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Evidence on the Origin of Cassava: Phylogeography of Manihot Esculenta

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Evidence on the Origin of Cassava: Phylogeography of Manihot Esculenta Proc. Natl. Acad. Sci. USA Vol. 96, pp. 5586–5591, May 1999 Evolution Evidence on the origin of cassava: Phylogeography of Manihot esculenta KENNETH M. OLSEN† AND BARBARA A. SCHAAL Department of Biology, Washington University, St. Louis, MO 63130 Communicated by Peter H. Raven, Missouri Botanical Garden, St. Louis, MO, March 23, 1999 (received for review January 11, 1999) ABSTRACT Cassava (Manihot esculenta subsp. esculenta)is copy’’ (low copy number) nuclear genes, has not been extensively a staple crop with great economic importance worldwide, yet its explored in plants (5, 9–11), although this genome can potentially evolutionary and geographical origins have remained unresolved provide multiple, unlinked allele genealogies at the intraspecific and controversial. We have investigated this crop’s domestica- level (12–14). tion in a phylogeographic study based on the single-copy nuclear This study reports on the use of a single-copy nuclear gene to gene glyceraldehyde 3-phosphate dehydrogenase (G3pdh). The examine the phylogeography of a plant species, Manihot esculenta G3pdh locus provides high levels of noncoding sequence variation Crantz (Euphorbiaceae), which includes the important tropical in cassava and its wild relatives, with 28 haplotypes identified subsistence crop cassava and its wild relatives. A portion of the among 212 individuals (424 alleles) examined. These data rep- gene encoding glyceraldehyde 3-phosphate dehydrogenase resent one of the first uses of a single-copy nuclear gene in a plant (G3pdh) provides high levels of sequence variation in Manihot. phylogeographic study and yield several important insights into The G3pdh data are used here to investigate the evolutionary cassava’s evolutionary origin: (i) cassava was likely domesticated origins of cassava, specifically the crop’s geographical origin from wild M. esculenta populations along the southern border of within the range of its wild relatives, and the potential role that the Amazon basin; (ii) the crop does not seem to be derived from interspecific hybridization may have played in the crop’s domes- several progenitor species, as previously proposed; and (iii) tication. cassava does not share haplotypes with Manihot pruinosa,a Study System. Cassava (M. esculenta subsp. esculenta)isa closely related, potentially hybridizing species. These findings staple root crop for over 500 million people living throughout the provide the clearest picture to date on cassava’s origin. When tropics (15). It is the primary source of carbohydrates in sub- considered in a genealogical context, relationships among the Saharan Africa (16) and ranks sixth among crops in global G3pdh haplotypes are incongruent with taxonomic boundaries, production (17). Despite its immense importance in the devel- both within M. esculenta and at the interspecific level; this oping world, cassava has historically received less attention by incongruence is probably a result of lineage sorting among these researchers than have temperate crops, earning it the status of an recently diverged taxa. Although phylogeographic studies in ‘‘orphan crop.’’ animals have provided many new evolutionary insights, appli- One of the most fundamental questions about cassava that cation of phylogeography in plants has been hampered by remains unresolved concerns its evolutionary origin. The genus difficulty in obtaining phylogenetically informative intraspecific Manihot (comprising 98 species; ref. 18) is distributed across variation. This study demonstrates that single-copy nuclear much of the Neotropics, and the identity of cassava’s closest wild genes can provide a useful source of informative variation in relatives within the genus has been a source of widespread plants. speculation (18–21). Most traditional domestication hypotheses have envisioned the crop to be a ‘‘compilospecies’’ derived from Understanding the process of population divergence is funda- one or more species complexes, either in Mexico and Central mental to the study of evolutionary diversification. This process America (18, 22) or throughout the Neotropics (21, 23, 24). More is inherently phylogenetic, such that the present population recently, wild populations of M. esculenta that are likely to be the structure of a species reflects not only current patterns of genetic crop’s direct progenitors have been identified in South America exchange but also the history of gene flow and isolation among (19, 25). However, the evolutionary relationship between cassava population lineages. In the past decade, workers have begun to and its conspecific wild relatives is only beginning to be examined employ phylogenetically informative data (most often allele (19, 26, 27), and there is continued speculation that the crop’s genealogies derived from DNA sequences) for investigating origins may extend beyond M. esculenta to hybridizing Manihot population divergence (1–3). This approach was first de- species (26, 27). scribed by Avise et al. (1), who termed it phylogeography, Wild populations of M. esculenta occur primarily in west central and it has since been hailed widely as the conceptual bridge Brazil and eastern Peru (19, 28). All wild populations of this linking population-level processes to macroevolutionary species are referred to here as M. esculenta subsp. flabellifolia phylogenetic relationships (2–4). (Pohl) Ciferri (see also ref. 27). This wild subspecies is found in Despite a recent explosion in phylogeography studies involving forest patches in the transition zone between the cerrado (savanna animal species (3), analogous studies in plants remain scarce, scrub) vegetation of the Brazilian shield plateau and the lowland primarily because of difficulties in detecting phylogenetically rainforest of the Amazon basin, where it grows as a clambering informative intraspecific genetic variation (5). Most attempts to understory shrub or treelet. In Brazil, populations occur along the detect such variation in plants have relied on the chloroplast southern and eastern borders of the Amazon basin, in the states genome, with success varying widely among taxa (e.g., refs. 5–7). of Tocantins, Goia´s, Mato Grosso, Rondoˆnia, and Acre. Al- The plant mitochondrial genome, with few exceptions (e.g., ref. though cassava is interfertile with subspecies flabellifolia (27) and 8), has not yielded useful amounts population-level variation. An is cultivated within its range, the population structure of the wild alternative source of variation, the noncoding regions of ‘‘single- subspecies is not thought to reflect introgression from the crop The publication costs of this article were defrayed in part by page charge Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. AF136119– payment. This article must therefore be hereby marked ‘‘advertisement’’ in AF136149). accordance with 18 U.S.C. §1734 solely to indicate this fact. †To whom reprint requests should be addressed. e-mail: olsen@biology. PNAS is available online at www.pnas.org. wustl.edu. 5586 Evolution: Olsen and Schaal Proc. Natl. Acad. Sci. USA 96 (1999) 5587 after domestication. Subspecies flabellifolia occurs in forested uals of M. pruinosa, representing 6 populations, were used in areas where cassava does not grow. In addition, cassava does not analyses. Voucher herbarium specimens from each population survive well in abandoned fields or as an escape from cultivation are housed at the Missouri Botanical Garden and at the Centro (refs. 19 and 22; K.M.O., unpublished observation). Finally, Nacional de Pesquisa de Recursos Gene´ticos e Biotecnologia in cassava is propagated almost exclusively by stem cuttings, mini- Brası´lia, Brazil. To represent the diversity of cassava, 20 cultivars mizing unintentional spread of the crop by humans. were sampled from the cassava ‘‘world core collection’’ main- To examine the possibility that cassava’s origins extend beyond tained by the Centro Internacional de Agricultura Tropical in subspecies flabellifolia, we have included in our study Manihot Cali, Colombia. pruinosa Pohl, a very closely related, potentially hybridizing DNA was extracted from dried leaves by using a cetyltri- species. M. esculenta and M. pruinosa are very similar, both methylammonium bromide protocol (29). PCR amplification of morphologically (28) and with respect to the internal transcribed the G3pdh region was performed with primers designed by Strand spacer region of nuclear ribosomal DNA (B.A.S., unpublished et al. (ref. 9; GPDX7F and GPDX9R, forward and reverse, data). Based on this close relationship, M. pruinosa has been respectively). These primers were designed from conserved re- proposed to fall within cassava’s ‘‘secondary gene pool’’ of gions identified in published G3pdh sequences of Arabidopsis potentially interfertile species (28); it is the only such species to thaliana and Ranunculus acris (A. Strand, personal communica- occur in sympatry with M. esculenta. M. pruinosa grows as a shrub tion). There were three 50-ml reactions carried out per individual, in the cerrado southeast of the Amazon basin, in the Brazilian and each reaction contained 10 mM TriszHCl (pH 9.0), 50 mM states of Tocantins, Goia´s, and Mato Grosso. Although M. KCl, 2.5 mM MgCl2, 0.1% Triton X-100, 2 units Taq Polymerase pruinosa and M. esculenta occur in different habitats, the patchy (Promega), 200 mM each dNTP, 0.2 mM each primer, and nature of the cerrado–forest transition zone permits the two '10–20 ng genomic DNA. Cycling conditions were 95°C
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