PLB143 - Lecture 16

How did plants evolve under domestication? Inheritance of the domestication syndrome

© Gepts and Poncet 1995-2008

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  • Required:
  • Additional readings:
    • Doebley J, Stec A, Wendel J, Edwards M (1990) Genetic and morphological analysis of a maize-teosinte F2 population: implications for the origin of maize. Proc. Nat. Acad. Sci. 87: 9888-9892
    • Hillman GC, Davies MS (1990) Domestication rates in wild-type wheats and barley under primitive cultivation. Biol. J. Linnean Soc. 39: 39-78
    • Koinange EMK, Singh SP, Gepts P (1996) Genetic control of the domestication syndrome in common- bean. Crop Sci 36: 1037-1045.
    • Ladizinsky G (1985) Founder effect in crop-plant evolution. Econ. Bot. 39: 191-199
    • Poncet V, Lamy F, Devos K, Gale M, Sarr A, Robert T (2000) Genetic control of domestication traits in pearl millet (Pennisetum glaucum L., Poaceae). Theor Appl Genet 100, 147-159.
    • Poncet V, Lamy F, Enjalbert J, Joly H, Sarr A, Robert T (1998) Genetic analysis of the domestication syndrome in pearl millet (Pennisetum glaucum L, Poaceae): inheritance of the major characters. Heredity 81, 648-658.
    • Poncet V, Martel E, Allouis S, Devos K, Lamy F, Sarr A, Robert T (2002) Comparative analysis of QTLs affecting domestication traits between two domesticated x wild pearl millet (Pennisetum glaucum L., Poaceae) crosses. Theor Appl Genet 104, 965-975.
    • Ross-Ibarra, J. 2004. The evolution of recombination under domestication: A test of two hypotheses. Amer. Nat. 163:105-112.
    • Gepts P (2004) Crop domestication as a long-term selection experiment. Plant Breed Rev 24 (Part 2): 1-44.  Pdf version
  • Presentation slides

Lecture 16 Plan

  • Recapitulation: Major elements of the domestication syndrome
  • Genetic analysis of individual traits
  • Joint analysis of multiple traits
    • Method to analyze quantitative traits
    • The case of maize, a cross-pollinated species
    • The case of beans, a selfing species
    • Pearl millet, a cross-pollinated species
  • Selection experiments
    • Tough rachis
  • Change in recombination rates?
    • Does domestication lead to higher recombination rates?

Recapitulation: Major elements of the domestication syndrome

  • Reduction/loss of means of dispersal
    • Brittle rachis
    • Shattering of pods
  • Reduction/loss of dormancy
  • More compact growth habit
  • Earliness
  • Gigantism
  • Photoperiod insensitivity
  • Reduction/loss of toxic compounds
    etc.


Analysis of individual traits

  • Seed dispersal (Ladizinsky 1985)
Crop
No. of loci
Type of genetic control of domesticated trait
Rice
1
Recessive
Oat: spikelet
1
Dominant
Oat: floret non-disjunction 
1
Recessive
Barley
2
Recessive in either
Sorghum

Recessive in either
Pearl millet 
3
Recessive
Lentil 
1
Recessive
Wheat
2
Recessive complementary

  • Seed dormancy (Ladizinsky 1985)
Crop
No. of loci
Type of genetic control of domesticated trait
Lupin   
1
Recessive
Vetch   
1
Recessive
  • Other individual traits: Similar results
  • Conclusionsimple control; cultivated traits is generally recessive

Joint analysis of multiple traits of the domestication syndrome

  • Analysis of quantitative traits: Methodology of Sax (1923)
  • Repeat previous analysis for set of markers distributed at regular intervals on each chromosome in the genome
  • Results: i.e. data obtained
    • minimum number of genes distinguishing the two parents
    • magnitude of the phenotypic effect of individual genes
    • total proportion of phenotypic variation in the segregating population for a given trait that can be accounted for in genetic terms
    • linkage relationships among genes
  • Same basic approach in human genetics but some modifications: e.g., affected siblings method



The domestication syndrome in maize

  • Goal: determine the genetic and morphological steps necessary for transformation of teosinte (wild maize) into maize 
  • Major morphological differences affecting:
    • growth habit 
    • female inflorescence ("ear")


  • Growth habit: wild (left) vs. domesticated

    (from B. Smith, The emergence of agriculture. © 1995 Scientific American Library)
  • Female inflorescence

    (from Doebley et al. 1990)

Main traits distinguishing teosinte (wild maize) and maize

Trait   
Teosinte   
Maize
Growth habit 
Terminal inflor. 
Tassel (male)
Tassel (male)
Lateral branch: length 
Long
Short
Lateral branch: terminal inflor. 
Tassel (male) 
Ear (female)
Female inflorescence
Ranks
2
>=4
Cupules   
Large, indurate
Reduced
Spikelets
Sessile   
Sessile + pedicellate
Glumes
Hard 
Soft
Abscission layer 
Present
Absent

Experiment of Doebley et al. (1990)


  • Cross: Chapalote (primitive maize) x Chalco (teosinte); F 2: 260 plants
  • Traits measured:
    • CUPR: no. cupules/rank
    • DISA: tendency of ear to shatter
    • GLUM: hardness of glumes
    • GLUM: hardness of glumes
    • LBIL: average length of internodes on primary lateral branch
    • LIBN: number of branches on primary lateral inflorescence
    • PEDS: % cupules lacking pedicellate spikelet
    • PROL: no. of ears on primary lateral branch
    • PROL: no. of ears on primary lateral branch
    • RANK: no. of rows of cupules
    • STAM: % of male spikelets in primary lateral inflorescence
  • Molecular markers:
    • 58: RFLPs and isozymes
  • Statistical analyses:
    • linkage map, identification of loci
Results

  • Morphological trait analysis:
    • wide range of phenotypes
    • many traits: recovered parental phenotype: <--> few genes
    • no plants combined all key traits characteristic of maize or teosinte
  • Associations between molecular markers and morphological traits
    • Associations: 4-8 genes
    • Most cases: associations as predicted: mazie allele associated with the maize phenotype (same for teosinte)
    • Distributed on all chromosomes; chromosomes with largest effects: 1 to 4; particularly long arm of 1 (5/9 traits); 5 regions with major effect; explains frequent recovery (1/500) of maize- or teosinte-like plants 
    • Certain traits (e.g., GLUM, RANK): major genes: r2 = 0.42





  • Summary
  • few genes
  • major genes
  • limited number of genomic regions with major effect
<--> consistent with results of single-trait analyses

Main traits distinguishing wild and domesticated beans (Phaseolus vulgaris)  

Koinange et al. 1996

  • Goals:
    • morphological and physiological traits: dormancy, photoperiod sensitivity
    • genomic distribution in predominantly self-pollinated crop
  • Methods:
    • Midas (snap bean; largest array of domestication traits in beans) x G12873 (typical wild bean)
    • 85 molecular markers: RFLPs, isozymes


Phenotype
General attribute
Trait 
Wild: G12873
Domesticated: 'Midas'
Seed dispersal
Pod suture fibers (St
Present
Absent

Pod wall fibers (St?)
Present 
Absent
Seed dormancy
Germination (DO) 
58% 
100%
Growth habit
Determinacy (fin)
Indeterminate    
Determinate

Twining (Tor
Twining    
Non-twining

Number of nodes on the main stem (NM)
23
8

Number of pods (NP)
29 
17

Internode length (L5) 
1.9 cm
2.6 cm
Gigantism
Pod length (PL)
5.7 cm
9.6 cm

100-seed weight (SW)
3.5 g
19.5 g
Phenology
Number of days to flowering (DF) 
69
46

Number of days to maturity (DM)
107
80
Photoperiod sensitivity
Number of days to flowering under 16 h days (PD)
44
35




Harvest index
Seed yield/total above-ground biomass (HI) 
42%
62%
Seed pigmentation
Presence vs. absence (P
Present (agouti)
Absent (white)
  
Results
  • For many traits: major genes:
    • number of nodes: 53%
    • dormancy: 52%
  • Large proportion of phenotypic variation accounted for in genetic terms
  • Limited number of genomic regions with major effect: D1, D2, D7, D8
  • Physiological traits: also simple control:
    dormancy: see above
    photoperiod sensitivity: 1 major gene
  • Linkage map: shows concentration of domestication genes on few linkage groups (D1, D2, D7, and D8 ; see map)





  • Linkage map of common bean



Other example: Pearl Millet (Pennisetum glaucum)


  • General characteristics: 
    • Majore crop in Western Africa 
    • Subsistence
    • More drought tolerant than sorghum
  • Domestication syndrome
    • Differences in growth habit:
    • Domesticate has fewer tillers and more apical dominance
    • Taller plants
  • Compare with maize: 
    • Growth habit 
    • Inflorescence


Differences in inflorescence

  • Spike: wild vs. domesticated 
  • Spikelet: wild vs. domesticated

  • Spike differences
    • Wild  
    • Domesticated 

Earlier results: linkage of key domestication genes


Summary of the domestication syndrome in pearl millet


QTL Analyses




A comparison of linkages with other species



(From Gepts 2004)

Summary of genetic studies on the domestication syndrome

  • Linkage-map based analyses:
    • Outcrossers: Maize, pearl millet
    • Selfers: Common bean, rice, tomato
  • Common features:
    • Few loci
    • Major phenotypic effect
    • Most of phenotypic variation accounted for in genetic terms = high heritability
  • Few regions of the genome = linked

Selection experiment for domestication traits

Tough rachis -- Hillman and Davies 1990


  • Goal: measure domestication rate (speed) for wild einkorn and barley (tough rachis)
  • Tough rachis would result as a consequence of selection during harvest (see Lecture 08 )
  • Questions:
    • which type of harvest?
    • which type of selection?
  • Harvest methods, likely to be known or used at that time:
    • Beating ripe spikelets into baskets:
      • harvest strongly favors brittle-rachised types --> next year's crop will be wild-type
      • left behind: tough-rachised; stripped by birds
      • least effort; greatest yields
    • Sickle-reaping; partially ripe crops
      • ripe stage: high losses
      • favors tough-rachised types; brittle-rachised types: loss in ripest part (top) of the ear
    • Sickle-reaping; unripe crops
      • advantage: minimize losses from brittle-rachised types
      • no effects either way: no differentiation between tough and brittle
      • unripe = partially ripe; still favorable effect for tough types but very low selection pressure
    • Harvesting by uprooting; partially ripe or unripe: see sickle-reaping
    • Harvesting by hand stripping
      • selective effects similar to beating
      • much slower

Additional considerations

  • Conscious or unconscious selection
    • Initially, unconscious:
      • mutants rare: 1/1,000,000
      • difficult to identify: uneven ripening, within and between ears
      • intact ears could have been predated by birds
    • After increase to sufficient level (1-5%) --> conscious selection
  • Shifting cultivation?
    • Same plot or different plot?
      • seeds: higher frequency of tough-rachised types
      • self-sown plants: higher frequency of brittle-rachised types
    • Balance between:
      • % survival of wild-type seeds falling to the ground
      • % harvested grain set aside for next year's planting

Computer model

  • Harvest method: see Table below
  • Fitness levels: probability of being harvested
  • Inbreeding frequency: <1-5%
  • Mutation rate: 1/1,000,000;
    • 1/4,000,000 is tough-rachised type;
      200 stems/sq. m; 1 mutant/1-2 ha

,

Genetic data (based on single traits) suggests rapid domestication (in less than 100-200 years), assuming constant parameters such as the level of selection and inbreeding

Table. Efficiency of different harvest methods for wild-type and domesticated rachis types (expressed relative to sickle harvest as 100%)

Harvest method 
Wild-type (brittle)
Domesticated (tough)
Beating repeated passes 
84
5
  • Beating single pass a
30

  • Beating single pass b
48

  • Beating single pass c
45

Beating single pass mean
44
5
  • Reaping with sickles a 
35

  • Reaping with sickles b
43

  • Reaping with sickles c
43

Reaping with sickles mean 
40
100
  • Uprooting a
41 

  • Uprooting b
37 

  • Uprooting c
51

Uprooting mean
43

100

 

Conclusion: The combination stiff rachis in the plant + sickle (or uprooting) harvesting provides the highest yield, which may explain why it has come to predominate in early agriculture.

             

An archaeologist's view on the speed of domestication

Tanno and Willcox (2006)

Necessary conditions to answer such a question:

  • S.W. Asia (the Fertile Crescent): Most abundant archaeological record
  • Can distinguish between wild and domesticated remains

(from Tanno and Willcox 2006)

Observations:

Progressive increase in frequency of domesticated spikelets over 1,000s years
(Qaramel, Nevali Cori, el Kerkh, Kosak Shamali: wheat; Aswad, Ramad: barley)

(from Tanno and Willcox 2006)

Conclusion:

The time frame for domestication based on archaeological data extends over severl 1000s of years. What could account for the discrepancy between genetic and archaeological data?


Evolution of recombination during domestication

(Ross-Ibarra 2004)

  • Did domestication increase recombination?
    • Selection favors increased recombination:
      • Population bottlenecks, genetic drift, negative interactions   OR
  • Was high recombination a pre-adaptation to domestication?
    • High recombination increases response to strong selection

How to test these hypotheses?

  • Comparison of linkages in: 
    • Progenitor – domesticate 
    • Progenitor – congener
  • Potential for domestication?

Recombination comparison

Comparison of recombination rates


Congener – Progenitor
Progenitor - Domesticated
Species pairs
20
20
Average difference (SE)
0.031 (0.037)
0.117 (0.045)
Paired t test
0.208
0.009
Wilcoxon
0.161
0.017
Conclusion: “Recombination is no pre-adaptation for domestication”

Conclusions

  • The genetic control of the domestication syndrome is relatively simple:
    • few genes involved
    • several genes have major phenotypic effect
    • large proportion of the phenotypic variation can be accounted for in genetic terms
    • few genomic regions involved (linkage)
  • Genes for domestication represent a small subset (possibly not representative) of all genes operating in a plant genome
    • may not adequately represent trends in genome diversity during domestication
  • Domestication could have occurred quite rapidly: possible limitations
    • mutants
    • selection intensity
    • recombination
  • nHigh recombination is no PRE-adaptation for domestication but might be an adaptation or consequence for domestication

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