Download Plant domestication versus crop evolution: a conceptual framework

Opinion
Plant domestication versus crop
evolution: a conceptual framework for
cereals and grain legumes
Shahal Abbo1*, Ruth Pinhasi van-Oss1, Avi Gopher2, Yehoshua Saranga1, Itai Ofner1,
and Zvi Peleg1
1
Robert H. Smith Institute of Plant Sciences and Genetics in Agriculture, The Levi Eshkol School of Agriculture, The Hebrew
University of Jerusalem, Rehovot 7610001, Israel
2
Sonia and Marco Nadler Institute of Archaeology, Tel-Aviv University, Ramat Aviv 6997801, Israel
‘Domestication syndrome’ (DS) denotes differences
between domesticated plants and their wild progenitors. Crop plants are dynamic entities; hence, not all
parameters distinguishing wild progenitors from cultigens resulted from domestication. In this opinion article,
we refine the DS concept using agronomic, genetic, and
archaeobotanical considerations by distinguishing crucial domestication traits from traits that probably
evolved post-domestication in Near Eastern grain crops.
We propose that only traits showing a clear domesticated–wild dimorphism represent the pristine domestication episode, whereas traits showing a phenotypic
continuum between wild and domesticated gene pools
mostly reflect post-domestication diversification. We
propose that our approach may apply to other crop types
and examine its implications for discussing the timeframe of plant domestication and for modern plant
science and breeding.
Plant domestication
Domesticated plants differ from their wild progenitors in
several morphophysiological traits, most of which are
associated with seed retention and germination, growth
habit, size, coloration, and/or edibility of economically
important organs [1–3]. Comparative analyses drew attention to the similarity between the ‘domestication traits’
(see Glossary) of both closely and more distantly related
crops [4,5], which underlay the ‘domestication syndrome’
(DS) concept [6], a collective term describing the overall
differences between cultigens and their wild progenitors.
Crop plants are dynamic genetic entities [2,7,8]; therefore,
not all morphological, physiological, and biochemical
Corresponding author: Abbo, S. ([email protected]).
Keywords: crucial domestication traits; crop evolution traits; domestication episode;
domestication syndrome traits; episodic versus protracted domestication.
*
S. Abbo is the incumbent of the Jacob and Rachel Liss Chair in Field Crops and Plant
Genetics.
1360-1385/$ – see front matter
ß 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2013.12.002
Glossary
Caryopses: plural of caryopsis, the dry monocarpellate fruit typical of many
Gramineae, species (e.g., wheat, barley, rice) in which the pericarp is adhered
to the seed coat, commonly referred to as grain or kernel.
Crucial domestication trait: a trait without which the adoption of a species for
domestication would be impossible. Often, a trait that was imperative for the
profitable cultivation of this species (e.g., free germination in the Near Eastern
grain legumes). For the archaeobotanist, a crucial trait would be any
morphological (at the macro or micro level) or biochemical trait, or indeed
any trait, that enables a clear unequivocal classification of plant remains as
having either wild or domesticated origin.
Domestication traits: common use of this term refers to any morphological,
biochemical, developmental, or physiological traits showing a different
phenotype between domesticated plants and their immediate wild progenitors
[4,6,14,19]. Although some of these traits were associated with the domestication episode, many such traits have accumulated during millennia of crop
evolution under domestication. Hence, we propose a distinction between
crucial domestication and crop evolution/diversification traits.
Free germination: a physiological or physical condition of mature seeds that
enables germination upon water imbibition. This phenotype is associated with
domesticated forms but also in prevalent weed species.
Improvement (crop evolution, diversification) trait: any plant trait that was not
imperative for domestication and did not limit the adoption and management
of the respective species by humans. Such traits may have evolved at any
time after the ancient domestication episode (Box 1); therefore, these traits
are the result of crop evolutionary processes under (post-) domestication.
These traits were selected by farmers in antiquity; a process that gave rise to
the immense variation observed among traditional landraces in many world
regions, whereas in modern times crop improvement is mostly carried out by
breeders. Crop improvement traits may include (but are not limited to)
features associated with growth habit, higher (or more stable) yields, pest
and disease resistance, grain quality, and adaptation to new growing
environments.
Intact seeds: herein, seeds as harvested from the mother plant without any
physical or chemical damage to their seed coat.
Rachis: the inflorescence (spike) axis. The wheat and barley spikes are carried
at a terminal position on the stem, hence the rachis is formed by a series of
short nodes, with sessile spikelets (carrying the florets and grains) carried
alternately at each internode.
Scarified seeds: herein, mature seeds whose seed coat was injured to enable
water uptake by the seed and further germination.
Shattering: herein, the propagule dispersal mechanism of wild plants, for
example, via spike disarticulation into individual spikelets resulting from the
development of an abscission zone at the spike internodes, or via single seed
shattering as a result of pod dehiscence in legumes.
Sympatric: sympatric distribution of two or more plants refers to geographical
overlap in the range of their distribution, co-existence in the same region.
Teleological: as defined by the Merriam-Webster dictionary, this term may
refer to (i) a doctrine that ends are immanent in nature and (ii) a doctrine
explaining phenomena by final causes. According to the Oxford dictionary, the
explanation of phenomena is by the purpose they serve rather than by
postulated causes.
Vernalization: usually defined as the hastening of flowering following
exposure to temperatures much cooler than those optimal for vegetative
growth (e.g., [67]).
Trends in Plant Science, June 2014, Vol. 19, No. 6
351
Opinion
differences between extant crops and their wild progenitors can be attributed to ancient domestication episodes
[2,9]. Indeed, it is widely accepted that there is a differentiation between genetic changes associated with domestication and those resulting from later crop diversification
and under domestication [9–16].
By definition, the distinction between domesticationand improvement-related genetic changes relies on a conceptual distinction between ‘plant domestication’ and ‘crop
evolution’ [9,15] (Box 1). If a suite of traits can be identified
as having been crucial for the domestication of certain
crops, it follows that other features differentiating between
extant domesticated germplasm and the respective wild
gene pools are likely to have evolved after domestication.
In this context, an appropriate method for defining crucial
domestication traits may improve our understanding of
plant domestication and crop evolution [10,12]. In this
opinion article, we propose a conceptual and practical
Box 1. Domestication episodes and crop evolution
processes
Conceptual framework
There should be a distinction between historical ‘events’ (i.e., short
episodes) and long-term historical processes [106] when discussing
plant domestication [9]. In our view, the domestication episode took
place in a short time window that separated two long-term historical
processes – the preceding build-up of the perceptual and technological background and the later crop evolution under domestication processes [9]. The choice of species, recognizing the advantage
of domesticated genotypes, and the selection of these genotypes by
Neolithic communities were elements of the domestication episode.
Once domesticated, each crop plant underwent a distinct evolutionary trajectory. Crop evolutionary processes may include (but are
not limited to) the following: emergence of new morphologies (e.g.,
changes in grain size and shape, free threshing, increase in floral
fertility, growth habit), accumulation of allelic variation controlling
adaptive mechanisms (e.g., day-length insensitivity, vernalization
insensitivity), and quality traits (e.g., scent, change in protein or oil
concentrations).
Definitions
Episode
As defined by the Cambridge, Merriam-Webster, and Oxford
dictionaries, we use the word ‘episode’ to denote: a single event; an
event that is distinctive; an incident or period considered in
isolation.
Domestication
In biological terms, domestication refers to the major genetically
based phenotypes characterizing plants selected by humans (e.g.,
non-brittle rachis and free germination). In cultural terms, domestication is an episode based on a decision and follow-up action by
which humans have chosen certain species and selected particular
stocks for growing. Thus, domestication involves obtaining desirable plants with distinct phenotypes by taking educated and
conscious decisions.
Cultivation
Cultivation is a chain of husbandry operations defining the
‘agronomic’ arena and, thus, human intervention in the life of wild
or domesticated plants. This may include (but is not limited to)
threshing, cleaning, sorting, selecting and stocking seeds, soil
preparation, sowing, tending, and harvesting. The manipulation of
plants by Neolithic communities involved a new perception of land
and plants, and a change in the relation between culture and nature
(e.g., [9,107,108]). In this framework, cultivation is not a prelude (nor
a prerequisite) to ‘true’ (morphological) domestication
[4,28,95,97,100,109,110].
352
Trends in Plant Science June 2014, Vol. 19, No. 6
framework for identifying genuine domestication traits
and distinguishing them from traits that evolved after
domestication based on published data obtained from studies of Near Eastern wheat, barley, pea, lentil, and chickpea and their wild progenitors.
Theoretical considerations
Although the biological distinction between domestication
traits and improvement traits is widely accepted, there are
no clear criteria for such a classification [3,14,16–20]. To
remedy this situation we propose the concept of ‘crucial
domestication traits’, herein defined as traits imperative
for domesticating a plant and necessary for its cultivation.
Classical examples of such traits are free germination (loss
of seed dormancy) in the Near Eastern grain legumes [21–
23] and loss of bitterness (e.g., Cucurbitaceae, almond) [24–
27]. Although the concept of crucial domestication traits is
unlikely to prove universal or solve all the problems associated with plant domestication studies, it should greatly
assist in resolving some confusion and debate, for example,
regarding the domestication timeframe [9,28–31].
The most diagnostic DS traits of grain crops are monoor di-genic and often the domesticated phenotype is conditioned by recessive alleles [2,27,32,33]; therefore, genuine DS traits are expected to be monomorphic among
populations of the wild progenitor and within crop germplasm, albeit with the alternative (allele and) phenotype in
each of the respective gene pools. This is because such
traits are assumed to have been targeted during the selection for domestication. Traits that are polymorphic in the
wild but monomorphic (or with lower allelic diversity) in
the domesticated gene pool were probably also selected
during the domestication episode, and are likely to show
evidence of genetic bottlenecks [13,34–36]. Traits that are
monomorphic in the wild but polymorphic in the domesticated gene pool are likely to have evolved under domestication, such as chickpea seed shape (Figure 1) [37]. Traits
with equivalent polymorphism levels in the wild and in the
domesticated gene pools are unlikely to have had a major
role in genetic changes associated with domestication [36].
If indeed selection during the domestication episode did
not target such traits, a wide array of alleles and, hence,
phenotypes, would have entered the populations managed
by the Neolithic ‘cultivators’ as opposed to the purifying
selection in favor of free germinating legumes [21,23]. To
test our hypothesis, we have selected several Near Eastern
grain crops as test cases to analyze the pattern of genetic
variation of several morphophysiological traits often mentioned as part of the DS [4,6].
Crop plant test cases
Emmer wheat
Shattering. Spikes of wild emmer (Triticum turgidum ssp.
dicoccoides) disarticulate upon ripening, whereas domesticated emmer (T. turgidum ssp. dicoccum, T. turgidum
ssp. durum) have non-brittle rachis and spikes that remain
intact upon ripening [38] (Figure 1). Quantitative treatment of spike brittleness in a diverse emmer collection
(wild and domesticated) has confirmed that there is no
phenotypic continuum of spike brittleness between wild
and domesticated genotypes [39].
Opinion
Trends in Plant Science June 2014, Vol. 19, No. 6
(A)
(B)
(C)
Wild cicer
(D)
Wild emmer
(E)
60
16
50
12
40
20
4
10
Domescated wheat
Domescated chickpea
75
150
225
300
375
450
525
5
5
4
4
3
3
2
2
1
1
600
Seed weight, mg
5
10
15
20
25
30
35
40
45
50
55
Number of genotypes
30
8
60
Grain weight, mg
(F)
TRENDS in Plant Science
Figure 1. Traits related to seed dispersal and size. (A) Mature pods of wild pea (Pisum elatius) in its natural habitat. (B) Left, non-brittle spike of domesticated barley
(Hordeum vulgare); right, mature brittle rachis spike of wild barley (Hordeum spontaneum). (C) Mature disarticulating spike of wild emmer wheat (Triticum turgidum ssp.
dicoccoides). (D) Frequency distribution of seed weight among 35 wild Cicer genotypes and 25 domesticated chickpea cultivars. (E) Frequency distribution of grain weight
among 128 wild emmer accessions and 17 domesticated wheat cultivars. (F) Example of the phenotypic continuum of seed size in wild Cicer reticulatum (top) and
domesticated chickpea (bottom).
Post-harvest treatment. Glume toughness (ease of threshing), expressed as the spike harvest index [grain fraction
divided by the total spike weight (chaff + grain)] shows a
range among wild emmer accessions as well as among
traditional landraces (hulled and free threshing), albeit
without overlap between the wild and hulled domesticated
groups [39].
Germination. As observed in our routine laboratory work,
mature grains of domesticated emmer (traditional and
modern cultivars) germinate readily upon imbibition
normally attaining 95% germination. In nature, wild
emmer generally shows 50% germination (Figure 2)
because only one of the two seeds of its dispersal unit
germinates during the first rainy season following maturation [40]. We are unaware of a widescale comparative study
of germination in wild and domesticated emmer.
Grain size. On average, wild emmer grains are smaller
than domesticated emmer (Figure 1). However, there is
considerable overlap in grain weight values between wild
and domesticated emmer, making it impossible to classify
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Opinion
Trends in Plant Science June 2014, Vol. 19, No. 6
Wild pisum
Domescated pea
Wild
Domescated
Barley
Scarified seeds
Wild cicer
Domescated chickpea (D)
Domescated wheat
Wild emmer wheat
Vernalizaon
Control
(C)
(B)
Wheat
Intact seeds
(A)
TRENDS in Plant Science
Figure 2. Traits associated with germination and phenology. (A) Germination test of intact (control) and scarified seeds of wild Pisum humile and domesticated pea. (B)
Germination tests of wild versus domesticated wheat and barley. (C) Developmental vernalization response of wild Cicer and domesticated chickpea. (D) Erect and low
tillering growth habit of domesticated wheat (Triticum turgidum ssp. durum) versus prostrate and profuse tillering of wild emmer (Triticum turgidum ssp. dicoccoides).
grains that fall within the size-overlap range as wild or
domesticated (Figure 4 in [41]). Indeed, the now extinct,
domesticated emmer taxon Triticum parvicoccum had
smaller seeds than wild emmer [42,43], suggesting that
grain size evolution under domestication was not unidirectional.
Vernalization. Both winter (requiring vernalization for
timely flowering) and spring types (vernalization insensitive), as well as intermediate genotypes, were identified
among wild emmer [44] and among domesticated emmer
cultivars [45,46].
Barley
Shattering. Spikes of wild barley (Hordeum spontaneum)
disarticulate upon ripening, whereas domesticated barley
(Hordeum vulgare) has a non-brittle rachis and its ripe
spikes remain intact [38] (Figure 1).
Germination. Seeds of domesticated barley germinate
readily upon imbibition. Fresh dispersal units of wild
barley usually germinate poorly, whereas naked caryopses
germinate more uniformly [47].
Grain size. A continuum of wild–domesticated grain
weight values exists in barley. Mean grain weight values
of 0.036 g among wild barley from diverse habitats were
reported, with a range of 0.02 to 0.05 g [48,49]. Domesticated two-row barley genotypes with mean grain weight
values above 0.05 g are known [50]; however, mean grain
weight values below 0.036 g were documented among
domesticated two-row barley [51–53].
354
Vernalization. Parallel genetic diversity of vernalization
requirements was identified among wild, traditional, and
modern domesticated barley (e.g., [54]).
Pea
Shattering. Wild peas show full pod shattering upon
maturity, whereas domesticated pea cultivars have indehiscent pods, including modern as well as traditional landraces (e.g., Pisum abyssinicum, which is endemic to the
Ethiopian highlands).
Germination. Wild peas show a strong seed dormancy
phenotype mediated by water-impermeable seed coats
[23,55,56], whereas domesticated peas germinate readily
upon wetting. Although P. abyssinicum landraces have
staggered uneven germination, this phenotype does not
hinder profitable cultivation, as evident from its status as a
major crop in Ethiopia.
Seed size. We are unaware of a report on widescale
screening of seed sizes of domesticated versus wild pea
genotypes. Wild Pisum accessions in our working collection
have seed weights of 0.09 to 0.11 g. A range of 0.12 to 0.30 g
per seed was measured in a random sample of eight
domesticated field pea cultivars grown in Israel that were
obtained from the United States Department of Agriculture germplasm collection.
Vernalization. Both winter (vernalization responsive) and
spring (vernalization insensitive) domesticated pea cultivars are known [57]. We are unaware of any studies of the
vernalization requirements of wild pea germplasm. In our
Opinion
collection, some genotypes obtained from eastern Turkey
or Mount Hermon (Israel) have a strong vernalization
response, whereas wild peas from habitats with mild winters (e.g., near the Sea of Galilee, Israel) flower early in the
season without vernalization.
Lentil
Shattering. Wild lentils (Lens spp.) show a strong pod
shattering phenotype upon maturity [58], whereas domesticated lentils have incompletely indehiscent pods [59].
This partial dehiscence of domesticated lentil pods necessitates harvest by pulling before the crop is completely dry
in traditional agriculture [2,22], whereas modern lentil
cultivars requires chemical desiccation prior to mechanical harvest to minimize grain losses (http://www.agric.
wa.gov.au/objtwr/imported_assets/content/fcp/lp/lent/cp/
f09999.pdf).
Germination. Wild lentils show a strong seed dormancy
phenotype mediated by water-impermeable seed coats.
After wild seed dispersal, only 10% of seeds germinate
during the new growth season (October–November). By
contrast, domesticated lentil cultivars germinate readily
upon imbibition [22,38,60,61].
Seed size. Domesticated lentil cultivars are grouped into
two categories: ‘microsperma’ (small seeded) and ‘macrosperma’ (large seeded). However, a continuum of seed
weights ranging from 0.01 to 0.08 g across the two cultivar
groups has been reported [62–64]. Wild lentils have a range
of seed sizes that are mostly smaller than those of microsperma cultivars. Nevertheless, a seed weight of 0.016 g is
not uncommon in wild Lens orientalis [65].
Vernalization. We are unaware of a comparative study of
the vernalization response shown by wild and domesticated lentils. The latitudinal range of wild L. orientalis
(from Israel to Tajikistan) and the yet wider range of
domesticated lentils from Ethiopia across the Mediterranean, Asia Minor, Central Asia, and northwards to Scandinavia suggests that there may be naturally occurring
variation in phenology genes other than day-length sensitivity (vernalization included) in wild and domesticated
lentils.
Chickpea
Shattering. Domesticated chickpea have indehiscent pods;
however, a certain degree of pod shattering may occur
under hot and dry weather conditions. In wild chickpea
(Cicer reticulatum), a considerable proportion of the
mature pods remain intact, which led to the species being
described as preadapted to domestication [64].
Germination. Wild chickpeas show a strong seed dormancy phenotype because of their hard seed coats,
whereas all domesticated chickpeas imbibe water upon
wetting and show a free germination phenotype.
Seed size. Domesticated chickpea cultivars are classified
into two groups according to a suite of morphological traits,
including seed size. ‘Desi’ cultivars are characterized by
Trends in Plant Science June 2014, Vol. 19, No. 6
small angular seeds, whereas large ram-head or nearly
rounded seeds are typical of the ‘Kabuli’ cultivar group
[66]. Seed weight of C. reticulatum ranges from 0.09 to
0.20 g, overlapping the Desi group range (Figure 1).
Seed shape. Seeds of the wild progenitor of chickpea are
angular, whereas domesticated chickpea germplasm contain a wide range of seed shapes, that is, angular but also
rounded, and ‘ram-head’ absent in the wild gene pool
(Figure 1).
Vernalization. Domesticated chickpea is considered vernalization insensitive [67], whereas wild C. reticulatum
accessions show a considerable flowering advance (of
up to 30 days) in response to vernalization [68]. The
vernalization requirement is a major adaptation of the
wild progenitor being native to southeastern Turkey, a
region with winter temperatures that are below freezing,
but a major disadvantage for chickpea under domestication because it is a traditional spring crop [35,69]
(Figure 2).
Domestication versus improvement traits
The Near Eastern wheat, barley, pea, lentil, and chickpea
crops demonstrate several morphophysiological differences between the cultigens and their wild ancestors.
Nonetheless, for each crop test case there is a specific trait
presenting a clear dichotomy between the wild and domesticated forms (e.g., brittle versus non-brittle rachis cereals,
hard seeded versus free germinating legumes). This observation corresponds with the mono- or di-genic inheritance
of most diagnostic DS traits of grain crops [2]; therefore, we
propose that only traits showing a clear dichotomy between
the wild and domesticated forms reliably represent the
pristine domestication episode, whereas traits showing a
phenotypic continuum (e.g., seed size) between wild and
domesticated gene pools reflect (mostly polygenic)
improvement traits that evolved under domestication
[7]. Inability to identify any wild–domesticated dimorphism would not suggest that a crop plant is not ‘fully
domesticated’ but rather that there was no crucial phenotypic hurdle for its adoption as a crop. The proposed
conceptual distinction and apparently different genetic
bases between crucial domestication traits and crop evolution traits should provide students of plant domestication,
crop physiologists, and plant breeders better genetic resolution [9,13,16].
Although our approach may seem narrow in scope as
applied only to Near Eastern grain crops, a thorough
literature survey indicates that it may well apply to crops
from other world regions, as well as to tree and vegetable
crops, all with simply inherited crucial domestication
traits [70]; as documented for potato glycoalkaloids [71],
the bitterness traits of almond [72], melon [33], cucumber
[27], watermelon [73], pumpkin, and squash [25]. Similarly, free germination is simply inherited in all four
domesticated lupin species [74–78], and soybean [79]. In
several domesticated Vigna species between two and six
quantitative trait loci (QTLs) conditioning free germination were identified, but in all cases one or two accounted
for 25–45% of the variation thereby suggesting that only a
355
Opinion
single crucial domestication change was required for profitable cultivation [32,80–82].
Implications for modern plant science and breeding
A study that analyzed three classes of maize (Zea sp.)
germplasm (wild, landraces, modern cultivars) defined
domestication genomic changes as differentiating between
the wild progenitor gene pool and maize landraces [13].
Improvement changes were defined as distinguishing
between landraces and modern cultivars. Based on a genome-wide scan, the domestication-related polymorphisms
were shown to have different chromosomal distribution
compared with improvement-related polymorphisms, and
putative domestication loci showed evidence for stronger
selection (apparently during the domestication episode)
compared with improvement loci (post-domestication
selection) [13]. A study of crop–wild introgression in
maize–Zea mays ssp. mexicana [83] revealed evidence
for consistent genome-wide reciprocal introgressions. However, it appears that introgression from wild mexicana into
maize is restricted at DS loci (e.g., grassy tillers1, teosinte
branched1), and that introgression from maize into mexicana is rare along the short arm of chromosome 4, which
carries among other DS loci the teosinte glume architecture
gene. Genomic regions with significantly lower introgressions were termed ‘resistant to introgression’. Introgressions of mexicana alleles associated with the adaptation of
maize to the Mexican highlands (an improvement, change)
were detected; however, there was little evidence for introgressions of maize alleles into mexicana in the highland
adaptation loci [83]. Our interpretation of these observations is that (at least a part of) those genomic regions
‘resistant to introgression’ are the crucial maize DS loci,
as evident from their role in maintaining the genetic (and
adaptive) integrity of these two cross-compatible wild and
domesticated sympatric entities. Identification of crucial
domestication loci in the maize genome fully accords with
our theoretical considerations and strongly supports the
notion that DS traits have different genetic architecture
relative to improvement traits [13].
A different experimental approach based on wild and
domesticated genotypes has been applied to pea (Pisum
sativum) and lentil (Lens culinaris). These studies propose
that only the change at the seed dormancy locus can be
regarded as a crucial DS trait in lentil [21,22,60] and pea
[23]. This is because without free germination, cultivation
of wild pea and lentil (and probably also chickpea and
bitter vetch) is likely to result in net loss of seeds and
labor [23]. It is probable that indehiscent pods would
minimize yield losses in legumes; however, it is not imperative for profitable lentil or pea growing, as shown by
experimental cultivation of wild pea with dehiscent pods
after first ensuring full germination by seed scarification
[23]. Based on this finding, it was suggested that apart
from free germination (and changes in linked loci that may
have occurred by a correlated response to selection for free
germination) the allelic variation in approximately 15
genes (indehiscence included), distinguishing wild from
domesticated pea [56], can be regarded as diversification
traits that may have evolved any time during pea evolution
after domestication [9,23].
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Trends in Plant Science June 2014, Vol. 19, No. 6
This distinction between ‘pristine’ domestication traits
and later crop evolutionary genetic changes is highly relevant for modern plant breeding. The narrow genetic basis
of crop plants relative to their wild progenitors is an almost
universal phenomenon [34,84]. The ancient domestication
‘sampling errors’ were partly ‘corrected’ by many generations of introgression when and wherever populations of
wild progenitors were available for cross-pollination and
when such introgressed traits suited farmers’ preferences
[83,85–87]. The genetic basis of many crops was further
narrowed down owing to the abandonment of traditional
landraces following post-World War II industrialization of
many countries [88]. The recognition of those past and
recent genetic erosion events led crop geneticists to use
wild germplasm as a source for novel allelic variation
absent in cultigens (e.g., [89]).
Our distinction between domestication and improvement traits (and the respective genomic regions) may offer
a new perspective to studies determining which parts of
crop genomes were not subject to severe allelic erosion and
which were deprived of genetic variation owing to the
ancient domestication episodes. For example, a genomewide scan of wild and domesticated barley exposed a
chromosomal single nucleotide polymorphism (SNP)
diversity pattern corresponding with the prediction of
our approach [36], including parallel low SNP diversity
around the btr1btr2 loci that control spike brittleness in
both wild and domesticated genotypes (similar to monomorphism in both gene pools). However, no diversity
reduction was associated with the vrs1 gene that conditions the six-row phenotype or with the nud (naked kernel)
gene that are often mistakenly considered domestication
traits (e.g., [19]). Interestingly, a strong reduction in SNP
diversity was documented in chromosome 6H of the
domesticated germplasm, albeit with no known DS locus
in that region [36]. This may suggest that certain important but subtle traits linked to this region were altered
during the domestication episode of barley and therefore
merit investigation. Such ‘domestication charting’ of chromosomal regions vis-à-vis the selective sweeps associated
with domestication episodes (e.g., [13]) is essential for
effective modern allele ‘mining’ approaches aimed at
enriching modern cultivars with agronomically important
traits (e.g., [90]).
Implications for archaeobotany
Some of the morphological DS traits can be identified in
carbonized archaeobotanical material and thereby in conjunction with 14C dating may help to determine the context
and timing of the first appearance of morphologically
domesticated plants. A classical example of such a trait
involves the diagnostic difference between the smooth
disarticulation scar of wild wheat and barley dispersal
units and the rough breakage points of the non-brittle
rachis of their domesticated counterparts (e.g., [38,91]).
Indeed, for decades, 14C dating of archaeobotanical
remains has been used to infer the age and location of
the earliest domesticated cereals in the Near East [38] and
other world regions (e.g., [92]).
Domesticated cereals mostly have a more erect growth
habit compared with their wild ancestors [4] (Figure 2D),
Opinion
Trends in Plant Science June 2014, Vol. 19, No. 6
Table 1. Examples of major morphological and physiological traits of Near Eastern crops
Trait
Archaeobotanical
visibility a
Polymorphism pattern
Legumes
Cereals
Legumes
Cereals
Propagule
retention
Invisible
Visible
Monomorphic
Monomorphic
Germination
Invisible
Invisible
Monomorphic
Monomorphic
Seed shape
Visible
Visible
Polymorphic
Polymorphic
Seed size
Visible
Visible
Polymorphic
Polymorphic
Growth habit:
determinate or
indeterminate,
prostate or erect
Phenology:
day-length or
vernalization
response
Invisible
Invisible
Polymorphic
Polymorphic
Invisible
Invisible
Polymorphic
Polymorphic
Documented
wild–domesticated
overlap
Potential domestication marker
Living plant
Certain degree of
shattering in lentil
and chickpea
No overlap
Emmer wheat,
barley, lentil, pea,
chickpea
Emmer wheat,
barley, pea, lentil,
chickpea
Emmer wheat,
barley
Emmer wheat,
barley, pea
Refs
Archaeobotanical
remains
Only cereals
[39,111]
Good, mostly
legumes
Good
None
[21,23,55]
Poor, except
Cicer
[37,41]
Poor
Poor
[41,48,
49,65,111]
Good
None
[4]
Poor, except Cicer
None
[1,3,8,26,
44,54]
Good
a
Detectability (visibility) in the archaeobotanical record and potential for classification of living plants and archaeobotanical remains based on the wild–domesticated
phenotypic overlap.
but this trait is archaeologically invisible (Table 1). Likewise, the vernalization response typical of wild chickpea
[35,68] and absent in domesticated chickpea [67] cannot be
detected in archaeobotanical material. Archaeobotanical
remains of Near Eastern legumes consist of charred seeds
[93,94]; therefore, in the absence of remains of pods, pod
indehiscence, often considered a key DS trait (e.g., [56,95])
is archaeologically invisible, making it impossible to date
the first appearance of legumes with indehiscent pods
(Table 1).
The thickness and breadth of charred einkorn, emmer,
and barley grains from two early Neolithic sites in northern Syria (Jerf el Ahmar, 11 400–10 700; Dja’de, 10 600–
10 200 calibrated years Before Present) have been measured and compared to domesticated specimens from late
Neolithic/Chalcolithic Kosak Shamali (which is a site in
the same region) dating to 7000 calibrated years Before
Present [96]. The study showed that grain dimensions
increased over time in some cases [96]. Grain sizes from
several species retrieved from archaeological sites covering
a wide chronological range were also measured [97].
Assuming that such data from different archaeological
sites are representative of species-wide evolutionary patterns, evolutionary rates were calculated to describe ‘the
domestication process’ of wheat and barley over a time
window spanning 4000 years starting at the point in time
when the authors suggest that the species were first cultivated [97]. These regression analyses based on seed size
change over time were described as ‘direct evidence from
archaeobotany’ in support of a protracted domestication
scenario [98]. However, it was also suggested that the selfpollination breeding systems of the Near Eastern crops
enabled the ancient ‘cultivators’ to quickly identify and
selectively propagate recessive DS mutants under
perpetual sowing and reaping regimes in their fields
(e.g., [4,99,100]), which would result in relatively rapid
(rather than protracted) domestication timeframes [9].
Furthermore, in our view, the archaeo-evolutionary
approach described in [97] is weakened by: (i) the teleological nature of the pre-domestication cultivation concept
[101,102]; (ii) the circular argument regarding archaeobotanical remains that were interpreted as ‘arable weeds’
being used as an indicator of cultivation [103] (see discussion in [9,31]); (iii) the assumption that archaeobotanical
assemblages from different sites across the Near East can
be considered in terms of meta-populations of the respective species [30]; and (iv) the inability to distinguish
between plant domestication episodes and later-in-time
crop evolutionary processes, thereby undermining the conceptual and practical resolution power while treating
either prehistoric domestication episodes or crop evolution
under domestication processes [9]. Similar to the emmer
case (Figure 1E), and based on similarity of grain weight
values between wild and domesticated barley, the authors
of another study [49] concluded that domestication did not
involve changes in barley grain weight. We conclude that
the phenotypic continuum documented for seed weight in
wheat, chickpea, and lentil (wild and domesticated,
Figure 1) leads to the same conclusions as our population
genetic perspective [30]. Namely, that seed size measurements of archaeobotanical material of wheat, barley, lentil,
or chickpea are not reliable diagnostic parameters for
describing Near Eastern plant domestication. This does
not mean that the ‘first cultivators’ did not select for largeseeded wheat, barley, or lentil (they may well have done so
from the outset) but rather that with the abovementioned
phenotypic continuum, seed dimensions cannot be used to
classify archaeobotanical material as wild or domesticated
(Table 1). Another difficulty is the inability to distinguish
in archaeobotanical records between genetic changes
357
Opinion
affecting seed dimensions and phenotypic changes caused
by agro-technological improvements (e.g., manuring).
Although genome-wide scans of selective sweeps do not
require any a priori assumption regarding the timing or
cause of sequence changes, it would be ironic if interpretation of genomic scans with fine-grained resolution between
crucial DS and improvement loci [12,13,36,83,90] would be
limited due to a poor and vague conceptualization of plant
domestication as a millennia-long domestication-improvement continuum [19,28,29,97,98,104,105].
Concluding remarks
Experimental morphophysiological findings support the
concept of crucial DS traits [23]. At the DNA level, such
crucial DS loci play a major role in maintaining the genetic
and adaptive integrity of sympatric crop–wild complexes
[36,83]. Based on our crop test cases, we suggest that only
traits showing a clear dichotomy between the wild and
domesticated forms are reliable descriptors of the pristine
domestication episode (i.e., are genuine DS traits). More
specifically, traits with a clear phenotypic continuum
between wild and domesticated gene pools cannot be used
to discuss or to describe plant domestication (e.g., [96,97]);
therefore, these traits cannot provide support for a protracted domestication model [28,29,97,104]. Yet, such
traits appear as highly effective descriptors of crop evolution under (post-) domestication [9]. The application of our
crucial DS traits concept could become a powerful tool for
deciphering the genetic changes underlying the domestication episodes on crop-specific bases, thereby enabling
more efficient future crop improvement.
Acknowledgments
We thank Professor G. Ladizinsky for many years of teaching and
numerous discussions on plant domestication and crop evolution. S.A. is
indebted to Professor P. Gepts for discussions in which crucial disagreements were clarified and for comments on earlier versions of this paper.
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