Origin Domestication and Dispersal Routes of Common Bean

Over a period of at least 7,000 years, the common bean has evolved from a wild-growing into a major leguminous food crop. During this period, which encompasses the initial domestication phase and the subsequent evolution under cultivation, evolutionary forces (mutation, selection, migration, and genetic drift) have acted on the raw material provided by wild-growing populations in Middle America and Andean South America. It is only since the late twentieth century that scientist have accepted a New World origin for the common bean and this was contrary to the belief in an Asian origin, which had been held for several centuries (Gepts and Bliss 1988; Gepts and Debouck 1991). Several common bean remains have been uncovered, not only in the Andes but also in Mesoamerica and North America consisting of seeds (Kaplan et al. 1973), pod fragments (Kaplan 1981) and even whole plants (Kaplan and MacNeish 1960) which date from 8,000 to 10,000 BP in the Andes and 6,000 BP in Mesoamerica. Dating methods have been recently the subject of much discussion among archaeologists for new world crops. The oldest records for common bean 4,300 years BP, revised using Accelerator Mass Spectrometry direct dating (Kaplan and Lynch 1999) is from Ancash, Peru, and 2,200 years BP for Puebla, Mexico, although much earlier dates have been repeatedly presented using radiocarbon indirect dating (Debouck 2000). These archaeological findings are phenotypically similar to current cultivars grown in the same area. Also, there are the historical and linguistic data as the sixteenth century Spanish texts mention the presence of the common bean in the Americas and the vocabulary (e.g., purputo) of several native Indian languages includes a specific word designating the common bean.

Thus, the common bean is a species of American origin derived from wild ancestors distributed from northern Mexico to northwestern Argentina (Gepts et al. 1986; Koenig et al. 1990; Toro et al. 1990; Payró de la Cruz et al. 2005) and was domesticated in two distinct regions of the New World, one in Mesoamerica and another along the eastern slope of the Andes in the South America (Gepts and Bliss 1985; Gepts et al. 1986; Gepts and Debouck 1991; Tohme et al. 1995; Chacón et al. 2005) (Fig. 7.2). The cultivated gene pools of common bean can be distinguished by their morphology and agronomical traits (Singh et al. 1991a), phaseolin seed protein electrophoretic type (Koenig et al. 1990); isozymes (Koenig and Gepts 1989; Singh et al. 1991b), molecular markers (Becerra-Velásquez and Gepts 1994; Haley et al. 1994; Freyre et al. 1996; Galvan et al. 2003; Chacón et al. 2005; González et al. 2005; Zizumbo et al. 2005; Blair et al. 2007; Lasry et al. 2007), and adaptation traits (Singh 1989; Voysest and Dessert 1991). Most cultivars from either the Middle American or the Andean region contain characteristics that are found in wild accessions from the same area, but not in wild accessions from the other gene pool (Koenig and Gepts 1989). Cultivars from Mesoamerica usually have small

Mapa Hispanoamerica Paises
Fig. 7.2 Distribution of the major gene pools of wild P. vulgaris L. in Latin America (Gepts et al. 1986), indicating two major domestications, in Mexico and in the Andes which led the two groups of cultivars with contrasting agronomic characteristics

(<25 g/100 seed weight) or medium-seeded (25-40 g/100 seed weight) and have a S and B phaseolin that differ from those of their South American counterparts, with large seeds (>40 g/100 seed weight) and T, C, H, and A phaseolin types (Gepts et al. 1986; Singh et al. 1991b). Six races (Singh et al. 1991c) have been proposed both for common bean from Mesoamerica (Mesoamerica, Durango, and Jalisco races) and from the Andean region in South America (Chile, Peru, and Nueva Granada races). In addition to these two major gene pools, recently discovered wild populations constitute a third gene pool ancestral in the evolution of wild common bean located in Ecuador and northern Peru (Debouck et al. 1993; Kami et al. 1995). These ancestral populations were not involved in domestication as shown by their phaseolin type, which is absent from the domesticated gene pool. Chloroplast DNA polymorphism data agree with other studies in supporting independent domestications in two regions and in demonstrating a founder effect associated with domestication. Andean landraces have been classified into three racial groups, but all share the same chloroplast haplotype. This suggests that common bean was domesticated once only in South America and that the races diverged post-domestication. Mesoamerican landraces have been classified into four racial groups (Beebe et al. 2000). The samples of races Jalisco and Guatemala differ from the races Mesoamerica and Durango in types and/or frequencies of haplotypes. Independent domestications of at least some of the races in Mesoamerica and/or conversion of some locally adapted wild beans to cultigens by hybridization with introduced domesticated beans, followed by introgression of the "domestication syndrome" seen the most plausible explanations of the chloroplast and other molecular data (Chacón et al. 2005).

During the evolution of common bean, some morphological, physiological, and genetically marked changes have occurred such as gigantism (seed, pod, stem, and leaves), suppression of seed dispersal mechanism, changed growth habit form (from climbing to dwarf plants), loss of seed dormancy, and photoperiodic sensitivity (Smartt 1988; Gepts and Debouck 1991). The divergence between the Andean and Middle American gene pools has implications for bean breeding that have not yet been fully explored (Blair et al. 2007). Despite their partial reproductive isolation (Singh and Gutiérrez 1984; Gepts and Bliss 1985; Koinange and Gepts 1992), the two gene pools still belong to the same biological species (Papa and Gepts 2003). Viable and fertile progeny obtained, and therefore, favorable genes alleles have been transferred between the two pools, although the transfer of quantitative traits such as seed yield appears to be problematic. Attempts to recombine desirable traits between both gene pools, such as the large seed size of the Andean gene pool with the yield potential of the Mesoamerican gene pool, have generally failed (Nienhuis and Singh 1986; Welsh et al. 1995).

Some limited bean germplasm exchange has taken place in pre-Columbian times between Mesoamerica and South America, but much more extensive seed movement occurred after the 1500s (Sonnante et al. 1994; Kaplan and Lynch 1999; Blair et al. 2007). Thus, outside the American centers of primary diversity one can identify several secondary centers which bean collectors should consider in search of diversity. The different genotypes found in these secondary zones were introduced from the Americas, either soon after the Spanish conquest or more recently. As secondary centers, one can tentatively suggest East Africa and Europe, since the Phaseolus beans were introduced in those regions by the Spaniards and the Portuguese in the sixteenth and the seventeenth centuries. Concerning the origin of the European beans, McClean et al. (1993) suggested that the germplasm dispersed to Europe was probably domesticated in the South American Andes since the Mesoamerican cultivars are not currently very popular in Europe. This suggests that, during crop expansion in Europe, sampling or selection favored the large-seeded races within the Mesoamerican S gene pool or possibly, introgression from Andean germplasm did occur. The domestication process may have excluded valuable genetic variability in the relation to adaptive characteristics, such as resistance to insects during storage and Rhizobium strain specificity (Acosta-Gallegos et al. 1998; Payró de la Cruz et al. 2005; Zizumbo et al. 2005). Gepts and Bliss (1988) suggested that the bean grown on the Iberian Peninsula was introduced from a different area (Chile) compared to those of the rest of Europe. Nevertheless, the introduction of beans in Europe is unclear and currently under discussion (Ocampo et al. 2005; Martins et al. 2006; Rodiño et al. 2006; Svetleva et al. 2006; Logozzo et al. 2007; Marotti et al. 2007).

Seed exchanges with Europe must have happened since the first visits of Europeans to the Americas. Sailors and traders, 500 years ago, could have brought the nicely coloured, easily transportable bean seeds with them as a curiosity, only for fun, as is often observed in the present day with children at home and school in the Andean region. Within Europe there was likely a quick distribution of seeds as curiosities (Zeven 1997). It is possible that the initial common bean accessions introduced in Europe (into Iberian Peninsula), were mainly from Mesoamerica around 1506 (Ortwin-Sauer 1966). There is evidence that common bean reached France in 1508, probably as an ornamental plant without value for human consumption in that time (Zeven 1997). Thus, because Columbus arrived in Central America, in reality in Cuba, in 1492 and Cortés reached Mexico in 1518, Castiñeiras et al. (1991) and Hammer et al. (1992) proposed the introduction of seeds from Cuba since 1492. In 1528, Pizarro explored Peru, opening the possibility to introduce common bean accessions from the Andes (Berglund-Brücher and Brücher 1976; Debouck and Smartt 1995). It was distributed widely in all part of Europe and the Mediterranean area where many landraces and varieties evolved that were grown to provide dry seeds or fresh pods. Zeven (1997) has found some descriptions of common bean as early as 1542 which indicate, in fact, the wide distribution of this species in Europe, starting obviously by means of its introduction in Spain by C. Columbus. No records of common bean earlier than 1543 have been found in NW European herbaria, suggesting that the common bean was distributed in NW Europe after 1540 and in 1669 it was cultivated on a large scale (Zeven 1997). Due to adaptation to new ecological and man-made conditions, a large diversity evolved in European germplasm that is of particular interest for plant breeding. There are evidences of seed exchange among farmers and gardeners in many countries of Europe for testing some new material or for avoiding the degeneration of cultivars sown year after year (Zeven 1999). Europeans still collect common beans from neighboring and faraway regions. Therefore, the species has undergone an adaptive evolutionary process in those regions for about 400 years, resulting in today's very important additional variation (Debouck 1988; Hidalgo 1988; Ocampo et al. 2005; Martins et al. 2006; Svetleva et al. 2006; Marotti et al. 2007).

In the sixteenth century there were harbors maintaining active commerce with the New World in the Northwest of Spain (Galicia). The introduction of some crops such as bean and maize and the distribution to other areas could have occurred in this area. The traditional cropping systems for the bean crop similar to those used in many areas of the Americas (Santalla et al. 1994) are strong arguments to support this hypothesis. The sensitivity to long day and low temperature during the growing season could have been a limiting factor for cultivated bean in many European latitudes in the early times. In fact, it is possible to grow primitive Andean landraces and wild populations in the North of Spain (Pontevedra, 42°N) but only under greenhouse conditions during the fall-winter-spring period (De Ron et al. 1999). Thus, subsequently new cultivars may have evolved within and between the two gene pools in Southern Europe (mainly Spain and Portugal) making this region a secondary center of diversity for the common bean (Santalla et al. 2002; Rodino et al. 2006). The consequential adaptation, occasional out crossing, cropping systems and strong selection for consumer preferences of seed types, might have played a significant role in arising of the new variation in the common bean of the Iberian Peninsula (Rodino et al. 2006). The introduction routes of African common bean cultivars are more difficult to ascertain. Whereas a majority of the cultivars ultimately originated in the Andes, it is not known by which route they were introduced. They could have been introduced directly from the Andes, indirectly through the Iberian Peninsula or through Western Europe during the colonial period. Because historical and linguistic information provide little evidence regarding the origin and dissemination of common bean in Europe and Africa, phaseolin protein pattern, an evolutionary marker (Gepts et al. 1986), was used to complement morphological and agronomic data. This phaseolin protein analysis was useful to identify gene pools and the origin of accessions to the Mesoamerican or Andean domestication centers.

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