Agricultural Origins: Centers and Noncenters; A Near Eastern Reappraisal

Understanding the evolutionary history of crop plants is fundamental to our understanding of their respective adaptation profiles, which in turn, is a key element in securing future yield and quality improvement. Central topics in this field concern the mono- or polyphyletic origin of crop plants, and our ability to identify the geographic location where certain crop plants have originated. Understanding the geographical pattern of domestication may also assist in reconstructing the cultural processes underlying the Neolithic (agricultural) Revolution. Here we review prevailing views on the geographic pattern of Near Eastern plant domestication, and highlight the distinction between genetic domestication events and independent cultural events. A critical evaluation of the wealth of newly published geobotanical, genetic, and archaeological data provides strong support in favor of a specific core area in southeastern Turkey where most, if not all, founder Near Eastern crops were likely domesticated.     

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.     

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 Ecology of Seasonal Stress and the Origins of Agriculture in the Near East

The time, place, and reasons for the first domestication of cereals and legumes in the Near East can now be securely identified using combined evidence from paleoenvironmental studies, models of ecosystem dynamics, and regional archeology. The heartland of domestication was the Jordan Valley and surrounding region in the Southern Levant. Approximately 10,000 years ago, people began planting crops where the wild ancestral species had proliferated over two millenia. Impetus for domestication came from the synergistic effects of climatic change, anthropogenic environmental change, technological change, and social innovation. At the end of the Pleistocene, after a long period of climatic instability, a mediterranean climate more strongly seasonal than any today emerged with hyper-arid summers that selected for annual species of cereals and legumes. This occurred long after people had invented tools suitable for grinding hard seeds, but the new, lengthy dry season and consequent need to use stored foods encouraged sedentism among human groups who subsequently depleted their immediate environments of wild resources. These preconditions facilitated the development of agriculture. The scenario developed here is specific to the Near East, for such case studies of specific factors in independent regions of domestication are essential before we attempt to explain cases all over the world with reference to global causes.     

Evidence of three maternal lineages in Near Eastern sheep supporting multiple domestication events

The variability of mtDNA was analysed in local sheep breeds reared throughout Turkey, for which a fragment of the D-loop region and the complete cytochrome b were sequenced. Phylogenetic analyses performed independently for the D-loop and the Cyt b gene revealed three clearly separated clusters indicating three major maternal lineages, two of which had been previously described as types B and A. The new type, C, was present in all the breeds analysed and showed considerable mtDNA variability. Divergence time was obtained on the basis of Cyt b gene and was estimated to be around 160,000-170,000 years ago for lineages B and A, whereas the divergence of lineage C proved to have occurred earlier (between 450,000 and 750,000 years ago). These times greatly predate domestication and suggest that the origin of modern sheep breeds was more complex than previously thought and that at least three independent sheep domestication events occurred. Our results, together with archaeological information and the current wild sheep populations in the Near East region support the high importance of this area in the sheep domestication process. Finally, the evidence of a third maternal lineage has important implications regarding the history of modern sheep.     

Genetics and geography of wild cereal domestication in the near east

About 12,000 years ago, humans began the transition from hunter-gathering to a sedentary, agriculture-based society. From its origins in the Near East, farming expanded throughout Europe, Asia and Africa, together with various domesticated plants and animals. Where, how and why agriculture originated is still debated. But newer findings, on the basis of genome-wide measures of genetic similarity, have traced the origins of some domesticated cereals to wild populations of naturally occurring grasses that persist in the Near East. A better understanding of the genetic differences between wild grasses and domesticated crops adds important facets to the continuing debate on the origin of Western agriculture and the societies to which it gave rise.     

Reassessing domestication events in the Near East: Einkorn and Triticum urartu

To reassess domestication events in the Near East, accessions of Triticum urartu from a well-described sampling were combined with a representative sample covering the Karacada? Einkorn wheat domestication. The observed DNA separation between the two wheat species accounts for the main differentiation, but geographic variation within T. urartu is evident and so is the domestication scenario among wild, feral, and domesticated Einkorn. In contrast to the clear DNA differences, it is difficult to separate living T. urartu from wild Einkorn based on morphology. With archaeobotanical material a distinction of carbonized remains of these two wheats is considered to be impossible. We reviewed the differences concerning morphology and maturity and combined these observations with information about archaeological sites in the Near East. In conclusion, the excavation sites in the middle Euphrates may contain T. urartu rather than Einkorn wheat and T. urartu may underlie the reported occurrence of the extinct 2-grained domesticated "Einkorn" wheat. The first Einkorn wheat domestication sensu stricto seems to have happened around the Karacada?, as reported earlier. The human dimension shown by the excavation of G?bekli Tepe can explain why domesticated phenotypes might have spread quickly.     

The chickpea, summer cropping, and a new model for pulse domestication in the ancient near east

The widely accepted models describing the emergence of domesticated grain crops from their wild type ancestors are mostly based upon selection (conscious or unconscious) of major features related either to seed dispersal (nonbrittle ear, indehiscent pod) or free germination (nondormant seeds, soft seed coat). Based on the breeding systems (self-pollination) and dominance relations between the allelomorphs of seed dispersal mode and seed dormancy, it was postulated that establishment of the domesticated forms and replacement of the wild ancestral populations occurred in the Near East within a relatively short time. Chickpea (Cicer arietinum L.), however, appears as an exception among all other "founder crops" of Old World agriculture because of its ancient conversion into a summer crop. The chickpea is also exceptional because its major domestication trait appears to be vernalization insensitivity rather than pod indehiscence or free germination. Moreover, the genetic basis of vernalization response in wild chickpea (Cicer reticulatum Ladiz.) is polygenic, suggesting that a long domestication process was imperative due to the elusive phenotype of vernalization nonresponsiveness. There is also a gap in chickpea remains in the archaeological record between the Late Prepottery Neolithic and the Early Bronze Age. Contrary to the common view that Levantine summer cropping was introduced relatively late (Early Bronze Age), we argue for an earlier (Neolithic) Levantine origin of summer cropping because chickpea, when grown as a common winter crop, was vulnerable to the devastating pathogen Didymella rabiei, the causal agent of Ascochyta blight. The ancient (Neolithic) conversion of chickpea into a summer crop required seasonal differentiation of agronomic operation from the early phases of the Neolithic revolution. This topic is difficult to deal with, as direct data on seasonality in prehistoric Old World field crop husbandry are practically nonexistent. Consequently, this issue was hardly dealt with in the literature. Information on the seasonality of ancient (Neolithic, Chalcolithic, and Early Bronze Age, calibrated 11,500 to 4,500 years before present) Near Eastern agriculture may improve our understanding of the proficiency of early farmers. This in turn may provide a better insight into Neolithic agrotechniques and scheduling. It is difficult to fully understand chickpea domestication without a Neolithic seasonal differentiation of agronomic practice because the rapid establishment of the successful Near Eastern crop package which included wheats, barley, pea, lentil, vetches, and flax, would have preempted the later domestication of this rare wild legume.     

From the cradle of agriculture a handful of lentils: History of domestication

Literature on lentil domestication is reviewed, particularly considering archeobotanical, phylogenetic, and molecular evidence. Lentils are one of the oldest crops cultivated and domesticated by man. Carbonized small lentil seeds have been found in several archaeological remains starting from the Neolithic. It is probable, however, that the most ancient remains refer to wild lentils; this is difficult to ascertain since seed size was probably selected after the establishment of a domesticated lentil. It is general opinion that cultivation occurred before domestication, but for how long is still an open question. It is now well accepted that the domestication of lentils was accomplished in the Near East, in an area called “the cradle of agriculture”. The genus Lens is very small, containing only 6 taxa. A wide range of morphological and molecular evidence supports the idea that the lentil wild progenitor is Lens culinaris ssp. orientalis. On the other hand, the most distantly related species within the genus appears to be L. nigricans, whose domestication was also attempted without success. The first characters involved in lentil domestication were pod dehiscence and seed dormancy. These traits are under a simple genetic control, and therefore mutants must have been fixed in a relatively short time. These and other morphological traits possibly involved in lentil domestication have been mapped in several linkage maps. However, generally these maps are not easily integrated since they are based on a limited number of markers. Newer maps, mainly built on different kinds of molecular markers, have been more recently produced. A consensus map is needed to fill the gap in lentil breeding and, at the same time, endow with deeper information on the genetics of lentil domestication, giving new insight into the origins of this crop, which present fragmented knowledge is unable.      

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.     

The origins of agriculture in the Americas

Three independent centers of domestication and agricultural origin have been identified in the Americas: the south-central Andes, Mexico, and most recently, eastern North America. Much of the evidence for early domesticates in these three regions has been excavated from higher elevation dry caves and rock shelters. These sites contain remarkably well preserved plant and animal remains, along with a record of short-term occupation by small groups of hunter-gatherers and early cultivators. As a result it has long been thought that plants and animals were brought under domestication in the Americas by small, seasonally mobile societies living in upland settings. The age of small seeds and other plant materials recovered from such dry caves and believed to represent early domesticates was, of necessity, determined indirectly, through conventional large-sample radiocarbon dating of organic material thought to be contemporaneous. In each of the three regions, the earliest domesticates were believed to date between 7,000 and 10,000 B.P. The origin of agriculture in the Americas was thought to be roughly contemporary with the transition from foraging to farming in the Near East (Fertile Crescent, ca. 10,000 B.P.) and China (Yangtze Corridor, ca. 8,500 B.P.). Since the mid-1980s, however, the age of many of the proposed early domesticates in the Americas, as well as their contexts of domestication, have been re-examined, beginning in eastern North America. The excavation of larger and more sedentary river valley settlements in eastern North America has yielded ample evidence of the cultivation of domesticated seed plants. This evidence is as old as or older than that recovered from seasonally occupied upland caves and rock shelters. In addition, a new and more rigorous standard for evidence of domestication has been adopted in eastern North America. That standard, which requires direct dating of seeds and other plant parts that exhibit clear, unequivocal, and well-documented morphological markers of domestication, is now being applied throughout the Americas, producing conservative timetables of domestication and agricultural origins that contradict alternative, more speculative chronological frameworks. Under the new standard of evidence, domestication of plants in all three independent centers (and in the Andes, domestication of animals) appears to have taken place between about 5,500 and 4,000 years ago, much more recently than previously was thought. Several lines of evidence also suggest that the Native American societies that first brought these species under domestication may not have been exclusively seasonally mobile hunter-gatherers of higher-elevation environments. In each of the three regions, domesticates recovered from upland caves may reflect a transition to a farming way of life accomplished by societies occupying more sedentary settlements in river valleys. In some cases, upland caves containing domesticates may represent one component in the seasonal round of early food production by societies occupying nearby river valleys; in others, they may mark the subsequent expansion of food production economies out of rich river valley resource zones into adjacent upland environments.     

Cultivation as slow evolutionary entanglement: comparative data on rate and sequence of domestication

Recent studies have suggested that domestication was a slower evolutionary process than was previously thought. We address this issue by quantifying rates of phenotypic change in crops undergoing domestication, including five crops from the Near East (Triticum monococcum, T. dicoccum, Hordeum vulgare, Pisum sativum, Lens culinaris) and six crops from other regions (Oryza sativa, Pennisetum glaucum, Vigna radiata, Cucumis melo, Helianthus annus, Iva annua). We calculate rates using the metrics of darwin units and haldane units, which have been used in evolutionary biology, and apply this to data on non-shattering cereal spikelets and seed size. Rates are calculated by considering data over a 4,000-year period from archaeological sites in the region of origin, although we discuss the likelihood that a shorter period of domestication (1,000–2,000) years may be more appropriate for some crops, such as pulses. We report broadly comparable rates of change across all the crops and traits considered, and find that these are close to the averages and median values reported in various evolutionary biological studies. Nevertheless, there is still variation in rates between domesticates, such as melon seeds increasing at twice the rate of cereals, and between traits, such as non-shattering evolving faster than grain size. Such comparisons underline the utility of a quantitative approach to domestication rates, and the need to develop larger datasets for comparisons between crops and across regions.     

The ripples of "The Big (agricultural) Bang": the spread of early wheat cultivation.

Demographic expansion and (or) migrations leave their mark in the pattern of DNA polymorphisms of the respective populations. Likewise, the spread of cultural phenomena can be traced by dating archaeological finds and reconstructing their direction and pace. A similar course of events is likely to have taken place following the "Big Bang" of the agricultural spread in the Neolithic Near East from its core area in southeastern Turkey. Thus far, no attempts have been made to track the movement of the founder genetic stocks of the first crop plants from their core area based on the genetic structure of living plants. In this minireview, we re-interpret recent wheat DNA polymorphism data to detect the genetic ripples left by the early wave of advance of Neolithic wheat farming from its core area. This methodology may help to suggest a model charting the spread of the first farming phase prior to the emergence of truly domesticated wheat types (and other such crops), thereby increasing our resolution power in studying this revolutionary period of human cultural, demographic, and social evolution.     

Molecular phylogeography of domesticated barley traces expansion of agriculture in the Old World

Barley (Hordeum vulgare ssp. vulgare) was first cultivated 10,500 years ago in the Fertile Crescent and is one of the founder crops of Eurasian agriculture. Phylogeographic analysis of five nuclear loci and morphological assessment of two traits in >250 domesticated barley accessions reveal that landraces found in South and East Asia are genetically distinct from those in Europe and North Africa. A Bayesian population structure assessment method indicates that barley accessions are subdivided into six clusters and that barley landraces from 10 different geographical regions of Eurasia and North Africa show distinct patterns of distribution across these clusters. Using haplotype frequency data, it appears that the Europe/North Africa landraces are most similar to the Near East population (F ST = 0.15) as well as to wild barley (F ST = 0.11) and are strongly differentiated from all other Asian populations (F ST = 0.34-0.74). A neighbor-joining analysis using these F ST estimates also supports a division between European, North African, and Near East barley types from more easterly Asian accessions. There is also differentiation in the presence of a naked caryopsis and spikelet row number between eastern and western barley accessions. The data support the differential migration of barley from two domestication events that led to the origin of barley--one in the Fertile Crescent and another farther east, possibly at the eastern edge of the Iranian Plateau--with European and North African barley largely originating from the former and much of Asian barley arising from the latter. This suggests that cultural diffusion or independent innovation is responsible for the expansion of agriculture to areas of South and East Asia during the Neolithic revolution.     

Genomics at the origins of agriculture,part two

Agricultural expansion was such a momentous event that cultural or genetic evidence of its impact should be apparent. Abundant evidence indicates that agriculture was introduced into Europe at least 9,000 years ago. The primary issue remains whether agriculture spread by contact or by farmers moving into Europe. If agriculture was brought by farmers moving into foragers' territory, then genetic evidence should be apparent in the genes of modern Europeans. If foragers weredisplaced, then European genetic profiles should reflect the source population from the Near East. If there was interbreeding with the foragers who had a distinct genetic profile, then the genes of the Europeans descendants should reflect this admixture, with a clinal distribution of traits radiating from the Near East. These scenarios have been the focus of decades of debates between anthropologists and geneticists. In addition, genomic studies have been applied to pathogens in order to explore the link between agriculture and infectious disease.     

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.     

Sheep mitochondrial DNA variation in European, Caucasian, and Central Asian areas

Three distinct mitochondrial maternal lineages (haplotype Groups A, B, and C) have been found in the domestic sheep. Group B has been observed primarily in European domestic sheep. The European mouflon carries this haplotype group. This could suggest that European mouflon was independently domesticated in Europe, although archaeological evidence supports sheep domestication in the central part of the Fertile Crescent. To investigate this question, we sequenced a highly variable segment of mitochondrial DNA (mtDNA) in 406 unrelated animals from 48 breeds or local varieties. They originated from a wide area spanning northern Europe and the Balkans to the Altay Mountains in south Siberia. The sample included a representative cross-section of sheep breeds from areas close to the postulated Near Eastern domestication center and breeds from more distant northern areas. Four (A, B, C, and D) highly diverged sheep lineages were observed in Caucasus, 3 (A, B and C) in Central Asia, and 2 (A and B) in the eastern fringe of Europe, which included the area north and west of the Black Sea and the Ural Mountains. Only one example of Group D was detected. The other haplotype groups demonstrated signs of population expansion. Sequence variation within the lineages implied Group A to have expanded first. This group was the most frequent type only in Caucasian and Central Asian breeds. Expansion of Group C appeared most recently. The expansion of Group B involving Caucasian sheep took place at nearly the same time as the expansion of Group A. Group B expansion for the eastern European area started approximately 3,000 years after the earliest inferred expansion. An independent European domestication of sheep is unlikely. The distribution of Group A variation as well as other results are compatible with the Near East being the domestication site. Groups C and D may have been introgressed later into a domestic stock, but larger samples are needed to infer their geographical origin. The results suggest that some mitochondrial lineages arrived in northern Europe from the Near East across Russia.     

Historical biogeography of olive domestication (Olea europaea L.) as revealed by geometrical morphometry applied to biological and archaeological material

Aim This study intends to improve our understanding of historical biogeography of olive domestication in the Mediterranean Basin, particularly in the north-western area. Location Investigations were performed simultaneously on olive stones from extant wild populations, extant cultivated varieties from various Mediterranean countries, and archaeological assemblages of Spanish, French and Italian settlements. Methods A combination of morphometrics (traditional and geometrical) allowed us to study both the size and shape of endocarp structure. Concerning shape, a size-standardized method coupled with fitted polynomial regression analysis was performed. Results We found morphological criteria for discriminating between wild and cultivated olive cultivars, and established patterns of morphological variation of olive material according to the geographical origin (for extant material) and to the age of the olive forms (for archaeological material). Levels of morphological convergences and divergences between wild olive populations and cultivated varieties are presented as evidence. Main conclusions Morphological changes of endocarps of olive under domestication at both geographical and chronological scales provide new criteria for the identification of olive cultivars. They allow to determine the origins of cultivated forms created and/or introduced in the north-western Mediterranean regions and to understand how human migrations affected the rest of the Western Mediterranean regions. A model of diffusion of olive cultivation is proposed. It shows evidence of an indigenous origin of the domestication process, which is currently recognized in the north-western area since the Bronze Age.     

Mitogenomes from Egyptian Cattle Breeds: New Clues on the Origin of Haplogroup Q and the Early Spread of Bos taurus from the Near East

Background

Genetic studies support the scenario that Bos taurus domestication occurred in the Near East during the Neolithic transition about 10 thousand years (ky) ago, with the likely exception of a minor secondary event in Italy. However, despite the proven effectiveness of whole mitochondrial genome data in providing valuable information concerning the origin of taurine cattle, until now no population surveys have been carried out at the level of mitogenomes in local breeds from the Near East or surrounding areas. Egypt is in close geographic and cultural proximity to the Near East, in particular the Nile Delta region, and was one of the first neighboring areas to adopt the Neolithic package. Thus, a survey of mitogenome variation of autochthonous taurine breeds from the Nile Delta region might provide new insights on the early spread of cattle rearing outside the Near East.

Methodology

Using Illumina high-throughput sequencing we characterized the mitogenomes from two cattle breeds, Menofi (N = 17) and Domiaty (N = 14), from the Nile Delta region. Phylogenetic and Bayesian analyses were subsequently performed.

Conclusions

Phylogenetic analyses of the 31 mitogenomes confirmed the prevalence of haplogroup T1, similar to most African cattle breeds, but showed also high frequencies for haplogroups T2, T3 and Q1, and an extremely high haplotype diversity, while Bayesian skyline plots pointed to a main episode of population growth ~12.5 ky ago. Comparisons of Nile Delta mitogenomes with those from other geographic areas revealed that (i) most Egyptian mtDNAs are probably direct local derivatives from the founder domestic herds which first arrived from the Near East and the extent of gene flow from and towards the Nile Delta region was limited after the initial founding event(s); (ii) haplogroup Q1 was among these founders, thus proving that it underwent domestication in the Near East together with the founders of the T clades.