As a portable source of food, water, fuel, and construction materials, the coconut (Cocos nucifera L.) played a fundamental role in human migrations and the development of civilization across the humid tropics. Here we investigated the coconut's domestication history and its population genetic structure as it relates to human dispersal patterns. A sample of 1,322 coconut accessions, representing the geographical and phenotypic diversity of the species, was examined using ten microsatellite loci. Bayesian analyses reveal two highly genetically differentiated subpopulations that correspond to the Pacific and Indo-Atlantic oceanic basins. This pattern suggests independent origins of coconut cultivation in these two world regions, with persistent population structure on a global scale despite long-term human cultivation and dispersal. Pacific coconuts show additional genetic substructure corresponding to phenotypic and geographical subgroups; moreover, the traits that are most clearly associated with selection under human cultivation (dwarf habit, self-pollination, and “niu vai” fruit morphology) arose only in the Pacific. Coconuts that show evidence of genetic admixture between the Pacific and Indo-Atlantic groups occur primarily in the southwestern Indian Ocean. This pattern is consistent with human introductions of Pacific coconuts along the ancient Austronesian trade route connecting Madagascar to Southeast Asia. Admixture in coastal east Africa may also reflect later historic Arab trading along the Indian Ocean coastline. We propose two geographical origins of coconut cultivation: island Southeast Asia and southern margins of the Indian subcontinent.

Funding: The study was funded by a National Geographic Society (CRE 8178-07) grant to KMO and BFG, http://www.nationalgeographic.com/field/ , and COGENT network and the CGIAR Generation Challenge Progamme to LB, http://www.inibap.org/cogent/ . The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

The impact of the coconut palm (Cocos nucifera L.) on the history of human dispersal in the humid tropics is unparalleled in the plant kingdom. As a portable source of both food and water, the coconut played a critical role in the ability of humans to voyage, establish trade routes, and colonize lands in the Pacific Rim and regions throughout the Old World tropics [1], [2]. This species continues to have hundreds of uses as a source of food, drink, fiber, construction material, charcoal, and oil (used in cooking, pharmaceuticals, industrial applications, and biofuels); over 12 million hectares of coconut are currently planted across 89 tropical countries [3]. The history of dispersal and cultivation of this species is thus fundamentally intertwined with human history in the tropics.

The long-term interaction between humans and coconuts has shaped both the geographical distribution of C. nucifera and its phenotypic diversity. While the coconut fruit is naturally adapted for dispersal by sea currents [4], its pantropical dissemination was achieved with the help of humans [5], [6]. A native of the Old World tropics, the species was spread to eastern Polynesia and subsequently introduced to the Pacific coasts of Latin America, most likely by pre-Columbian Austronesian seafarers from the Philippines [7]. In the Indian Ocean, the composition of coconut populations was likely influenced by Austronesian expansions westward to Madagascar. Later, coconuts were introduced by Europeans from India to the Atlantic coasts of Africa and South America and to the Caribbean [8]. The species is typically found in areas of present or past human activity, and all or nearly all coconut populations worldwide have likely been influenced by human cultivation and dispersal.

Phenotypically, coconuts vary widely in the degree to which they show evidence of selection under human cultivation. Classic analyses of coconut fruit morphology revealed two predominant fruit types, named after traditional Polynesian varieties: the ‘niu kafa’ form, characterized by oblong, triangular fruits with a large proportion of fibrous husk; and the ‘niu vai’ form, whose fruits are rounded and often brightly colored, with a large proportion of liquid endosperm [9], [10]. The ‘niu kafa’ form has been interpreted as the more ancestral morphology, reflecting natural selection for ocean dispersal, and the ‘niu vai’ form as reflecting selection under human cultivation [1]. Coconuts have also been traditionally classified into ‘Dwarf’ and ‘Tall’ varieties based on tree habit. ‘Dwarfs’ represent about 5% of coconut palms and are cultivated worldwide; they are typically found near human habitation and show traits closely associated with human selection: slow trunk growth, self-pollination, and the production of niu vai fruits [11]. The more common ‘Tall’ coconuts are outcrossing and grow faster than ‘Dwarfs,’ resulting in greater height at reproductive maturity. Many ‘Talls’ are grown for the production of copra for oil extraction and coir for fiber; while actively cultivated, these varieties lack the obvious domestication traits of the self-pollinating Dwarfs.

The lack of universal domestication traits among coconut varieties, combined with the long history of human interaction with this species, have made it difficult to trace the coconut's cultivation origins. However, applications of molecular markers for purposes of crop germplasm characterization have provided some insights into the coconut's evolutionary history, genetic diversity and population structure (e.g., [12], [13]). Analyses using RFLPs (e.g., [14]), microsatellites [15], [16] and AFLP markers [17] have suggested the presence of two genetically distinct groups, corresponding broadly to the Pacific Ocean basin on one side and the Indian and Atlantic Oceans on the other (see also [18], [19]).

In the last decade, a worldwide coconut germplasm collection, coordinated through the International Coconut Genetic Resources Network (COGENT) and the French Agricultural Research Centre for International Development (CIRAD), with further support through the Generation Challenge Programme (GCP: http://gcpcr.grinfo.net/index.php), has served as the primary source of materials for genetic characterizations. Together with a polymorphic microsatellite marker kit [20], the GCP/CIRAD coconut collection has been used to characterize genetic diversity in regional coconut collections (e.g., [21], [22]), infer origins of specific cultivars [7], and assess planting material for trueness to type [23]. Importantly, this worldwide collection has not been used previously to examine the coconut's cultivation history. Moreover, while global in scope, the GCP/CIRAD collection has left some geographical regions under-represented. Most notably, it contains few coconuts from the western Indian Ocean, which would be key to elucidating any influence of ancient Austronesian expansions in this region.

In the present study, we have employed ten polymorphic loci from the GCP/CIRAD microsatellite kit to examine genetic variation in a worldwide collection of >1300 coconuts, representing GCP/CIRAD germplasm plus collections from key under-sampled regions of the western Indian Ocean: Madagascar, Comoros, and Seychelles islands. We use population structure analyses, together with ethnographic and archaeobotanical evidence, to examine the impacts of human-mediated dispersal and domestication on this important tree crop. Our analyses suggest the following: 1) Despite the widespread movement of coconuts by humans, both historically and today, the species has retained clear population structure on a global scale; 2) Present-day cultivated coconuts arose through independent domestications in the Indian and Pacific Ocean basins; however, the definitive domestication traits — dwarf habit, self-pollination, and niu vai fruits — arose only with the Pacific domestication event; and 3) Geographical locations of genetically admixed populations are consistent with human introductions of Pacific germplasm along the ancient trading routes connecting Asia to Africa.