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Proc Natl Acad Sci U S A. Sep 6, 2005; 102(36): 12801–12806.
Published online Aug 26, 2005. doi:  10.1073/pnas.0505447102
PMCID: PMC1200284
Evolution

Domestication of a Mesoamerican cultivated fruit tree, Spondias purpurea

Abstract

Contemporary patterns of genetic variation in crops reflect historical processes associated with domestication, such as the geographic origin(s) of cultivated populations. Although significant progress has been made in identifying several global centers of domestication, few studies have addressed the issue of multiple origins of cultivated plant populations from different geographic regions within a domestication center. This study investigates the domestication history of jocote (Spondias purpurea), a Mesoamerican cultivated fruit tree. Sequences of the chloroplast spacer trnG–trnS were obtained for cultivated and wild S. purpurea trees, two sympatric taxa (Spondias mombin var. mombin and Spondias radlkoferi), and two outgroups (S. mombin var. globosa and Spondias testudinus). A phylogeographic approach was used and statistically significant associations of clades and geographical location were tested with a nested clade analysis. The sequences confirm that wild populations of S. purpurea are the likely progenitors of cultivated jocote trees. This study provides phylogeographic evidence of multiple domestications of this Mesoamerican cultivated fruit tree. Haplotypes detected in S. purpurea trees form two clusters, each of which includes alleles recovered in both cultivated and wild populations from distinct geographic regions. Cultivated S. purpurea populations have fewer unique trnG–trnS alleles than wild populations; however, five haplotypes were absent in the wild. The presence of unique alleles in cultivation may reflect contemporary extinction of the tropical dry forests of Mesoamerica. These data indicate that some agricultural habitats may be functioning as reservoirs of genetic variation in S. purpurea.

Keywords: crop origins, Mesoamerica, phylogeography, genetic variation

The geographic origins of most cultivated plants can be traced to several global centers of domestication (e.g., Fertile Crescent Region of the Middle East, Mesoamerica, the Andes, eastern Asia, sub-Saharan Africa; refs. 15). In each center, humans selected and cultivated a suite of native plants. Over time, the cultivated populations became genetically distinct from their wild progenitors as the evolutionary process of domestication proceeded (6). Recently, much attention has focused on the centers of domestication and their associated crops and putative wild ancestors as concerns mount about the lack of genetic diversity in cultivated plants (7). It has been estimated that the diversity found in cultivated populations has declined by as much as 80% over the past 100 years (79). How this loss occurs, either all at once or gradually over generations, is not clear. Scientific investigations focusing on the genetic resources contained in cultivated plants and their wild ancestors have documented the historical processes associated with domestication, providing new perspectives on contemporary patterns of genetic variation in cultivated populations and their wild ancestors (e.g., ref. 10).

One of the most elusive questions regarding the evolution of cultivated plants is the number of times a species was taken into cultivation within a domestication center (5, 11). In the Near East center of domestication (the “Fertile Crescent”), the wild ancestors of the crops upon which agriculture was founded are known (e.g., wheats, barley, pea, lentil, and chickpea) (12). The geographic distributions of these wild ancestors, together with biochemical and genetic data, have been used to suggest that emmer wheat, einkorn wheat, peas, chickpeas, and lentils were domesticated from wild progenitors just once or a few times in a single geographic region (1218)

In contrast to the Near East center, crops domesticated in the Mediterranean region and other parts of the world have been derived more than once from their wild progenitors [e.g., olives (1921), rice (22, 23), and breadfruit (24)]. Within the Mesoamerican center of domestication (Central Mexico to north-western Costa Rica), at least 80 native species have been cultivated historically (2, 3 2529). Some native crop species have complex evolutionary histories, and may have been domesticated multiple times within Mesoamerica [e.g., avocados (30) and one of the cultivated chili pepper species, Capsicum frutescens (25)]. Today, many of the native crop species of Mesoamerica are cultivated in traditional agricultural habitats, such as backyard gardens and living fences (13, 12, 3133). They are grown and sold on a regional scale and have not yet undergone the intensive selection and large-scale cultivation characteristic of modern agriculture. Consequently, some Mesoamerican crop populations often resemble their wild relatives, with transitional, morphologically intermediate forms existing between cultivated populations and their progenitors (3). The native crop species of Mesoamerica provide a unique opportunity to document the domestication process in its incipient stages. In this paper, we report on the origins of one of the Mesoamerican cultivated fruit trees, Spondias purpurea L. (Anacardiaceae).

Study System

Spondias purpurea L. (known locally as jocote, ciruela mexicana, or hog plum) is a small (3–10 m) tree native to the tropical dry forests of Mexico and Central America (3439). Jocotes are cultivated throughout the tropics and subtropics for their fruits, which are eaten fresh, sold in local markets, and made into jams and beverages (34, 35). The majority of trees are found in backyard gardens and living fences, although some formal cultivation exists in orchards (39). Jocotes are propagated vegetatively from large branch-size cuttings. The existence of at least 180 common names for the species suggests that jocotes have been used by many cultures, and that there is considerable variation within the species (40). Cultivated, mature fruits vary widely in color (green, yellow, orange, red, violet), size (3–5.5 cm long), texture (chalky, juicy), and taste (sweet, acidic) (39). At the time of the European colonization, jocotes were grown widely from Mexico to the northern regions of South America, as described by the first chroniclers of the region (39).

Today, wild jocote populations are found in the fragmented tropical dry forests of Mexico and Central America (36). The native habitat of wild jocotes is severely restricted; it is estimated that <2% of the Mesoamerican tropical dry forests remain (41, 42). Fruits of wild jocotes are usually bright red (A.M., personal observation). They are smaller and more acidic than the cultivated fruits, with considerably less flesh surrounding the seed. Unlike cultivated populations, wild jocotes reproduce from seed and native populations are age-structured with a variety of juvenile and mature individuals present. The contrast in morphology and method of reproduction between wild and cultivated jocotes indicates that S. purpurea is a species that has been altered genetically during the course of domestication. During this process, humans have selected for trees that bear large, fleshy, sweet fruits, and that can be reproduced easily from cuttings.

The genus Spondias L. comprises ≈17 species including seven taxa in the Neotropics and ≈10 species in the Asian tropics (refs. 4345 and D. Daly and J. D. Mitchell, personal communication). Nearly all Spondias species have a fibrous endocarp and leaflets with an intramarginal vein (45). Neither the relationship of Spondias to closely allied genera nor the relationships among the species of Spondias are well understood (46).

Spondias purpurea is one of three Spondias species native to Mexico and Central America. Spondias mombin L. var. mombin (jobo) is a widespread taxon occuring from Mexico to Paraguay (47). Native to the tropical wet forests, S. mombin var. mombin is a large tree that grows to a height of 30 m. Spondias mombin var. mombin differs from S. purpurea in flower and fruit color, inflorescence structure, leaflet size and number, and bark characteristics (37). In Mesoamerica, S. mombin var. mombin is cultivated occasionally for its fruits and in living fences, although it is not nearly as common as the cultivated jocotes. The third native Spondias species in Mesoamerica is Spondias radlkoferi Donn. Sm., is morphologically similar to S. mombin var. mombin, although it is distinct in fruit shape and flowering time (48). It is rarely cultivated.

In this study, we apply a phylogeographic approach based on chloroplast sequence data to investigate the geographic origins of domesticated jocotes in Mesoamerica and to examine the changes in genetic diversity associated with domestication. Our objectives are to (i) identify the ancestors of the cultivated jocotes, (ii) document the impact of domestication on the diversity of trnG–trnS sequences of S. purpurea, and (iii) to discern one (or more) geographic regions within Mesoamerica where cultivated jocotes originated.

Materials and Methods

Plant Collection. Field studies were conducted during the summers of 2000–2002 in Costa Rica, El Salvador, Guatemala, Honduras, Mexico, Nicaragua, and Panama (Fig. 1). Ninety-six individuals of S. purpurea were sampled, representing 11 geographic regions (Table 1). In each region, individuals were sampled from both wild and various cultivated habitats (backyards, living fences, orchards). Multiple accessions of sympatric Mesoamerican Spondias species were collected [S. mombin var. mombin (n = 25) and S. radlkoferi (n = 9)]. Three Brazilian taxa that are morphologically similar to the Mesoamerican species were included as South American outgroups [S. mombin var. mombin (n = 4), S. mombin var. globosa (n = 4), Spondias testudinus (n = 6)] (A. Costello, Ross School, New York; J. D. Mitchell, personal communication). Leaves for DNA extraction were preserved in silica gel. Herbarium specimens (collected from each population) were deposited at the Missouri Botanical Garden and in herbaria in the country of origin (CR, USJ, ITIC, UVAL, EAP, TEFH, GUADA, CICY, YUC, MEXU, ENAG, SCZ, STRI, PMA). The precise geographic location of each population was determined by using a Garmin Etrex GPS.

Fig. 1.
The Mesoamerican Center of Domestication. Spondias samples were collected in Mexico, Guatemala, El Salvador, Honduras, Nicaragua, Costa Rica, and Panama.
Table 1.
S. purpurea populations in Mexico and Central America

DNA Extraction, Amplification, and Analysis. Dried leaves were frozen with liquid nitrogen, mixed with powdered glass, and pulverized by using a mortar and pestle. Crushed leaves (≈200 mg) were washed with a Hepes buffer. DNA was extracted from washed leaf material by using a modified (5×) cetyltrimethylammonium bromide (CTAB) extraction (49) and then purified by using the GeneCleanII kit (Qbiogene, Irvine, CA).

Approximately 1,000 bases of the chloroplast spacer trnG–trnS were amplified by using the forward primer trnG 5′-GAA CGA ATC ACA CTT TTA CCA C-3′ and reverse primer trnS5′-GCC GCT TTA GTC CAC TCA GC-3′ (50). The chloroplast genome is assumed to be maternally inherited in S. purpurea, as it is maternally inherited in most angiosperms (51, 52). Cycling conditions were 94°C (5 min); then for 30 cycles 94°C (1 min), 55°C (45 s), 72°C (1 min), and a final extension at 72°C (5 min). Two 50-μl reactions were completed for each individual, resulting in 100 μl of PCR product per sample. PCR products were purified by using the Viogene Gel Extraction kit (Viogene, Illkirch, France). Purified templates were sequenced in two directions by using the dideoxy chain termination method. Sequencing reactions were carried out by using the trnG forward primer and several Spondias-specific internal primers: trnG 11.11 5-CGG CAC TGA ACG AAT CAC AC-3′, trn GSp 5′-TTT GAC AGA TAT GGC TGG AC-3′, and trnS 755 5′-CGG CCT GGC CCT GGC AGT ACC-3′. A string of A's in the middle of the region complicated sequencing efforts and forced the removal of 400 bp in the final alignment. Bases were fluorescently labeled with Big Dye Terminator versions 3.1 and 1.1 sequencing reagents (Applied Biosystems). Sequences were visualized by using the Base Station DNA Fragment Analyzer and cartog-rapher software (MJ Research). Clean sequences were difficult to obtain from some samples; these samples were cloned. Ligation was carried out in a 4.5-μl reaction (2.5 μl of Rapid Ligation Buffer, 1.5 μl of PCR product, 0.5 μl of pGEM T Easy Vector; Promega). Two clones per sample were sequenced in both directions.

Tests of neutrality using Tajima's D statistic and Fu and Li's statistic were completed by using dnasp (version 3.53, ref. 53). Gene flow within and among regions (populations) was approximated as Nm, the number of migrants per generation between populations, and was estimated by using the expression Fst = 1/(1 + 2Nm), where N is the female effective population size and m is the female migration rate (54). Geographic distances between populations were quantified by using passage (55) and used to conduct Isolation By Distance analyses with both Fst and Nm values. A phylogeographic analysis was used to examine the geographic distribution of alleles (56, 57). Haplotypes (= alleles) were identified and assigned a unique letter code. A haplotype network depicting the mutational relationships among distinct haplotypes was drawn following the principle of parsimony. A nested contingency analysis was conducted (5860). Haplotypes were grouped into one-, two-, and three-step clades following ref. 59, and statistically significant associations between geographic localities and clades were detected by using the program geodis (version 2.0; ref. 61).

Results and Discussion

Chloroplast Sequence Variability. Sequences of the chloroplast trnG–trnS spacer resulted in 610 aligned bases with 16 substitutions and 13 indels that varied in size from 1 to 219 bp (Table 3, which is published as supporting information on the PNAS web site). Sequence divergence, as measured with Kimura two-parameter algorithm in paup* (62), ranged from 0% to 3.37% for all Spondias samples, and from 0% from 0.86% within S. purpurea. Sequences of the trnG–trnS spacer in Spondias conform to the expectation of neutrality by Tajima's criterion (D = –1.32250, P > 0.10) and Fu and Li's D* (D = –2.41966, P > 0.05) and F* = –2.36326, P > 0.05) criteria. Thirty unique haplotypes were identified from the trnG–trnS sequences. The number of individuals carrying a given haplotype varied from 1 to 60. Pairwise Fst values ranged from 0 to 0.66379. Tests for isolation by distance based on Nm and Fst were not significant (popgene, version 1.31, ref. 63).

Ancestors of Cultivated S. purpurea Based on the Distribution of trnG–trnS Haplotypes. The 30 trnG–trnS haplotypes recovered in this study fell into two distinct groups (groups 1 and 2, Fig. 2A). Haplotypes in the two groups differed by at least 10 mutations. The 13 haplotypes found in group 1 were carried exclusively by S. mombin, S. radlkoferi, and S. testudinus trees from Central and South America; none of the ≥100 S. purpurea phenotypes surveyed carried any of the alleles of group 1. All individuals identified as either wild or cultivated S. purpurea carried one group 2 haplotype (Fig. 2 A), reflecting the close relationship of wild and cultivated S. purpurea trees. In addition, four of the group 2 haplotypes (haplotypes AA, AC, R, and Z) were recovered in five Mesoamerican trees identified as either S. mombin var. mombin or S. radlkoferi. The S. mombin var. mombin and S. radlkoferi trees carrying group 2 haplotypes occurred in southern Central America (southwestern Nicaragua and northwestern Costa Rica). Shared haplotypes among species can be attributed to secondary gene flow (hybridization) or incomplete lineage sorting, where branching events in gene geneaologies do not correspond to branching in population history (57). Based on the trnG–trnS sequence data, Mesoamerican S. purpurea trees either share a common ancestor with other Spondias taxa in southern Central America, are experiencing ongoing gene flow with sympatric congeners in this region, or both.

Fig. 2.
Relationships among trnG–trnS alleles recovered in Spondias trees. (A) Haplotype network depicting mutational relationships among 30 trnG–trnS alleles found in S. purpurea (squares), S. mombin var. mombin (diamonds), S. mombin var. globosa ...

Haplotype Distribution in Cultivated and Wild Mesoamerican Jocotes. Of the 17 haplotypes detected in S. purpurea trees, 12 (71% of the total allele diversity) were recovered in wild populations, and nine (53% of the total allele diversity) were carried by cultivated individuals. During the course of jocote domestication, both the number of trnG–trnS alleles and the relative abundance of those alleles have changed under the influence of human selection (Fig. 3).

Fig. 3.
trnG–trnS alleles found in wild and cultivated (including backyard trees, living fences, and orchard trees) S. purpurea. Alleles were more numerous and more evenly distributed in wild samples as compared with cultivated samples, of which 71% carried ...

Four alleles (24% of total allele diversity) were found in both wild and cultivated populations. Three of the four shared alleles (R, V, and Z) were recovered sporadically in wild populations, living fences, and backyard gardens in a region spanning from southern Mexico to Panama. Allele AC was found in wild and cultivated populations throughout Mesoamerica. This mosaic-like geographic pattern of shared alleles in cultivated and wild populations is consistent with the idea that genetically distinct individuals from different geographic regions were taken into cultivation and subsequently distributed by humans.

In most cases, the variation detected in cultivated populations is a subset of the total haplotype diversity recorded for a species (10, 6466). In S. purpurea, five haplotypes were found in cultivated populations but were not detected in wild populations. The presence of unique haplotypes in agricultural habitats may be the result of incomplete sampling of wild populations, or it may be the result of new alleles that have arisen in cultivation. Alternatively, it may reflect contemporary extinction of the tropical dry forests of Mexico and Central America and, consequently, the extinction of alleles carried by S. purpurea trees in these forests. Four of the five unique alleles were recovered from informal agricultural habitats. These data provide evidence for previous claims that traditional agricultural habitats may be acting as important reservoirs of genetic variation (6769).

The trnG–trnS Haplotype Network. The haplotypes recovered in S. purpurea trees were organized into haplotype networks based on their mutational differences (Fig. 2B). Two most parsimonious networks were identified. Both contain three homoplasious sites and are two steps shorter than the next most parsimonious network. Analyses were conducted with both networks, one of which is shown in Figs. Figs.2B2B and and4.4. The other most parsimonious network differed in the placement of the clade that included haplotypes AA, AB, S, Q, Y, and Z. In the alternative network, this clade was attached to haplotype O instead of haplotype R. The placement of this clade does not affect overall conclusions of this paper. The distribution of the trnG–trnS alleles (Fig. 2B) conform to the predictions of coalescent theory (70).

Fig. 4.
Geographic distribution of trnG–trnS alleles in cultivated and wild S. purpurea populations. (A) Distribution of trnG–trnS alleles in wild populations. Alleles found in wild populations fall in two groups: southern Mexico and Central America ...

The trnG–trnS spacer had 13 indels, each of which was coded as a single binary character following the six rules described in ref. 71 (see also refs. 72 and 73) (Tables 3 and 4, which are published as supporting information on the PNAS web site). One of the gaps (gap six) was mapped on the haplotype network twice (indicated with an asterisk on network, Fig. 2B). Of particular interest is the region from position 169 to 229, a series of three adjacent sequences (19–21 bp in length). The string of gaps created by the lacking nucleotides in this region were labeled 4, 5, and 6 (Table 4). Alleles recovered from wild and cultivated S. purpurea individuals contained nucleotides in some or all of the regions corresponding to gaps 4, 5, and 6, whereas those carried by S. mombin and S. radlkoferi individuals lacked nucleotides in this region. All alleles common in S. purpurea contained nucleotides at 169–188 (gap 4), and all but three had an insertion in gap 6 (210–228). The three alleles lacking sequence in gap 6 (O, P, and T) were carried exclusively by S. purpurea trees from wild populations in the states of Jalisco, Michoacan, and Nayarit in western central Mexico. In addition to their restricted geographic distribution and their absence from cultivated S. purpurea trees, the status of alleles O, P, and T as putatively primitive within S. purpurea is further substantiated by their interior status in the trnG–trnS haplotype network (see below for detailed discussion).

Distribution of Haplotypes in S. purpurea Populations. Ancestral haplotypes. Coalescent theory predicts that older alleles will occupy interior positions in the haplotype network (70). In the trnG–trnS network, haplotypes R, O, and P are the most interior haplotypes (Fig. 2B). These haplotypes were recovered from wild S. purpurea populations in western Central Mexico (Jalisco, Michoacan, and Nayarit; alleles O and P) and from wild populations in Guatemala and El Salvador (allele R) (Fig. 4A).

Multiple origins of cultivated S. purpurea. The trnG–trnS haplotype network reveals two groups of S. purpurea haplotypes, one centered in western Central Mexico and the other spanning from southern Mexico through Central America (Fig. 4 A and B). The first group comprises alleles recovered from wild and cultivated populations in southern Mexico and Central America (alleles Q, R, S, V, W, X, Y, Z, AA, and AB). The second group includes seven alleles, four of which were recovered exclusively in the wild populations of western Central Mexico (O, P, T, and AF). AC was the most common haplotype; it was detected in wild populations of western Central Mexico, as well as in cultivated and wild populations throughout Mexico and Central America. Alleles AD and AE were recovered from a backyard tree in Nicaragua and living fence in Guatemala, respectively.

Geographical Structuring. A nested clade analysis (NCA) was used to test for statistically significant associations between clades and geographical locations (refs. 59 and 60; but see ref. 74) (Fig. 4C). The NCA rejected the null hypothesis of no association between geographical location and clades for clades 1-6, 2-3, 3-1, and 3-2 (Fig. 4C and Table 2). Clade 1-6 included alleles in cultivated populations from El Salvador, Costa Rica, and Panama, and wild populations from southern Mexico (Chiapas) to northern Costa Rica. The null hypothesis was rejected for the next level of nesting as well (clade 3-1), which includes alleles found in cultivated and wild populations in southern Mexico and Central America. In addition, statistically significant results were obtained for clades 2-3 and 3-2, which include alleles found exclusively in wild populations in western Central Mexico (alleles AF, T, O, and P), a widespread allele found in cultivated and wild populations throughout the region (AC), and two singletons from Central America (AD and AE). The NCA provides statistical support for two distinct groups of S. purpurea haplotypes, corroborating the inference that S. purpurea was domesticated more than once in Mesoamerica.

Table 2.
Nested clade analysis for trnG-trnS alleles recovered in cultivated and wild jocote trees (S. purpurea)

Conclusions

This study provides phylogeographic evidence of multiple domestications of a cultivated fruit tree within the Mesoamerican center of domestication. Sequences of the chloroplast spacer trnG–trnS confirm that wild populations of the Mesoamerican tree S. purpurea are the likely progenitors of cultivated jocote trees. Our data reveal that trnG–trnS haplotypes detected in S. purpurea trees form two clusters, each of which includes haplotypes recovered in both cultivated and wild populations. One cluster spans the region from southern Mexico through Central America; the second cluster includes haplotypes from western Central Mexico, plus one widespread allele. A nested clade analysis detected significant associations between the mutational relationships and geographic localities of the alleles. Previous studies have suggested that various Mesoamerican species may have been taken into cultivation more than once within this center of domestication. Our study provides genetic evidence for this phenomenon, highlighting the importance of multiple domestications in the evolutionary history of Mesoamerican crops.

As a human-mediated evolutionary process, domestication impacts contemporary patterns of genetic variation in cultivated populations. At the trnG–trnS locus, >50% of the total genetic variation sampled was recovered in cultivated trees. The elevated levels of genetic variation in cultivated populations are consistent with vegetative propagation, multiple domestications, and ongoing distribution of domesticated alleles. Notably, five of the 17 haplotypes detected in cultivated S. purpurea trees (≈29% of the total variation at this locus in S. purpurea) were not recovered in wild populations. The presence of unique haplotypes in informal agricultural habitats (gardens, fences) provides support for traditional agriculture as an important reservoir of genetic variability in cultivated species when native populations of the wild ancestor are declining.

Supplementary Material

Supporting Tables:
Supporting Tables:

Acknowledgments

We thank members of the B.S. laboratory, Toby Kellogg, Gayle Fritz, Jason Knouft, and members of the Ranter laboratory (University of Colorado, Boulder) for helpful comments. Yu-Chung Chiang provided valuable assistance with analysis. Leaf material of Brazilian taxa was generously provided by A. Costello (Ross School, New York). We thank field collaborators R. Aguilar, A. Anzueto, G. Borjas, G. Carnevali, J. Castilla Canales, L. Chavez V., I. Diaz, A.-C. Gomez, A. Herrera, M. Diaz, A. MacVean, C. MacVean, M. Merello, A. Molina R., P. Moreño, A. Muehlenbachs, M. Olson, E. O'Mahoney-Cubbison, A. Paschke, E. Pimienta Barrios, B. Ramirez Hernandez, R. Rueda, R. Ruenes, N. Ventura, and B. Wong. This work was supported by National Science Foundation Grant PD 0105134, the Organization for Tropical Studies, the Botanical Society of America, the Andrew W. Mellon Foundation support of Missouri Botanical Garden graduate students, Washington University Division of Biology and Biomedical Sciences Graduate Fellowship, and a Danforth Foundation Grant to support undergraduates in plant biology research at Washington University.

Notes

Author contributions: A.M. and B.S. designed research; A.M. performed research; B.S. contributed new reagents/analytic tools; A.M. and B.S. analyzed data; and A.M. and B.S. wrote the paper.

Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ163952–DQ164096).

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