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Home , Plant breeding

Plant breeding and farmer participation breeding and farmer participation

Edited by

S. Ceccarelli

E.P. Guimarães

E. Weltzien

FOOD AND ORGANIZATION OF THE UNITED NATIONS Rome, 2009 The conclusions given in this report are considered appropriate at the time of its preparation. They may be modified in the light of further knowledge gained at subsequent stages.

The designations employed and the presentation of material in this information product do not imply the expression of any opinion whatsoever on the part of the and Agriculture Organization of the United Nations (FAO) concerning the legal or development status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. The mention of specific companies or products of manufacturers, whether or not these have been patented, does not imply that these have been endorsed or recommended by FAO in preference to others of a similar that are not mentioned.

The views expressed in this information product are those of the authors and do not necessarily reflect the views of the Food and Agriculture Organization of the United Nations. ISBN 978-92-5-106382-8

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© FAO 2009 iii

Contents

Foreword vii Abbreviations and acronyms ix Contributors xiii

Chapter 1 domestication and the first plant 1 S!"# C$%

Chapter 2 Theory and application of plant breeding for quantitative traits 27 J"&'() B(!)*#, J(+ú+ M$)(#$-G$#/*0(/ "#1 I2#"3'$ R$4"2$+"

Chapter 3 Main stages of a plant breeding programme 63 S"0&"!$)( C(33")(00'

Chapter 4 Methodologies for priority setting 75 E&" W(0!/'(# "#1 A#5" C6)'+!'#37

Chapter 5 Methodologies for generating variability. Part 1: Use of genetic resources in plant breeding 107 B(!!'#" I.G. H":++4"## "#1 H('7$ K. P")/'(+

Chapter 6 Methodologies for generating variability. Part 2: Selection of parents and crossing strategies 129 J$6# R. W'!3$4;( "#1 D"05'! S. V')7

Chapter 7 Methodologies for generating variability. Part 3: The development of base and their improvement by recurrent selection 139 J$6# R. W'!3$4;(

Chapter 8 Methodologies for generating variability. Part 4: Mutation techniques 159 M')$+0"< M"0:+/=#+7', I<$#" S/")(57$, C6'!!")"#5"# R. B6"!'", K")'# N'36!()0('# "#1 P'())( J.L. L"2$1" iv

Chapter 9 Selection methods. Part 1: Organizational aspects of a plant breeding programme 195 S"0&"!$)( C(33")(00'

Chapter 10 Selection methods. Part 2: Pedigree method 223 F0"&'$ C">(!!'#'

Chapter 11 Selection methods. Part 3: breeding 229 D$#"01 N. D:&'37

Chapter 12 Selection methods. Part 4: Developing open-pollinated varieties using recurrent selection methods 259 F)(1 R"!!:#1(, K')+!(# &$4 B)$37(, E&" W(0!/'(# "#1 B(!!'#" I.G. H":++4"##

Chapter 13 Selection methods. Part 5: Breeding clonally propagated 275 W$0?2"#2 G)@#(;()2, R$;()! M<"#2", M")'" A#1)"1( "#1 J$)2( E+>'#$/"

Chapter 14 Breeding for quantitative variables. Part 1: Farmers’ and ’ knowledge and practice in choice and plant selection 323 D"#'(0" S$0()' "#1 D"&'1 A. C0(&(0"#1

Chapter 15 Breeding for quantitative variables. Part 2: Breeding for durable resistance to crop pests and diseases 367 R"$:0 A. R$;'#+$#

Chapter 16 Breeding for quantitative variables. Part 3: Breeding for resistance to abiotic stresses 391 S!(?"#'" G)"#1$ "#1 S"0&"!$)( C(33")(00'

Chapter 17 Breeding for quantitative variables. Part 4: Breeding for nutritional quality traits 419 Y:+:? G(#3, J:0'" M. H:4>6)'(+, G)"6"4 H. L=$#+ "#1 R$;'# D. G)"6"4 v

Chapter 18 Breeding for quantitative variables. Part 5: Breeding for yield potential 449 J$+O L. A)":+, G:+!"&$ A. S0"?(), M"!!6(< P. R(=#$01+ "#1 C$#%'!" R$=$

Chapter 19 Marker-assisted selection in theory and practice 479 A#1)(< R. B"))

Chapter 20 Coping with and exploiting -by-environment interactions 519 P"$0$ A##'336'")'3$

Chapter 21 Variety release and policy options 565 Z(<1'( B'+6"< "#1 A#!6$#= J.G. &"# G"+!(0

Chapter 22 Participatory seed diffusion: experiences from the field 589 H:4;()!$ RQ$+ L";)"1"

Chapter 23 Towards new roles, responsibilities and rules: the case of participatory plant breeding 613 R$##'( V()#$$= <'!6 P)"!"> S6)(+!6", S"0&"!$)( C(33")(00', H:4;()!$ RQ$+ L";)"1", Y'36'#2 S$#2 "#1 S"00= H:4>6)'(+

Chapter 24 Breeders’ rights and IPR issues 629 S:+"##( S$4()+"0$ "#1 J$6# D$11+

Chapter 25 The impact of participatory plant breeding 649 J"3T:(0'#( A. A+6;= vii

Foreword

Participatory Plant Breeding (PPB) originated in the early 1980s as part of a movement promoting the concept of participatory research, in response to criticisms of the failure of post-green-revolution, experiment-station-based research to address the needs of poor farmers in developing countries. Rooted in debate over the social consequences of the narrow focus of the scientific type of research, PPB gained recognition as an activity mostly promoted by social scientists and agronomists based in anti-establishment non- governmental organizations (NGOs). In consequence, rather than being perceived from the beginning as an additional option available to breeders, PPB for a long time had the image of being one of two contrasting types of plant breeding, with PPB being more “socially correct” than conventional plant breeding. Even now, nearly thirty years later, this view is still common. Few professional breeders accept that farmers can be full partners in a plant breeding programme, even though everyone agrees that it was farmers that domesticated crops about 10 000 years ago and, in some regions of the world, continued to modify and manipulate them to the present day. Even before the re-discovery of Mendel’s laws of inheritance, the work of a number of amateur breeders become an inspiration for Darwin’s theories. In several respects, the relationship with farmers on which PPB is based is similar to the ways in which plant breeders worked with producers in North America and Europe in the early twentieth century. At that time it was commonplace for breeders to spend time interacting with producers, and to test new materials collaboratively in farmers’ fields in order to understand what producers considered to be desirable traits for an improved variety. However, the combination of industrialization of agriculture and formal training for plant breeders created a gap between breeders and farmers, a gap that was exported to developing countries in the post-war era. As the profession of plant breeding lost the habit of interacting closely with producers, concern for how to address farmers’ needs and constraints fell by the wayside. PPB revived this as a central issue, because by the late 1970s it was increasingly evident in developing countries that post-green-revolution “improved” varieties were too often failing to satisfy farmer requirements and were being shunned. Today there is widespread recognition that the conventional package of new varieties and external inputs, while successful in the more favourable production areas, has often failed to benefit small-scale farmers in marginal areas. As a result, the vital role of PPB as an additional strategy is better understood. Experience has taught that PPB is complementary to conventional plant breeding rather than an alternative type of plant breeding. Demand for a complementary approach has expanded considerably because of pressure to ensure the relevance of research to poor farmers and their diverse agricultural systems, and because PPB allows selection for the specific adaptation required for such a diversity of target environments. Today, about 80 participatory breeding programmes are known worldwide, involving various institutions and various crops. In 2000, an international review of plant viii

breeding research methodologies concluded that PPB should be an “organic” part of every plant breeding programme aimed at benefiting small-scale farmers in difficult, high- risk environments. In fact, traditional farming and low-input systems, including organic agriculture, are a very heterogeneous of target environments and not easily served by centralized, conventional plant breeding. The book demonstrates that PPB is in essence no different from conventional plant breeding, being based on the very same principles of Mendelian, quantitative and population , and therefore has complemented the traditional approach to plant breeding with a number of chapters addressing issues specifically related to the participation of farmers in a plant breeding programme. The authors of the various chapters have been carefully selected to represent three groups of scientists: the first comprises internationally recognized experts in genetics as related to plant breeding, and in the various aspects of plant breeding (from general methodological issues to more specific issues, such as breeding for resistance to biotic and abiotic stresses, high yield potential, and genotype × environment interactions); the second group is represented by professional breeders who have actually practised participatory plant breeding with a number of different crops and in a number of socially and climatically different areas, using the range of methods presented by the first group; and, finally, the third is represented by a group of scientists with specific expertise in areas not usually covered in classical plant breeding books, such as variety release mechanisms, seed diffusion, institutional issues associated with PPB, and rights. A chapter documenting the impact that participatory plant breeding has had after about thirty years of practice has been chosen to be the logical conclusion of the book. The book is aimed at plant breeders, social scientists, students and practitioners, with the hope that they all will find a common ground to discuss ways in which plant breeding can be beneficial to all and can contribute to alleviate poverty. Finally, we would like to acknowledge everyone who has, directly or indirectly, contributed to the book: the CGIAR Participatory Research and Gender Analysis Program (PRGA) for the initial idea of producing such a book, the contributors of the chapters for sharing their scientific experience and for enduring a number of revisions of their respective chapters, Dr P.G. Rajendran for his help in the initial editorial efforts and the Directors-General of our Institutions for their continuous support. Final editing and preparation for publication was done by Mr Thorgeir Lawrence. ix

Abbreviations and acronyms

AB-QTL Advanced Backcross QTL Analysis AFLP Amplified fragment length polymorphism AMMI Additive main effects and multiplicative interaction AMOVA Analysis of molecular variance ANOVA Analysis of variance AOSCA Association of Official Seed Certifying Agencies ABS Accelerated Breeding System [for sweet ] ASSINSEL International Association of Plant Breeders for the Protection of Plant Varieties AVP Asexually or vegetatively propagated

BC n Back-cross generation n BLUE Best Linear Unbiased Estimate BLUP Best Linear Unbiased Prediction BPE Before present era BSA Bulked Segregant Analysis Bt [] BYDV Yellow Dwarf CBD Convention on Biological Diversity CBP Centralized breeding programmes CCN cyst nematode CE Common era CGIAR Consultative Group for International Agricultural Research CIDA Canadian International Development Agency CIE Commission Internationale l’Eclairage CIAL Local agricultural research committees [in Latin America] CIAT International Center for CIMMYT International and Improvement Center CIP International Potato Center CPB Conventional plant breeding cv [= cultivated variety] DArT Diversity Arrays Technology DBP Decentralized breeding programmes dES Diethyl sulphate [a ] DF Degrees of freedom DH Doubled haploid DHPLC Denaturating high performance liquid chromatography DM Dry matter x

DPBP Decentralized-participatory breeding programmes DUS Distinctness, Uniformity, Stability DW Dry weight ELISA Enzyme-linked immunosorbent assay EMS Ethane methyl sulphonate [a mutagen] EPA Environmental Protection Agency [ of America]

Fn Filial generation n FAO Food and Agriculture Organization of the United Nations FDA Food and Drug Administration [United States of America] FFS Farmer field school FIPAH La Fundación para La Investigación Participativa con Agricultores de Honduras FK Farmer knowledge FPB Formal plant breeding FR Farmers’ Rights FV farmer variety [± locally selected] G×E Genotype × Environment (Interaction) GGE Genotype main effect (G) plus Genotype × Environment (GE) Interaction GIS Geographical Information System GMO Genetically modified organism GURT Genetic Use Restriction Technology G×L Genotype × Location G×Y Genotype × Year HPLC High performance liquid chromatography IAEA International Atomic Energy Agency IARC International Agricultural Research Center ICARDA International Center for Agricultural Research in the Dry Areas ICP Inductively coupled plasma [mass spectrometry] ICPOES Inductively Coupled Plasma Optical Emission Spectrometer ICRISAT International Crops Research Institute for the Semi-Arid Tropics ID depression IDRC International Development Research Centre [Canada] IFPRI International Food Policy Research Institute IITA International Institute of Tropical Agriculture INCA National Institute for [Cuba] IP Intellectual property IPGRI International Plant Genetic Resources Institute [now Bioversity International] IPM Integrated management IPR Intellectual Property Rights IRRI International Rice Research Institute ITPGRFA International Treaty on Plant Genetic Resources for Food and Agriculture LD Linkage disequilibrium xi

LD 50 Lethal dose killing 50% of target

LD 100 Lethal dose killing 100% of target MAS Marker-assisted selection MCA Multiple correspondence analysis MET Multi-environment Trials MFN Most favoured nation MNU Methylnitrosourea [a mutagen] MRRS Modified reciprocal recurrent selection MS Mean square MTA Material Transfer Agreement MV Modern variety MVD [FAO/IAEA] Varieties Database NARS National agricultural research system NDVI Normalized Difference Vegetation Index NERICA NIL Near-isogenic line NIRS Near Infrared Spectroscopy NIR Near-infrared [spectrum] OECD Organisation for Economic Co-operation and Development OFSP Orange-fleshed sweet potato OPC Open-pollinated cultivar PBK Plant knowledge PBR Plant breeder’s rights PC Principal components PCR Polymerase chain reaction PGR Plant genetic resources PPB Participatory plant breeding PRA Participatory rural appraisal PRGA [CGIAR] Participatory Research and Gender Analysis [Program] PRI Photochemical reflectance index PSD Participatory seed dissemination PVP Protection PVS Participatory varietal selection PVX Potato virus X PVY Potato virus Y QTL R&D Research and development RAPD Random amplified polymorphic DNA RCB Randomized complete block [experiment design] REML Restricted Maximum Likelihood RFLP Restriction fragment length polymorphism RFSRS Reciprocal full-sib recurrent selection RIL Recombinant inbred line xii

RRS Reciprocal recurrent selection

Sn Selfed generation n SD Standard deviation SE Selection environment SE Standard error SFNB Spot form of Net blotch SMTA Standard Material Transfer Agreement SNP Single nucleotide polymorphism SPCSV Sweet potato chlorotic stunt virus SPFMV Sweet potato feathery mottle virus SPVD Sweet potato virus disease SR Simple Ratio Vegetation Index SS Sum of squares SSR Simple sequence repeat SSTW Small-scale Third World TGV Transgenic crop variety TILLING Targeting Induced Local Lesions In TLC Thin-layer chromatography TPE Target population of environment TPS True potato seed TRIPs [Agreement on] Trade-Related Aspects of Intellectual Property Rights UPOV International Union for the Protection of New Varieties of USDA United States Department of Agriculture UV Ultraviolet [] VCU Value for Cultivation and Use VIS Visible spectrum WARDA Africa Rice Centre [formerly the West Africa Rice Development Association] WI Water index WIPO World Intellectual Property Organization WTO World Trade Organization WUE Water-use efficiency xiii

Contributors

Maria I. ANDRADE Zewdie BISHAW International Potato Center (CIP), Head, Seed Unit, ICARDA, PO Box 5466, Avenida das FPLM 2698, PO Box 2100 Aleppo, Maputo, Syrian Arab Republic Mozambique Flavio CAPETTINI Paolo ANNICCHIARICO International Center for Agricultural CRA - Centro di Ricerca per le Research in the Dry Areas (ICARDA), Produzioni Foraggere e Lattiero-Casearie, PO Box 5466, Aleppo, viale Piacenza 29, I-26900 Lodi, Syrian Arab Republic Italy Salvatore CECCARELLI José Louis ARAUS formerly with The International Center International Maize and Wheat for Agricultural Research in the Dry Areas Improvement Centre (CIMMYT), (ICARDA), PO.Box 5466, Aleppo, Apdo. Postal 6-641, 06600 México, D.F., Syrian Arab Republic Mexico Anja CHRISTINCK Jacqueline A. ASHBY Gichenbach 54, D-36129 Gersfeld, International Potato Centre (CIP), Lima, Peru David A. CLEVELAND Andrew R. B ARR Environmental Studies Program, Affiliate Professor, University of Adelaide, University of California, Santa Barbara, Waite Campus, Glen Osmond, South CA 93106-4160, Australia 5064 United States of America

Javier BETRÁN Stan COX Syngenta Seeds, , 2440 E. Water Well St. Sauveur, Rd., Salina, Kansas 67401, France United States of America

Chittaranjan R. BHATIA John DODDS New Bombay 400 703, Dodds and Associates, 1707 N Street NW, India Washington DC 20036, United States of America xiv

Donald N. DUVICK ( DECEASED ) Julia M. HUMPHRIES formerly with Department of , Department of Clinical Pharmacology, Iowa State University, Ames, Iowa, Flinders Medical Centre, United States of America Bedford Park SA 5042, Australia Jorge ESPINOZA International Potato Center (CIP) Sally HUMPHRIES Apartado 1558, Lima 12, Department of Sociology and Peru Anthropology, MacKinnon Building, University of Guelph, Guelph, ON, Yusuf GENC Canada, N1G 2W1 Molecular Plant Breeding Cooperative Research Centre, University of Adelaide, Humberto RÍOS L ABRADA Waite Campus, PMB 1, National Institute of Agricultural Sciences, Glen Osmond SA 5064, Havana, Cuba Australia Pierre J.L. LAGODA Robin D. GRAHAM Plant Breeding and Genetics Section, Joint School of Agriculture, Food and Wine, FAO/IAEA Division, Vienna, University of Adelaide, Waite Campus, Austria PMB 1, Glen Osmond SA 5064, Australia Graham H. LYONS School of Agriculture , Food and Wine, Stefania GRANDO University of Adelaide, Waite Campus, International Center for Agricultural PMB 1, Glen Osmond SA 5064, Research in the Dry Areas (ICARDA), Australia P.O. Box 5466, Aleppo, Syrian Arab Republic Miroslaw MALUSZYNSKI Department of Genetics, University of Wolfgang GRÜNEBERG Silesia, Katowice, International Potato Center (CIP) Poland Apartado 1558, Lima 12, Peru Jesús MORENO -G ONZÁLEZ Centro de Investigaciones Agrarias de Bettina I.G. HAUSSMANN Mabegondo, Xunta de Galicia, International Crops Research Institute for Spain the Semi-Arid Tropics (ICRISAT), BP 12404, Niamey, Robert MWANGA Niger National Crops Resources Research Institute (NCRRI), Namulonge, Box 7084, Kampala, Uganda xv

Karin NICHTERLEIN Pratap K. SHRESTHA Food and Agriculture Organization of Local Initiatives for , Research the United Nations (FAO), Research and and Development (LI-BIRD), P.O. Box Extension Division, 00153 Rome, 324, Pokhara, Kaski, Italy Nepal

Heiko K. PARZIES Gustavo A. SLAFER University of Hohenheim, Institute ICREA (Catalonian Institution for of Plant Breeding, Seed Science and Research and Advanced Studies) and Population Genetics, D-70593 Stuttgart, Department of Crop and Forest Sciences, Germany University of Lleida, Centre UdL-IRTA, Av. Rovira Roure 191, 25198 Lleida, Fred RATTUNDE Spain International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), BP 320, Daniela SOLERI Bamako, Department of Geography, University of Mali California, Santa Barbara, CA 93106-4060, United States of America Matthew P. REYNOLDS International Maize and Wheat Susanne SOMERSALO Improvement Centre (CIMMYT), Apdo. Dodds and Associates, 1707 N Street NW, Postal 6-641, 06600 México, D.F., Washington DC 20036, Mexico United States of America

Raoul A. ROBINSON Yiching SONG Retired Agricultural Botanist 445 Provost Center for Chinese Agricultural Policy Lane, Fergus, Ontario, (CCAP), Chinese Academy of Sciences, Canada, N1M 2N3 Institute of Geographical Sciences and Natural Resources Research Jia 11, Ignacio ROMAGOSA Datun Road, Anwai, Beijing 100101 Centre UdL-IRTA, Universitat de Lleida, China Lleida, Spain Iwona SZAREJKO Department of Genetics, University of Conxita ROYO Silesia, Katowice, Institut de Recerca i Tecnologia Poland Agroalimentˆries (IRTA), Area de Conreus Extensius, Centre UdL-IRTA, Alcalde Anthony J.G. VAN G ASTEL Rovira Roure 191, 25198 Lleida, Harspit 10, 8493KB, Terherne, Spain Netherlands xvi

Ronnie VERNOOY Eva WELTZIEN International Development Research International Crops Research Institute for Centre (IDRC), 150 Kent Street, PO Box the Semi-Arid Tropics (ICRISAT), BP 320, 8500, Ottawa, ON, Bamako, Mali Canada, K1G 3H9 John R. WITCOMBE Daljit S. VIRK CAZS-Natural Resources, Bangor CAZS-Natural Resources, Bangor University, Bangor LL57 2UW, University, Bangor LL57 2UW, United Kingdom United Kingdom

Kirsten VOM B ROCKE Centre de Coopération Internationale en Recherche Agronomique pour le Dévelopment (Cirad) c/o ICRISAT, BP 320, Bamako, Mali 1

CHAPTER 1 Crop domestication and the first plant breeders

Stan Cox 2 Plant breeding and farmer participation

1.1 INTRODUCTION Conventional wisdom usually gains its If the story of modern from the status by being accurate in its generalities beginning to the present day could be com- but off the mark in some of its specifics. pressed into a feature-length movie, the As we will see, that is the case with crop era of crop domestication would occupy domestication. My purpose in this chapter a scene approximately six minutes long, is not to summarize the ‘where’ and ‘when’ starting about ten minutes from the movie’s of domestication, species by species, nor end. During that scene, the action would is it to analyse theories on the origins of be scattered and sporadic; the domestica- agriculture. Those tasks would entail the tion of any individual crop species would boiling-down, if not the over-cooking, of almost always occur in only a single local- a vast and fascinating literature (e.g. see ity and occupy only about 15 seconds to 2 Zeder et al ., 2006; Sauer, 1993; and Harris minutes of the film. and Hillman, 1989). Rather than attempt In that brief era, in those rare places to summarize that literature, I briefly tabu- where today’s crops were born, every lated in Table 1.1 what is believed to be farmer was a plant breeder. And through true, both geographically and chronologi- succeeding millennia, as agriculture spread cally, about the domestication of today’s across the surface of the planet, much of major crops. settled humanity came to participate in Keeping in mind that humanity’s brief plant breeding. experiment with domestication involved Studies of ancient artefacts and botanical people in every quadrant of the globe, I remains, ancient DNA, phytoliths, living will concentrate on the ‘how’ and ‘why’ of plant populations, and the agricultural domestication, on questions about the first practices of surviving indigenous societies plant breeders themselves and the species have converged to provide us with a they transformed: Why did they domes- vivid but still incomplete account of the ticate some species and not others? How first plant breeders’ genetic revolution. did their farming practices change gene fre- Conventional wisdom based on those quencies in plant populations? How long studies tells us that domestication was did domestication take? Why did people preceded by a period of archaic cultivation, select for particular traits: unconsciously, during which people encouraged the intentionally or indirectly? How did their growth of particular species and harvested actions affect the genetic structure and their seed or other plant parts; that diversity of today’s crop species? And, when people began to sow a portion finally, what kinds of skills and knowledge of their harvested seed, they selected— did they pass down to the farmer-breeders automatically and unconsciously—for of more recent times? of domestication, such as those Any effort to answer those questions curtailing seed dispersal and dormancy; and must draw upon examples from the availa- that, as our ancestors developed a mutual ble literature, in which today’s major crops, dependency with domesticated plants, largely and grain legumes, feature they became intentional and versatile plant most prominently. Although no set of breeders, selecting for a wide range of examples can represent the full geographi- desired traits in species grown for grains, cal and botanical range of domestication, I roots, tubers, fruits, or fodder. have attempted to rely upon those people, Crop domestication and the first plant breeders 3

TABLE 1.1 Species domesticated in each of eight world regions, with approximate age of the oldest evidence of domestication

Region Species Common name Age of the oldest evidence of domestication (years BPE)

West Asia Hordeum vulgare Barley 10 500 Triticum turgidum Wheat 10 500 Cicer arietinum Chickpea 9 500 Africa Sorghum bicolor Sorghum 8 000 a Pennisetum glaucum Pearl Millet ?(1) Eurasia Brassica campestris Rape 3 500 East Asia Oryza sativa Rice 7 000 Glycine max Soybean 4 000 New Guinea Musa spp. Banana 7 000 (2) Saccharum officinarum Sugar Cane ? South America Ipomoea batatas Sweet Potato 4 500 Arachis hypogaea Groundnut 4 500 Solanum tuberosum Potato 4 500 Manihot esculenta 4 500 Phaseolus vulgaris(3) Common Bean 7 500 Mesoamerica Zea mays Maize 7 500 Gossypium hirsutum Cotton 7 500 North America Helianthus annuus Sunflower 3 000

NOTES: (1) Wendorf et al. (1992) found archaeological evidence that wild millet and sorghum were being used in the Sahel 8000 years before present. The sorghum specimens showed evidence that they were in the process of domestication. (2) Denham et al., 2003. (3) Independently domesticated in Mesoamerica as well. Species listed are among the world’s 20 most widely grown crops, on a land-area basis (FAO, 2005). Information is from Sauer (1993) unless otherwise indicated. places and plants that best illustrate the abundance, annuality, lower seed dormancy, important features of domestication. diploidy, harvestability and relative ease of seed dehulling. 1.2 SELECTION AMONG SPECIES A common characteristic among crop There is little doubt that certain species ancestors was their weediness: their tenden- were ‘pre-adapted’ (Zohary, 1984) for cy to thrive in disturbed, fertile soils like domestication. Either entire populations or those associated with habitation. individual plants within populations had to The circumstances of domestication are, of attract the attention of humans before they course, different for every species. In some could be manipulated. With exceptions, places, people started out by harvesting plants or populations that exhibited conveniently large stands of annual grasses; unusually large or numerous edible parts; in others, variations on the so-called ‘rub- self- (in sexually propagated bish heap’ theme were at work (Hawkes, species); ease of propagation (in vegetatively 1969). Many crop ancestors were just as propagated species); or delayed seed responsible for seeking out humans and dispersal (e.g. chickpea: Ladizinsky, 1979) human-made environments as were peo- caught the eyes of early cultivators. Bar- ple for tracking down the plants. Indeed, Yosef and Kislev (1989) listed characteristics according to Hawkes (1969), it “must have of certain wild cereals (relative to other seemed little short of miraculous to find wild plant species) that attracted early west that plants needed for food sprang up by Asian domesticators: larger grain, local their very huts and paths”. 4 Plant breeding and farmer participation

In west Asia, however, those destined increase seed yield and produce perennial to become the first tended grain crops (DeHaan, Van Tassel and Cox, to make their homes near reliable water 2005), but only if the right combination of sources, whereas they gathered wild grains breeding objectives is established. from stands that were often some distance When we think of how many civi- away (Willcox, 2005). Also relying on lizations built on annual cropping have the west Asian domestication experience, fallen not to the sword but to the plough Abbo et al . (2005) labelled the rubbish-heap (Hillel, 1991; Lowdermilk, 1953) and the hypothesis ‘environmental determinism’ that soil degradation that continues to haunt “tends to underestimate the role of human agriculture today, we can only lament the initiative in the Neolithic transition”. fact that the domesticators did not focus One thing is certain: the original domes- more on erosion-resistant perennial species. ticators did not adopt just any species that Apparently, ancient gatherers did utilize showed up at their doorstep. Then, as now, the seed of perennial species as food. Weiss people had strong ideas about the useful- et al. (2004) identified charred seeds from ness of some plant species and the unac- 3 perennial and 12 annual species of small- ceptability of others. Plants with the most grained grasses that people were consuming to offer were domesticated long ago, while 23 000 years ago at a site in what is now others that were sufficiently weedy, but less Israel. Bohrer (1972) discussed traditional desirable, repeatedly presented themselves methods of harvesting seed from assorted to humans, only to be ignored or targeted perennial grasses in Poland, Mongolia and for eradication (Hawkes, 1969). North America. Harlan (1989a) listed a Prehistoric people gathered and ate wide range of perennial grasses that people from a huge range of plant species, but once living south of the Sahara have harvested they began domesticating, it was annual for food. Perennial lymegrass ( Leymus are- plants that they transformed. Among the narius) was probably cultivated by Vikings staple crops in Table 1.1 that yield edible before barley reached Scandinavia (Griffin reproductive biomass, the banana is the lone and Rowlett, 1981). Yet no domesticated herbaceous perennial. Herbaceous, grain- species were handed down producing, perennial species are not to be to us by the first plant breeders. found at all among the world’s crops plants Perennials did not compete well with (Cox et al ., 2002). Herbaceous perennials annuals in disturbed soil and would not have generally produce less seed in a season than followed people back to the fertile, churned do annuals. Also, rapid climatic change soil around their dwellings; if some plants across the Asian continent at the end of did happen to make their way there, they the Pleistocene dramatically increased the would have been overwhelmed by repeated availability of those annual, seed-producing disturbance and competition from weedy species that attracted the attention of culti- annuals. More importantly for Neolithic vators (Whyte, 1977). The difference in seed domesticators, farming and plant breeding production between annuals and perennials were one and the same activity. As a result, is a result of contrasting selection pres- they inevitably carried plant populations sures during the two groups’ evolutionary rapidly through sexual cycles, thereby ful- histories. Selection pressure applied in yet filling an essential requirement of gene-fre- a different direction by plant breeders can quency change. Perennial plants re-growing Crop domestication and the first plant breeders 5

from vegetative structures would have been contrast to annual domesticates from that much more vigorous than either volun- region (Zohary and Spiegel-Roy, 1975). teer seedlings or intentionally sown plants; Of course, early farmers also practised therefore, even if people tried to cultivate selection in vegetatively propagated herba- perennials, they would have felt little incen- ceous species. As with woody species, they tive to sow new generations from seed. selected clones with desirable character- As we shall see, the act of sowing har- istics – often the results of unusual muta- vested seed applied strong selection pres- tions – and distributed them far and wide. sure. Selection for non-shattering was Occasional hybridization or somatic muta- strengthened when people began tilling tion fuelled some continuing selection; for new land year after year to sow their example, spontaneous yam (Dioscorea spp.) seed, perhaps as a part of shifting cultiva- clones selected for cultivation by present- tion to avoid build-up of non-domesticated day farmers in Benin either are wild or are weeds (Hillman and Davies, 1990). Stands hybrids between and wild yams of perennial plants on undisturbed land (Scarcelli et al. , 2006; Mignouna and Dansi, would have been much less vulnerable to 2003). But with only rare sexual recombi- weeds, much more poorly adapted to shift- nation, there was little opportunity for the ing cultivation, and therefore less suscepti- degree of domestication seen in grain crops ble to domestication. One harvest method (Zohary, 2004). that spurred selection for seed retention in The earliest plant breeders’ dispropor- the annual cereals—uprooting of the plant tionate attention to seed-propagated annual (Bohrer, 1972; Hillman and Davies, 1990)— plants has been replicated by most modern is very difficult with most perennials. students of plant domestication. That pref- Woody perennials of the Mediterranean erence will be evident in the range of exam- and west Asia—including olive (Olea euro- ples on which the following sections draw. paea), grape (Vitis vinifera ), fig (Ficus car- ica) and date ( Phoenix dactylifera)—were 1.3 INITIAL SELECTION WITHIN SPECIES domesticated in the same region as cereals, It is widely recognized that crops were but by descendants of the first plant - not domesticated simply through gather- ers, several millennia after agriculture had ing or cultivation. Even the most intensive been well established (Zohary and Spiegel- harvesting of cereals does not apply suf- Roy, 1975). Fruit-producing trees and vines ficient selection pressure to domesticate did not have to compete with annual coun- a crop fully . Intentional sowing, in con- terparts for humans’ attention. They were trast, applies strong, unconscious selection vegetatively propagated, and, even today, pressure (Zohary, 2004). Alleles for non- most sexual progeny derived from them shattering, lack of dormancy, reproductive are “not only economically worthless, but determinacy and increased fertility of for- often regress towards the mean found in merly sterile florets are all favoured by the spontaneous populations, showing striking sowing-harvesting-sowing cycle (Harlan, resemblance to the wild form” (Zohary, De Wet and Price , 1973). 1984). The lack of far-reaching genetic In the west Asia of 10 000 years ago, changes in Mediterranean tree crops is also wild cereals grew naturally in large fields manifested in their failure to spread very of near-, but they were not a far beyond their original climatic range, in food source that could simply be browsed 6 Plant breeding and farmer participation

at one’s convenience. The time between full season. At that point, they write, “farmers ripening and total loss of seed through shat- gathering their first seed stocks from wild tering was only a week or two, and with hot stands will have been totally unaware of the dry weather, the period was shortened to existence of these tough-rachised mutant two or three days (Zohary, 1969). Gatherers forms, and they would have remained would have needed to be as timely in their oblivious of them as long as the crop stayed harvest as today’s farmers, but the harvest in its essentially wild state.” season was lengthened somewhat by dif- Beating spikes or panicles into a basket ferences in time of maturity among differ- is the most time-efficient way to harvest ent cereal species and by elevation differ- wild grain crops (Hillman and Davies, ences in the hilly Levant. Staggered harvests 1990), but it does not apply selection pres- would have allowed people to amass large sure for non-shattering. Harlan (1967) quantities of grain with a relatively long famously collected wild cereals at the rate shelf-life. At the heart of the wild cereals’ of 1 kg/hr by hand-stripping of spikes, native range, people could obtain reliable but that method would not select effec- harvests from naturally re-seeded stands; it tively against shattering either (Hillman is therefore most likely that the west Asian and Davies, 1990). Sickling or uprooting grain crops were first domesticated at the ripe or partially ripe crops does apply fringes of their progenitors’ distributions selection pressure, because it shakes loose (Harlan and Zohary, 1966). It was there some seed from wild-type plants, seed that that people would have found intentional is lost to the harvester. Hillman and Davies sowing most helpful in maintaining stands (1990) found experimentally that a consist- of their proto-crops. At the same time, ently low 40 percent of wild-type seed was Willcox (2005) emphasized the patchiness recovered by sickling or uprooting. Under of wild wheat stands throughout the area those conditions, selection would strongly where emmer wheat was domesticated. favour genes for non-shattering. People may have felt some incentive to sow In their simulations, such strong selec- seed, thereby initiating domestication, in tion intensity, combined with the high any productive localities in that area where degree of self-pollination typical of wheat wild wheat was not already growing. and barley, would have resulted in com- A study by Hillman and Davies (1990) plete fixation of a recessive non-shattering deserves to be discussed at some length, gene within 20 to 30 harvest seasons, if peo- because it takes into account many of the ple sowed seed each year on ‘virgin land’. factors that affect methods and rates of They further predicted that even if early domestication in grain crops. They started farmers inadvertently relaxed the selection by calculating that the rare, recessive muta- pressure by harvesting less fully ripened tions for non-shattering that were necessary plants or repeatedly sowing on the same for domestication of the west Asian cereals land, domestication would have been com- were likely to have appeared once every 5 pleted within two to four centuries. It is no to 20 years in a typical-sized plot tended wonder that we know so little about the by an early cultivator. In predominantly mechanics of domestication, according to self-pollinating wheat and barley, plants Hillman and Davies (1990). If it came and homozygous for recessive non-shattering went as quickly as they envisioned it, the alleles would have appeared the following process was “unlikely to be preserved on Crop domestication and the first plant breeders 7

most Mesolithic or Neolithic [archaeologi- and (3) it may simply have become custom- cal] sites as a recognizable progression”. ary during a series of wet summers when Having assumed in their analysis that ini- wild cereals did not shatter as readily and the tial domestication was entirely unconscious, beating method of harvest was inadequate. Hillman and Davies (1990) then demonstrat- When wild cereals of west Asia shatter, ed that even if Neolithic farmers had practised their morphologically distinct basal spikelet intentional selection, they could not have remains attached to the culm. That spikelet greatly speeded up the process. With con- would have been recovered by harvesters scious selection, people could have done no who sickled or uprooted plants, but not better than halve the length of time required by those who gathered already-shattered for domestication, because they could have spikelets from the ground. Basal spikelets started selecting only when the were might also have been left behind by hand- frequent enough to be obvious, perhaps at stripping, but that technique requires that a frequency of 1 to 5 percent of the stand. grain be harvested before it is fully ripe, By that point, the frequency of mutants had to avoid loss through shattering. Among already passed through a lag phase and was wild barley and wild emmer remains from poised for a rapid increase in frequency, even four archaeological sites greater than 11 000 under unconscious selection. years old, Kislev, Weiss and Hartmann What if, because of a thunderstorm (2004) found no basal spikelets and a or perhaps an excessive delay in harvest, miniscule number of unripe grains. These the only intact spikes from which new observations, they maintained, point to seed stocks could be recovered were those ground collecting as the original harvest of mutants? Could domestication have method among pre-agricultural people of occurred in a single season? Hillman and the region. The authors experimented with Davies (1990) discounted this possibility, ground collection, finding that at any time based on variation in ripening time and during the region’s rainless summer they the likelihood that birds or other ani- could pick up large clumps of spikelets by mals would find the isolated spikes before grasping the upward-pointing awns. humans did. Nevertheless, any environ- Kislev, Weiss and Hatmann (2004) rea- mental factor that hastened shattering could soned that after the first autumn rains, have increased the selection pressure and ground gatherers would have noticed seed- speeded up domestication. lings sprouting from spikelets, and that Hillman and Davies’s argument begs the sight would have inspired them to sow a question of why early cultivators resorted portion of their harvested seed. Of course, to sickling or uprooting, if beating is the sowing of ground-collected seed would most time-efficient harvest method for wild have selected not against but for shattering. cereals. They suggested three reasons that Kislev, Weiss and Hatmann (2004) do not sickling or uprooting apparently was pre- speculate on how the transition to sow- ferred at some point: (1) it recovered more ing of non-shattered seed occurred, but a seed per unit land area (which, as people scenario based on their results comes to became more settled, may have become a mind. In collecting seed from the ground, more important criterion than seed quantity people would have been moving slowly per unit time); (2) it permitted utilization of through stands of wild cereals long after the for fire-lighting and brick-making; full ripening. Any tough-rachised mutant 8 Plant breeding and farmer participation

with its spike still intact atop the culm may Zohary (1989) forcefully rejected have attracted their interest, and they may Ladizinsky’s model, arguing that legume and well have collected it for sowing in a special cereal domestication followed very similar plot; if that happened, it would have been a paths, starting with cultivation and sowing very early case of intentional breeding. of the wild progenitors. He maintained that Using lentil ( Lens culinaris ) as a model, wild lentils can produce not ten, but rather Ladizinsky (1987, 1993) showed how domes- 40 to 70 seeds per plant when well tended in tication of west Asian legumes might have fertile soil; therefore, people might well have followed a sequence different from that of found sowing to be worthwhile. Ladizinsky cereals. He noted that wild lentil ( L. orienta- (1989a) responded that the fields of early, lis ) plants are tiny, requiring that an estimated inexperienced cultivators would not have 10 000 plants be gathered in order to obtain been very conducive to high yields, and one kilogram of clean grain. Therefore, len- that conditions would have been more like tils could not have been a major part of the those encountered by wild legume stands gatherers’ diet, as were cereals, which could than those in Zohary’s (1989) tilled, weeded be gathered much more quickly (Harlan, and well fertilized experiments. 1967). Furthermore, Ladizinsky argued, Some researchers have concluded that there would have been no incentive for sow- domestication was a rapid process in the ing; an incipient lentil farmer would have crops they have studied, certainly when had to sow their entire harvest simply to compared with evolution through natural produce another crop of equal size. That is selection. Harter et al. (2004) estimated that because each wild lentil plant produces only in sunflower, “genetic composition of the about ten seeds, of which only one seed on domesticates has changed at least 50-fold average will germinate the first year, given faster than the wild populations since they the seeds’ strong dormancy. diverged.” Wang et al. (1999) calculated that Lentils and perhaps other pulses differed it took approximately 300 to 1 000 years from cereals, argued Ladizinsky (1987, to completely fix the crucial domestication 1993), in that at least partial domestication gene tb1 that telescopes the lateral branches had to precede sowing. Through intensive in maize. Other studies indicate a some- harvesting, people would have drastically what slower process. Jaenicke-Despres et curtailed natural reseeding, thereby leav- al. (2003) found that as far back as 4 400 ing fields more open to fast-germinating years ago, modern mutant alleles of the mutants and selecting against seed dorman- genes tb1 , pbf (prolamin box binding fac- cy. Once dormancy was largely eliminated tor) and su1 (starch debranching, which and people were able to sow seed to good affects tortilla quality) were common. But effect, selection pressure for indehiscent, that was almost 2 000 years after the date of non-shattering pods would have been feasi- the oldest known archaeological evidence ble. But traditional harvesters in southwest of maize domestication. Based on archaeo- Asia uproot lentil plants before full maturi- logical evidence from northern Syrian Arab ty, then sun-dry and thresh them—a process Republic and southeastern Turkey, Tanno that largely avoids shattering. If that was the and Willcox (2006) argued that “wild cereals harvest method in Neolithic times, selection could have been cultivated for over 10 000 for non-shattering would have been much years before the emergence of domestic weaker in legumes than in cereals. varieties”, partly because Neolithic cultiva- Crop domestication and the first plant breeders 9

tors may have taken care to harvest grain 1.4 THE DOMESTICATION BOTTLENECK before any of it began shattering. That AND GENE FLOW would have reduced the selection pressure The number of domestication events experi- on alleles for non-shattering. Fuller (2007) enced by individual species has long been a argued that during the domestication of favourite topic of debate among researchers. rice, einkorn and barley, selection for grain Blumler (1992) and Zohary (1999) have size proceeded faster than selection for non- argued that multiple domestications within a shattering, but that grain-size increases were species have happened only rarely. They much slower in pearl millet and leguminous pointed out that genetic variation is much crops. Surveying the archaeological data, greater in most wild progenitors than in he found significant grain-size increases in derived domesticates. They also noted the Asian cereals within a matter of centuries, rarity of parallel domestication in related a result, he reasoned, of the advantage large taxa above the species level. For example, seeds had when early cultivators sowed people selected ( Triticum them deeply in tilled soil. In contrast, he monococcum ), ( Pisum sativum : concluded, shattering was not fully elimi- Ladizinsky, 1989b), emmer wheat, maize nated for 1 000 to 2 000 years. and chickpea from their wild ancestors while Gepts (2002) concluded that models leaving sympatric, phenotypically similar, based on a few genes can estimate only closely related species undomesticated. the minimum duration of the domestica- Matsuoka et al. (2002) detected a single tion process, whereas archaeological data domestication event in maize by analysing provide a ‘reality check’. Physical remains microsatellite variation. Based on amplified often indicate that domestication took fragment length polymorphism (AFLP) much longer than would be predicted by variation, Heun et al. (1997) concluded genetic models. that einkorn was domesticated only once, Whether farmers’ transformation of in southeastern Turkey, but that result has various wild plants into crops went quick- been challenged on archaeological and cli- ly or slowly, it was not always permanent. matic grounds (Hole, 1998; Jones, Allaby False starts on the road to domestication and Brown, 1998). Willcox (2005) sum- may have been common. At sites in west marized archaeological evidence indicating Asia and North America, groups of peo- that einkorn, emmer and barley all experi- ple practised relatively intense cultivation enced multiple domestications. of wild progenitors, and even partially No ting that evidence for single versus domesticated some species before even- multiple domestication events in Andean tually abandoning them; those orphaned crops such as amaranth and peppers is plant populations did not contribute to inconclusive, Blumler (1992) cited several the founding gene pools of today’s crops factors that render it “seldom if ever possible (Weiss, Kislev and Hartmann , 2006). In to rule out multiple independent invention”: one dramatic example of that phenom- the progenitor species may have diversified enon, domestic may have arisen 10 000 after domestication of the crop; loci used years ago in the Syrian Arab Republic and in comparing the wild and cultivated types Anatolia, only to disappear for several may be linked to loci affecting traits of millennia before being re-domesticated in domestication or ecological adaptation; or Anatolia and Europe (Willcox, 2005). sampling by researchers may be unknowingly 10 Plant breeding and farmer participation

biased. In a simulation study, Allaby and ple had a chance to distribute it over a large Brown (2003) showed that analyses relying geographical area. on anonymous genetic markers might The founder effect often occurred when provide seemingly conclusive evidence that domestication depended upon rare mutants, a species was domesticated through a single but it was most severe when natural amphip- event when it was in fact domesticated more loids (doubled interspecific hybrids) were than once. domesticated. A rare amphiploid taken The people of South America and those under human care, as was wheat, of Mesoamerica probably took the common would have represented a gene pool consist- bean through two separate domestications ing of a single plant—the tightest possible (Sauer, 1993). Xu et al. (2002) concluded, genetic bottleneck (Cox, 1998). on the basis of chloroplast DNA variation, Tenaillon et al . (2004) found that loss of that the soybean had a polyphyletic origin, diversity in maize relative to teosinte was but cluster analysis of nuclear random only 20 percent for putatively neutral loci, amplified polymorphic DNA (RAPD) compared with 65 percent for loci affected markers indicated that local differentia- by selection for traits of domestication. tion of soybean occurred in farmers’ fields They estimated that the bottleneck that after domestication was complete (Xu and caused this mild contraction of variability Gai, 2003). In any case, the soybean passed had a ratio of population size to duration through a very tight domestication bottle- ranging from approximately 2 to 5. That neck (Hyten et al., 2006). Barley is unusual is, the bottleneck population might have among the west Asian cereals in harbour- consisted of 10 000 plants over 2 000 gen- ing a high level of genetic polymorphism. erations, or perhaps 2 000 plants over 1 000 Ladizinsky (1998) concluded that early generations. Based on data from the Adh-1 cultivators must have selected at least 100 locus, Eyre-Walker et al. (1998) estimated a non-shattering mutant plants in order to bottleneck size/duration ratio for maize of capture the level of variability seen in bar- approximately 2; assuming that domestica- ley. Because the crop is highly self-pollinat- tion took 300 years—similar to the dura- ed, post-domestication gene flow from its tion estimated for einkorn wheat—they wild progenitor Hordeum spontaneum can- envisioned a bottleneck population of only not have accounted for the high degree of 600 plants. variability that is evident today (Ladizinsky Sunflower apparently went through and Genizi, 2001). a ‘substantial’ domestication bottleneck, Whatever the initial number of domes- with inbreeding levels of Native American tication events, it is clear that because of varying from 0.3 to 0.5 (Harter et genetic drift the diversity of most crop al ., 2004). Abbo, Berger and Turner (2003) species is low compared with that of their counted three successive bottlenecks that wild ancestors. Drift results from a genetic tightly restricted the genetic variability of ‘bottleneck’, usually at the point of initial the chickpea crop from its earliest days domestication—the well known ‘founder onward: the highly restricted distribution effect’ (Ladizinsky, 1985). A bottleneck of its wild ancestor Cicer reticulatum; the could also be caused by some later event, founder effect resulting from domestica- but generally would have to occur very tion; and an early shift by west Asian farm- early in the history of the crop, before peo- ers from autumn to spring sowing of chick- Crop domestication and the first plant breeders 11

pea (to avoid crop loss due to the Ascochyta often an important source of new variation blight disease). That shift required selection in crops (Harlan, De Wet and Price , 1973; of plants without a vernalization require- Small, 1984). People tend to remove from ment. This third bottleneck, which, they a field those weedy hybrids that do not argue, occurred early in the crop’s history, suit their needs, and those weeds tend to affected chickpea uniquely among the major be less competitive in the natural environ- west Asian crops. However, it reminds us ment as well. However, when weeds man- that many species may have passed through aged to backcross to crop plants, their less bottlenecks caused by intense, early farmer- weedy-looking progeny might well have directed selection for traits other than seed escaped the early cultivator’s hand or hoe, non-dispersal and lack of dormancy. remaining in the domesticated population Haudry et al. (2007) found that domes- and exchanging genes with it. Weeds often ticated emmer wheat showed a 70 percent migrate over larger areas than domesticates loss of nucleotide diversity relative to its and jump from one domesticated popula- progenitor Triticum dicoccoides . tion to another, exchanging genes along the wheat, derived by further selection from way (Small, 1984). emmer, showed an additional diversity loss, Sang and Ge (2007) attempted to rec- for a total loss of 84 percent. Bread wheat’s oncile seemingly contradictory evidence diversity unexpectedly showed only a regarding the origin of the two rice subspe- 69 percent loss relative to T. dicoccoides , cies indica and japonica by showing that the suggesting extensive introgression from current genetic situation could have arisen tetraploid during the 8 000 years from either one or two initial domestica- since the origin of bread wheat. tions, followed by gene flow from the two Finally, we should take note of a much potential wild progenitors or between the more recent, possibly catastrophic, bot- partially domesticated subspecies, or both. tleneck. Clement (1999) documented 138 It follows, they wrote, that introgression Amazonian plant species—the bulk of them practised by modern plant breeding pro- either fruits, nuts or vegetables—that were grammes is, in effect, “the continuation of in ‘an advanced state of domestication’ at domestication”. the time of the first contact with Europeans Weeds unrelated to the crop have at times five centuries ago. Because these species enticed humans to adopt and domesticate had become to some extent dependent on them as secondary crops. The ancestors of humans for their propagation, Clement (Avena sativa ) and rye ( Secale cereale), maintains that the cataclysmic post-1492 for example, caught the eyes of cultivators loss of 90 to 95 percent of the area’s human while growing as weeds in European wheat population resulted in an approximate and barley fields (Holden, 1976). 90 percent loss of in plant Through analysis of microsatellites, species then under cultivation. Matsuoka et al . (2002) determined that the Introgressive hybridization between genetic diversity of maize was expanded domesticates and their wild or weedy rela- greatly by introgression from teosinte. tives has often expanded genetic diversity, Wilkes (1977) found maize farmers in the counteracting the effects of the domesti- Nobogame Valley of Mexico encouraging cation bottleneck. Hybridization among the growth of teosinte near and even domestic, weedy and wild populations is within their maize fields. They told Wilkes 12 Plant breeding and farmer participation

that the teosinte germplasm makes kernels contrast between bread wheat and grain ‘more flinty and stronger’. Nobogame sorghum is instructive (Cox and Wood, was the only area in which Wilkes found 1999). Hexaploid bread wheat may well hybridization intentionally fostered, and, have originated from only one or two interestingly, it was the only place where hybrid plants with genomic constitution the flowering times of maize and teosinte ABD (Cox, 1998; Haudry et al ., 2007). were somewhat synchronized. In other The tetraploid ancestor (AB) had experi- areas, people weeded out teosinte, but, enced only limited introgression from dip- at least in Chalco, they fed it to cattle as loid plants, mostly of the A- spe- fodder, then inadvertently returned its seed cies. Subsequent gene flow from AB into to the field when applying manure. It is ABD wheat plants occurred to some extent possible that such mechanisms also played (Haudry et al ., 2007), but gene flow from a part in the introgression of teosinte the extremely diverse D-genome donor genes into maize in the early phases of Aegilops tauschii into bread wheat was domestication. either non-existent or extremely rare until Gene flow into crops has been impor- it was done by twentieth-century plant tant in crop evolution, but there is a much breeders (Cox, 1998). Therefore, through- larger flow in the opposite direction: from out the entire bread wheat species, there the domesticate into the wild form. That is limited genetic variability in the A and would probably have been the case in B genomes, while its D genome contains Neolithic grain fields as well. Migration only a tiny fraction of the diversity found of large amounts of wild into fields in Aegilops tauschii (Reif et al ., 2005). of self-pollinated crops was limited, and In contrast, people of Africa have because pollen from the wild conveyed always grown grain and fodder sorghum dominant genes for shattering, hybrid in areas where the crop comes into close progeny were not likely to be collected or contact and interbreeds with wild sor- planted by farmers (Ladizinsky, 1985). At ghum races (Doggett and Majisu, 1968). the same time, there is much evidence that They probably domesticated sorghum in genes regularly migrated out of fields and various, widespread locales on multiple into wild populations (Ladizinsky, 1985; occasions, after which it was exposed to a Harlan, De Wet and Price, 1973). Many continuous inflow of variability from the studies have estimated hybridization rates wild and weedy gene pools. As a result, by looking for crop-specific alleles in pop- grain sorghum today harbours vastly more ulations of the crops’ wild relatives grow- genetic diversity than does bread wheat ing at various distances from cultivated (Cox and Wood, 1999). fields. They generally find surprisingly high rates, even hundreds of metres away 1.5 GENETIC CONSEQUENCES OF (Ellstrand, 2003). SELECTION Differences among crop species in the Van Raamsdonk (1995) proposed that most sizes of their founding populations and domesticated crops were developed through subsequent opportunities for gene inflow one of four genetic models (Table 1.2). The from the wild have profoundly affected models differ in the role of ploidy and the levels of genetic diversity available the degrees and mechanisms of reproduc- to present-day plant breeders. Here, the tive isolation. Differences in genetic and Crop domestication and the first plant breeders 13

cytogenetic mechanisms meant that the self-incompatibility systems is easily accom- key role of the domesticator varied from plished, whereas selection in favour of self- model to model (Table 1.2). For instance, incompatibility would have been genetically with some crops, people functioned as complex and very difficult (Rick, 1988). matchmakers, bringing species into contact Inbreeding is a powerful accelerator for the first time; in others, they enforced of unconscious selection for traits gov- reproductive isolation. erned by recessive genes. The fixation of Domestication tends to intensify the genes for non-shattering that might have degree of inbreeding in seed-propagated required only a few centuries in highly species (Zohary, 2004). The inflorescences of self-pollinated wheat and barley would, tomato, chili and eggplant ( Solanum melo- with 100 percent cross-pollination, have gena ), among other species, were uncon- taken more than 8 000 years (Hillman and sciously selected by domesticators to have Davies, 1990)! shorter styles, which promoted self-pollina- Each of two recessive alleles at differ- tion (Rick, 1988; Pickersgill, 1969). Artificial ent loci in domesticated rice that reduce selection can push largely self-incompat- seed shattering resulted from single-nucle- ible populations toward self-compatibility otide substitutions (Li, Zhou and Sang , 2006; (Rick, 1988), as is believed to have happened Konishi et al ., 2006). Five of six well studied in types of , including sum- domestication genes in maize, wheat, rice mer (Thompson, 1976). Here, and tomato exhibit differences in regulatory there is a kind of ratchet effect: disruption of regions between the wild and domestic alleles

TABLE 1.2 Four models proposed by van Raamsdonk (1995) by which the genetic mechanisms of crop domestication can be classified, along with his lists of crops that exemplify each model and some crucial points at which humans intervened in the domestication process under each model

Domestication model Examples Crucial actions by domesticators

Reproductive isolation between a Soybean, common bean, chickpea, Selection for self-pollination and diploid domesticate and its diploid lentil, cowpea (Vigna unguiculata), against weedy hybrids; fostering of wild ancestor is caused by internal lettuce (Lactuca sativa), fruits genetic drift barriers, post-zygotic barriers, (Citrus spp.) external reproductive barriers or apomixis. Development of crop-weed- Maize, rice, barley, grape, sorghum, Adoption of weeds that invade wild complexes in which genetic pearl millet, foxtail millet (Setaria cultivated land; toleration or information is exchanged more italica), radish (Raphanus sativus), encouragement of weeds that can or less freely among diploid beet (Beta spp.), chili ( Capsicum spp.), backcross to less wild domesticates and their sexually quinoa (Chenopodium quinoa) compatible wild progenitors. One or more rounds of hybridization Cotton, sweet potato, groundnut, Selection at the level and polyploidization occur among tobacco (Nicotiana spp.), cucumber wild species prior to domestication. (Cucumis spp.), coconut ( Cocos nucifera), alfalfa (Medicago sativa) Interspecific hybridization involving Bread wheat, potato, banana, coffee Bringing formerly isolated plant at least one domesticated species (Coffea arabica), yam (Dioscorea spp.) populations into contact; selection is followed by polyploidization. and propagation of rare amphiploid Resultant amphiploids are plant(s) found in or near cultivated reproductively isolated. fields. In some cases, domestication Sugar cane, , Brassica spp., tomato — occurs through a combination of (Lycopersicon esculentum ) mechanisms from more than one of the above models. 14 Plant breeding and farmer participation

(Doebley, Gaut and Smith, 2006). Whatever selection in vegetatively propagated species the nature of their mutations, alleles initial- allowed, or even encouraged, variations in ly selected by domesticators often showed chromosomal number and structure, dis- the simplest modes of inheritance. Many rupting reproductive development to vary- genes governing traits of domestication are ing extents (Zohary, 2004). recessive or additive, and would have been In a simulation study, Le Thierry expressed more strongly among the prog- d’Ennequin et al . (1999) predicted that to eny of plants that tended to self-pollinate fix a full complement of alleles for domes- most frequently. An increased tendency to tication, either linkage among loci or a inbreed may also have been an indirect result significant degree of reproductive isolation of selection for higher grain yield; self-pol- is essential. By their models, in predomi- lination ensures seed and fruit development, nantly self-pollinating species subject to especially if the new crop was transported little migration, people easily fixed alleles at out of the range of its natural pollinators. unlinked loci through selection; however, Inbreeding also leads to greater within- in species with a high degree of out-cross- line uniformity, but it is hard to imagine ing, human selection favoured blocks of uniformity being a direct selection criterion linked domestication genes. for early domesticators, as it would have Empirical experiments have demonstrat- required that they plant out the progeny ed that linkage among domestication loci of individual plants in separate plots. It is common, regardless of breeding system is almost certain that they practised mass (Paterson, 2002). In crosses between pearl selection, not progeny testing. But genes millet and its wild progenitor Pennisetum promoting self-pollination might have been mollissimum , Poncet et al . (1998, 2000, 2002) favoured in very small populations main- found linkage among genes affecting spike tained in isolation. Such isolation could characters—important components of the have resulted from individual preferences, domestication syndrome—but not among or perhaps community customs, such as genes affecting vegetative characters or total a belief in parts of Guatemala that plants grain yield. Burke et al . (2002) mapped 78 should be grown only from seed produced quantitative trait loci (QTLs) affecting 18 on the same plot of ground (Pickersgill, traits in a cross between sunflower and its 1969). ‘Colour coding’ (Wilkes, 1989) based conspecific wild progenitor. The domestica- on endosperm pigmentation may have tion-associated loci were spread across 15 of helped farmers maintain small, genetically 17 linkage groups, but were highly clustered isolated maize populations. within those groups. Both pearl millet and Strong selection to reinforce inbreeding sunflower are highly cross-pollinated. In did not occur in crops that were propa- rice, a selfing species, QTLs affecting domes- gated vegetatively; in them, self-incompat- tication traits also tended to be clustered in ibility and out-crossing remained common linkage groups (Cai and Morishima, 2000). (Zohary, 2004; Rick, 1988). Through clonal Wright et al . (2005) found that 2 to 4 per- propagation, cultivators could produce cent of the genes in maize have probably large, genetically desirable populations. undergone artificial selection. Much of that In contrast to seed-propagated species, in selection, especially for the genes involved which human selection for improved grain in plant growth and auxin response that are harvests also reinforced meiotic stability, responsible for the dramatic differences in Crop domestication and the first plant breeders 15

plant morphology between teosinte and favoured during periods of rapid evolu- maize, appears to have occurred during ini- tionary change, of which domestication is tial domestication. Those growth-pattern an extreme example. Ross-Ibarra found no genes were clustered, whereas genes affect- support for the alternative possibility: that ing amino acid composition were not. species with higher recombination rates are In wild progenitors, significant numbers ‘pre-adapted’ to domestication. of agronomically beneficial alleles are often Even under domestication, the recom- embedded in linkage blocks with other, bination rate is under stabilizing rather deleterious, genes. Such desirable alleles than unidirectional selection, because the tended to be left behind during domestica- same high rates that help break up repul- tion. For example, in a tetraploid wheat sion linkages also speed up the decay of population, Peng et al . (2003) found 24 per- co-adapted gene complexes (Dobzhansky, cent of positive QTL effects to be coming 1970). Indeed, Ross-Ibarra’s comparison of from the wild Triticum dicoccoides parent. crop and wild species provided evidence for By breaking up such linkage blocks, mod- selection against excessive recombination. ern-day breeders can utilize genes that were There are, of course, other mechanisms for ‘hidden’ from early domesticators. maintaining favourable multilocus combi- Gepts (2002), surveying studies of nations, including paracentric inversions domestication traits in maize, pearl millet, (Dobzhansky, 1970) and self-pollination common bean and rice, found an aver- (Clegg, Allard and Kahler, 1972). age of 2.2 to 5.3 loci per trait. Those loci accounted for only about 50 percent of the 1.6 INTENTIONAL SELECTION total variation per trait, and loci affecting Although crops were domesticated through all traits were spread among 3 to 5 linkage largely unintentional selection, there is lit- groups per species, indicating rather diffuse tle doubt that the domesticators quickly genetic control. Paterson (2002) found sim- became aware of their own ability to change ilar patterns in the QTL-mapping literature the phenotypic composition of their crops on sorghum, rice, maize and tomato. He from generation to generation. Genetic concluded that loci with larger statistical modification, once initiated, spread in ever- effects were probably biologically signifi- widening ripples through plant genomes. cant as well, because they occurred in simi- Sowing spurred unconscious selection for lar genomic regions in different crop spe- traits like non-shattering; changes caused cies (Paterson, 2002; Paterson et al ., 1995). by unconscious selection prompted observ- During domestication, people may have ant farmers to practise intentional selection; unknowingly favoured plants or popula- and intentional selection for one trait often tions with a higher inherent rate of recom- affected other traits as well, through linkage bination per unit of physical chromosomal and pleiotropy. Studies of a grain-quality length. A comprehensive survey showed trait in rice show that human selection at a that mean numbers of chiasmata per biva- single locus can exert very strong selection lent were significantly higher in 46 crop pressure on a large chromosomal region species than in 150 wild species (Ross- surrounding it, causing a so-called ‘selec- Ibarra, 2004). This result was in accord tive sweep’ that can affect other traits much with theory, the bulk of which predicts more strongly than would that an increased rate of recombination is (Olsen et al ., 2006). 16 Plant breeding and farmer participation

From the dawn of agriculture until affected others; for example, selection for the twentieth century, farmers acted as larger spikes in the cereals produced wider plant breeders, working almost exclusively leaves and thicker culms as well. through mass selection; that is, by ensuring Smartt (1969) catalogued the many that some individual plants made a pro- traits for which early domesticators applied portionately greater genetic contribution selection pressure in species of Phaseolus: to the following generation than did oth- a reduced number of lateral branches (to ers. Natural out-crossing would have been avoid excessive tangling in fields where frequent enough, even in highly self-pol- beans were meant to climb maize plants); linating species, to generate useful genetic more robust leaves and stems; larger flow- recombinants. Early plant breeders worked ers; increased photoperiod sensitivity; without the benefits of progeny testing increased pod and seed size; greater per- or replication, both of which can enhance meability of the testa; and reduced pod gain from selection, but they had two dehiscence. However, in examining four other important factors working in their cultivated species, he found that not all of favour: time and ecosystems. Even small those traits were affected in every species. gene-frequency changes from year to year Chang (1976a, b) noted a similarly translated into large improvements when increased size of vegetative organs and they continued over vast numbers of grow- kernels in rice, along with a more exten- ing seasons. And plant populations upon sive root system; higher tillering capacity; which people exerted gradual selection in synchronization of tillering; more pani- a particular locality, through the full range cle branches; a longer grain-filling period; of weather conditions and pest, pathogen, tolerance to non-flooded conditions; and weed and intercrop populations that the loss of pigmentation. However, increases locality had to offer, were bound to be in kernel size and harvest index associ- resilient and reliable food producers. ated with domestication of rice were less When people applied direct selection than those in most other cereals (Cook pressure for some traits, whether inten- and Evans, 1983). In several species of chili tional or unconscious, they put indirect (Capsicum), people rejected erect-fruited selection pressure on others. For example, wild plants in favour of mutants with attached glumes increase seed dormancy, pendant fruits, which were hidden under so selection for non-dormancy may have the foliage canopy and therefore protected increased the frequency of free-threshing from bird damage (Pickersgill, 1969). plants. Deep sowing may have favoured Maize is often recognized as a crop that larger-seeded (Fuller, 2007), underwent some of the most remarkable which, in turn, would have had lower morphological changes during domestica- grain concentrations via dilution. tion, but, as in most crops, the most obvi- Selection for greater allocation of resources ous transformation was in its reproductive to reproductive growth (higher harvest structures. In the words of Iltis (2000), index) could have increased susceptibil- Cover the ears, and it sometimes takes a ity to pests (Rick, 1988). Because plant specialist to tell teosinte from maize … But parts growing from the same meristematic compare a many-rowed, 1000-grained ear regions exhibit allometric growth, selection of maize to a 2-rowed, 5-to-12-grained to increase the size of one organ generally ear of teosinte – and be perplexed! How Crop domestication and the first plant breeders 17

could such a massive, useful monster be niques, all of which were certain to reveal derived from such a tiny, fragile, inedible, genetic variation in the crops upon which useless mouse? they were practised. Perhaps just as surprising is the find- Human selection for nutritional qual- ing that morphological differences between ity of crop domesticates occurred in the maize and its wild ancestor are under rela- context of other crops that were evolv- tively simple genetic control (Doebley and ing simultaneously. The most commonly Stec, 1993). cited example is the complementarity of Maize is not the only species whose amino acid profiles in cereals and legumes. reproductive structures evolved into mon- Selection among and within species was strosities under the guiding hand of early a matter of health, even life and death. breeders. For example, pearl millet’s wild Indeed, Wilkes (1989) declared an ‘ethno- ancestor has heads measuring no more than botanical rule’, stating that when “crops are 10 cm in length, but from it, early breed- consumed and not sold, a reasonable level of ers selected cultivars with heads up to 2 m nutritional adequacy has evolved and been long (Harlan, 1989b). In bringing about the maintained”. Neither the single-minded visually dramatic domestication of the sun- selection for high grain yield per unit area flower, Native Americans selected for the nor the pursuit of high-lysine maize would fusion of many smaller heads into fewer, have occurred to a Mesoamerican farmer of larger ones. People worldwide selected 3 000 years ago. for often dramatically larger reproductive Plant breeding requires differential phe- structures in and fruit crops. notypic expression. For example, people Plant breeding theory, as well as obser- could not venture very deeply into the vation of crop domesticates, tells us that domestication and improvement of a species the first breeders had their biggest impact as a food source if its consumption always on traits that (i) were of the most intense resulted in serious illness or death. Indeed, interest to the people who used the plants the process by which the sweet almond was for food; (ii) were under relatively simple derived from its cyanogenic ancestor is still genetic control; and (iii) had a relatively shrouded in mystery (Ladizinsky, 1999). high heritability on a single-plant or single- People could begin selecting for lower tox- propagule basis. Therefore, humans altered icity once they accomplished at least par- the appearance and food quality of the har- tial breakdown of toxins through cooking. vested product more rapidly than they did Other strategies were developed farther traits such as yield per unit area. Contrasting back in the human family tree. Geophagy— intentional selection with the unconscious consumption of clays—is practiced by at selection that preceded and paralleled it, least eight primate species (Johns, 1989). Harlan, De Wet and Price (1973) wrote: People commonly eat clay along with wild Deliberate selection adds new dimensions potatoes (Johns, 1986) and yams (Irvine, to the process [of domestication]. Human 1952) to de-toxify them, and the prac- selection may be more intense and abso- tice might have provided latitude for early lute and is often biologically capricious or domesticators to distinguish among dif- even whimsical. ferent degrees of bitterness without falling They went on to list a bewildering too ill too often. Once foods were rendered array of food products and processing tech- edible via such practices, selection for lower 18 Plant breeding and farmer participation

toxicity might have been furthered simply be consumed by rival species. Reducing through dilution, as people selected for the mean toxicity to a safer level allowed greater root or tuber size (Johns, 1989). them to detect and exploit genetic variation In the potato, there is a remarkable within species. coincidence between toxic thresholds and Toxins aside, the simplification of diet human capacity for detection. The plant’s that followed the expansion of agriculture most common glycoalkaloid is toxic in appears in itself to have caused a decline in concentrations above 200 ppm (Johns and overall human health (Kates, 1994). Gepts Keen, 1986), and tubers with a concentra- (2002) even implies that had regulatory tion of greater than 140 ppm are considered agencies existed in Neolithic times, domes- unpleasantly bitter by North Americans ticated plants might well have failed to (Sinden and Deahl, 1976). In contrast, the receive approval! Aymara Indians of the Andes classify pota- Selection for food quality involved more toes with concentrations above a range of than nutritional considerations. Where 200 to 380 ppm as bitter (Johns and Keen, muscle and fuel power were resources not 1986). Because several wild and cultivated to be squandered, genotypes that produced Solanum species are crucial sources of calo- food with lower energy requirements for ries in the Andes, the Aymara and other processing and cooking may have been indigenous people may have developed more highly valued. For example, Harlan a taste for somewhat riskier genotypes. (1989b) described how modern cultivators Selection for improved nutritional qual- in Mali select sorghum heads with softer ity can also work against improvement of grains for ease of pounding, but also keep other traits. For example, potato popula- hard-seeded, more -resistant types, tions selected for lower glycoalkaloid con- for longer-term storage. centrations had lower resistance to potato In some cases, people may have utilized leafhopper (Sanford et al ., 1992). the progenitor of a crop for one pur- In a seeming paradox, cyanogenesis (the pose only to find, once they became more production of poisonous hydrocyanic acid) familiar with the species, that it possessed is more common in crop plants than in the one or more other traits that warranted plant kingdom as a whole. Jones (1998) its full domestication. For example, many noted that 16 of the world’s 24 leading crop East Asian plants may have been used for species (by total production) are cyano- medicinal purposes before being domesti- genic in some plant part(s) at some stage cated for food production (Chang, 1970). of growth. Cyanogenesis, Jones observed, Bohrer (1972) maintained that the wild is an important mechanism of resistance to grasses that eventually gave rise to cereal pests. People looking to become cultiva- crops were originally cut or uprooted for tors, given a wide range of plant species use as animal fodder. However, Hillman from which to choose, would probably and Davies (1990) disputed that idea, argu- have been attracted to plants that had not ing that at the time and place of west Asian already been damaged or largely consumed crop domestication there were no domestic by other species. Having the unique abil- cattle and few domestic sheep or goats. The ity to eliminate cyanogenic glycosides by squash ( Cucurbita pepo) may have been grinding, steeping and cooking, humans domesticated first for its seed, or for its took advantage of plants that could not hard gourds to be used as containers; once Crop domestication and the first plant breeders 19

fleshy vegetable genotypes were select- ...injects desirous human agents into the ed, people may have stopped growing the account, a palliative for the stern ‘food gourd types to prevent the appearance of crises’ and ‘population pressures’ that bitter squashes through cross-pollination haunt our angst-driven prehistories. How (Heiser, 1989). charming it would be to have a snack- Iltis (2000) concluded that teosinte was and-party crowd, hassled by only an occa- first grown by Mesoamericans for its green sional aggrandizer or two, at the base of shoots and sugary pith and not for its grain, the Neolithic! which remained enclosed in a hard fruit- The initial domestication of crops case. Later, through increased contact with prompted expansion of farming into new teosinte as a snack or vegetable, an alert environments, where people continued cultivator may have noticed an extremely selection under different conditions, while rare, ‘grain-liberating’ mutant—on possi- perhaps repeating the domestication proc- bly a single occasion—thus kicking off the ess with new species. Although the ability process of maize domestication. to accumulate a large excess of grain during Amplifying Iltis’s hypothesis, Smalley a brief harvest season provided, in itself, a and Blake (2003) suggested and then strong incentive to settle in one locality for defended a possible sequence of events by at least a good part of the year [as Flannery which teosinte domestication proceeded: (1969) asked regarding a hypothetical com- (1) people began casually harvesting and munity of Neolithic gatherers, “…after all, chewing the sweet stalks and shoots of where could they go with an estimated met- Zea plants; (2) they found that they could ric tonne of clean wheat?”], people eventu- extract more juice by mechanical mashing; ally and inevitably migrated. The ability to (3) to preserve the juice, they adopted fer- take with them a food source that doubled mentation techniques already in use with as the means of sowing future crops allowed other species; (4) they spread maize far and people to expand agriculture into previous- wide, as a new resource for making alcohol- ly unsettled areas, where the crops encoun- ic beverages; and, finally, (5) to expand Zea tered new selection pressures and the people cultivation, they began sowing harvested encountered new species of plants. seed. Once that sequence proceeded as far Abandoned fields created by early as step (5)—along with the discovery of the shifting cultivation in tropical forests may free-kernel mutant—domestication of Zea have provided environments in which mays as a grain crop would have followed useful wild plants could survive and quickly. But the time between its very first grow unusually well, possibly to become utilization by chewing and its full domesti- domesticates themselves (Piperno, 1989). cation as a grain may have been as long as Barley’s early maturity allowed farming at 2 500 years (Smalley and Blake, 2003). very high altitudes; pearl millet’s - Perhaps too often, researchers tend to extended agriculture into parts of portray the era of crop domestication as India and Africa that receive 200 mm or less one of constant struggle against scarcity of annual rainfall; and maize brought more and hardship. DeBoer (2003) commented people into the sparsely populated, mid- that the possibility of people first having altitude hill country of India and Pakistan utilized maize for sweet and fermented (Harlan, 1972). However, once settled in products. new environments, thanks to a reliable 20 Plant breeding and farmer participation

staple crop, people have not always sought Keen observation and use of genetic var- out additional species for domestication; iation in plant species has been a hallmark rather, are common on the of societies that depend directly on those fringes of agriculture (Harlan, 1972). plants, whether the people in those societies were hunter-gatherers, the originators of 1.7 CONCLUSIONS agriculture, or today’s subsistence farmers. In recent decades, institutional plant breed- As the millennia have passed, knowledge has ers have come to realize the importance expanded and methods have evolved, but of integrating breeding methodology with that thread remains intact. Today’s institu- farmers’ knowledge. Doing so has benefits tional plant breeders also benefit from that for breeders—whose selection goals become accumulated knowledge. Although modern more embedded in the ‘real world’—and breeders’ methodologies are often very dif- for farmers, who come to appreciate better ferent, they are rooted firmly in the past. their own ability to change gene frequen- They also utilize that major part of the first cies of their crops in favourable directions. plant breeders’ unwritten knowledge that This would appear to bring us full circle, survives in code, the genetic code of the to a time like that of agriculture’ s earliest plants themselves. days, when breeding and farming were Had the original crop domesticators been fully integrated. But today’s agriculturalists familiar with the principles of genetics, the also have ten millennia worth of hard-won crop species that they handed down to his- farming and breeding knowledge on which tory might have been even more profoundly they can draw by working together. transformed. Had they understood the haz- The first plant breeders lived in pre- ards of genetic erosion or pest and pathogen historic times, so they left us no direct epidemics, they might have domesticated accounts of the methods they used to a wider range of species and avoided the domesticate and improve crops. As we have genetic bottlenecks that restricted variation seen, many of our hypotheses about their in many crops from the very beginning. activities are influenced by our knowledge And could they have foreseen the devastat- of the methodologies that farmer-breed- ing consequences of soil erosion and water ers have used in historic times. That is no contamination under long-term annual accident. By extrapolating recent methods cropping (Cox et al ., 2006), they might have back to the origin of agriculture, we are mounted an effort to domesticate resource- acknowledging a 10 000-year-long, unbro- efficient perennial food crops. ken thread of skills and knowledge that Nevertheless, that relative handful of is derived from growing plants for food people was responsible for the most impor- while simultaneously breeding them for the tant turning point humanity has yet experi- future. Nevertheless, we should not forget enced, laying the foundation for the material that by coming to rely largely on domesti- and cultural world that surrounds us today. cated plants and animals, we humans have But in the evolution of agriculture, it has also lost vast amounts of knowledge of not been the case that superior knowledge other species and ecosystems; there is much and techniques continuously replace inferior that we could re-learn from hunter-gath- ones. Knowledge survives from every era, all erer societies of the present, the recent past the way back to the origin of crops (and even and the days before agriculture. well before), so that farmers, plant breeders Crop domestication and the first plant breeders 21

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