Quinoa. Atul Bhargava

farmers along the Andes of South America took the first steps in domesticating quinoa from its wild or weedy forms in a domestication/cultivation period of approximately 5000 years. In this context, quinoa has been subjected to diverse selection processes for desirable traits for its cultivation and consumption by people belonging to different cultures and territories in South America, such as Chibchas, Andaki, Inganos in southern Colombia; Aymara and Quechua in areas of Peru, Bolivia and northern Chile; Diaguitas and Calchaquies in northern Argentina; and Mapuches in southern Chile (Mujica, 2004). This process, conducted in multiple local landraces, led to the loss of many allele combinations that were disadvantageous to farmers, such as dehiscent seeds (seed shattering) and thick seed coats, as well as the gain of useful ones such as increased seed size and environmental adaptations. Similarly, modern breeding procedures have also continued this process by crossing the best phenotypes to increase yields and agronomic performance and, thereby, narrowing the genetic diversity of quinoa in a wide sense. Nevertheless, the diversity can still be observed in the fields in a wide array of colours in plants and seeds, and differences in the types of branching and panicles, as well as having differences in grain productivity, abiotic stress tolerance and disease resistance (Fuentes and Bhargava, 2011; Ruiz-Carrasco et al., 2011) (Fig. 2.1).

      Fig. 2.1. Morphological variation in C. quinoa: (a) Lax panicle of quinoa in Salta, Argentina. (b) Compact panicle and colour variation of quinoa in Peru. (c) Glomerulate panicle of quinoa in Bolivia. (d) Amaranthiform panicle of quinoa in Salta, Argentina. (e) Glomerulate panicle of yellow quinoa in Temuco, Chile. (f) Semi-amaranthiform panicle of quinoa in Pichincha, Ecuador. (g) Representative quinoa seeds from highlands Chile (north). (h) Representative quinoa seeds from coastal/lowland Chile (south).

      Quinoa diversity, at a continental scale, has been associated with five main ecotypes: Highlands (Peru and Bolivia), Inter-Andean valleys (Colombia, Ecuador and Peru), Salares (salt lakes; Bolivia, Chile and Argentina), Yungas (Bolivia) and Coastal/Lowlands (Chile); each of these are associated with sub-centres of diversity that originated around Lake Titicaca (Risi and Galwey, 1984). In the beginning, Gandarillas (1979) and Wilson (1988) identified the southern highlands of Bolivia as the genetic diversity centre for quinoa. Subsequently, Christensen et al. (2007), using SSR (simple sequence repeats) markers, identified the genetic diversity centre in the Altiplano area between Peru and Bolivia (Central Andean highlands). Germplasm from Ecuador and Argentina in the same study showed limited diversity, indicating that the most probable point of introduction for Ecuadorian accessions was the Altiplano (Peru–Bolivia), while for Argentina the original introduction could have been from the Chilean highlands and coastal zone (south of Chile) (Fig. 2.2). In addition, Christensen et al. (2007) highlighted the differences between coastal/lowlands accessions from Chile and those from the northern highlands of Peru, confirming the hypothesis proposed by Wilson (1988) that quinoas from Chile show more similarity with quinoas from the southern Altiplano of Bolivia. Nevertheless, Fuentes et al. (2009), while assessing genetic diversity on Chilean germplasm using SSR markers, reported for first time that Chilean coastal/lowland germplasm was much more genetically diverse than was previously believed. This finding was consistent with a cross-pollination system in the coastal/lowland quinoa fields with weed populations of C. album and/or C. hircinum and agrees well with the difficulty experienced by coastal/lowland quinoa breeders to obtain pure new cultivars in south-central Chile (I. and E. von Baer, personal communication). Taken together, the recent genetic-based analyses are consistent with the idea that quinoa itself has existed until now as two distinct germplasm pools: Andean highland quinoa with its associated weedy complex (ajara or ashpa quinoa, C. quinoa ssp. milleanum Aellen, also referred to as C. quinoa var. melanospermum Hunziker) and kinwa among the Mapuche people of the central and southern Chilean coastal/lowlands, representing in addition a second centre of major quinoa diversity (Jellen et al., 2011). Interestingly, the weedy C. hircinum from lowland Argentina can be mentioned as a third distinct germplasm pool, which may represent remnants of archaic quinoa cultivation in that part of South America (Wilson, 1990).

      When quinoa was originally classified in 1797, it was assumed to be an exclusively domesticated species in a section of the genus from the New World. In 1917 other important cultivated tetraploid chenopods were discovered in Central America (Wilson and Heiser, 1979). These plants were originally classified by Safford as C. nuttalliae, consisting of three different cultivars: huazontle, red chia and quelite. From its original classification, these plants have been reclassified several times, including a period in which they were considered conspecific with quinoa. These species are part of the complex of C. berlandieri, commonly known as C. berlandieri var. nuttalliae (Wilson and Heiser, 1979), including some extinct subspecies (subsp. jonesianum for example) that have been identified in several archaeological sites in the east of North America (Smith and Funk, 1985; Smith and Yarnell, 2009). Although it is widely accepted that these species share a common gene pool with quinoa, several studies have pointed out that it is likely that they were grown independently (Heiser and Nelson, 1974). Since systematic genetic research on quinoa began at the end of 1970s, it was believed that quinoa originated in South America from diploid descendants from the highlands such as C. pallidicaule Aellen (Kañawa), C. petiolare Kunth and C. carnasolum Moq., as well as from tetraploid weed species from South America such as C. hircinum Schard, or C. quinoa var. melanospermum (Mujica and Jacobsen, 2000). An alternative hypothesis, originally raised by Wilson and Heiser (1979), is that quinoa descended from the tetraploid C. berlandieri in North America. However, when the Mexican complex of C. berlandieri was described, it was considered conspecific with quinoa. Thus, the prevalent paradigm is whether C. quinoa comes from early tetraploids of C. berlandieri; most probably C. berlandieri var. zschackei, considering that domesticated Mexican tetraploids descend from C. berlandieri var. sinuatum. This idea has been supported by diverse studies based on morphological, experimental crosses, isozymes and genetic analysis (Heiser and Nelson, 1974; Wilson and Heiser, 1979; Wilson, 1980; Walters, 1988; Maughan et al., 2006). If this hypothesis is correct, it could be indicated that the tetraploid origin of C. quinoa is in North America, from an ancestor similar to C. berlandieri var. zschackei. If so, it is possible that this wild North American tetraploid progenitor travelled to Mexico and South America through human migration or by longdistance bird dispersals, probably as C. hircinum, and was subsequently domesticated as quinoa (Wilson, 1990).

      Fig. 2.2. Model of biodiversity dynamics of quinoa associated with the five ecotypes in the Andes: (a) Inter-Andean Valley (Ecuador–Colombia). (b) Yungas (Bolivia). (c) Highlands (Peru–Bolivia–Argentina). (d) Salares (northern Chile–southern Bolivia). (e) Coastal/lowland (southern Chile). Arrows show most likely seed migration routes, as inferred from genetic similitude and from ancestral people’s interactions and cultural exchanges. [Reprinted from Fuentes et al. (2012), with permission from Cambridge University Press.]

      Archaeobotanical studies based on patterns of seed morphology and frequencies of C. quinoa and its associated weedy complex have shown interesting perspectives to support Wilson’s hypothesis. Studies conducted by Bruno and Whitehead (2003) have shed light on some processes contributing to the development of agricultural systems between 1500 BC and AD 100 in the southern Lake Titicaca Basin (Bolivia). The results of this study suggest that during the Early Formative period, farmers maintained small gardens where both the crop and weed species were grown and harvested. However, around 800 BC there was a drastic decrease in frequency of weedy seeds compared with quinoa seeds, revealing a significant change in crop management and use. This suggests that in the Middle Formative period farmers became more meticulous cultivators of quinoa, perhaps through weeding, careful seed selection and creating formal fields for cultivation. Although there have been an increasing number of