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a Unidad de Recursos Naturales, Centro de Investigación Científica de Yucatán, Mérida, México
b Facultad de Ciencias Biológicas y Agropecuarias, Universidad de Colima
c Dep. of Agronomy and Range Science, Univ. of California, Davis, CA
* Corresponding author (zizumbo{at}cicy.mx)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Abbreviations: ISSR, inter simple sequence repeat • QTLs, quantitative trait loci
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Genetic compatibility between wild and domesticated populations leads to wild–weedy–domesticated hybrid complexes in sites with sympatric distribution by introgression of genes from wild populations to domesticated ones or vice versa. Weedy populations are defined here as wild populations growing in crop fields that were not planted by farmers. Because they may be the result of this introgression, they usually show morphological traits reminiscent of one or the other parent, such as larger seeds than the wild parent or seed color or color patterns similar to those observed in wild beans. These hybrid complexes constitute a valuable source of genes to the farmer or to the plant breeder (Debouck and Smartt, 1995; Beebe et al., 1997); however, at the same time they also represent a risk for the massive introduction of genes from the domesticated to wild populations (Gepts et al., 1999; Papa and Gepts, 2003).
Comparisons of wild and domesticated populations in their whole area of distribution indicate two main gene pools in which domestication took place (Becerra-Velásquez and Gepts, 1994; Debouck and Smartt, 1995; Gepts and Debouck, 1991; Koenig and Gepts, 1989; Tohme et al., 1996). One center of domestication is located in Mesoamerica and the other in the Andes. Studies on gene dynamics of wild–weedy–domesticated complexes within the Mesoamerican area of domestication are important, since four of the five domesticated species and 45 of the 50 species of the genus Phaseolus grow in this area, and their natural reproductive relationships are mostly unknown at present. Genetic bridges may exist between these species, as in the case reported by Escalante et al. (1994) regarding gene flow between wild populations of P. vulgaris and P. coccineus L.
Recent studies on wild populations of Mesoamerica, in areas where traditional agriculture continues, indicate that opportunities for wild–domesticated hybridization are common in spite of a predominantly autogamous reproductive system. They suggest that gene flow is asymmetric, at least three times greater from the domesticated to the wild, compared with the opposite direction (Papa and Gepts, 2003; Payró de la Cruz et al., 2005). Thus, a displacement of genetic diversity in wild populations because of gene flow from the domesticated populations can take place (Papa and Gepts, 2003). Farmers in traditional farming systems can have an influence on the magnitude and characteristics of gene flow by distancing the crop from the wild populations and by the management of diversity in domesticated landraces (Payró de la Cruz et al., 2005).
There is evidence that the domestication of P. vulgaris in Mesoamerica originated in the central western sector of Mexico, where the modern states of Jalisco, Michoacán, and Guanajuato meet (Gepts and Debouck, 1991). Primitive cultivars could have spread from this area to other regions where they crossed with local wild populations, giving rise to present day landraces (Gentry, 1969; Beebe et al., 2000). This area of possible domestication of common bean corresponds to the early frontier of Mesoamerica with Aridoamerica, in the southern portion of an old lakes system formed by the river Lerma. Some of the lakes were drained by the Europeans during the first hydraulic works of drainage and irrigation performed in the Americas around 1548, allowing the establishment of one of the most important regions of intensive agriculture in Mexico, known as El Bajío. Alongside this intensive agricultural area, on the slopes of the surrounding mountains, traditional agricultural systems are still practiced today in extremely stony soils of volcanic origin, without the possibility of irrigation or mechanization.
In this area, we find a climatic transition from subhumid to semiarid and vegetation varying from tropical deciduous forest to a forest of mesquite, Prosopis laevigata (Humb. et Bonpl.) Johnst. The average annual rainfall is around 700 mm, with a high coefficient of variation between years, close to 25%, with a high variation in the initiation and establishment of the rainy season, and with an intraseasonal dry period that is variable in intensity, amplitude, and date of appearance. Traditional agriculture, therefore, is performed with a high risk factor. As a consequence, the production rationale of the farmer focuses on securing the harvest using plant genetic resources with a high diversity of response (Zizumbo-Villarreal et al., 1988). Within this area, evidence has been found of agricultural villages dating back to the Preclassic period (800–100 BCE) (Branniff, 1975; Oliveros, 1975). At present in this area, there is a high incidence of seasonal migration of farmers to the USA, where some of them work in the cultivation of bean. Occasionally, these farmers incorporate varieties from the USA in their crops (Zizumbo-Villarreal, 1985).
According to Zizumbo-Villarreal (1985), three main types of agriculture are practiced in this area, each one in a different agro-ecological condition.
The aims of this work were (i) to analyze the morphological variation, diversity, structure, genetic flow and evolutionary relationships within and among three wild–weedy–domesticated complexes of P. vulgaris growing under traditional agricultural systems in the El Bajío region, Mexico, in addition to one wild population isolated from crops in the same region; (ii) to compare their levels of diversity with the diversity of a local commercial variety and a breeding line, both cultivated with modern technology; and (iii) to analyze the role played by farmers in the present evolutionary dynamics through selection and agronomic management.
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MATERIALS AND METHODS |
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Diversity, Genetic Structure, Gene Flow, and Evolutive Relationships
Diversity and genetic structure were evaluated by polymorphism for ISSR markers, which is a dominant molecular marker. An average of 20 individuals was used per population, chosen at random among the individuals that were evaluated morphologically. Domesticated individuals were analyzed without identification of the landrace to which they belonged. The genomic DNA was obtained from young leaves by the CTAB method (González et al., 2005) and three ISSR primers [(GACA)3 RG, (GACAC)2, and (GA)8 RG] were used that had been reported to be highly polymorphic (González et al., 1988). Each 20-µL amplification reaction consisted of 10 mM Tris-HC1 (pH 9.0), 50 mM KCI, 0.1% (v/v) Triton X-100, 2 mM MgC12, 200 µM each dNTPs, 1 µM of primer, 1 unit of Taq polymerase (Promega, Madison, WI) and 50 ng of template DNA. Amplification was performed in a GeneAmp PCR System 9700 (Applied Biosystems, Foster City, CA) following the conditions established by González et al. (2005). The fragments of DNA generated were separated by electrophoresis (Hoefer SQ3 sequencer, Amersham Pharmacia Biotech, San Francisco, CA) in 320- x 380- x 0.4-mm gels containing 5% (w/v) of nondenaturing 29:1 acrylamide-bisacrylamide (González et al., 2005). Visualization of the fragments was performed by means of silver nitrate staining with the modifications reported by Bassam et al. (1991) and Creste et al. (2001).
Data were scored as presence and absence of bands and analyzed as diploid data for dominant markers by standard POPGENE 1.31 (Yeh et al., 1999) procedures for summary multilocus genetic statistics: percentage polymorphic loci (%) in the populations within complexes, in the populations of the same type across the complexes, and in the whole sample, Nei's (1973) genetic diversity (h) and Shannon's information index (I) (Lewontin, 1972) for populations within complexes, genetic structure for populations within complexes and for populations of the same type across complexes [total diversity (Ht), intrapopulation diversity (Hs), population differentiation (Gst) (Nei, 1987)], and homogeneity tests of gene frequencies across populations within each complex (Sokal and Rohlf, 1995). Since some studies have demonstrated high levels of autogamy in the common bean and others have demonstrated allogamy when pollinators are abundant (Brunner and Beaver, 1989; Triana et al., 1993; Ibarra-Pérez et al., 1997), the statistics just mentioned were calculated twice: assuming Hardy-Weinberg equilibrium (H-W) (Fis = 0) and assuming autogamy (Fis = 0.95) to decide which assumption should be made under our study conditions. As most estimators were different under both assumptions, the values presented here were those obtained under the assumption of autogamy (H-W disequilibrium). Gene flow (Nm) was estimated indirectly by calculating the number of migrants from Gst (McDermott and McDonald, 1993), since this estimator considers the combined effects of flow of genes (by means of pollen or seeds) and its selection in a large number of populations over a wide temporal scale (Slaktin and Barton, 1989). It was estimated among populations within each complex and among populations of the same type from different complexes, considering that even though complexes were in different valleys, seed movement by humans may have occurred. Results were the same when analyzed as haploid data, assuming total autogamy, as Papa and Gepts (2003) assumed in a study of this same species.
A dendrogram based on Nei's genetic distance (1972) using UPGMA (Unweighted Pair Group Method with Arithmetic Means). Swofford and Olsen (1990) was computed by the TFPGA program (Tools for Population Genetic Analyses; Miller, 1997) using the bootstrapping option for 1000 permutations (Felsestein, 1985), which reports the proportion of permuted data sets that result in the formation of the node seen in the original data set.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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In years when the production of domesticated populations is low, the seeds from weedy plants are harvested and consumed, which was the case in the year this study was performed. The farmers' wives mentioned that weedy seeds cook very slowly and heterogeneously; however, they are appreciated because they help to complement the food requirements for the family. The wives also mentioned that the consumption of these seeds is considered socially demeaning. The farmers store part of the harvest for planting the following year. The infected or damaged seeds are eliminated before planting, and the landraces mixed together are once again cultivated.
Morphological Variation of the Seed
Significant differences were found in seed mass among wild bean populations (6 g/100 seeds), weedy bean populations (20 g/100 seeds), and domesticated bean populations (39 g/100 seeds) (Table 2). Similar results were presented by Delgado-Salinas et al. (1988) and Tohme et al. (1996).
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The homogeneity test indicated a high percentage of alleles with different frequencies among the populations of each complex (P < 0.05): Tupátaro 62%, Yuriria 57%, and Jéruco 54%, which suggests high autogamy in these populations. The values of Hs and Ht were positive and different from zero within the complexes, also indicating effects of autogamy (Table 6). These results are reflected in the high values obtained for the average genetic structure of the three complexes (Gst = 0.31), for which the Tupátaro and Jéruco complexes showed the greatest genetic structure (Table 6). Thus, between 26 and 34% of the diversity observed is explained by the genetic differences among the populations within each complex.
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UPGMA analysis indicated a small genetic distance between the weedy and domesticated populations from each complex, grouping them together with a support between 0.73 and 0.99 for 1000 permutations (Fig. 4). Wild populations of Tupátaro and Yuriria grouped together with the wild population of San Agustín, which was isolated from bean crops, with a support of 0.54, whereas the wild population from the Jéruco complex, the one closest to the crop field, clustered with the domesticated and weedy population from the complex, although with a weak support of 0.32 (Fig. 4).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Diversity of domesticated populations within the complexes is positively related to the number of landraces in the mixture sown. Zizumbo-Villarreal (1985), in a study of the traditional agriculture in one of the locations included in the present study (Yuriria), found that this number is the result of a balance struck by the farmer between his need to confront the variability and adversity of the agroecological conditions under which he cultivates and his need to obtain cash through the sale of bean seeds in the local markets. Planting a high number of landraces with different ecological requirements permits him to have some harvest regardless of the annual growing conditions. At the same time, he needs to reduce this number and plant only those landraces that fetch high market prices. This is what we found in the three locations studied: Tupátaro (farmer Ignacio Fernández with 11 landraces) is the town with less dependence on the markets and Jéruco (farmer Nicolás Rico with 5 landraces) with the greatest.
Although the presence of Cacahuate landraces, which may be of Andean origin, could inflate the genetic diversity of domesticated types, this is unlikely to have a major effect since Cacahuate was but one of several components grown by the three farmers: Melo: 1/8; Fernández (1/11); and Rico (1/5). Furthermore, one of the goals of this research was to investigate the possible role of farmers in the maintenance of genetic diversity, regardless of the evolutionary origin of the landraces, which is actually unknown to the farmers.
The lower geographic differentiation among the domesticated populations across the complexes (Gst = 0.26) compared with the value for the wild ones (Gst = 0.40), and the higher value of gene flow among domesticated populations across the complexes (Nm = 1.4) compared with the value for the wild populations (Nm = 0.77) support our hypothesis that landraces are actively exchanged by farmers. Papa and Gepts (2003) also observed lower levels of spatial autocorrelation in domesticated populations compared to wild populations in Mexico, consistent with a lower level of geographic differentiation in the former compared with the latter. Furthermore, by protecting the weedy populations within the cultivated plots, the farmers further encourage the formation of hybrids and backcrosses. In contrast, the genetic diversity of the local commercial variety cultivated under modern agricultural technology was between two and four times lower than that of the domesticated populations cultivated under traditional agriculture. This is even more noticeable in the breeding line cultivated in monoculture, whose diversity was between four and nine times lower. This has considerable importance for the design of germplasm collecting strategies for ex situ conservation programs, which must focus on collecting in the traditional agroecosystems instead of in local markets, to achieve representativeness of the diversity of domesticated populations.
The high level of autogamy suggested by the high percentage of alleles with different frequency among populations within the complexes, in spite of gene flow values close to one, could be a result of a strong negative farmer selection of cultivated plants with morphological characters suggesting introgression. Similar gene flow values were observed between wild and domesticated populations in Chiapas, and evidence that the selection of alleles of the domestication syndrome is the evolutionary mechanism that maintains the identity of wild and domesticated populations in sympatric situations (R. Papa and P. Gepts, unpublished data).
The UPGMA dendrogram indicates that, in the Jéruco complex, where the geographic distance between the wild and the domesticated population is the smallest (10 m), the wild population grouped with the domesticated and the weedy populations, also differentiating it from the other wild populations of the region. This observation suggests that gene flow from domesticated to wild populations has decreased the genetic distance between wild and domesticated types at Jéruco, presumably by displacement of the wild genetic diversity in wild populations, as indicated by Papa and Gepts (2003). These authors found that the gene flow is asymmetric, three to four times greater from domesticated to wild, which could be explained by the greater size of the domesticated populations and a greater adaptation of the hybrids to the natural environment promoted by the dominance of the wild phenotype. Payró de la Cruz et al. (2005) reported a negative correlation between the wild–domesticated distance and the genetic diversity in wild populations, with the exception of the wild population in the Jéruco complex. They argued that the genetic diversity of the nearest domesticated population was probably low. The results presented in this study further support this assumption. The genetic diversity of the nearest domesticated population was low and similar to that of the wild population (h = 0.13).
The high genetic differentiation of populations within the complexes is explained mainly by the genetic distance from the wild to the domesticated population, the farmer selection of seeds generation after generation, and the effects of natural selection in two contrasting environments. The smaller weedy–domesticated genetic distance can be explained by the selection performed by the farmer for domesticated traits in both types of populations, by similar selection pressures in the domesticated plot, and predominant gene flow from domesticated to wild-types.
The wild populations of Yuriria and Tupátaro, separated from the domesticated population by 25 to 60 m, showed high genetic similarity with the wild population of San Agustín, isolated from bean crops, indicating that the gene flow from the domesticated population to the wild has not been sufficiently high to result in a grouping with their respective domesticated populations. The data mentioned above indicate, therefore, that the geographic distance between domesticated and wild has a strong influence on the level of genetic infiltration and is a factor of great importance for in situ conservation.
Origin of Weedy Populations
The analysis of variance of seed mass (Table 2) suggests that the weedy populations are a product of genetic infiltration between wild and domesticated populations, since they present an intermediate seed mass between wild and domesticated and a high coefficient of variation in this character. These results concur with those suggested by Delgado-Salinas et al. (1988) on the basis of the purple coloring of the flowers and pod dehiscence in weedy types, characters which are found in wild populations. The short genetic distance obtained between domesticated and weedy populations suggests, in effect, that they were indeed derived from hybridization between wild and domesticated populations, as indicated by Papa and Gepts (2003). The hybrid character of the weedy types was demonstrated by Beebe et al. (1997) on the basis of the segregation of wild and domesticated characters in weedy types. The cases in which this segregation did not occur were explained by Beebe et al. (1997) as resulting from character fixation due to a historic selective process by humans.
The Role of the Farmer in the Evolutionary Dynamics
The protection of wild populations in the plots by traditional farmers can lead to hybridization of wild and domesticated populations, thereby generating weedy plants. In the same way, this protection favors backcrossing of weedy with domesticated plants and subsequently the establishment of segregants with high morphological similarity to the domesticated. These segregants are harvested and eventually returned to the plots in the next agricultural cycle. As the harvesting of weedy types is not particularly exhaustive, some of these escape and disperse naturally, appearing in the same way in the following agricultural cycle. The harvesting and storage of weedy plants in close proximity to seeds from domesticated plants in the barns, may also allow the weedy seeds to return eventually to the plot and to be cultivated inadvertently. In this way, the farmer himself has facilitated the existence of genetic complexes. The management of geographic distance between wild and domesticated populations, the selection and management of domesticated diversity, and farmer tolerance and harvesting of weedy populations, are traditional agricultural practices that influence the magnitude and characteristics of gene flow in wild–weedy–domesticated complexes, and which have made recurrent evolutionary processes possible after the initial domestication in the Mesoamerican area.
Under these conditions, how could the Mesoamerican farmer isolate the desired characters involved in the domestication syndrome, with the presence of both wild and domesticated populations within outcrossing distance? Probably, the mechanisms involved in the asymmetry of wild–domesticated gene flow permitted this. Harvesting before pod dehiscence to avoid the loss of seed and selection of large, white or light-colored seeds, could have had an influence on the process of reproductive isolation. Selection of precocious plants with early and short periods of pollen receptivity and seed production as well as attractiveness to insects (white flowers) may have limited gene flow from wild to domesticated types.
Conservation In Situ
Bean breeding and germplasm conservation programs require new approaches to achieve an increase in productivity and adaptation of the domesticated gene pool through the use of genes from wild and weedy populations (Singh et al., 1995; Beebe et al., 1997; Mauro Herrera, 2003). The in situ conservation of the wild–weedy–domesticated complexes within the traditional agricultural systems, where the farmers are producing advanced generations of wild–domesticated hybrids, could be an important approach to achieve this goal. The importance of weedy seeds for the survival of traditional farmers is a factor that has permitted and facilitated their presence in the agricultural system and the continuity of genetic relationships between the populations that form the wild–weedy–domesticated complexes. Our results also encourage further emphasis on both ex situ and in situ collections of common bean and other crops. For ex situ collections, the current Phaseolus world collection at CIAT (Colombia) contains some 25000 domesticated accessions of P. vulgaris but only some 1200 accession of wild P. vulgaris. Wild populations that have been the object of gene flow studies conducted recently on common bean, including this one, are not well represented in ex situ collections. Thus, more intensive exploration and collection of wild populations are warranted. For in situ conservation, our results suggest that increased efforts should be placed on the conservation of wild populations in more remote areas. Diversity in wild populations is very localized so its conservation is difficult and should include farmers' participation under a strategy that evaluates economically their agricultural products from an economic standpoint, to decrease economic pressures to extend the cultivated areas, eliminating wild populations or planting domesticated beans too close to them.
One important survival strategy of the traditional farmers in the study area has been the incorporation of exogenous varieties to their crops as a test; the idea being to test both their adaptive capacity to the traditional agricultural systems and consumer preferences. These varieties have come from places as far away as the Central Valley of California, brought back by temporary migratory workers (Zizumbo-Villarreal, 1985). Both the introduction of new varieties and the maintenance of hybrid forms and their segregants could be favored by the farmers, thereby complicating the conservation of the genetic resources of wild populations in situ.
Under the technological and socioeconomic conditions in which traditional agriculture is performed, should new genes be introduced, the deployment of new cultivars, whether transgenic or not, could signify the introduction of these new genes into local landraces and wild populations, given the intense interchange of seeds among peasant farmers and the practice of cultivating various types of seeds, even in spite of limited genetic flow. Phaseolus vulgaris has been already transformed (Russell et al. 1993; Aragão et al., 1996, 1998, 1999, 2002) and the first field trials of transgenic beans have been approved in Brazil. Thus, it is just a matter of time before such beans might be introduced to other countries. Availability of the data presented here suggests that although common bean is a selfing species, genes from domesticated beans (including transgenes) will be introduced in other populations, whether wild or domesticated. Whereas wild populations that are more distantly located from domesticated ones are less affected by gene flow, they tend to be less frequent. Thus, wild populations closer to cultivated fields, which are more abundant, will suffer the brunt of the impact of gene flow. On the other hand, gene flow estimated by Nm considers the combined effects of flow of genes (by means of pollen or seeds) and its selection in a large number of populations over a wide temporal scale. This study shows low influence of domesticated populations on wild ones but this result could be influenced by a low adaptive value of the domesticated alleles. Other genes that could be introduced (including transgenes) may have a higher adaptive value and eventually persist in the wild populations.
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ACKNOWLEDGMENTS |
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Received for publication June 2, 2004.
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s). Annu. Rep. Bean Improv. Coop. 41:99–100.Related articles in Crop Science:
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