Robin G. Allaby

Current perspectives and the future of domestication studies

It is difficult to overstate the cultural and biological impacts that the domestication of plants and animals has had on our species. Fundamental questions regarding where, when, and how many times domestication took place have been of primary interest within a wide range of academic disciplines. Within the last two decades, the advent of new archaeological and genetic techniques has revolutionized our understanding of the pattern and process of domestication and agricultural origins that led to our modern way of life. In the spring of 2011, 25 scholars with a central interest in domestication representing the fields of genetics, archaeobotany, zooarchaeology, geoarchaeology, and archaeology met at the National Evolutionary Synthesis Center to discuss recent domestication research progress and identify challenges for the future. In this introduction to the resulting Special Feature, we present the state of the art in the field by discussing what is known about the spatial and temporal patterns of domestication, and controversies surrounding the speed, intentionality, and evolutionary aspects of the domestication process. We then highlight three key challenges for future research. We conclude by arguing that although recent progress has been impressive, the next decade will yield even more substantial insights not only into how domestication took place, but also when and where it did, and where and why it did not.

The complex origins of domesticated crops in the Fertile Crescent

A combination of genetics and archaeology is revealing the complexity of the relationships between crop plants and their wild ancestors. Archaeobotanical studies are showing that acquisition of the full set of traits observed in domesticated cereals was a protracted process, intermediate stages being seen at early farming sites throughout the Fertile Crescent. New genetic data are confirming the multiregional nature of cereal domestication, correcting a previous view that each crop was domesticated by a rapid, unique and geographically localised process. Here we review the evidence that has prompted this reevaluation of the origins of domesticated crops in the Fertile Crescent and highlight the impact that this new multiregional model is having on modern breeding programmes.

The genetic expectations of a protracted model for the origins of domesticated crops

Until recently, domestication has been interpreted as a rapid process with little predomestication cultivation and a relatively rapid rise of the domestication syndrome. This interpretation has had a profound effect on the biological framework within which investigations into crop origins have been carried out. A major underlying assumption has been that artificial selection pressures were substantially stronger than natural selection pressures, resulting in genetic patterns of diversity that reflect genetic independence of geographic localities. Recent archaeobotanical evidence has overturned the notion of a rapid transition, resulting in a protracted model that undermines these assumptions. Conclusions of genome-wide multilocus studies remain problematic in their support of a rapid-transition model by indicating that domesticated crops appear to be associated by monophyly with only a single geographic locality. Simulations presented here resolve this conflict, indicating that the results observed in such studies are inevitable over time at a rate that is largely influenced by the long-term population size. Counterintuitively, multiple origin crops are shown to be more likely to produce monophyletic clades than crops of a single origin. Under the protracted transition, the importance of the rise of the domestication syndrome becomes paramount in producing the patterns of genetic diversity from which crop origins may be deduced. We identify four different interacting levels of organization that now need to be considered to track crop origins from modern genetic diversity, making crop origins a problem that could be addressed through system-based approaches.

Convergent evolution and parallelism in plant domestication revealed by an expanding archaeological record

Significance Agriculture was a transformative development in the history of human societies and natural environments and drove the evolution of new domesticated species. Crop plants are the predominant domesticated species in most agricultural systems and are an essential component in all the food production systems that underpinned the development of urban societies. Archaeological plant remains provide a range of insights into the processes by which plants were domesticated in different parts of the world. The present paper provides a unique synthesis of evidence, including quantitative evidence on the trajectory and rate of domestication in seed crops and patterns in the development of tropical vegetatively propagated crops. Recent increases in archaeobotanical evidence offer insights into the processes of plant domestication and agricultural origins, which evolved in parallel in several world regions. Many different crop species underwent convergent evolution and acquired domestication syndrome traits. For a growing number of seed crop species, these traits can be quantified by proxy from archaeological evidence, providing measures of the rates of change during domestication. Among domestication traits, nonshattering cereal ears evolved more quickly in general than seed size. Nevertheless, most domestication traits show similarly slow rates of phenotypic change over several centuries to millennia, and these rates were similar across different regions of origin. Crops reproduced vegetatively, including tubers and many fruit trees, are less easily documented in terms of morphological domestication, but multiple lines of evidence outline some patterns in the development of vegecultural systems across the New World and Old World tropics. Pathways to plant domestication can also be compared in terms of the cultural and economic factors occurring at the start of the process. Whereas agricultural societies have tended to converge on higher population densities and sedentism, in some instances cultivation began among sedentary hunter–gatherers whereas more often it was initiated by mobile societies of hunter–gatherers or herder–gatherers.

Domestication as innovation: the entanglement of techniques, technology and chance in the domestication of cereal crops

Abstract The origins of agriculture involved pathways of domestication in which human behaviours and plant genetic adaptations were entangled. These changes resulted in consequences that were unintended at the start of the process. This paper highlights some of the key innovations in human behaviours, such as soil preparation, harvesting and threshing, and how these were coupled with genetic ‘innovations’ within plant populations. We identify a number of ‘traps’ for early cultivators, including the needs for extra labour expenditure on crop-processing and soil fertility maintenance, but also linked gains in terms of potential crop yields. Compilations of quantitative data across a few different crops for the traits of non-shattering and seed size are discussed in terms of the apparently slow process of domestication, and parallels and differences between different regional pathways are identified. We highlight the need to bridge the gap between a Neolithic archaeobotanical focus on domestication and a focus of later periods on crop-processing activities and labour organization. In addition, archaeobotanical data provide a basis for rethinking previous assumptions about how plant genetic data should be related to the origins of agriculture and we contrast two alternative hypotheses: gradual evolution with low selection pressure versus metastable equilibrium that prolonged the persistence of ‘semi-domesticated’ populations. Our revised understanding of the innovations involved in plant domestication highlight the need for new approaches to collecting, modelling and integrating genetic data and archaeobotanical evidence.

Cultivation and domestication had multiple origins: arguments against the core area hypothesis for the origins of agriculture in the Near East

Abstract This paper debates claims that plant domestication occurred rapidly in a single restricted sub-section of the Near Eastern Fertile Crescent. Instead we argue for numerous parallel processes of domestication across the region in the Early Holocene. While a previous generation of genetic results seemed to support a single ‘core area’, the accumulation of genetic evidence and refinements in methods undermine this, pointing increasingly towards multiple geographical origins. We stress that it is important to recognize that modern germplasm collections are an imperfect sample of the diversity of wild and cultivated populations of the past, which included some extinct lineages. We briefly synthesize the accumulated data from archaeobotany, defending the reliability of archaeological science to inform us about the past plant populations used by people. These data indicate an extended period of pre-domestication cultivation of at least a millennium and the slow evolution of morphological domestication adaptations in crop plants. The appearance of early cultivars and domesticates was spread piecemeal around the Near East, and a whole crop package is not evident. The ‘core area’ claimed by some authors has no better claim for primacy or completeness in comparison to other parts of the Near East. Evidence from zooarchaeology similarly points towards a diffuse appearance of various domesticated animals. The ‘non-centric’ appearance of domesticates from the Near East is therefore similar to the emerging evidence from many other regions of the world where plants were domesticated. We develop a hypothesis of why this should be expected given that anatomically modern human ancestors shared practices of vegetation management and planting, the necessary background knowledge for cultivation. Cultivation then was not a rare discovery but was a strategic and systematic shift in economies. The question then becomes why it was developed in the particular regions and periods where it appeared.

Elevated substitution rates estimated from ancient DNA sequences.

Ancient DNA sequences are able to offer valuable insights into molecular evolutionary processes, which are not directly accessible via modern DNA. They are particularly suitable for the estimation of substitution rates because their ages provide calibrating information in phylogenetic analyses, circumventing the difficult task of choosing independent calibration points. The substitution rates obtained from such datasets have typically been high, falling between the rates estimated from pedigrees and species phylogenies. Many of these estimates have been made using a Bayesian phylogenetic method that explicitly accommodates heterochronous data. Stimulated by recent criticism of this method, we present a comprehensive simulation study that validates its performance. For datasets of moderate size, it produces accurate estimates of rates, while appearing robust to assumptions about demographic history. We then analyse a large collection of 749 ancient and 727 modern DNA sequences from 19 species of animals, plants and bacteria. Our new estimates confirm that the substitution rates estimated from ancient DNA sequences are elevated above long-term phylogenetic levels.

DNA from primitive maize landraces and archaeological remains: implications for the domestication of maize and its expansion into South America

Abstract To study the origins of South American maize, without the complicating factors introduced by the extensive movement of genotypes during the post-Columbian period, we made a genetic analysis of primitive landraces and preserved maize remains. Fifteen alcohol dehydrogenase 2 ( Adh2 ) allele sequences were obtained from the landraces and 11 from the archaeological specimens. When these and six previously published Adh2 sequences were aligned, three allele groups were seen, distinguished by the structure of a dinucleotide repeat sequence. The three allele groups had distinct distributions within South America, the distributions supporting a model in which the two Central American agricultural systems—highland and lowland—generated separate expansions of maize cultivation into South America. One expansion centred on a highland culture that spread from Central America through the Panama highlands into the Andean regions on the western side of South America, and the second expansion centred on a lowland culture which spread along the lowlands of the northeast coast of South America, entering the continent through the river systems. The Adh2 biogeography was consistent with limited cultural contact across the Andes between northern Chile and Paraguay. From the diversity of the Adh2 allele sequences, we deduced that maize has undergone a rapid rate of evolution since domestication.

Integrating the processes in the evolutionary system of domestication

Genetics has long been used as a source of evidence to understand domestication origins. A recent shift in the emphasis of archaeological evidence from a rapid transition paradigm of hunter-gatherers to agriculturalists, to a protracted transition paradigm has highlighted how the scientific framework of interpretation of genetic data was quite dependent on archaeological evidence, resulting in a period of discord in which the two evidence types appeared to support different paradigms. Further examination showed that the discriminatory power of the approaches employed in genetics was low, and framed within the rapid paradigm rather than testing it. In order to interpret genetic data under the new protracted paradigm it must be taken into account how that paradigm changes our expectations of genetic diversity. Preliminary examination suggests that a number of features that constituted key evidence in the rapid paradigm are likely to be interpreted very differently in the protracted paradigm. Specifically, in the protracted transition the mode and mechanisms involved in the evolution of the domestication syndrome have become much more influential in the shape of genetic diversity. The result is that numerous factors interacting over several levels of organization in a domestication system need to be taken into account in order to understand the evolution of the process. This presents a complex problem of integration of different data types which is difficult to describe formally. One possible way forward is to use Bayesian approximation approaches that allow complex systems to be measured in a way that does not require such formality.

Sedimentary DNA from a submerged site reveals wheat in the British Isles 8000 years ago

Early wheat movement into Britain The transition into the New Stone Age, or Neolithic period, in Great Britain and Europe was characterized by a change from hunter-gatherers to farmers. However, the early stages of this transition are not well understood. Smith et al. studied archaeological remains at an 8000-year-old site that has been underwater ever since the Neolithic (see the Perspective by Larson). The finds include evidence of wheat (or a relative of wheat) 2000 years before the first documented farmers in Britain. It seems that trade may have preceded the adoption of farming. Science, this issue p. 998; see also p. 945 Wheat was being consumed in Britain 2000 years earlier than expected. [Also see Perspective by Larson] The Mesolithic-to-Neolithic transition marked the time when a hunter-gatherer economy gave way to agriculture, coinciding with rising sea levels. Bouldnor Cliff, is a submarine archaeological site off the Isle of Wight in the United Kingdom that has a well-preserved Mesolithic paleosol dated to 8000 years before the present. We analyzed a core obtained from sealed sediments, combining evidence from microgeomorphology and microfossils with sedimentary ancient DNA (sedaDNA) analyses to reconstruct floral and faunal changes during the occupation of this site, before it was submerged. In agreement with palynological analyses, the sedaDNA sequences suggest a mixed habitat of oak forest and herbaceous plants. However, they also provide evidence of wheat 2000 years earlier than mainland Britain and 400 years earlier than proximate European sites. These results suggest that sophisticated social networks linked the Neolithic front in southern Europe to the Mesolithic peoples of northern Europe.