1. Clonal and sexual reproduction interact to shape evolutionary dynamics
As in wild ‘clonal’ plants (Eckert, 2002; Gabrielsen & Brochmann, 1998; Mock et al., 2008), the frequency of sexual reproduction and its impact on patterns of genetic diversity in clonally propagated crops have often been underestimated (McKey et al., in press). Whether sex is still important in crop populations today depends largely on whether farmers incorporate sexual progeny into their stocks of vegetative propagules. This practice is common in many ‘traditional’ farming systems (which we may define as those in which farmers produce their own ‘seed’ for the next generation), and has probably been continuous from the origin of domestication up to the present time. In such crops, a mixed clonal/sexual reproductive system persists and the crop population consists of two interlinked compartments: clonally propagated plants and sexually produced plants. In the long run, farmer management of these two compartments shapes the evolutionary processes presented above. Examining the genetic and ecological dynamics of mixed clonal/sexual systems at small scales of space and time gives insight into these long-term processes.
Sex is incorporated into the cultivation cycle when farmers decide to propagate clonally ‘volunteer’ (spontaneous) plants, issued from sexual reproduction, that appear in their fields, in fallows, or in secondary forests. Farmers observe young seedlings and may decide to spare them from weeding, and in some cases (e.g. cassava seedlings in Vanuatu; D. McKey, pers. obs.) they actively transplant seedlings to locations where they can grow better or simply be more conveniently observed. Farmers can thus select, and then multiply clonally, advantageous variants resulting from recombination, and benefit from the advantages of each reproductive system while minimizing their disadvantages.
Although the mating system of most clonally propagated crops is documented, their sexual reproductive ecologies are poorly known. We know that in aibika (Abelmoschus manihot), ensete (Ensete ventricosum), potato, sweet potato, taro, guinea yam (Dioscorea rotundata) and cassava, farmers in traditional systems incorporate plants originating from seeds into the stock of clones (McKey et al., in press). However, we know next to nothing about the ecology and genetics of this process. What insects pollinate these plants, and what mating systems result from the interaction of their behaviour, farmers’ planting practices, and the plant’s reproductive traits? How diverse is the compartment of volunteer seedlings, and what selective forces act on it? How and when do farmers decide what plants to incorporate? How, and how far, are seeds dispersed, and can they remain dormant in the soil? We usually have no answers to these questions, but they are crucial, and the answers certainly vary among crops (McKey et al., in press).
2. A well-studied example: cassava
In only one clonally propagated crop, cassava, has reproductive ecology been studied in some detail. The results of this work, carried out in fields of Amerindian farmers in Amazonia, have been synthesized and discussed elsewhere (McKey et al., in press; Rival & McKey, 2008), and will be only briefly summarized here. This crop, whose starch-rich tuberous roots provide the staple food for more than 600 million people throughout the tropics, is propagated by stem cuttings. Most varieties of cassava have retained sexual fertility, with farmers regularly incorporating ‘volunteer’ plants from seeds into the stock of clonal landraces (Elias et al., 2000, 2001b).
Fig. 6(a) describes the mixed clonal/sexual reproductive system of cassava in Amerindian fields. Sexual reproduction begins when insects (mostly stingless bees; D. McKey, pers. obs.) pollinate the plant’s flowers. While unisexual flowers and protogynous inflorescences limit self-pollination in this self-compatible preferential outcrosser, they do not exclude it. When the fruit matures, it dries and dehisces explosively, scattering seeds on the ground up to several metres from the mother plant. Ants then play a crucial role in the plant’s reproductive ecology: attracted by the seed’s caruncle, ants transport and bury seeds in their nest or in refuse heaps nearby (Elias & McKey, 2000). Thus is formed a soil seed bank, in which seeds can remain dormant for up to dozens of years. Dormancy is physiological and based on thermal cues. Seeds remain dormant if vegetation cover maintains soil temperatures around 25°C (as during fallow periods), and germinate if the vegetation cover is removed by a disturbance, such as field clearing and burning, that heats the soil. Cassava’s dormancy system was inherited from its wild ancestors, which are adapted to periodic disturbances, often fire, in forest-savannah ecotone habitats (Pujol et al., 2002). Seedlings thus emerge when a farmer opens a new field by clearing and burning an old fallow and plants stem cuttings. Young plants in the field are a mixture of planted clones and recombinant genotypes issued from sexual reproduction. Amerindian farmers can easily distinguish plants derived from seed from those derived from stem cuttings (e.g. by the shorter basal internodes of the former), even when plants become very large. Farmers observe volunteer plants with interest, spare them when weeding and allow them to grow. Those that survive to harvest time are examined, and some are incorporated into the stock of clonal propagules, each usually being assigned by the farmer to the landrace it most resembles (Duputiéet al., 2009; Elias et al., 2001a). Each landrace is thus a diverse assemblage of multiple clones sharing phenotypic characteristics.
Figure 6. Life cycles of clonal crops under mixed clonal/sexual reproduction. The case of cassava is exemplified here. (a) Cultivation cycle of cassava begins with the opening of a new field, which triggers seedling germination at about the time that clonal propagules are planted. Seedlings endure several steps of natural and artificial selection, and reach sexual maturity at the same time as the plants issued from cuttings. Sexual reproduction takes place freely and results in the formation of a bank of dormant seeds, which will germinate at the beginning of the next cycle (which may be decades later). Farmers then harvest the tuberous roots and make stem cuttings for further propagation in a different field, and the frequency of each clone will be different in the next crop generation. Plants issued from sex that attract the interest of farmers may also be selected for propagation. (b) Evidence of seedling selection during the cultivation cycle. The first graph shows the schematic distribution of multilocus heterozygosity in established clones (dashed black line). Subsequent graphs show multilocus heterozygosity in established clones and in seedlings (grey line) at germination, after weeding and after mortality resulting from competition among seedlings. Throughout the cycle, both very inbred and very outbred seedlings are selected against, and the multilocus heterozygosity of the seedling compartment tends towards that of the compartment of established clones.
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Long-established clones are highly heterozygous, while plants originating from seeds are characterized by high variance in the degree of inbreeding (Pujol et al., 2005a; Fig. 6b). Indeed, landraces are planted in monovarietal patches: intra-patch crosses are highly inbred, while inter-patch crosses are outbred. Both natural and artificial selection favour outcrossed, highly heterozygous volunteer plants, which are larger than inbred ones. During weeding, early in the cultivation cycle, farmers unconsciously remove small volunteers, which are too small to be distinguished amidst other adventitious plants (Pujol et al., 2005a). Later in the cultivation cycle, intraspecific competition among volunteers is the major source of mortality, striking smaller volunteers (Pujol & McKey, 2006; Fig. 6b). Finally, at harvest time farmers select from among surviving volunteers those that display interesting agronomic qualities, and prepare from them stem cuttings that will serve as propagules for the next generation. Throughout the cultivation cycle, the decreasing number of survivors are increasingly outbred, coming to resemble established clones in this respect (McKey et al., in press; Fig. 6b). Of course, in the approximate process of natural and artificial selection, some favourable genotypes are eliminated and some less favourable genotypes survive, as a result of chance and environment-related variation. Selection during the first cycles of clonal multiplication should weed out new recombinant clones whose incorporation was a result more of chance than of a favourable genotype (Duputiéet al., 2009).
By allowing (and contributing to) selection against inbred volunteers, farmers solve one of the major problems associated with sexual recombination in this clonally propagated crop. Because volunteer plants constitute only a small fraction of all the plants in the field, and because farmers invest no time in managing them, the high selective mortality in this compartment imposes a negligible cost to the farmer. With the problem of inbreeding depression thus cheaply solved, and the diversity-generating advantage of sex fully exploited by selective incorporation of new variants, sexuality of the crop continues to provide advantages to farmers. The importance of sex in the crop’s life cycle is shown by the fact that seedling morphology has evolved under domestication, allowing faster initial growth of the seedlings (Pujol et al., 2005a,b).
Amerindian cassava fields in some ways resemble breeding programmes that use backcrosses to selectively add new favourable genes to already ‘elite’ genotypes (Cooper et al., 2001). These farms thus combine two functions – production today and the generation of new genotypes that will ensure continued adaptation and production tomorrow – that are usually performed by separate populations (in fields and in breeding stations, respectively) in ‘modern’ agriculture.
Cassava is so far the only clonal crop for which we have much information on how mixed clonal/sexual systems work. Scattered information from other crops suggests that many of the features discussed above may be quite general, but that there is also interesting variation among crops (McKey et al., in press). For example, in guinea yam the great difference in the environments experienced by established clones (farms) and by volunteer seedlings (secondary forest of old fallows nearby) could have a profound impact on many traits, among them the overarching trait of phenotypic plasticity, which must be considerable if a single genotype is to survive such divergent environments at different stages of its life cycle (McKey et al., in press). Differences in techniques of clonal propagation also lead to variation in how mixed clonal/sexual systems function. In the many fruit-bearing trees and vines propagated clonally by grafting, populations may include nongrafted plants (often ‘wild’ or feral plants from seed), some of which are used as rootstocks for the clonally propagated landraces (Janick, 2005). Intrapopulation genetic diversity might thus present very different patterns between rootstock and graft compartments. Such possibilities, and their potential consequences for population functioning, appear not to have been investigated. However, as early as Roman times there are records of specific easily rooted apple (Malus pumila) rootstock landraces, clonally propagated like the fruit-bearing landraces (Janick, 2005). ‘Modern’ cropping systems routinely employ improved rootstock cultivars, distinct from fruit cultivars, in crops such as grapevine and apple.
Given such diversity in the functioning of mixed clonal/sexual systems across different crops, their comparative study offers rich scope for advancing our understanding of evolutionary dynamics under domestication.