Vietnam; A.S. and D.S. collected plant materials in Remote Oceania; K.-F.C. collected plant (3, 4, 9 12), whereas alternative models suggest S China to North materials in China; H.-L.L., X.M., and K.-F.C. analyzed data; and A.S., D.S., and K.-F.C. wrote Vietnam (N Vietnam) (7) or a Southeast Asian (SE Asian) origin the paper. based mainly on human genetic data (5). The complexity of the The authors declare no conflict of interest. subject is further manifested by models theorizing how different This article is a PNAS Direct Submission. spheres of interaction with Near Oceanic indigenous populations Freely available online through the PNAS open access option. during Austronesian migrations have contributed to the origin of Data deposition: The sequences reported in this paper have been deposited in the GenBank Lapita culture (1–3), ranging from the “Express Train” model, database (accession nos. KP728381–KP728458). assuming fast migrations from S China/Taiwan to Polynesia with 1C.-S.C. and H.-L.L. contributed equally to this work. “ ” limited interaction (4), to the models of Slow Boat (5) or 2To whom correspondence should be addressed. Email: [email protected]. “ ” “ ” Voyaging Corridor Triple I, in which Intrusion of slower This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. Austronesian migrations plus the “Integration” with indigenous 1073/pnas.1503205112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1503205112 PNAS Early Edition | 1of6 Downloaded by guest on September 30, 2021 approach,” first used to investigate the transport of the Pacific rat which eventually replaced proto-Austronesian language as well as Rattus exulans (6), has also been applied to other intentionally culture (27). transported animals such as pigs, chickens, and the tree snail In some regions (e.g., Philippines and Solomon Islands), tapa Partula hyalina, as well as to organisms transported accidentally, is made of other species of the mulberry family (Moraceae) such such as the moth skink Lipinia noctua and the bacterial pathogen as breadfruit and/or wild fig (Ficus spp.); however, paper mul- Helicobacter pylori (see refs. 2, 8 for recent reviews). berry remains the primary source of raw material to produce the Ancestors of Polynesian settlers transported and introduced a softest and finest cloth (20, 23). Before its eradication and ex- suite of ∼70 useful plant species into the Pacific, but not all of tinction from many Pacific islands due to the decline of tapa these reached the most isolated islands (15). Most of the com- culture, paper mulberry was widely grown across Pacific islands mensal plants, however, appear to have geographic origins on the inhabited by Austronesians (15, 20). Both the literature (15, 20) Sahul Plate rather than being introduced from the Sunda Plate or and our own observations (28–30) indicate that extant paper East Asia (16). For example, Polynesian breadfruit (Artocarpus mulberry populations in Oceania are only found in cultivation or altilis) appears to have arisen over generations of vegetative prop- as feral populations in abandoned gardens as on Rapa Nui agation and selection from Artocarpus camansi that is found wild in (Easter Island), with naturalization only known from the Solomon New Guinea (18). Kava (Piper methysticum), cultivated for its seda- Islands (20). For tapa making, its stems are cut and harvested tive and anesthetic properties, is distributed entirely to Oceania, before flowering, and as a majority of Polynesian-introduced from New Guinea to Hawaii (16). On the other hand, ti (Cordyline crops (16), paper mulberry is propagated clonally by cuttings or
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