Contrasting patterns in crop domestication and domestication rates: recent archaeobotanical insights from the Old World

BACKGROUND: Archaeobotany, the study of plant remains from sites of ancient human activity, provides data for studying the initial evolution of domesticated plants. An important background to this is defining the domestication syndrome, those traits by which domesticated plants differ from wild relatives. These traits include features that have been selected under the conditions of cultivation. From archaeological remains the easiest traits to study are seed size and in cereal crops the loss of natural seed dispersal. SCOPE: The rate at which these features evolved and the ordering in which they evolved can now be documented for a few crops of Asia and Africa. This paper explores this in einkorn wheat (Triticum monococcum) and barley (Hordeum vulgare) from the Near East, rice (Oryza sativa) from China, mung (Vigna radiata) and urd (Vigna mungo) beans from India, and pearl millet (Pennisetum glaucum) from west Africa. Brief reference is made to similar data on lentils (Lens culinaris), peas (Pisum sativum), soybean (Glycine max) and adzuki bean (Vigna angularis). Available quantitative data from archaeological finds are compiled to explore changes with domestication. The disjunction in cereals between seed size increase and dispersal is explored, and rates at which these features evolved are estimated from archaeobotanical data. Contrasts between crops, especially between cereals and pulses, are examined. CONCLUSIONS: These data suggest that in domesticated grasses, changes in grain size and shape evolved prior to non-shattering ears or panicles. Initial grain size increases may have evolved during the first centuries of cultivation, within perhaps 500-1000 years. Non-shattering infructescences were much slower, becoming fixed about 1000-2000 years later. This suggests a need to reconsider the role of sickle harvesting in domestication. Pulses, by contrast, do not show evidence for seed size increase in relation to the earliest cultivation, and seed size increase may be delayed by 2000-4000 years. This implies that conditions that were sufficient to select for larger seed size in Poaceae were not sufficient in Fabaceae. It is proposed that animal-drawn ploughs (or ards) provided the selection pressure for larger seeds in legumes. This implies different thresholds of selective pressure, for example in relation to differing seed ontogenetics and underlying genetic architecture in these families. Pearl millet (Pennisetum glaucum) may show some similarities to the pulses in terms of a lag-time before truly larger-grained forms evolved.     

Early Holocene cultivation before domestication in northern Syria

Charred plant remains from the sites of Tell Qaramel, Jerf el Ahmar, Dja’de and Tell ‘Abr situated in northern Syria and dated to the tenth and ninth millennia cal b.c. demonstrate that a wide variety of wild pulses, cereals, fruits and nuts was exploited. Five lines of evidence suggest that cultivation was practised at three of the sites. (1) Wild einkorn, wild rye and lentils occur outside their natural habitats. (2) The founder crops barley, emmer and single-grained einkorn appear at different times. (3) An assemblage of weeds of cultivation was identified. (4) There is a gradual decrease in gathered plants such as small seeded grasses and Polygonum/Rumex. (5) Barley grains increase in breadth and thickness. Morphological domestication did not become established, perhaps because seed stock was regularly collected from wild stands. Charred rodent droppings indicate large-scale grain storage.     

Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no reduction of nucleotide diversity during Triticum monococcum (Einkorn) domestication: implications for the origin of agriculture

The diploid wheat Triticum monococcum L. (einkorn) was among the first crops domesticated by humans in the Fertile Crescent 10,000 years ago. During the last 5,000 years, it was replaced by tetraploid and hexaploid wheats and largely forgotten by modern breeders. Einkorn germplasm is thus devoid of breeding bottlenecks and has therefore preserved in unfiltered form the full spectrum of genetic variation that was present during its domestication. We investigated haplotype variation among >12 million nucleotides sequenced at 18 loci across 321 wild and 92 domesticate T. monococcum lines. In contrast to previous studies of cereal domestication, we sampled hundreds of wild lines, rather than a few dozen. Unexpectedly, our broad sample of wild lines reveals that wild einkorn underwent a process of natural genetic differentiation, most likely an incipient speciation, prior to domestication. That natural differentiation was previously overlooked within wild einkorn, but it bears heavily upon inferences concerning the domestication process because it brought forth 3 genetically, and to some extent morphologically, distinct wild einkorn races that we designate here as alpha, beta, and gamma. Only one of those natural races, beta, was exploited by humans for domestication. Nucleotide diversity and haplotype diversity in domesticate einkorn is higher than in its wild sister group, the einkorn beta race, indicating that einkorn underwent no reduction of diversity during domestication. This is in contrast to findings from previous studies of domestication history among more intensely bred crop species. Taken together with archaeological findings from the Fertile Crescent, the data indicate that a specific wild einkorn race that arose without human intervention was subjected to multiple independent domestication events.     

Evidence for plant exploitation and vegetation history from three Early Neolithic pre-pottery sites on the Euphrates (Syria)

Archaeobotanical results based on a limited number of samples from three aceramic sites dating from 9800 to 7800 B.P., which are under excavation in the valley of the Middle Euphrates, are discussed. The finds are presented simply by presence, and are compared to the contemporary vegetation and finds from similar sites. Carbonised plant remains recovered by flotation from levels dated to between 9800 and 9200 B.P. (Dja'de and Jerf al Ahmar) indicate that wild cereals (einkorn wheat, rye and barley) and pulses (lentils, pea and bitter vetch) were exploited. Other plants such as wild grasses, Pistacia, wild almond and oak, suggest that the local vegetation provided a rich diversity of resources. A study of possible weed taxa is being carried out in order to see whether this assemblage could be used to identify the cultivation of morphologically wild cereals for this period. Ninth millennium B.P. levels at Halula see the appearance of domestic crops such as emmer, naked wheat and barley, but wild-type cereals persist. The cultivars appear to have been introduced from elsewhere and later ninth millennium B.P. species include olive and flax. Ash, vine, maple, plane, alder and elm from the gallery forest, wild rye, wild einkorn, deciduous oak, wild almond, Pistacia, and Pyrus, from the hinterland, indicate cooler conditions.     

AFLP data and the origins of domesticated crops.

Amplified fragment length polymorphism (AFLP) datasets have been used to construct neighbor-joining trees from which monophyletic origins for crops such as einkorn wheat, barley, and emmer wheat have been inferred. We simulated several different multiple domestication scenarios for an imaginary cereal crop and examined the resulting domesticated populations. The simulations showed that the population biology aspects of the domestication process can result in independently domesticated populations merging in such a way that a monophyletic origin is erroneously inferred when the resulting population is examined by AFLP genotyping a nd neighbor-joining analysis. The resultsbring into question the use of this method to infer the origins of real crops.     

Pulse domestication and cereal domestication: How different are they?

Evidence is brought to indicate that the domestication of lentil and pea is not very different from that of wheat and barley. All these Near East crops are characterized by basically the same domestication traits the key elements of which are breakdown of the wild mode of seed dispersal and loss of germination regulation. It is argued that both in the pulses and in the cereals these traits evolved in the same way. The changes are best explained by assuming that mutations causing the loss of the wild-type adaptations were automatically selected for soon after people transferred the wild progenitors into a system of planting and reaping.     

A critical review of the protracted domestication model for Near-Eastern founder crops: linear regression, long-distance gene flow, archaeological, and archaeobotanical evidence

The recent review by Fuller et al. (2012a) in this journal is part of a series of papers maintaining that plant domestication in the Near East was a slow process lasting circa 4000?years and occurring independently in different locations across the Fertile Crescent. Their protracted domestication scenario is based entirely on linear regression derived from the percentage of domesticated plant remains at specific archaeological sites and the age of these sites themselves. This paper discusses why estimates like haldanes and darwins cannot be applied to the seven founder crops in the Near East (einkorn and emmer wheat, barley, peas, chickpeas, lentils, and bitter vetch). All of these crops are self-fertilizing plants and for this reason they do not fulfil the requirements for performing calculations of this kind. In addition, the percentage of domesticates at any site may be the result of factors other than those that affect the selection for domesticates growing in the surrounding area. These factors are unlikely to have been similar across prehistoric sites of habitation, societies, and millennia. The conclusion here is that single crop analyses are necessary rather than general reviews drawing on regression analyses based on erroneous assumptions. The fact that all seven of these founder crops are self-fertilizers should be incorporated into a comprehensive domestication scenario for the Near East, as self-fertilization naturally isolates domesticates from their wild progenitors.     

Subsistence strategies of two Bronze Age hill-top settlements in the eastern Alps—Friaga/Bartholomäberg (Vorarlberg, Austria) and Ganglegg/Schluderns (South Tyrol, Italy)

Up to now, archaeobotanical investigations of prehistoric sites in the eastern Alpine region have been rare. Recent palaeoethnobotanical investigations of carbonised plant remains from two Bronze Age hill-top settlements, one located north and the other south of the main Alpine range, contribute essentially to the knowledge of subsistence strategies and husbandry regimes in the Alps in prehistoric periods. The principal cereals were Hordeum vulgare (hulled barley), Triticum dicoccon (emmer) and Panicum miliaceum (broomcorn millet). In general, hulled barley was the most important cereal crop in the eastern Alps. Legumes such as Vicia faba (horse bean) and Pisum sativum (pea) also occurred regularly in both hill-top settlements. In addition to these field crops, a large variety of wild plants was still gathered and contributed considerably to the daily diet. The arable weed flora suggests that crops were sown in spring and autumn and it indicates crop rotation in this period. The results of the plant macrofossils imply a complex pattern of plant resource utilisation in the Alpine area during the Bronze Age.     

The distribution, natural habitats and availability of wild cereals in relation to their domestication in the Near East: multiple events, multiple centres

In this article we examine the natural habitats and distribution of the six wild cereals: Triticum urartu (wild urartu wheat), T. boeoticum aegilopoides (single-grained wild einkorn), T. boeoticum thaoudar (two-grained wild einkorn), T. dicoccoides (wild emmer wheat), Secale spp. (wild ryes) and Hordeum spontaneum (wild barley). A comparison of late Pleistocene/early Holocene archaeobotanical assemblages in the Near East with present-day distributions of wild cereals shows a good correlation. The regional variation in the archaeobotanical cereal assemblages and the ensuing domestication provide evidence that different cereal species were domesticated independently in different areas. Some sites were not situated near wild cereal habitats and a few were located outside the limits of distribution, even accounting for moister climatic conditions. I argue here that current models which try to explain the shift to farming have tended to over-emphasize the effect of the Younger Dryas climatic change. First, it would have had only a minor effect on cereal availability. Secondly, agriculture appears to have been established after the Younger Dryas. Thirdly, there is no evidence for a single centre of origin; agriculture arose in widely separated geographic and climatic regions. And fourthly, agriculture depends on stable climatic conditions which were not established until after the Younger Dryas.     

Trends in Biomass Fractionation in Wheat and Barley from Wild Ancestors to Modern Cultivars

Abstract: We tested the hypothesis that cultivar selection during the process of domestication in cereal plants led to a change in dry mass allocation, e.g., less root mass and more leaf mass or more leaf area per unit leaf mass. We divided 24 varieties of diploid, tetraploid and hexaploid winter wheat and two-rowed winter barley into three categories of domestication levels (wild species, old landraces and modern cultivars) and compared the patterns of dry matter fractionation at the time of anthesis under standardized outdoor growth conditions. In both cereals, total biomass per individual increased significantly with domestication level but, to our surprise, we found no significant change in dry matter investment between domestication levels: neither the dry mass fraction of leaves increased, nor was there a trend of reduced investment in stems and roots, contrary to what we expected. Specific leaf area (SLA) and leaf area ratio (LAR) of modern wheat and barley cultivars were significantly lower compared to wild varieties. Major differences in both cereals were of a purely morphological nature, namely a decrease in the number of stems and ears from wild species to domesticated varieties, along with more synchronous tiller development and therefore similar tiller size. Fertilizer increased total biomass in all domestication levels in both cereals, but influenced the dry matter fractionation only in barley. Tissue nitrogen concentration was unresponsive to both domestication and fertilization. The expected shift in functional traits, conventionally considered to determine plant growth, was not found. Indeed, dry matter fractionation among the major plant biomass components seems to be very conservative.     

A simulation of the effect of inbreeding on crop domestication genetics with comments on the integration of archaeobotany and genetics: a reply to Honne and Heun

Archaeobotanical evidence for Near Eastern einkorn wheat, barley, and Chinese rice suggests that the fixation of key domestication traits such as non-shattering was slower than has often been assumed. This suggests a protracted period of pre-domestication cultivation, and therefore implies that both in time and in space the initial start of cultivation was separated from eventual domestication, when domesticated and wild populations would have become distinct gene pools. Archaeobotanical evidence increasingly suggests more pathways to cultivation than are represented by modern domesticated crop lines, including apparent early experiments with cultivation that did not lead to domestication, and early domesticates, such as two-grained einkorn and striate-emmeroid wheats, which went extinct in prehistory. This diverse range of early crops is hard to accommodate within a single centre of origin for all early Near Eastern cultivars, despite suggestions from genetic datasets that single origins from a single centre ought to be expected. This apparent discrepancy between archaeobotany and genetics highlights the need for modelling the expected genetic signature of different domestication scenarios, including multiple origins. A computer simulation of simple plant populations with 20 chromosomes was designed to explore potential differences between single and double origins of domesticated populations as they might appear in genomic datasets millennia later. Here we report a new simulation of a self-pollinating (2% outbreeding) plant compared to panmictic populations, and find that the general outcome is similar with multiple starts of cultivation drifting towards apparent monophyly in genome-wide phylogenetic analysis over hundreds of generations. This suggests that multiple origins of cultivation of a given species may be missed in some forms of modern genetic analysis, and it highlights the need for more complex modelling of population genetic processes associated with the origins of agriculture.     

The development and application of molecular markers for abiotic stress tolerance in barley

This article represents some current thinking and objectives in the use of molecular markers to abiotic stress tolerance. Barley has been chosen for study as it is an important crop species, as well as a model for genetic and physiological studies. It is an important crop and, because of its well-studied genetics and physiology, is an excellent candidate in which to devise more efficient breeding methods. Abiotic stress work on cultivated gene pools of small grain cereals frequently shows that adaptive and developmental genes are strongly associated with responses. Developmental genes have strong pleiotropic effects on a number of performance traits, not just abiotic stresses. One concern is that much of the genetic variation for improving abiotic stress tolerance has been lost during domestication, selection and modern breeding, leaving pleiotropic effects of the selected genes for development and adaptation. Such genes are critical in matching cultivars to their target agronomic environment, and since there is little leverage in changing these, other sources of variation may be required. In barley, and many other crops, greater variation to abiotic stresses exists in primitive landraces and related wild species gene pools. Wild barley, Hordeum spontaneum C. Koch is the progenitor of cultivated barley, Hordeum vulgare L. and is easily hybridized to H. vulgare. Genetic fingerprinting of H. spontaneum has revealed genetic marker associations with site-of-origin ecogeographic factors and also experimentally imposed stresses. Genotypes and collection sites have been identified which show the desired variation for particular stresses. Doubled haploid and other segregating populations, including landrace derivatives have been used to map genetically the loci involved. These data can be used in molecular breeding approaches to improve the drought tolerance of barley. One strategy involves screening for genetic markers and physiological traits for drought tolerance, and the associated problem of drought relief-induced mildew susceptibility in naturally droughted fields of North Africa.     

Limited evolutionary divergence of seedlings after the domestication of plant species

The most vulnerable stage in the life of plants is the seedling. The transition from wild to agricultural land that plants experienced during and after domestication implied a noticeable change in the seedlings′ environment. Building on current knowledge of seedling ecology, and on previous studies of cassava, we hypothesise that cultivation should have promoted epigeal germination of seedlings, and more exposed and photosynthetic cotyledons. To test this hypothesis, we phenotyped seedling morpho‐functional traits in a set of domesticated and wild progenitor accessions of 20 Eudicot herbaceous crop species. Qualitative traits like epi‐ versus hypogeal germination, leafy versus storage type of cotyledons, or crypto‐ versus phanerocotyledonar germination, remained conserved during the domestication of all 20 species. Lengths of hypocotyls and epicotyls, of cotyledon petioles, and indices of cotyledon exposure to the aboveground environment changed during evolution under cultivation. However, those changes occurred in diverse directions, depending on the crop species. No common seedling phenotypic convergence in response to domestication was thus detected among the group of species studied here. Also, none of the 20 crops evolved in accordance with our initial hypothesis. Our results reject the idea that strong selective filters exerted unconsciously by artificial selection should have resulted in generalised channelling of seedling morphology towards more productive and more herbivore risky phenotypes. This result opens up unexplored opportunities for directional breeding of seedling traits.     

Domestication and crop evolution of wheat andbarley: Genes,genomics, and future directions

Wheat and barley are two of the founder crops of the agricultural revolution that took place 10,000 years ago in the Fertile Crescent and both crops remain among the world's most important crops. Domestication of these crops from their wild ancestors required the evolution of traits useful to humans, rather than survival in their natural environment. Of these traits, grain retention and threshability, yield improvement, changes to photoperiod sensitivity and nutritional value are most pronounced between wild and domesticated forms. Knowledge about the geographical origins of these crops and the genes responsible for domestication traits largely pre-dates the era of nextgeneration sequencing, although sequencing will lead to new insights. Molecular markers were initially used to calculate distance(relatedness), genetic diversity and to generate genetic maps which were useful in cloning major domestication genes. Both crops are characterized by large,complex genomes which were long thought to be beyond the scope of whole-genome sequencing. However, advances in sequencing technologies have improved the state of genomic resources for both wheat and barley. The availability of reference genomes for wheat and some of its progenitors,as well as for barley, sets the stage for answering unresolved questions in domestication genomics of wheat and barley.     

Wheat domestication: lessons for the future

Wheat was one of the first crops to be domesticated more than 10,000 years ago in the Middle East. Molecular genetics and archaeological data have allowed the reconstruction of plausible domestication scenarios leading to modern cultivars. For diploid einkorn and tetraploid durum wheat, a single domestication event has likely occurred in the Karacadag Mountains, Turkey. Following a cross between tetraploid durum and diploid T.?tauschii, the resultant hexaploid bread wheat was domesticated and disseminated around the Caucasian region. These polyploidisation events facilitated wheat domestication and created genetic bottlenecks, which excluded potentially adaptive alleles. With the urgent need to accelerate genetic progress to confront the challenges of climate change and sustainable agriculture, wild ancestors and old landraces represent a reservoir of underexploited genetic diversity that may be utilized through modern breeding methods. Understanding domestication processes may thus help identifying new strategies.     

Domestication of plants in the Americas: insights from Mendelian and molecular genetics

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 domestication syndrome is improving as a result of the development of saturated linkage maps for major crops, identification 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 understood, 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.     

Analysis of promoters in transgenic barley and wheat

Advances in the genetic transformation of cereals have improved the prospects of using biotechnology for plant improvement, and a toolbox of promoters with defined specificities would be a valuable resource in controlling the expression of transgenes in desired tissues for both plant improvement and molecular farming. A number of promoters have been isolated from the important cereals (wheat, barley, rice and maize), and these promoters have been tested mostly in homologous cereal systems and, to a lesser extent, in heterologous cereal systems. The use of these promoters across the important cereals would add value to the utility of each promoter. In addition, promoters with less sequence homology, but with similar specificities, will be crucial in avoiding homology-based gene silencing when expressing more than one transgene in the same tissue. We have tested wheat and barley promoters in transgenic barley and wheat to determine whether their specificity is shared across these two species. The barley bifunctional α-amylase/subtilisin inhibitor ( Isa ) promoter, specific to the pericarp in barley, failed to show any activity in wheat, whereas the wheat early-maturing ( Em ) promoter showed similar activity in wheat and barley. The wheat high-molecular-weight glutenin ( HMW-Glu ) and barley D-hordein ( D-Hor ) and B-hordein ( B-Hor ) storage protein promoters maintained endosperm-specific expression of green fluorescent protein (GFP) in wheat and barley, respectively. Using gfp , we have demonstrated that the Isa and Em promoters can be used as strong promoters to direct transgenes in specific tissues of barley and wheat grain. Differential promoter activity across cereals expands and adds value to a promoter toolbox for utility in plant biotechnology.     

Genetic variations in the digestibility in sheep of selected whole-crop cereals used as silages

Whole-plant winter cereals could be of great interest if used as silages for ruminant feeding as opposed to summer crops in that they would spare water resources or valorize low-input management. This study aimed to compare the feeding value of rye, barley, wheat (two genotypes) and triticale (six genotypes). The cereals were sown in October and harvested as silage in June. Forages were offered to Texel castrated sheep in order to evaluate the organic matter digestibility (OMd). The OMd of the wheat cultivars was higher (61.6%, P<0.05) than those of barley (57.2%) and rye (54.7%) but no different from that of triticale (60.6%). Within the triticale genotypes, OMd ranged from 54.7 to 62.3%. The presence of rough barbs should explain the relatively low intake of the cereals with the exception of wheat. Winter cereals provide good-quality forage for feeding ruminants. Wheat has a higher nutritional value than barley and rye and a wide variability for digestibility seems to exist within the triticale cultivars. Such variability in a species known for its ability to be cropped under limiting conditions should be explored in much greater depth as it could result in providing farmers with genotypes of good quality with an acceptable yield at a lower cost.     

Social Complexification and Pig (Sus scrofa) Husbandry in Ancient China: A Combined Geometric Morphometric and Isotopic Approach

Pigs have played a major role in the economic, social and symbolic systems of China since the Early Neolithic more than 8,000 years ago. However, the interaction between the history of pig domestication and transformations in Chinese society since then, have not been fully explored. In this paper, we investigated the co-evolution from the earliest farming communities through to the new political and economic models of state-like societies, up to the Chinese Empire, using 5,000 years of archaeological records from the Xiawanggang (XWG) and Xinzhai (XZ) sites (Henan Province). To trace the changes of pig populations against husbandry practices, we combined the geometric morphometric analysis of dental traits with a study of the stable carbon and nitrogen isotope ratios from bone collagen. The domestication process intensified during the Neolithic Yangshao, prompted by greater selective pressure and/or better herd control against wild introgression. After that, pig farming, in XWG, relied on local livestock and a gradual change of husbandry practices overtime. This was characterized by a gentle increase in millet foddering and animal protein intake, until a complete change over to household management during the Han dynasty. The only rupture in this steady trend of husbandry occurred during the Longshan period, with the appearance of small sized and idiosyncratic pigs with specific feeding practices (relying on millet and household scraps). From three exploratory hypothesis, we explored the possibility of anti-elite pig production in XWG during the Longshan period, as a means to resist incorporation into a new economic model promoting intensified domestic production. This exploratory hypothesis is the most suitable to our dataset; however, numerous areas need to be explored further in order to adequately document the role of pigs in the rise of China’s complex societies.