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Traditional Banana Diversity in Oceania: an Endangered Heritage

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Traditional Banana Diversity in Oceania: an Endangered Heritage RESEARCH ARTICLE Traditional Banana Diversity in Oceania: An Endangered Heritage Valérie Kagy1*, Maurice Wong2, Henri Vandenbroucke3, Christophe Jenny3, Cécile Dubois3, Anthony Ollivier1, Céline Cardi3, Pierre Mournet3, Valérie Tuia4, Nicolas Roux5, Jaroslav Doležel6, Xavier Perrier3 1 Institut Agronomique néo Calédonien (IAC), Connaissance et Amélioration des Agro-Systèmes, BP 32 98880 La Foa, Nouvelle Calédonie, 2 Service du Développement Rural (SDR), Département de la Recherche Agronomique, BP 100, 98713 Papeete—Tahiti, Polynésie française, 3 Centre de Coopération Internationale en Recherche Agronomique pour le Développement (CIRAD), Unité Mixte de Recherche Amélioration Génétique et Adaptation des Plantes (AGAP), Avenue Agropolis, F-34398 Montpellier Cedex 5, France, 4 Pacific Community, Land Resources Division, Centre for Pacific Crops and Trees (CePaCT), Private Mail Bag, Suva, Fiji Islands, 5 Bioversity International, Parc Scientifique Agropolis II, F-34397 Montpellier Cedex 5, France, 6 Institute of Experimental Botany, Centre of the Region Haná for Biotechnological and Agricultural Research, Šlechtitelů 31, CZ-78371 Olomouc, Czech Republic * [email protected] OPEN ACCESS Citation: Kagy V, Wong M, Vandenbroucke H, Jenny Abstract C, Dubois C, Ollivier A, et al. (2016) Traditional Banana Diversity in Oceania: An Endangered This study aims to understand the genetic diversity of traditional Oceanian starchy bananas Heritage. PLoS ONE 11(3): e0151208. doi:10.1371/ in order to propose an efficient conservation strategy for these endangered varieties. SSR journal.pone.0151208 and DArT molecular markers are used to characterize a large sample of Pacific accessions, Editor: Randall P. Niedz, United States Department from New Guinea to Tahiti and Hawaii. All Pacific starchy bananas are shown of New Guinea of Agriculture, UNITED STATES origin, by interspecific hybridization between Musa acuminata (AA genome), more precisely its Received: October 13, 2015 local subspecies M. acuminata ssp. banksii, and M. balbisiana (BB genome) generating triploid Accepted: February 23, 2016 AAB Pacific starchy bananas. These AAB genotypes do not form a subgroup sensu stricto Published: March 16, 2016 and genetic markers differentiate two subgroups across the three morphotypes usually identi- fied: Iholena versus Popoulu and Maoli. The Popoulu/Maoli accessions, even if morphologi- Copyright: © 2016 Kagy et al. This is an open access article distributed under the terms of the cally diverse throughout the Pacific, cluster in the same genetic subgroup. However, the Creative Commons Attribution License, which permits subgroup is not strictly monophyletic and several close, but different genotypes are linked to unrestricted use, distribution, and reproduction in any the dominant genotype. One of the related genotypes is specific to New Caledonia (NC), with medium, provided the original author and source are morphotypes close to Maoli, but with some primitive characters. It is concluded that the diffu- credited. sion of Pacific starchy AAB bananas results from a series of introductions of triploids originating Data Availability Statement: SSR and DArT data in New Guinea area from several sexual recombination events implying different genotypes of were made freely available on TropGene DataBase M acuminata banksii by Chantal Hamelin: http://tropgenedb.cirad.fr/ . ssp. This scheme of multiple waves from the New Guinea zone is con- tropgene/JSP/interface.jsp?module=BANANA, and in sistent with the archaeological data for peopling of the Pacific. The present geographic distribu- S1 Dataset. tion suggests that a greater diversity must have existed in the past. Its erosion finds parallels Funding: The authors acknowledge the South with the erosion of cultural traditions, inexorably declining in most of the Polynesian or Melane- Pacific Integrated Observatory For Environment and sian Islands. Symmetrically, diversity hot spots appear linked to the local persistence of tradi- Terrestrial and Marine Biodiversity (GOPS), which tions: Maoli in New Caledonian Kanak traditions or Iholena in a few Polynesian islands. These funded this project associating the following: the ‘Institut Agronomique néo Calédonien’ (IAC), New results will contribute to optimizing the conservation strategy for the ex-situ Pacific Banana Col- Caledonia; the ‘Regional Pacific Plantain Collection’ lection supported collectively by the Pacific countries. at the ‘Centre for Pacific Crops and Trees’ (CePaCT), Secretariat of the Pacific Community (SPC); PLOS ONE | DOI:10.1371/journal.pone.0151208 March 16, 2016 1/19 Banana Diversity in Oceania ‘Bioversity International’; ‘Service de Développement Introduction Rural de la Polynésie Française’; and UMR AGAP Centre de Coopération Internationale en Recherche Bananas are widely distributed and cultivated throughout all the Pacific Islands. Various his- Agronomique pour le Développement (CIRAD). The torical traits, through various periods of time and an extended geographical area, led to a diver- project Leader was Valérie Kagy (IAC, New sified range of clonally propagated varieties. All currently cultivated varieties fall into two Caledonia). The authors thank also the French distinct introduction waves. The most recent wave followed the exploratory travels of Captain National Research Agency (ANR), program th ‘ ’ Cook at the end of the 18 century, with numerous introductions from almost all the other SYSTERRA, which funded the Vegeculture project ‘ ’ associating CIRAD-AGAP, IRD, University of banana areas in the world [1]. However, it occurred well after a first Oceanian wave, which Montpellier 2 (France), Jean Monnet University of brought traditional starchy bananas to all the Pacific Islands. Like most other cultivated species, Saint Etienne (France), CNRS-CREDO, Geo- these traditional varieties were introduced to the Pacific Islands and their dissemination is Consult, and CTRAV (Technical Centre for directly related to the original eastward peopling of the Pacific from South East (SE) Asia, as Agricultural Research in the Vanuatu). The described by geneticists, ethnologists, ethnobotanists, linguists and archaeologists [2–8]. ‘Vegeculture’ project coordinator was Vincent Lebot (CIRAD-AGAP, Vanuatu). Jaroslav Doležel has been The presence of Homo sapiens has been attested in the Southeast Asian islands and in near supported by the National Program of Sustainability Oceania for at least 50,000 years. Advantage was taken of the very strong drop in sea levels dur- (award no. LO 2014). The funders had no role in ing the different glaciation periods to move from island to island and even easily cross the Wal- study design, data collection and analysis, decision to lace line, towards Sahul: New Guinea and Australia (The term ‘New Guinea’ is used here in a publish, or preparation of the manuscript. generic sense to refer to the country of Papua New Guinea (PNG), the independent state com- Competing Interests: The authors have declared prising the eastern half of the island of New Guinea and various close islands, as well as the that no competing interests exist. Indonesian western half of the island of New Guinea) [4] At around 30,000 years ago, the islands of the Bismarck Archipelago to the east of New Guinea were already occupied. Around 3,500 years ago, the Lapita cultural complex characterized by its typical “dot-patterned” pottery was developing in the Bismarck Archipelago [5,8]. This Lapita culture, with its language brought by Austronesian mariners, appeared as a complex aggregating innovations borrowed from various SE Asian peoples in the field of stone tools, navigation, but also agriculture [3,7]. Horticulture, in particular, had already been widely developed by the earlier populations, such as at Kuk Swamp, in Highland New Guinea, where tuber plants and bananas were grown 7,000 years ago [9]. Starting from the Bismarck Islands, the Lapita people progressed several thou- sand kilometres eastwards within a few centuries and settled throughout Melanesia: the Solo- mon Islands, Vanuatu, New Caledonia, Fiji, and lastly to the western edges of Polynesia, Samoa, where their presence has been attested at 3,000 years ago. Wherever they settled, these migratory proto-Polynesians peoples brought with them their animals [10] and domestic plants [11,12], including many traditional banana cultivars [13,14]. Subsequent, most easterly crossings were much more difficult and it took a further two mil- lennia for the ancestral Polynesians to leave Tonga or Samoa and settle in Tahiti and the Mar- quesas Islands in 200 AD, then Hawaii around 300–500 AD, Easter Island around 900–1200 AD and New-Zealand only around 1100–1300 AD. Among the banana varieties specific to the Pacific area, Fe’i bananas, with their distinctive erect bunch, were once important in Tahiti but are today generally under-utilized [15–18]. Fe’i bananas belong to the Autralimusa/Callimusa section (2n = 2x = 20) of genus Musa within which a few varieties have been domesticated in the New Guinea area. They are botanically very distinct from other traditional Oceanian bananas, and thus were not considered in this study. Representatives of the Eumusa/Rhodochlamys section (2n = 2x = 22) of genus Musa are largely more frequent. They are triploid clones (AAB genome), originating from interspecific hybridization between Musa balbisiana (B genome) and Musa acuminata (A genome), more precisely M. acuminata ssp. banksii, present mainly in Papua New-Guinea [19,20]. The histori- cal and geographical process
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