1. Introduction
At least 138 crops with some degree of domestication were being cultivated or managed by native Amazonians in various types of production systems at the time of European conquest, including 83 crops native to Amazonia and immediately adjacent areas in northern South America, and 55 exotic ones,
i.e., from other Neotropical regions, such as northeastern Brazil, the Caribbean and Mesoamerica [
1]. Among the 52 crops with domesticated populations, 14 are fruit or nut trees or woody vines (27%); among the 41 crops with semi-domesticated populations, 35 are trees or woody vines (87%); and among the 45 crops with incipiently domesticated populations, all but one are fruit and nut trees. Overall, 68% of these Amazonian crops are trees or woody perennials. In landscapes largely characterized by forest, a predominance of tree crops is perhaps not surprising [
1]. Nonetheless, the most important subsistence crop domesticated in Amazonia is an herbaceous shrub, manioc [
2], and several other domesticates are also root or tuber crops, most of which are adapted to savanna-forest transitional ecotones with pronounced dry seasons.
Two types of domestication can be distinguished conceptually: landscape domestication and plant (or animal) population domestication [
1]. Only the latter will be considered here because plant population domestication can now be examined with new genetic techniques, even though both sorts of domestication are of potential interest to historical ecology, since landscapes and the biota in them are profoundly affected, indeed molded by human actions. Additionally, these two kinds of domestication are intimately related because domesticated populations require some kind of landscape management, especially cultivation. Plant population domestication is a co-evolutionary process by which human selection on the phenotypes of promoted, managed or cultivated individual plants results in changes in the descendent population’s phenotypes and genotypes that make them more useful to humans and better adapted to human management of the landscape [
1]. The degree of change in populations can vary along a continuum from wild (the baseline, with no human-mediated change), through incipiently domesticated, to semi-domesticated, to domesticated. An incipiently domesticated population has gone through a founder event (defined as human selection of a small sample of the wild population and propagation of descendents from this sample; also called a bottleneck) that reduces its genotypic diversity and its phenotypic diversity varies only somewhat from the ancestral wild population in the traits selected by humans. A semi-domesticated population has gone through several sequential founder events that reduce further its genotypic diversity, but its phenotypic diversity is enhanced by accumulation of diverse alleles for traits selected by humans. Semi-domesticated populations tend to have more ample geographic distributions than incipient domesticates, which may permit introgression with other wild, incipient or semi-domesticated populations of the same species; in turn, such introgression may offer additional alleles for selected traits, thus somewhat enhancing genetic diversity. The ample geographic distribution may include areas where wild populations do not exist, which reduces introgression of wild-type alleles and permits more rapid response to human selection. A domesticated population has been further selected for adaptation to human-modified landscapes, especially cultivated gardens and fields, and has lost its original ecological adaptations for survival without humans, especially its original dispersal mechanisms and survival capabilities [
1]. Observe that domestication is a process that occurs at the population level, not the species level, so that it is incorrect to affirm that species X is a domesticate, unless all wild populations have become extinct, which is an uncommon occurrence; it is most generally correct to affirm that species X exhibits domesticated populations. Exceptions to this generalization exist, for example, when the end-result of the domestication process is a new species; a particular case of the latter is interspecific hybridization followed by chromosome doubling, resulting in the formation of allopolyploids [
3], as in guaraná, discussed below. An aside is worth adding here: the term “proto-domesticate” is often used, but
protós is Greek for “first”, leading to definitions such as ‘original’ and ‘primitive’ (as in “first order”); since domestication is a process and the domesticated population is the result, the domesticate is not primitive, but derived. Hence, the term should be avoided.
The degree of modification during domestication can be dramatic in many crops, including some tree crops, such as peach palm, where the difference in fruit size between the wild type and the most derived domesticated population is on the order of 2000% [
4]. Several other Amazonian tree crops show considerable, although not as dramatic, modification due to domestication [
5]. Given the long generations and typically outcrossing reproductive systems, these degrees of change suggest that domestication started quite early, perhaps at the beginning of the Holocene, rather than when production systems coalesced and became prominent 3,000 to 4,000 years before present (BP). The archaeological record, however, does not contain early records of Amazonian tree crops, although manioc and sweet potato were present between 8,000 and 6,000 BP in caves along the western Andean foothills of Peru [
6], indicating that they were domesticated earlier. The earliest lowland tree crop, guava, was present in the same area before 5,000 BP [
6]. The archaeological record of lowland South America east of the Andes is much less studied than the dry Pacific coast, western foothills and the highlands, where preservation is better, but is gradually gaining attention and patterns will become apparent as critical mass increases.
Better ethnographic and historical information exists for more recent periods. The crops in Amazonia at conquest were distributed in numerous centers, regions and micro-centers of crop genetic diversity, located principally where Native Amazonian populations were most abundant [
7],
i.e., along the principal white water rivers, but also in the upper Negro River, which was and still is a major center of Amazonian ethnic and linguistic diversity. Some tree crops, such as Brazil nut, are quite long-lived (500 to 1,000 years), so that their pre-conquest distribution can be mapped from their modern distribution. Balée [
8] used this type of information to estimate the proportion of the Amazon basin that had been modified by pre-conquest human activity (nearly 12%). Unfortunately, few species permit this type of analysis, but living plants can provide other information that permits inferences about their origin, domestication and dispersal before and since European conquest. This information is in their DNA and is accessed with different molecular techniques.
There are numerous types of molecular markers used in genetic analysis, each with advantages and disadvantages, as well as different information contents [
9]. In plants, both nuclear DNA (diploid) and chloroplast DNA (haploid) offer important and somewhat different information, with nuclear DNA subject to rapid change via recombination and chloroplast DNA subject to less rapid change; the latter is generally maternally inherited, which makes it especially useful for some kinds of analyses, such as distinguishing seed dispersal from pollen dispersal. So called dominant markers are cheaply and easily generated, but are less informative because they do not distinguish between homozygotes and heterozygotes at a particular DNA locus; the primary marker cited here is Random Amplified Polymorphic DNA—RAPDs, which are generated principally from nuclear DNA. Co-dominant markers are often more expensive to generate, but are more informative because they distinguish homozygotes and heterozygotes; examples are protein polymorphisms, especially in enzymes, Simple Sequence Repeats—SSRs (also called microsatellites), and Restriction Fragment Length Polymorphisms—RFLPs; the latter two can be either nuclear or chloroplast. Direct sequencing of specific regions of DNA is becoming the most important strategy to study genetic variability as the cost falls continually; it is also the most informative. Sequence polymorphisms include insertions and deletions of base pairs or sections of DNA, as well as substitutions in nucleotide sequences, such as Single Nucleotide Polymorphisms—SNPs. Ideally molecular markers should be selectively neutral, that is they should not be under selective pressures so that they do not reflect different local adaptations to natural or human selection.
New research with these molecular tools attempts to identify origins and possible dispersals via the patterns of genetic diversity in living populations of native Amazonian crops, a field of study known as phylogeography [
9]. Phylogeography is the analysis of the geographic distribution of genetic variants, especially lineages of genes, which is generally due to dispersal of organisms (seed dispersal in plants) and thus provides insight into the history of a species. The same information permits inferences about the domestication process [
10,
11,
12] and can even be used to estimate the approximate age of the founder events, although this has yet to be attempted with an Amazonian crop. This contribution reviews recent molecular studies of a set of native Amazonian crops, some important, others less so, and identifies emergent patterns that can be used to interpret crop domestication and dispersal before conquest.
3. Patterns of Diversity
Although the number of species with molecular genetic analyses is still small, some patterns are congruent with previous thinking about the origin, domestication and dispersal of native Amazonian crops. The first important pattern is the antiquity of several important Amazonian domesticates, such as manioc (more than 8,000 BP), Capsicum (more than 6,000 BP), pineapple (possibly more than 6,000 BP) and, perhaps, peach palm (possibly as early as 10,000 BP). The first two have archaeological support from coastal Peru, while the latter two are projections based on morphological differences among wild and fully domesticated populations. No estimates of the dates of the primary domestication event with genetic coalescence analysis have been presented to date, but this type of analysis will certainly be attempted within the next decade.
Although these dates are quite old, they are more recent than the initial peopling of Amazonia, which occurred before 11,200 BP when the Pedra Pintada site was occupied in Central Amazonia, in what is now Monte Alegre, Pará [
142]. These early occupants were broad-spectrum foragers, who may have begun domestication of the landscape near the site [
143], but who did not possess any plant populations with signs of domestication. Somewhat later (7,100 BP) and on the other side of the Amazon River at Taperinha, near Santarém, Pará, settled villages appeared, based on exploitation of fluvial resources and forest foraging, as well as the first pottery in the Americas [
144]. Some of the pottery suggests the presence of food production, but no evidence of domesticated plants exists [
143]. Again, we can assume that landscape domestication was certainly underway. The lack of domesticated crops in settings where dump heaps were certainly becoming home gardens [
145] is curious, as at least manioc was already being dispersed from its origin in southwestern Amazonia.
This leads to a second important pattern: the relation between antiquity and origin. All but one of the species examined originated in the periphery of Amazonia (
Figure 3), rather than along the major white water rivers where pre-conquest population densities were greatest. The exception is guaraná, a very recently domesticated crop, although cupuassu may be a similar case. The most important crops with domesticated populations are also the oldest, and all come from the periphery: manioc, pineapple,
Capsicum, peach palm, tobacco, perhaps sweet potato. The importance of the periphery has been highlighted previously [
121], with emphasis on extreme northwestern Amazonia and the adjacent Llanos of the Orinoco River basin, the Guiana shield and southwestern Amazonia, especially the Llanos de Mojos, in Bolivia. Work on Amazonian fruits permits the addition of numerous species with domesticated populations to the list, as well as several semi- and incipiently domesticated populations [
1,
146], without changing the emphasis on the periphery, although this region has now been expanded to include the Andean foothills and immediately adjacent lowlands in western Amazonia and some of southeastern Amazonia (
Figure 3).
Figure 3.
Confirmed and hypothetical origins of some native Amazonian crops. The confirmed origins are (from north to south): pineapple, cubiu (Solanum sessiliflorum), cacao, assai (Euterpe oleracea), guaraná, manioc, coca (Erythroxylum coca), tobacco (Nicotiana tabacum), peanut (Arachis hypogaea). The hypothetical origins are: genipap (Genipa americana), leren (Calathea allouia), sweet potato (Ipomoea batatas), cocoyam (Xanthosoma sagittifolium), yam (Dioscorea trifida), murupi pepper (Capsicum chinense), mapati (Pourouma cecropiifolia), abiu (Pouteria caimito), bacuri (Platonia insignis), inga (Inga edulis), cashew (Anacardium occidentale), sapota (Quararibea cordata), cupuassu, biriba (Rollinia mucosa), guava (Psidium guajava), Brazil nut, peach palm, cocoyam, annato (Bixa orellana), malagueta pepper (Capsicum frutescens). Note that there is continued uncertainty about Mesoamerican origins for guava and malagueta pepper.
Figure 3.
Confirmed and hypothetical origins of some native Amazonian crops. The confirmed origins are (from north to south): pineapple, cubiu (Solanum sessiliflorum), cacao, assai (Euterpe oleracea), guaraná, manioc, coca (Erythroxylum coca), tobacco (Nicotiana tabacum), peanut (Arachis hypogaea). The hypothetical origins are: genipap (Genipa americana), leren (Calathea allouia), sweet potato (Ipomoea batatas), cocoyam (Xanthosoma sagittifolium), yam (Dioscorea trifida), murupi pepper (Capsicum chinense), mapati (Pourouma cecropiifolia), abiu (Pouteria caimito), bacuri (Platonia insignis), inga (Inga edulis), cashew (Anacardium occidentale), sapota (Quararibea cordata), cupuassu, biriba (Rollinia mucosa), guava (Psidium guajava), Brazil nut, peach palm, cocoyam, annato (Bixa orellana), malagueta pepper (Capsicum frutescens). Note that there is continued uncertainty about Mesoamerican origins for guava and malagueta pepper.
Whether the peripheral origin of the earliest domesticated populations is due to the plants themselves or to human activity is an interesting question. During the terminal Pleistocene, when humans were already in Amazonia, much of western Amazonia is thought to have been forested, while large parts of central and eastern Amazonia were open forest that was quite different from current open forests [
147,
148,
149]. The drier areas along the northern and southern peripheries probably expanded further into the basin than they do currently. The crops that were domesticated early, e.g., manioc, peach palm, pineapple, probably
Capsicum, originated in these open ecosystems, some of which remain in place, others of which have been transformed into more humid forest as this expanded during the Holocene. Some of the difficulties in identifying origins may be due to forest expansion during the Holocene, although better geographic sampling may resolve many of these difficulties.
Root and tuber crops generally originated in seasonally dry open ecosystems, where they fill their starchy storage organs before the dry season, making them attractive to hunter-gatherers during the dry season [
121]. This also makes them well adapted to human modified niches in the landscape, such as dump heaps that later became home gardens [
145] and incipient horticultural systems. Manioc was also selected for growth in anthropogenic soils (terra preta de índio), some of which also originated as dump heaps [
150], and floodplain soils [
33], although most landraces are well adapted to nutrient poor upland soils. It is probable that the other root and tuber crops also had some varieties adapted to floodplain soils, but they may have been lost in the post-conquest wave of genetic erosion that accompanied population decline [
1].
The humid periphery in western Amazonia appears to be home to numerous fruit crops and different adaptations might be expected. Some, like cacao, survive well in humid forest under-stories, whereas others, like inga, have adapted well to open horticultural systems. Many of those that have not yet been subjects of genetic analysis appear to have originally adapted to successional ecotones, as they do not survive long when the second growth forest grows enough to shade them out. The exception is sapota, which is a canopy emergent when mature.
As highlighted above, however, early occupation of central Amazonia did not include domesticates, even though the ecosystems around Pedra Pintada and Taperinha were probably relatively more open at the time than currently, and landscapes within them were probably being domesticated. It is possible that sufficient natural resources were available so that the home gardens were such a small fraction of subsistence that they are difficult to find in the archaeological record. In contrast, in the headwaters of the same rivers in the periphery, less abundant aquatic resources may have increased the importance of home gardens. In fact, the earliest terra preta de índio is also in the periphery, along the Jamarí River, in the upper Madeira River basin [
151]. Rindos [
51] and Tudge [
152] hypothesize that foragers who also practiced plant domestication would be more successful than those who did not, and it was from the southwestern periphery that two language diasporas occurred: Tupi-Guaraní and Arawak-Maipuran [
122]. The southern and southwestern periphery eventually was the stage for the development of complex societies as well [
153], but a detailed search is still required for signs of
in situ crop domestication, with
Caryocar brasiliense mentioned as a possible candidate.
A pattern whose explanation is less clear is why certain crops were widely dispersed and others not. Crops with good adaptation to environmental variation, e.g., manioc, were widely dispersed quite rapidly, appearing in the archaeological record of the Pacific coast of Peru by 8,000 BP or earlier [
6] and southern Mesoamerica by 5,600 BP at the latest [
154]. Those with early adaptation to human disturbance, e.g.,
Capsicum, were certainly excellent camp followers, although it is difficult to determine which peppers appear first on the coast of Peru, since only the genus is mentioned for the earliest records [
6].
It is probable that ethnic preferences determined dispersal patterns. For example, peach palm’s double dispersal of smaller oilier fruits down the Madeira River and along the Amazon River, and larger starchier fruits down the Ucayali River, throughout western Amazonia, along the Pacific coast of Ecuador and Colombia, and into Central America, but not the Caribbean islands, may be related to the Tupi and Arawak dispersals, respectively [
53], even though these dispersals are much later than the initial domestication events. The absence of Brazil nut in the Juruá River basin is another example.
Genetic evidence also sheds light on dispersal patterns. When a domesticate was important and taken into cultivation early, generally clear genetic structuring occurs among populations, such as the landraces of peach palm. When the crop was important, early and also annual, numerous varieties were developed and spread locally, but less regional structuring is evident, as seen in manioc, although superimposed on the bitter-sweet distinction, and in Capsicum and pineapple. When the crop is an incipient domesticate or became important only recently, no clear genetic structuring occurs, as in Brazil nut, cupuassu and guaraná.
What is quite clear, however, is that the major pre-conquest population centers concentrated crop genetic resources to guarantee their subsistence and trade (
Figure 4). The major centers and regions of diversity are along the major white water rivers and in northwestern Amazonia, where ethnic diversity is extremely high [
7]. The minor centers are all related to areas where pre-conquest populations transformed the landscape with earthworks of various types [
7]. It may also be appropriate to consider the upper Xingu River a minor center, given the intensity of landscape domestication, complex social structure, and possible incipient domestication of local fruit trees, such as
Caryocar brasiliense [
155]. The fact that the majority of Amazonia is not included in these concentrations does not imply that crop genetic resources were absent, but that they had not been concentrated to the same degree, principally because human population densities were lower.
Figure 4.
Centers, regions and minor centers of crop genetic resources diversity at the time of European conquest (modified from [
7]). Centers of diversity: 1―western Amazonia; 2―central Amazonia. Minor centers: 3―Marajo Island; 4―Llanos de Mojos; 5―middle Orinoco River. Regions of diversity: 6―Solimões River; 7―upper Negro River; 8―Madeira River.
Figure 4.
Centers, regions and minor centers of crop genetic resources diversity at the time of European conquest (modified from [
7]). Centers of diversity: 1―western Amazonia; 2―central Amazonia. Minor centers: 3―Marajo Island; 4―Llanos de Mojos; 5―middle Orinoco River. Regions of diversity: 6―Solimões River; 7―upper Negro River; 8―Madeira River.
The contrast between the presumed origins of native Amazonian crops in the periphery (
Figure 3) and their concentration in the centers of pre-conquest population density (
Figure 4) is dramatic. Clearly, centers of origin and centers of diversity are not equivalent concepts, as Nikolai I. Vavilov [
156] understood, although many students of crop genetic resources throughout the 20th century claimed otherwise. Because crop domestication began thousands of years before food production systems became important [
51,
121], it is not at all surprising to see a dramatic contrast such as that in Amazonia. As the archaeology of Amazonia becomes better understood [
153] and as the number of species studied with genetic and phylogeographic methods expands, we will certainly be able to clarify the patterns mentioned here and perhaps identify others.