plant and animal domestication as human- made evolution aibs-nabt... · time frame of domestication...
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Plant and Animal Plant and Animal Domestication as HumanDomestication as Human--
Made EvolutionMade EvolutionPaul Gepts
University of California, [email protected]
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IntroductionIntroduction• Examples of the importance of evolutionary
studies in agriculture and biotechnology• Resistance management in pesticide application and the
conservation of valuable pest control tools• DNA shuffling and the production of more efficient enzymes• Host-pest co-evolution and the development of more
resistant crops• Crop and animal domestication and evolution and the
genetic improvement of crops and animal breeds[... No doubt man selects varying individuals, sows their seeds, and again selects their varying offspring ... Man therefore may be said to have been trying an experiment on a gigantic scale; and it is an experiment which nature during the long lapse of time has incessantly tried ...]
C. DARWIN (1868), The Variation of Animals and Plants under Domestication
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C. Darwin (1809C. Darwin (1809--1882)1882)
• Darwin's conundrum: "The laws of inheritance are quite unknown.“– Chapter 1 of The Origin of Species by
Means of Natural Selection or The Preservation of Favored Races in the Struggle for Life (1859)
– The Variation of Plants and Animals under Domestication (1868)
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• Evidence for selection and inheritance? – Gigantism of harvested organs: e.g.,
• udders of cows and goats• seeds of domesticated plants
– “Comparing the diversity of leaves, pods, or tubers, or whatever part is valued in the kitchen-garden, in comparison with the flowers of the same varieties“
– "Very many of the most strongly-marked domestic varieties could not possibly live in a wild state.“
• Observations about domestication– “ ...in a vast number of cases, we cannot recognize ... the wild parent-stocks of
the plants which have been longest cultivated in our flower and kitchen-gardens.“– “In the case of most of our anciently domesticated animals and plants, I do not
think it is possible to come to any definite conclusion, whether they have descended from one or several species."; i.e. which is the wild ancestor(s), single or multiple domestications, where?
Questions raised/Observations Questions raised/Observations made by Darwinmade by Darwin
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Evidence for Origin and Dispersal of Domesticated Evidence for Origin and Dispersal of Domesticated Plants and Animals Plants and Animals
(modified from Harlan and de Wet 1973)
• Plants & Animals– Living:
• Experimental taxonomy• Geographic distribution• Ecological distribution• Genetic systems• Variation patterns• Morphology, physiology• Genetic reconstruction
– Dead:• Archaeology• Palynology• Paleobotany
• Humans– Living:
• Language• Oral tradition,
creation stories• Techniques• Attitudes towards the
crop, animals• Nutrition
– Dead:• History• Art• Archaeology• Physical
anthropology
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What is domestication?What is domestication?
• Definition of domestication: “Process by which wild plants or animals become adapted to humans and the environment they provide.”
• More than captive rearing or cultivation, taming
• Selection process leading to heritable morphological, physiological, genetic, and behavioral changes
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Domestication as an Evolutionary Domestication as an Evolutionary Study SystemStudy System
• In many cases, wild progenitor (or its immediate descendant) and domesticated plant or animal exist
• Traits subject to selection have been identified (“domestication syndrome)
• Time frame is generally known (approx. 10,000 years)
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Wheat, barley, pea, lentil, chickpea; pistachio, almond
Sorghum, pearl millet, cowpea, melon, coffee,
oil palm
Maize, bean,
squash, pepper, cotton, cacao
Potato, cassava, bean, cotton, pepper, peanut,
pineapple
Rice, peach, soybean, chestnut, quince, tea,
Chinese cabbage
Rice, banana, sugarcane, coconut,
cucumber, jute
Centers of Domestication of Crop Plants
Gepts 2002, 2003
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PutativePutative DomesticationDomesticationSitesSites
Olsen and Schaal 1999
Smith 2001Bean, maize, squash
Cassava
Heun et al. 1997
Einkorn wheat
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Domestication as an evolutionary Domestication as an evolutionary study systemstudy system
• In many cases, wild progenitor (or its immediate descendant) and domesticated plant or animal exist
• Traits subject to selection have been identified (“domestication syndrome)
• Time frame is generally known (approx. 10,000 years)
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Seed Dispersal
Zea mays
Aegilops sp.
Phaseolus vulgaris
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Increase in Size of Inflorescence, Fruit and/or Grain
W D
Zea mays
DW
Cucurbita sp.
W D
Pennisetum glaucum
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Changes in Growth Habit
Zea mays
W D
Pennisetum glaucum
WD
Phaseolus vulgaris
WD
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P. Bruegel the Elder (1565)
Photo: B. Bigbee (Utah State)
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GigantismGigantism
P. Gepts
Frary et al. 2000
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From Gepts 2002a
Consumerchoice
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Early Steps in Maize DomesticationEarly Steps in Maize Domestication
• Stiff rachis• Shallow cupules,
perpendicular orientation of lower glumes
• Two or four rows of seeds:– a, b: Single spikelet/node– c: Two spikelets/node
(Guila Naquitz: 5,400 BP: Benz 2001)
Cob apex
Cob apex
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Changes in YieldChanges in Yield
• Evolution of wheat yields in Mesopotamia (Araus et al. 2001) :– c. 8000 BC: estimated
grown yield was 1.56 Mg/ha
– contemporary yields: roughly 1.0 Mg/ha
• Maize yields in U.S.A.– Flat until 20th century?
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Domestication as an evolutionary Domestication as an evolutionary study systemstudy system
• In many cases, wild progenitor (or its immediate descendant) and domesticated plant or animal exist
• Traits subject to selection have been identified (“domestication syndrome)
• Time frame is generally known (approx. 10,000 years)
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Time Frame of DomesticationTime Frame of Domestication
z Only the earliest domesticated crop remains are listedy Uncertainty as to the domestication statusx Additional centers of domestication for the goat (in the Indian subcontinent) and the pig (in Eastern Asia) have been postulated
4,300Sunflower4,300SquashEastern United States
9,000-8,000RiceChina10,000Pigx
10,000Goatx9,200-8,500Flaxy
9,500-9,000Lentily9,400-9,000Einkorn wheatFertile Crescent
6,200Maize10,000SquashMesoamerica
Age (years BP)CropzLocation
Gepts 2004
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Major Findings about Major Findings about DomesticationDomestication
• Multiple, independent origins of plant and animal agriculture in last 10,000 years
• Genetic bottlenecks in genetic diversity• Important role of genes with major
phenotypic effect• Are genes for domestication clustered?• Molecular function of genes for
domestication• Is there a potential for domestication?
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Wheat, barley, pea, lentil, chickpea; pistachio, almond
Sorghum, pearl millet, cowpea, melon, coffee,
oil palm
Maize, bean,
squash, pepper, cotton, cacao
Potato, cassava, bean, cotton, pepper, peanut,
pineapple
Rice, peach, soybean, chestnut, quince, tea,
Chinese cabbage
Rice, banana, sugarcane, coconut,
cucumber, jute
Centers of Domestication of Crop Plants
Gepts 2002, 2003
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Major Findings about Major Findings about DomesticationDomestication
• Multiple, independent origins of plant and animal agriculture in last 10,000 years
• Genetic bottlenecks in genetic diversity• Important role of genes with major
phenotypic effect• Are genes for domestication clustered?• Molecular function of genes for
domestication• Is there a potential for domestication?
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Jaenicke-Després et al. 2003
Early allelic selection in maizeas revealed by ancient DNA
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Selection during domesticationSelection during domestication• Selection intensity:
– Wang et al. 1999: tb-1 in maize
• S = 0.04 – 0.08– Hillman and Davies:
tough rachis in einkorn (1990)
• Time to fixation:– Wang et al. 1999:
• Time to fixation: 315 to 1,000 years
– Hillman and Davies:• Time to fixation: 20 to
200 years
ToughBrittle
Relative fitness
1.000.43Uprooting
1.000.40Sickle
0.050.44Beating -single
0.050.84Beating -repeated
Harvest
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Major Findings about Major Findings about DomesticationDomestication
• Multiple, independent origins of plant and animal agriculture in last 10,000 years
• Genetic bottlenecks in genetic diversity• Important role of genes with major
phenotypic effect• Are genes for domestication clustered?• Molecular function of genes for
domestication• Is there a potential for domestication?
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Inheritance of the domestication syndrome in crops
• Species studied:– Maize, common bean, rice, pearl millet, sunflower
• Common features:– Few loci– Major phenotypic effect– Most of phenotypic variation accounted for in genetic
terms = high heritability– Few regions of the genome = linked
• Consequence:– Fast response to selection
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Ppd
PD, NM,DF, DM, SW, HI
NM, NP,DF, DM
L5
1 Growth habit, photoperiodsensitivity
Common bean,2n = 2x = 22(Koinange etal. 1996)
fin,Tor
Pl Al BlCtPb
NNPT, Hmax, NS, WES
6,7Spikelet architecture andshedding, plant and spikemorphologies and flowering
Pearl millet,2n = 2x = 14
20 cM
Rice,2n = 2x = 24
1
TP,PNL,SH
SBP,PL,PH
CC
Plant and paniclemorphology, shedding
FSDE,DTL
FC,DR,PVH
FW, FD,FP
ATL,DFR
Tomato,2n = 2x = 24
2 Fruit traits, earliness
6 sp
NSF FC,SSC,NFLT ATW
Growth habit, fruit traits
(Poncet et al.2000)
(Xiong et al. 1999)
(Grandilloand Tanksley1996)
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Major Findings about Major Findings about DomesticationDomestication
• Multiple, independent origins of plant and animal agriculture in last 10,000 years
• Genetic bottlenecks in genetic diversity• Important role of genes with major
phenotypic effect• Are genes for domestication clustered?• Molecular function of genes for
domestication• Is there a potential for domestication?
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Cloning of Domestication GenesExamples
• Tb-1 in maize: growth habit (Doebley et al 1997; Wang et al. 1999)
• fw2.2 in tomato: fruit weight (Frary et al. 2000)
• Hd1 in rice: flowering time (Yano et al. 2000)
• SHATTERPROOF in Arabidopsis: fruit dehiscence (Liljegren et al. 2000)
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Major Findings about Major Findings about DomesticationDomestication
• Multiple, independent origins of plant and animal agriculture in last 10,000 years
• Genetic bottlenecks in genetic diversity• Important role of genes with major
phenotypic effect• Are genes for domestication clustered?• Molecular function of genes for
domestication• Is there a potential for domestication?
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Is There a Potential for Domestication?Is There a Potential for Domestication?• Animals
– Docile (or selectable for docility); not afraid of humans
– Non-territorial; tolerant to herding, i.e. not afraid of each other
– Dominance hierarchy (Humans co-opt leadership role)
– Uninhibited breeding– Rapid growth
• Plants– Some 250,000 angiosperm species
• Less than 500 species domesticated– Trial and error domestication
• Northern China, northeastern USA• Alfalfa domestication?
– Inherent genetic potential?• Genetic variability• Morphological potential• Linkage of domestication genes• Probably not toxicity
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General characteristics of domestication
• Selection for adaptation to:– Growing or rearing condition– Utilization by humans
• Heritable changes as a consequence of bi-directional selection
• Dependence on humans for survival in thoroughly domesticated species
• Mutually beneficial relationship• Necessary condition for the development of
civilizations
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Domestication
HumansCultural development:
knowledge of plants, animalstechnology
Population growth
EnvironmentClimate changeContrast between dry
and humid seasonDiversity of niches
Plant or Animal MorphologyBehaviorGenetics
Gepts 2004
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Applications to AgricultureApplications to Agriculture
• Where to go for biodiversity?
• What plant material to use to broaden crop diversity?
• Co-evolution with pathogens and useful organisms
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Wheat, barley, pea, lentil, chickpea; pistachio, almond
Sorghum, pearl millet, cowpea, melon, coffee,
oil palm
Maize, bean,
squash, pepper, cotton, cacao
Potato, cassava, bean, cotton, pepper, peanut,
pineapple
Rice, peach, soybean, chestnut, quince, tea,
Chinese cabbage
Rice, banana, sugarcane, coconut,
cucumber, jute
Centers of Domestication of Crop Plants
Gepts 2002, 2003
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Nuña or kopuru(popping bean) growers
(Gepts 2004)
Sillani
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Applications to AgricultureApplications to Agriculture
• Where to go for biodiversity?
• What plant material to use to broaden crop diversity?
• Co-evolution with pathogens and useful organisms
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Reduction in Genetic Diversity in Common Reduction in Genetic Diversity in Common Bean during and after DomesticationBean during and after Domestication
0
0.05
0.1
0.15
0.2
0.25
Wild Landraces US Cultivars
MesoAndean
Sonnante et al. 1994
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SourcesSources ofof CropCropBiodiversityBiodiversity
Kelly et al. 1998
IncreasedRelatedness
Breadth of Genetic Basis
+ transgenes + genomic information
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Applications to AgricultureApplications to Agriculture
• Where to go for biodiversity?
• What plant material to use to broaden crop diversity?
• Co-evolution with pathogens and useful organisms
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Potato late blight (Phytophtora infestans)
Corn Southern leafBlight (BipolarisMaydis)
Coffee Rust (Hemileia vastatrix)
© Copyright 2000 The American Phytopathological Society
From ARC-ITSC, South Africa
(National Research Council (1972) Genetic vulnerability of crops. National Academy of Sciences, Washington, DC
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Conclusions
• Crop and domestic animal domestication: – Used by Darwin as an example of the potent effect of
selection – Experimental model:
• Known progenitor and descendants• Traits known• Time frame based on archaeological data
• Crop and animal breeding– Evolution in action– Measurable effect within lifetime (or PhD thesis!)
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Sources• General domestication:
– Darwin, C. On the origin of species. http://www.esp.org/books/darwin/origin/facsimile/
– Darwin, C. The variation of plants and animals under domestication. http://www.esp.org/books/darwin/variation/facsimile/title3.html
– Diamond, J. 1997. Guns, germs, and steel Norton, New York. – Diamond, J. 2002. Evolution, consequences and future of plant and animal
domestication. Nature 418:700-707 http://www.nature.com/cgi-taf/DynaPage.taf?file=/nature/journal/v418/n6898/full/nature01019_fs.html
– Gepts, P. 2004. Domestication as a long-term selection experiment. Plant Breed. Rev. 24 (Part 2):1-44. http://www.agronomy.ucdavis.edu/gepts/LTS.pdf
– History of food and agriculture: http://museum.agropolis.fr/english/pages/expos/fresque/la_fresque.htm
• Plant domestication:– Gepts, P. n.d. PLB143: The evolution of crop plants. Course notes.
http://www.agronomy.ucdavis.edu/gepts/pb143/pb143.htm• Animal domestication:
– Price, E.O. Animal domestication and behavior. CABI, UK. Chapter 1: http://www.cabi-publishing.org/pdf/Books/0851995977/0851995977Ch1.pdf