Review Tansley review Patterns and processes in crop domestication: an historical review and quantitative analysis of 203 global food crops Author for correspondence: Rachel S. Meyer1,2*, Ashley E. DuVal3* and Helen R. Jensen4* Helen Jensen 1 2 Tel: +1 514 425 3540 The New York Botanical Garden, Science Division, Bronx, NY 10458, USA; The Graduate Center, City University of New York, Email: [email protected] Biology Program, 365 Fifth Ave, New York, NY 10016, USA; 3Yale University, School of Forestry and Environmental Studies, 195 Prospect Street, New Haven, CT 06511, USA; 4McGill University, Department of Biology, 1205 Dr Penfield Avenue, Montreal, Received: 13 May 2012 QC, Canada H3A 1B1 Accepted: 15 June 2012 Contents Summary 1 VII. Reproductive strategies 12 I. Introduction 2 VIII. The domestication syndrome 14 II. Key concepts and definitions 2 IX. Spatial and temporal trends 14 III. Methods of review and analysis 7 X. Utilization of plant parts 16 IV. Trends identified from the review of 203 crops 9 XI. Conclusions 16 V. Life cycle 10 Acknowledgements 17 VI. Ploidy level 12 References 17 Summary New Phytologist (2012) Domesticated food crops are derived from a phylogenetically diverse assemblage of wild doi: 10.1111/j.1469-8137.2012.04253.x ancestors through artificial selection for different traits. Our understanding of domestication, however, is based upon a subset of well-studied ‘model’ crops, many of them from the Poa- Key words: center of origin, conservation, ceae family. Here, we investigate domestication traits and theories using a broader range of domestication, domestication syndrome, crops. We reviewed domestication information (e.g. center of domestication, plant traits, wild ethnobotanical uses, food crops, life history, ancestors, domestication dates, domestication traits, early and current uses) for 203 major selection. and minor food crops. Compiled data were used to test classic and contemporary theories in crop domestication. Many typical features of domestication associated with model crops, including changes in ploidy level, loss of shattering, multiple origins, and domestication outside the native range, are less common within this broader dataset. In addition, there are strong spatial and temporal trends in our dataset. The overall time required to domesticate a species has decreased since the earliest domestication events. The frequencies of some domestication syndrome traits (e.g. nonshattering) have decreased over time, while others (e.g. changes to secondary metabolites) have increased. We discuss the influences of the ecological, evolutionary, cultural and technological factors that make domestication a dynamic and ongoing process. *These authors contributed equally to this work. Ó 2012 The Authors New Phytologist (2012) 1 New Phytologist Ó 2012 New Phytologist Trust www.newphytologist.com New 2 Review Tansley review Phytologist I. Introduction 1. Historical context The transition from hunter-gatherer societies to settled agri- It is estimated that 2500 plant species have undergone domes- culture (the ‘Neolithic revolution’; Childe, 1949) occurred inde- tication worldwide, with over 160 families contributing one pendently over a dozen times in different regions around the world or more crop species (Zeven & de Wit, 1982; Dirzo & from c. 10–12 000 yr ago (ya) to as recently as 3000–4000 ya Raven, 2003). Much of our understanding of the processes (Diamond, 2002; Diamond & Bellwood, 2003). Theories to driving domestication comes from a subset of well-studied explain the origins and development of agriculture have consid- crops, particularly crops of major economic importance and ered factors ranging from changes in climate and population model crops (i.e. crops that have had their genomes analyzed expansion to cultural practices and religious beliefs (Harlan, and are transformable). These crops have been critical for 1992). developing our fundamental understanding of domestication Current works continue to explore when, where, why and how as a continuum of ongoing processes. In particular, they have wild plants became our modern food crops, while also consider- been critical for revealing the underlying genetic mechanisms ing the new technical, ethical and environmental challenges of responsible for the suite of phenotypic changes associated with emerging agricultural technologies (Murphy, 2007; Vaughan domestication that comprise the domestication syndrome. et al., 2007; Ellstrand et al., 2010; Thrall et al., 2010; Cuevas- They have also contributed to our knowledge of useful crop Badallo & Vermaas, 2011; Domingo & Gine´ Bordonaba, 2011; breeding traits, such as pathogen resistance, and of fundamen- Ekici & Sancak, 2011). In recent years, scientists have used tal biological processes, such as polyploidization. However, molecular techniques to test and apply theories of crop origins information on such well-studied crops contributes dispropor- put forward 150 yr ago by Darwin (1868) and De Candolle tionately to the literature on domestication. In order to (1884) (Doebley et al., 1995; Gepts, 2004; Zohary, 2004; Fuller, explore global trends and historical patterns in domestication, 2007; Gregory, 2009; Brown, 2010). New works have increas- large datasets are required that consider a broad selection of ingly recognized the importance of combining the relevant data species, including understudied crops and crops of minor eco- from several fields to inform observations on crop domestication nomic importance, in addition to well-studied major global (Kroll, 2000; Nesbitt & Tanksley, 2002; Zeder et al., 2006; crops. Often, the data relevant to the history of use, selection Vaughan et al., 2007; Wang et al., 2008; Purugganan & Fuller, and domestication of a particular crop are scattered across the 2009; Richards et al., 2009; Meyer et al., 2012). literature of diverse disciplines. For many minor food plants, Although recent innovations are causing drastic modifications information relevant to domestication history may be difficult to the domestication pathways for many species (Vaughan et al., to access, if it is available at all. Most reviews have not 2007), domestication has always been a dynamic process. New included all the major agricultural regions but rather have artificial selection pressures have arisen throughout the history of concentrated on regional subsets of crops (Duke & Terrell, crop cultivation driven by many factors, including new uses for 1974; Harlan, 1992), or focused on specific groups, including existing crops (e.g. grain crops adapted for biofuel production) recent studies of the Asteraceae (Dempewolf et al., 2008) and and the movement of crops to new environments. These have Poaceae (Gle´min & Bataillon, 2009), and on previously neglected continually reshaped the evolution and geographic distribution groups such as vegetatively propagated crops, perennials, and of crops over time. underutilized crops (Padulosi et al., 2002, 2011; McKey et al., 2010; Miller & Gross, 2011). This review considers information on 203 major and minor II. Key concepts and definitions crop plants compiled across 36 categories, including center of domestication, changes in phenotype and use from the wild 1. Food crop to the cultivated forms, uses, exploited organs, and conser- To meet our criterion of being a food crop, a plant species must vation status. The threefold objectives of this paper are: to have been used at some time as a food, spice, edible oil, beverage, identify and interpret patterns in domestication by identifying or fasting aid with nutritional value (e.g. khat). In the cases of trends across numerous categories of data on crop domesti- some of the crops we selected, food uses are secondary, such as cation and use; to test current and classic theories in domesti- fiber crops with oil seeds (e.g. cotton, flax, hemp). cation against this large sample; and to identify promising areas for further research based on the critical questions and gaps in the literature identified by this study. Data summa- 2. Reproductive strategy ries and key analyses are presented and discussed in this Many wild plant species are characterized by more than one review, while more detailed information, further analy- reproductive strategy, including sexual breeding systems (e.g. out- ses and crop bibliographies are provided as Supporting crossing or self-fertilizing), and asexual strategies (e.g. vegetative Information (Tables S1–S6). Updated versions of crop bib- or clonal propagation). Under cultivation, however, only one of liographies (Tables S2, S4, S5) are maintained at: www. these strategies is usually exploited as a propagation method for a cropdomestication.com. New Phytologist (2012) Ó 2012 The Authors www.newphytologist.com New Phytologist Ó 2012 New Phytologist Trust New Phytologist Tansley review Review 3 given species. Here, we refer to crop reproductive strategies based can therefore work in opposition to natural selection, and domes- on the strategy primarily used under cultivation. ticated crops have reduced fitness, or, in some cases, an inability to survive outside of cultivation (Gepts, 2004; Pickersgill, 2007; Allaby et al., 2008; Purugganan & Fuller, 2011). 3. Domestication syndrome Selection can be unconscious or conscious. In unconscious The suite of traits that marks a crop’s divergence from its wild selection, likely the driver of many early domestications, the act ancestor(s) is defined as the ‘domestication syndrome’ (Harlan, of moving plants from the wild into man-made environments