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Domestication of Plants in the Americas: Insights from Mendelian and Molecular Genetics

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Domestication of Plants in the Americas: Insights from Mendelian and Molecular Genetics CORE Metadata, citation and similar papers at core.ac.uk Provided by PubMed Central Annals of Botany 100: 925–940, 2007 doi:10.1093/aob/mcm193, available online at www.aob.oxfordjournals.org REVIEW Domestication of Plants in the Americas: Insights from Mendelian and Molecular Genetics BARBARA PICKERSGILL* School of Biological Sciences, The University of Reading, Reading, UK Received: 24 November 2006 Returned for revision: 4 June 2007 Accepted: 23 July 2007 Published electronically: 31 August 2007 † Background Plant domestication occurred independently in four different regions of the Americas. In general, different species were domesticated in each area, though a few species were domesticated independently in more than one area. The changes resulting from human selection conform to the familiar domestication syndrome, though different traits making up this syndrome, for example loss of dispersal, are achieved by different routes in crops belonging to different families. † Genetic and Molecular Analyses of Domestication Understanding of the genetic control of elements of the dom- estication syndrome is improving as a result of the development of saturated linkage maps for major crops, identi- fication and mapping of quantitative trait loci, cloning and sequencing of genes or parts of genes, and discoveries of widespread orthologies in genes and linkage groups within and between families. As the modes of action of the genes involved in domestication and the metabolic pathways leading to particular phenotypes become better under- stood, it should be possible to determine whether similar phenotypes have similar underlying genetic controls, or whether human selection in genetically related but independently domesticated taxa has fixed different mutants with similar phenotypic effects. † Conclusions Such studies will permit more critical analysis of possible examples of multiple domestications and of the origin(s) and spread of distinctive variants within crops. They also offer the possibility of improving existing crops, not only major food staples but also minor crops that are potential export crops for developing countries or alternative crops for marginal areas. Key words: Domestication syndrome, archaeobotanical record, Mendelian genetics, molecular genetics, quantitative trait loci, American crops. INTRODUCTION entire species, or just some of the variants within a species. Where there is intraspecific variation in the Domestication is generally considered to be the end-point degree of domestication, it is possible to study the genetic of a continuum that starts with exploitation of wild plants, control of traits of the domestication syndrome in segregat- continues through cultivation of plants selected from the ing generations of appropriate intraspecific crosses. wild but not yet genetically different from wild plants, Vegetatively propagated root crops and perennial fruit crops and terminates in fixation, through human selection, of show fewer features of the domestication syndrome than morphological and hence genetic differences distinguishing annual seed crops, and domestication may occur more a domesticate from its wild progenitor. These differences slowly because fewer sexual generations occur in a given constitute the domestication syndrome and generally period of time. Clement (1999) proposed two intermediate render the domesticate less capable of survival in the categories, incipiently domesticated and semi-domesticated, wild, thus dependent on man for its growth and reproduc- to cover the spectrum of changes resulting from human tion. Features of the domestication syndrome include loss interactions with species of tree fruits in Amazonia. Semi- of dispersal, increase in size (especially of the harvested domesticated also fits the situation described by Casas et al. part of the plant), loss of seed dormancy and loss of chemi- (1999) for Stenocereus stellatus, a giant cactus exploited and cal or mechanical protection against herbivores. cultivated for its fruit in the Tehuaca´nValleyofMexico. Crops vary within and between species in their degrees of Some plants in home gardens have fruits with pulp of domestication. All known accessions of Capsicum pubes- colours not recorded in the wild, and most have sweet fruit cens have large fruits that have lost their dispersal mechan- whereas most wild plants have sour fruit. Wild and cultivated ism, and this species occurs only in cultivation. The four populations differ statistically in various characters likely to be other species of domesticated chile pepper each includes targets of human selection, though some cultivated plants are a range of variation from wild peppers, through cultivated morphologically indistinguishable from some wild plants. peppers with somewhat larger fruits that are still capable Cultivated populations are thus not genetically fixed for any of natural dispersal, to fully domesticated peppers with characters distinguishing them from wild populations, but fre- large fruits that remain firmly attached to the parent plant quencies of alleles governing the characters subject to human after maturity. ‘Domesticated’ may therefore describe an selection presumably differ. Casas et al. (1999) considered that such changes in allele frequencies resulting from human selec- * E-mail [email protected] tion constitute at least incipient domestication. # 2007 The Author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http:// creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 926 Pickersgill — Domestication of New World Crops Gepts (2004) considered cultivation a necessary but and the tropical lowlands of South America. Table 1 insufficient condition for domestication. However, domesti- shows the approximate dates of the first appearance in the cation (or at least incipient or semi-domestication) without archaeological record of some of the cultigens associated cultivation may occur by selective removal of undesirable with each region. phenotypes and/or enhancement of desirable phenotypes in wild populations, thus changing the proportion of pheno- Eastern North America types in the managed populations, as described by Casas et al. (1997, 1999) and Anderson (2004) for various Only four species are currently regarded as having been species. Casas et al. (1997) noted that in open- or cross- domesticated in eastern North America (Smith, 2006), far pollinated species, selective retention of desirable pheno- fewer than the number of species domesticated in the types in managed populations will promote mating other regions. The eastern North American domesticates between these plants. More progeny will then show the also appear later in the archaeological record than the first desired characters, leading eventually to fixation of these domesticates in the other regions. characters. Casas et al. (1997) termed this in situ domesti- Rivers in eastern North America provided abundant fish cation and suggested that, since in situ management of wild and shellfish, while gathered nuts were the primary plant and weedy species is very common in Mesoamerica, in situ staple (Watson, 1989). Cucurbita pepo ssp. ovifera was domestication may also have occurred frequently and may apparently the first domesticate, possibly because its fruits explain how various outbreeding species became some of were useful as containers and fishnet floats, though the the first domesticates in this region, in contrast to the oil-rich seeds may have been eaten (Asch and Hart, Middle East, where most of the early domesticates are 2004). Vegetable forms (crookneck, acorn and scallop inbreeders (Zohary, 1984). squashes) developed later. Iva annua (marshelder) and Despite difficulties in defining domestication, most Helianthus annuus (sunflower) were also domesticated for workers agree that there were several independent regions their oil-rich seeds. The first sign of domestication in all of plant domestication in the Americas and that, quite fre- three is the appearance of large seeds or fruits, outside quently, different species of the same genus were domesti- the range of modern wild forms (Smith, 2006). Cucurbita cated independently, in different regions and by different pepo and sunflower are still important crops, but marshelder peoples. More rarely, the same species was domesticated had disappeared from cultivation by the time of European more than once, in different parts of the range of a wide- contact (Asch and Asch, 1978). Seeds of the fourth dom- spread wild progenitor. These different, but congeneric esticate, Chenopodium berlandieri, are not significantly (or conspecific), domesticates show similar changes result- larger than those of wild chenopods but do have thinner ing from human selection. This raises the question of testas (Smith, 1984), presumably reflecting loss of seed dor- whether their similar phenotypes are produced by similar mancy. This species survived as a crop plant until the 18th genotypes, or whether selection in different environments, century (Smith, 1995) but is now only a weed. Other by humans of different cultural backgrounds, exerted species thought to have been cultivated but not showing on progenitor populations that differed genetically, any morphological changes indicative of domestication resulted in different genetic pathways to the domesticated include Polygonum erectum,
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