Historical collections reveal patterns of diffusion of sweet potato in Oceania obscured by modern plant movements and recombination

Abstract

The history of sweet potato in the Pacific has long been an enigma. Archaeological, linguistic, and ethnobotanical data suggest that prehistoric human-mediated dispersal events contributed to the distribution in Oceania of this American domesticate. According to the "tripartite hypothesis," sweet potato was introduced into Oceania from South America in pre-Columbian times and was then later newly introduced, and diffused widely across the Pacific, by Europeans via two historically documented routes from Mexico and the Caribbean. Although sweet potato is the most convincing example of putative pre-Columbian connections between human occupants of Polynesia and South America, the search for genetic evidence of pre-Columbian dispersal of sweet potato into Oceania has been inconclusive. Our study attempts to fill this gap. Using complementary sets of markers (chloroplast and nuclear microsatellites) and both modern and herbarium samples, we test the tripartite hypothesis. Our results provide strong support for prehistoric transfer(s) of sweet potato from South America (Peru-Ecuador region) into Polynesia. Our results also document a temporal shift in the pattern of distribution of genetic variation in sweet potato in Oceania. Later reintroductions, accompanied by recombination between distinct sweet potato gene pools, have reshuffled the crop's initial genetic base, obscuring primary patterns of diffusion and, at the same time, giving rise to an impressive number of local variants. Moreover, our study shows that phenotypes, names, and neutral genes do not necessarily share completely parallel evolutionary histories. Multidisciplinary approaches, thus, appear necessary for accurate reconstruction of the intertwined histories of plants and humans.

Fig. 1.

Prehistoric and historical dispersal of sweet potato in Oceania, as postulated by the tripartite hypothesis. This map summarizes the tripartite hypothesis, as updated by Green (26) and reviewed by Clarke (27). Dispersal events and the terms commonly used to designate sweet potato in the different regions [compiled mostly from Yen (25)] are represented. Archaeological and early historical records providing strong evidence for the presence of sweet potato in Oceania in the prehistoric period are also indicated.

Fig. 2.

Geographical distribution of nuclear and chloroplast genetic variation in sweet potato through space and over time. (A) Proportion of individuals belonging to each chloroplast lineage [lineage 1 in orange (Cp 1); lineage 2 in blue (Cp 2)] for each sampling site (country or archipelago). Only sites with four or more accessions were represented. Area of the circle is proportional to the square root of the sample size for the site. Values by region correspond to the frequency of chloroplast lineage 1. (B) Proportion of individuals belonging to each nuclear cluster (cluster K1 in orange; K2 in blue) for each sampling site, as determined by the DAPC analysis. Only sites with four or more accessions were represented. Area of the circle is proportional to the square root of the sample size for the site. Values by region correspond to the mean K1 ancestry, as determined by the Bayesian clustering. (C) Three bar plots showing for each individual: (i) the probabilities of membership in nuclear clusters K1 and K2 as determined by DAPC (Top); (ii) the probabilities of membership in nuclear clusters K1 and K2 as determined by the Bayesian clustering method implemented in Structure (Middle); and (iii) the individual’s chloroplast lineage (Bottom). Each individual is represented as a vertical bar, with colors corresponding to membership probabilities in clusters K1 (orange), K2 (blue), and chloroplast lineages 1 (orange) and 2 (blue). Individuals are organized by geographical origin, S for the Southern neotropical region, N for the Northern neotropical region, P for Polynesia, M for Melanesia, NG for New Guinea, and SEA for South-East Asia. (D) Genetic constitution of herbarium specimens collected from the 18th century to the early 20th century. Lower and upper halves of each circle represent the chloroplast lineage and nuclear cluster (as determined by DAPC), respectively.

Fig. 3.

Global patterns of genetic differentiation. Neighbor-joining tree based on the Lynch distance for the global dataset. Individuals are labeled according to their geographical origin, in orange, blue, cyan, green, yellow, magenta, and black for accessions from the Southern region, the Northern region, Polynesia, Island Melanesia, New Guinea, South-East Asia, and “other regions” (Micronesia, Madagascar, Madeira), respectively. Herbarium specimens from Polynesia are indicated by red open circles.