Annual Plant Reviews (2009) 38, 238–295
doi: 10.1002/9781444314557.ch7
www.interscience.wiley.com
Chapter 7
SEED DISPERSAL AND CROP
DOMESTICATION:
SHATTERING, GERMINATION
AND SEASONALITY IN
EVOLUTION UNDER
CULTIVATION
Dorian Q. Fuller1 and Robin Allaby2
1
2
Institute of Archaeology, University College London, London, UK
Warwick, HRI, University of Warwick, Wellesbourne, Warwick, UK
‘The Angiosperm seed had a double significance. It not only gave command of dry
land to plant life, but it provided the means by which mankind has been able to
obtain an ample and assured food supply. To the Angiosperm seed, perhaps more
than to any other structure, the economic evolution of the human race is due.’
Oakes Ames (1939, p. 5)
Abstract: The transition between wild plant forms and domesticated species can
be considered an evolutionary adaptation by plants in response to a human driven
ecology. Evidence from archaeobotany and genetics is providing deeper insight
into this evolutionary process in terms of its scale, mechanism and parallelism
between species. The evidence indicates that the timescale of this evolution was
considerably longer than previously supposed, raising questions about the mode
of human mediated selection pressure and increasing the importance of the role of
pre-domestication cultivation. Different selection pressures were chronologically
separated into at least three stages, each important at different points of the evolutionary process affecting different traits. Early selection pressures were ultimately
driven by the pre-domestication sowing activities affecting the polygenically controlled germination and seed size traits. Later, in the second stage, release of natural selection pressures of dispersal requirements led to modification of architecture
such as awns loss of awns and increase in dispersal unit size. The loss of dispersal requirement combined with positive pressure through harvesting practice led
238
Fruit Development and Seed Dispersal Edited by Lars Østergaard
© 2010 Blackwell Publishing Ltd. ISBN: 978-1-405-18946-0
Seed Dispersal and Crop Domestication 239
to the typically monogenically controlled non-shattering phenotypes. At the tertiary stage new selection pressures were imposed with changing climate caused by
movement of the crops into different latitudes, resulting in typically monogenically
controlled aseasonal phenotypes. The genetic evidence shows in most cases that
genetically similar mechanisms have been affected in different plant species implying an evolutionary convergence in response to adaptation to human ecology.
These adaptations can be considered various types of heterochrony; a mechanism
of major importance generally in plant evolution.
Keywords: archaeology; genetics; cereals; legumes; convergent evolution;
dehiscence; dormancy
7.1 Introduction
In the long-term view of human history, the beginnings of agriculture was
one of the great turning points, and a central part of this turning point was
the evolution of new plant forms, domesticated crops. Anthropologists and
botanists alike have argued about how precisely to demarcate ‘domestication’ from non-domesticated wild species (e.g. Higgs and Jarman, 1969, 1972;
Harris, 1996, 2008; Zeder, 2006). But, in general, all agree that domestication
implies an increased interdependence between human cultivators and the
plants they cultivate, and that this can be considered a case of symbiotic
coevolution (Higgs and Jarman, 1969; Reed, 1977; Rindos, 1980). It is certainly true that different kinds of crops have experienced different selective
pressures and show different adaptations for domestication; thus fruit trees
and vines differ fundamentally from tuber crops or seed crops. In the present
contribution, we will focus on seed crops and review the role of changes
in seed dispersal, broadly interpreted, and how these have been essential
aspects of the domestication process. By seed crops, we mean those species
which are cultivated primarily for their harvested seeds or fruits and which
are plants grown from seed. As such, this category not only includes all cereals, pulses (grain legumes) and oilseeds, but also some fibre crops. We will
assess examples of changes in dispersal traits and how their evolution can
be studied through archaeological plant remains (archaeobotany) as well as
through genetics. While we will not attempt to provide a comprehensive list
of seed crops and domestication traits, we will draw from a selection of examples from across different regions of origin, taxonomic families and degrees
of current knowledge.
Domestication, as we use it here, is a quality of plants in which morphological (and genetic) changes are found amongst cultivated populations by comparison to free-growing wild populations. These changes represent adaptations to systems of cultivation and human harvesting, and as
such evolved by frequency changes of key alleles in the genomes of cultivated populations. These changes would have first appeared during a period of pre-domestication cultivation when human behaviours modified the
240 Fruit Development and Seed Dispersal
environments and reproductive cycles of plants, especially by human intervention in the dispersal of seeds (Harris, 1989; Hillman and Davies, 1990,
1999; Fuller, 2007a). One of the key changes often regarded as the characteristic of domesticated grain crops was a shift from natural seed dispersal
through shattering mechanisms (pod dehiscence, or spikelet shedding of
grass ears/panicles) to obligate dispersal by people (Zohary, 1969; Harlan
et al., 1973; Hillman and Davies, 1990, 1999). Populations can be regarded as
fully domesticated when they are dominated by such non-dispersing genotypes, and the term ‘semi-domesticated’ has been proposed for populations
which show other changes associated with domestication prior to fixation of
the non-shattering traits (Fuller, 2007a). Some of these other changes include
loss of wild-type germination inhibition and changes in seed size, which are
also linked to successful early growth of seeds planted in cultivated fields
(Harlan et al., 1973; Harlan, 1992: Ch. 6; Smith, 2006a; Fuller, 2007a). All of
these changes were essential to the success of domesticated plants, and archaeobotanical studies are providing increased evidence for the process and
timing of their evolution. Another important set of changes in many crops,
which is broadly related to dispersal, is seasonality control, through processes
of photoperiodicity and vernalization. Changes in the control of seasonality
of growth and flowering played an important role in the dispersal of some
domesticated plants by farmers into new geographical zones, which differed
in climate or environment. The genetic dissection of these traits is providing
new insights into the history of this process. In the sections that follow, we
will review these traits and their study, drawing selected examples from those
species that have been best documented.
7.2
Loss of natural seed dispersal in wheat and barley:
archaeobotanical evidence
‘. . . wild wheats and barley have fragile spikes, and their ears disarticulate immediately upon maturity. The fragility of the spike is, in fact, the main diagnostic
character that serves for distinction of wild cereals from their cultivated counterparts. But what is less emphasized is that brittleness is only the most conspicuous
reflection of one of the major adaptations of these wild cereals to their wild environment: their specialization in seed dispersal.’
Daniel Zohary (1969, pp. 57–58)
This is often regarded as the single most important domestication trait
(‘domestication’ sensu stricto) because it makes a species dependent upon
the human farmer for seed dispersal. In cereals, this occurs by the loss of
abscission at the abscission scars, such as the rachis attachment points in
wheat or barley ears or the rachilla to spikelet base attachment in panicled
cereals (rice and millets). The result is that instead of shedding seeds when
they are mature, a plant retains them, and they are then usually separated
Seed Dispersal and Crop Domestication 241
(a)
(b)
Figure 7.1 Comparisons between wild and domesticated plants in terms of seed
dispersal. (a) Comparison between a wild shattering wheat ear (left) and domestic wheat
ear with a tough rachis, which requires pounding to break apart (right). The form of
rachis segments that can be recovered archaeologically is shown in the middle. (b)
Generalized wild bean with pod that twists and opens, dispersing seeds (left) compared
with a domestic pod that remains closed (middle) and must be split open by human
force (right).
by the addition of human labour (threshing and winnowing) (Fig. 7.1). For
farmers, this increased the efficiency of harvest and thus yields. Higher yields
can be produced because the farmer could wait until all, or most, of the
grains on a plant have matured, whereas earlier harvesting would have had
to balance loss of grain through shedding, as they matured, with reduced
yields through grains harvested immature (i.e. before spikelets have filled
entirely). This would have been a particular problem with cereals such as
242 Fruit Development and Seed Dispersal
wild rice which has a long period of grain maturation, and which may have
grown in wetland environments in which shed grains were lost (Fuller et al.,
2007a; Fuller and Qin, 2008).
The evolution of non-shattering would have occurred as a result of particular methods of harvesting that favoured non-shattering (tough rachis) mutants in harvested populations which were then sown (Hillman and Davies,
1990, 1999). Archaeologists have long attributed this to the use of sickles for
harvesting (e.g. Wilke et al., 1972; Hillman and Davies, 1990, 1999; Bar-Yosef,
1998; Willcox, 1999), although recently Fuller (2007a) has questioned this
on the grounds that non-shattering cereals appear to have evolved slower
than what sickle harvesting models have predicted; in some regions such as
the Near East, sickles precede domestication by many thousands of years,
while in other regions such as the Yangtze valley of China, sickles or stone
harvesting knives were introduced to artefact toolkits after rice was already
domesticated. This is currently an area of debate and discussion amongst
archaeobotanists (see Balter, 2007). What is clear is that other methods of
harvesting might not have selected for this domestication trait. Ethnographically gatherers of wild seeds have often used paddle and basket harvesting
methods (Harris, 1984; Harlan, 1989, 1992) and some harvest by uprooting immature grasses (Allen, 1974). It has been suggested that early hunter–gatherer
groups in the Near East could have gathered wild wheat and barley spikelets
from the ground after shedding, which is also one method that would not
be expected to select for domestication traits (Kislev et al., 2004). The methods of harvesting, together with their timing in relation to spikelet maturity,
created some level of selection for non-shattering domestic-type mutants.
While archaeologists may continue to debate what those human behaviours
were, archaeobotanical studies are beginning to provide hard evidence, at
least for a few species, for the proportions of wild (shattering) and domesticated (non-shattering) morphotypes in populations at particular times and
places and thus we are able to document that rate at which domestication
evolved.
Wheat and barley have the best documented record of domestication which
took place in the Near East (Fig. 7.2). In these cereals, the distinction between
shattering and non-shattering forms is clearly manifest in the attachment
scars on the rachis segments, which are part of the spikelet base in wheats.
Therefore, a clear distinction between wild and domesticated plants, and
documenting the transition between them, should involve a study of rachis
remains. While this was already clear to Helbaek (1959), data were limited,
mainly to a few impressions in mud-brick. Early flotation in the Near East
did recover rachis remains but large assemblages in which wild and domesticated morphtypes were distinguished did not begin to be published until the
mid-1980s, with Van Zeist’s study of the barley rachis from Tell Aswad (Van
Zeist and Bakker-Heeres, 1985). It is only in the past few years that studies
have directly examined the time gap between the beginnings of cultivation,
and the initial appearance of non-shattering cereal ears, and the end of the
Seed Dispersal and Crop Domestication 243
Figure 7.2 Map of Southwest Asia, showing the locations of sites with
archaeobotanical evidence that contribute to understanding the origins and spread of
agriculture (after Fuller, 2007a). Sites are differentiated on the basis of whether they
provide evidence for pre-domestication cultivation, enlarged grains, mixed or
predominantly domestic-type rachis data. Note that these sites represent a range of
periods, and many sites have multiple phases of use, in which case the earliest phase with
significant archaeobotanical data is represented. Shaded areas indicate the general
distribution of wild progenitors (based on Zohary and Hopf, 2000 with some refinements
from Willcox, 2005). It should be noted that wild emmer (Triticum diococcoides) occurs
over a subset of the wild barley zone, and mainly in the western part of the crescent.
domestication process marked by the predominance or fixation of domestictype non-shattering cereals (Tanno and Willcox, 2006; Fuller, 2007a). Although
theoretically it could have happened very quickly, as demonstrated under
ideal experimental conditions (Hillman and Davies, 1990, 1999; see also Zohary, 2004), this no longer appears to be the case.
As already indicated, there is now growing recognition of a long period of
pre-domestication cultivation. In a compilation of data from five representative sites, three with einkorn wheat and two with barley, Tanno and Willcox
(2006) suggested that cereal domestication might take millennia, perhaps as
long as 3000 years, while Weiss et al. (2006) accepted at least a 1000-year period. A comprehensive compilation of nearly 5000 barley rachises (Hordeum
spontaneum/vulgare) and 1800 einkorn wheat (Triticum boeitucm/monococcum)
spikelet bases (Fuller, 2007a) similarly indicated slow domestication with an
estimated 1500–2000 years for the transition to predominantly non-shattering
morphotypes, starting from ca. 9500 BC (Fig. 7.3). But if weed flora evidence
for pre-domestication cultivation is accepted for Abu Hureyra and Mureybit (Colledge, 1998; Hillman et al., 2001; Willcox et al., 2008) and assumed
to be continuous with later cultivation and domestication, then it should be
244 Fruit Development and Seed Dispersal
Figure 7.3 Domesticate rates in barley and einkorn wheat modelled from
archaeobotanical data (after Fuller, 2007a). Proportion of domesticated type for each site
is plotted by a box against a median estimate of site age. A margin of error is indicated by
the line which connects the sum of domesticated and uncertain types (indicated by a
cross or x). Trend lines are shown based on the lower estimate. (a) Barley domestication
rate model, on which period averages are also plotted for the PPNA, Early PPNB and Late
PPNB, in which the diamond indicates the proportion of domesticated types and the
circle the sum of domesticated and uncertain types. (b) Einkorn domestication rate
model; trend line does not consider the much later Kosak Shamali.
assumed that cultivation began a further 1000–1500 years earlier, bringing the
estimate to 3000–3500 years. The recognition of pre-domestication cultivation
together with a slow domestication process reopens the question as to just
how early some cultivation might have begun. It also dissociates the beginnings of cultivation from subsequent domestication leaving an open question
Seed Dispersal and Crop Domestication 245
as to how many centres of origin there were for cultivation and whether all
of these were equally involved in selection for domesticated plants. Most
archaeologists now assume that there were multiple independent centres of
early cultivation and eventual domestication in the Near East (Nesbitt, 2004;
Willcox, 2005; Weiss et al., 2006; Fuller, 2007a; Zeder, 2008) but further research
is still needed to delineate these.
The overall regional pattern is the replacement of entirely/predominantly
morphologically wild barley with predominantly domesticated barley by the
end of the Pre-Pottery Neolithic periods. How we explain this long domestication period, however, remains uncertain. Willcox et al. (2008) have suggested
that continued collecting from wild stands to replenish stores would slow
down the rate at which domesticated types were selected, and harvesting
of ears somewhat immature would also act against strong selection for domesticated types (as already noted by Hillman and Davies, 1990, 1999; see
also Fuller, 2007a; and parallel issues with Asian rice, Fuller et al., 2007a).
Certainly, even in the late Pre-Pottery Neolithic B (PPNB) period of the Near
East, there is intersite variability in the proportion of wild barley rachis, which
may relate to different degrees of continued reliance on gathering from wild
stands. As suggested by Ladizinsky (2008), local bottlenecks may have been
caused by drought or disease and forced cultivation of additional stock from
wild populations. Another alternative is to reconsider the presumption that
hunter–gatherers would have sickle-harvested wild cereals, which has long
been the basis for our models of the evolution of non-shattering domesticates,
but which should have led to rapid domestication (Hillman and Davies, 1990,
1999). It can be suggested that the sickle was transferred to harvesting crops
after non-shattering ears were a significant component of crops (Fuller, 2007a).
Sickle harvesting of crops was an exaptation as sickles were developed earlier as a technology for cutting basketry or building materials (Sauer, 1958;
Sherratt, 1997; Kislev et al., 2004; and note the cut wild straw as bedding
material at 23 000 bp Ohalo II: Nadel et al., 2004). Hillman and Davies (1999)
had discussed how harvesting by cultivators would be expected to maximize
yield per unit area (cultivated plots) rather than unit of time, as expected for
hunter–gatherers (also Bar-Yosef, 1998). Fuller (2007a) proposes that multiple
harvests over time of a single crop, which would increase total yields from
a crop that matured unevenly, would lead to the latest harvests favouring
domesticates, even if sickles were not used. Variation between households in
terms of whether first or last harvests were stored for sowing could create
very weak selection at the community level for domestic morphotypes from
those late harvests.
Another emerging issue is whether full cereal domestication (fixation of
tough-eared mutants) took place first outside the area of the wild progenitors
and earliest cultivation. While the predominance of domesticated type barley
on most Near Eastern sites may have waited until ca. 7500–7000 BC, by this
period crops had dispersed towards Europe, reaching mainland Greece and
Crete by ca. 7000 BC (see Colledge et al., 2004, 2005), where fully domesticated
246 Fruit Development and Seed Dispersal
forms dominate. Even earlier by 8000 BC, cereals had been transferred to
Cyprus, where domesticated chaff remains also dominate (although assemblages are very small) (Colledge, 2004). This may suggest that local bottleneck
effects when crops were carried away from their centres of origin sped up domestication within the translocated population. The recent genetic diversity
study of einkorn wheat indicates that early domestics retained high levels of
genetic diversity (Kilian et al., 2007), and this is to be expected where proximity allowed continued introgression between cultivated and free-growing
populations, especially since the domestication that differentiated them was
slow to evolve. By contrast, major genetic diversity bottlenecks can be expected with dispersal events beyond the wild range when farming spread to
new regions, such as Cyprus or Europe.
It must also be kept in mind that in centres of origin, because there remained wild populations, natural selection for wild-type adaptations continued alongside artificial selection amongst cultivars. The invasion of crop
fields of weedy, wild-types, as well as the abandonment of old fields, would
have provided contexts that favoured persistence of the wild, shattering morphotype. This could have been further reinforced by cross-pollination with
wild populations. All of this would have bolstered the wild-adapted genetic diversity amongst early crops, which may have provided degrees of
resistance to the ‘artificial’ selection of cultivated populations (Allaby, 2008;
Allaby et al., 2008). Those crops which were dispersed in small founding
populations to Cyprus, Crete and Greece would have been removed from
conflicting selection for wild-type adaptations.
7.3
Non-shattering in other cereals: rice, pearl
millet and maize
No other cereals are as well documented archaeologically as einkorn wheat
and barley, although there are growing data sets for rice (Oryza sativa), pearl
millet (Pennisetum glaucum) and maize (Zea mays). For most crops early archaeobotanical evidence documents use. Meanwhile, domestication is inferred by other traits, such as grain size (see below) or else from associated
archaeological context or changes in distribution that suggest dispersal outside of the wild habitat. For example in Sorghum bicolor, early Holocene finds
in the Western Desert of Egypt at Nabta Playa indicate that wild-type shattering spikelets were harvested together with other wild grasses by ca. 7500 BC
(Wasylikowa et al., 1995, 1997, 2001), as also in central Sudan by ca. 4000 BC
(Magid, 1989, 2003; Stemler, 1990). A single possible non-shattering specimen
is reported from the Sudan (Stemler, 1990). Subsequent evidence for sorghum
comes from grains that appear domesticated in size and shape that had been
translocated from Africa to India around 2000 BC (Fuller, 2003). But there
remains no data from which to infer when selection for the domesticated
Seed Dispersal and Crop Domestication 247
forms began or ended. Some have hypothesized that domesticated forms
first appeared outside Africa in South Asia aided by the separation from wild
populations (Haaland, 1999), although the archaeobotanical record in eastern
Africa remains so depauperate during the period between 4000 BC and 1000
BC that this hypothesis cannot yet be tested.
Rice shattering is controlled by abscission layers where the spikelet attaches to the rachilla (Li et al., 2006) and this can be studied archaeologically
from the spikelet base which preserves the scar (Thompson, 1996, 1997; Zheng
et al., 2007; Fuller and Qin, 2008). These spikelet bases are very small and until
recent changes in how archaeological sites were sampled for plant remains,
they were not recovered from early sites in either China or India where rice
domestication events have been postulated. It is now clear that these can preserve in quantity, and current research programmes in the Yangtze valley are
quantifying the proportions of wild, domesticated and potentially immature
harvested spikelet base types (Fig. 7.4). Work by the author and others will
Figure 7.4 Archaeological remains of rice spikelet bases that allow the distinction
between wild and domesticated types. At left are the drawings of three spikelet base
types from the archaeological sites of Caoxieshan, Jiangsu, China ca. 4000 bc (after Fuller
and Qin, 2008), showing domesticated, non-shattering scar (top), smooth scar of
shattering wild mature type (middle), and protruding scar of probable immature type
(bottom). At right are the scanning electron micrographs of archaeological spikelet bases
from Neolithic Tian Luo Shan, ca. 4700 bc, Zhejiang Province China (see Fuller et al.,
2009): at top right is domesticated type and at lower right is wild-type. Reproduced with
permission from Antiquity Publications Ltd.
248 Fruit Development and Seed Dispersal
Figure 7.5 Diagram of differences between a domesticated (top) and wild (bottom)
spike of pearl millet (Pennisetum glaucum). In domesticated type, non-shattering
involucres are born on a stalk, and often include more than one grain, whereas in wild
pearl millet sessile spikelets, normally one-grained, are shed by dehiscence (based on
Poncet et al., 2000; Fuller et al., 2007b). Images provided by University of Groningen,
Groningen Institute of Archaeology.
soon provide some quantitative results from which to estimate how quickly
non-shattering rice evolved and when domestication was completed, but current estimates suggest this process began sometime before 6000 BC and was
completed by ca. 4000 BC (cf. Zheng et al., 2007; Fuller et al., 2007a; Fuller and
Qin, 2008; Fuller et al., 2009).
Pennisetum glaucum, pearl millet, is the only African cereal for which existing archaeobotanical evidence provides some indicators of the domestication
process, but this is still limited and hampered by an absence of data sets of
ancient wild-type pearl millet prior to the start of domestication. The involucres, which contain spikelets and bristles, change from being sessile and shed
when mature to being non-shedding and stalked in the domesticated form
(Fig. 7.5; also, Brunken et al., 1977; Poncet et al., 2000; D’Andrea et al., 2001;
Zach and Klee, 2003; Fuller et al., 2007b). Evidence for the early occurrence
of domesticated, stalked involucres comes from impressions in ceramics of
pearl millet chaff that had been mixed with clay during pottery production
(Amblard and Pernes, 1989; MacDonald et al., 2003; Klee et al., 2004; Fuller
et al., 2007b). These impressions can preserve the threshed involucre stalks
(Fig. 7.6), of which the earliest are now from 2500 BC to 2200 BC at
Karkarichinkat (unpublished data of Fuller and K. Manning; cf. Finucane
Seed Dispersal and Crop Domestication 249
Figure 7.6 Examples of archaeological pearl millet remains of domesticated type. At
left is a cast (in polyvinylsiloxane) of an impression of pearl millet chaff used to temper
pottery from Neolithic Djiganyai Mauretania (1500–1700 bc) (after MacDonald et al.,
2003; Fuller et al., 2007b); at right is an image of charred macro-remains of pearl millet
involcure from Cubalel, Senegal (ca. ad 500) (after Murray et al., 2007). Images provided
by University of Groningen, Groningen Institute of Archaeology.
et al., 2008). Chaff can also sometimes be preserved carbonized although we
still lack very early assemblages (Fig. 7.6; cf. Murray et al., 2007).
The most important cereal domesticate in the New World was maize which
also differs from its wild progenitor in terms of being non-shattering. While
the small alternating involucres of wild teosinte ears (Zea mexicana) shatter
at maturity, the cobs of maize do not and grains must be forcibly removed
from their cupules (Iltis, 2000). The presence of this trait is apparent from
the earliest preserved maize cobs from dry caves in southern Mexico that
date back about 6200–6300 years (Benz, 2001; Long and Fritz, 2001; Piperno
and Flannery, 2001; Smith, 2001). However, the beginnings of cultivation is
inferred to be much earlier based on evidence from phytoliths and starch
grains, including evidence that maize had dispersed already towards South
America before this time, ca. 7000 BC (Dickau et al., 2007). The beginnings
of cultivation remain obscure and there is no significant early archaeological
record for wild teosinte use, or how quickly this was transformed into the
small non-shattering cobs of maize.
7.4 The genetics of non-shattering cereals
Breeding experiments have long shown that the genetic control of seed shattering is simple in that the trait is usually governed by a single locus as
evidenced by simple Mendelian inheritance ratios of brittle and tough rachis
phenotypes. The tough rachis alleles have been found to be loss of function
250 Fruit Development and Seed Dispersal
genes that are recessive. The synteny of the grass genomes and initial quantitative trait loci analyses led to the initial supposition that the same genes
might be responsible in the different grass lineages in a neat example of
evolutionary convergence (Paterson et al., 1995). While this was a reasonable
hypothesis given the evidence at the time, the picture has subsequently developed into something more complex. It now appears to be the case that
different grass lineages have had different genes modified to produce the
loss of seed shattering (Li and Gill, 2006). The number of genes responsible
that have been characterized by DNA sequence still remains low, with rice
leading the way.
Two different genes have been identified in rice, qSH1 (Konishi et al., 2006)
and sh4 (Li et al., 2006), which carry mutations leading to the non-shattering
phenotype. The qSH1 gene codes for a homeodomain protein highly similar
to REPLUMLESS (RPL) in Arabidopsis that is responsible for down-regulating
two other homeodomain proteins (SHP1 and SHP2) involved in developing
a dehiscent zone in silique maturation (Roeder et al., 2003). It seems likely
that the qSH1 is also involved in an interaction between MADS-box homeodomain genes in dehiscence regulation, although it should be noted that the
dehiscence zones between the two plants are not homologous and the SHPs
of Arabidopsis have no known orthologues in rice. In this case, the change
of function at the qSH1 gene is associated with just one single nucleotide
polymorphism (SNP), although the mechanism of action is as yet unclear.
The second gene identified in rice to produce a non-shattering phenotype
sh4 is different to qSH1 and has only low levels of similarity to genes found
in Arabidopsis, or elsewhere in the rice genome. It has a Myb3 DNA binding domain, which suggests it is a transcription factor. Again a single SNP,
leading to a single conserved amino acid change, results in the change in
function, which appears to result in either the incomplete formation of the
abscission zone (Li et al., 2006), or the failure to initiate cell degradation (Lin
et al., 2007). In this case, these two studies have found allelic variations of
the sh4 gene, suggesting an allele of some antiquity and perhaps with interesting phylogeography. In the case of rice then, two independent genetic
pathways to non-shattering have occurred. Haplotype analysis including one
of these, qSH1, suggests that the non-shattering phenotype came after other
mutations associated with an increase in grain size and the waxy phenotype
(Shomura et al., 2008), supporting the idea that the mutation arose in the ‘domesticated’ population of rice. Interestingly, although the sh4 non-shattering
genotype was found in the wild progenitor Oryza nivara, this was thought
to be due to an introgression from domesticated rice, as the alleles that were
most closely related to the non-shattering type in the wild were found in
O. rufipogon rather than O. nivara. Since O. rufipogon is generally regarded as
the ancestor of domesticated japonica rices in East Asia, while O. nivara has
closer affinities in general with indica cultivars (Cheng et al., 2003; Fuller, 2006;
cf. Sweeney and McCouch, 2007; Vaughan et al., 2008), this evidence implies
that sh4 evolved during japonica rice domestication, and entered indica rice
Seed Dispersal and Crop Domestication 251
through a more complex process involving hybridization between lineages
(Sang and Ge, 2007). Two alternative hypotheses exist: either there were high
levels of introgression from wild South Asian rices as domesticates spread
from a single origin in the Yangtze valley, the ‘snowball model’ (Sang and
Ge, 2007; Vaughan et al., 2008), or else there were separate origins of cultivation and subsequent hybridization of cultivars, the ‘combination model’
(Sang and Ge, 2007; preferred by Kovach et al., 2007; and consistent with the
archaeobotany of South Asia, cf. Fuller, 2006). Similarly the mutation for a
white pericarp evolved once in early japonica and was introgressed into South
Asian rices (Kovach et al., 2007; Sweeney and McCouch, 2007; Sweeney et al.,
2007; Vaughan et al., 2008).
In barley, two closely linked loci btr1 and btr2 have long been implicated in
tough rachis formation on two independent occasions in the evolution of domesticated varieties (Takahashi, 1955). While these two genes have yet to have
their sequences characterized, sequence analysis of closely linked biomarkers found through amplified fragment length polymorphism (AFLP) have
supported this suggestion strongly by clearly showing two clades of brittle
rachis origin for the two respective loci (Azhaguvel and Komatsuda, 2007).
Based on mapping positions, it seems unlikely that the two Btr loci in barley
are orthologous to the Br1 locus responsible for tough rachis in lower wheats
(Li and Gill, 2006). Two loci have been identified in wheat to confer tough
rachis formation in different types of disarticulation, W (wedge type) and B
(barrel type), respectively. The W-type disarticulation occurs in the A, B, S, G
and T genomes and is governed by Br1 located on the short arm of chromosome 3. Einkorn, emmer and Iranian spelt wheats have this disarticulation
type, for instance. The B-type shattering originates from A. tauschii and is
found on the long arm of chromosome 3D, and gives rise to the shattering
found in European spelt. Comparison with QTLs derived from maize also
suggests that these loci are not orthologous between maize, rice and wheat
(Li and Gill, 2006). It should be noted that a number of other loci have been
identified to be involved with rachis fragility (Janatasuriyarat et al., 2004),
through the pleiotropic action of glume tenacity (Tg) on chromosome 2D,
and the free threshing gene Q on chromosome 5A. Interestingly, the Q gene
has been characterized by sequence, and found to be similar to APETALA 2
(AP2) of Arabidopsis, an important transcription factor in floral development
(Simons et al., 2006). What makes the Q gene especially interesting is that
the free threshing allele, q, is a gain of function mutation. A single amino
acid change from Q to q has resulted in the ability of the protein to form
homodimers, which has had consequences on its transcription regulation
activity.
There is little information on the remaining principal panicoid grasses
maize, sorghum and Pennisetum. A discrete shattering locus was identified
through QTL in sorghum (Paterson et al., 1995), which was syntenic to a high
scoring region for the trait in maize, which also had further seven regions
associated with shattering. Pennisetum is thought to have oligenic control of
252 Fruit Development and Seed Dispersal
shattering in a tightly linked cluster (Poncet et al., 1998, 2000), but further
characterization has not yet been published.
Finally, another crop in which tough rachis loci have been identified is
buckwheat (Matsui et al., 2003, 2004). In this case, two independent loci have
been identified (Sht1 and Sht2), which are not closely linked but both can
confer the non-brittle phenotype independently. The sht1 allele that confers
the first non-brittle phenotype is fixed within the cultivated population, but
the sht2 is not. On this basis, the authors argue that the sht2 mutant may have
occurred after the crop was domesticated and has not been subject to strong
selection. Further phylogeographic evidence will help to elucidate this story.
7.5
Reduction in seed dispersal aids
Accompanying the loss of natural seed dispersal was the reduction of appendages that aid dispersal. De Candolle (1885, p. 460) summarized this as
changes in the ‘form, size, or pubescence of the floral organs which persist
round the fruits or seeds.’ Plants, and especially grasses, have a range of
structures that aid seed dispersal, including hairs, barbs, awns and even the
general shape of the spikelet in grasses. Thus, domesticated wheat spikelets
are less hairy, have shorter or no awns and are plump, whereas in the wild,
they are heavily haired, barbed and aerodynamic in shape. All of these tend
to be greatly reduced in the domesticated form. While this is connected to
the loss of shattering, we expect it to have evolved by a different process
(Fuller, 2007a). Instead of being positively selected for by human activities,
as the tough rachis was, this probably came about by the removal of natural selection for effective dispersal. The recent study by Elbaum et al. (2007),
demonstrated how the awns in wild wheat function mechanically to help the
spikelet work its way into the soil by daily cycles of humidity. Dispersal by
wind and by sticking to animal fur may be co-selected (see Schurr et al., this
volume), and the wild progenitors of several cereals include bristly diaspore
units for such dispersal, such as in Setaria spp. and Pennisetum glaucum. Once
natural selection was removed to maintain such dispersal aids, smaller and
fewer appendages may have developed by genetic drift, in which case we
would expect to find a great deal of diversity in early cultivars. Certainly, there
remains a great deal of variation in this regard: some cultivated rices have
awns while others do not; there are ‘bearded’ and ‘unbearded’ wheats. However, it may also be the case that selection operated by reducing metabolic
‘expenditure’ creating a parallel trend towards less barbed and hairy cereal
spikelets, which can be observed across species.
Unfortunately, there is little archaeological evidence on this evolutionary
trend, as hairs and awns survive poorly in the archaeological record. Some
remains of early rice from China have been examined in this regard (e.g.
Sato, 2002; Tang et al., 1996), and the reduction of the number of spikelets
with awns, the density of hairs on the awns, and the length of those hairs can
Seed Dispersal and Crop Domestication 253
Figure 7.7 Comparison of awn hair (bristle) density and bristle length on wild and
domesticated rice awns, together with a few archaeological specimens from Hemudu,
Zhejiang Province China, ca. 4800 bc (after Tang et al., 1996).
potentially be studied (Fig. 7.7). Evidence for variation in both the number
of unicellular trichomes (bristles) on awns and the length of these trichomes
suggests that shorter trichomes are typical of domesticated rices that have
awns at all (Fig. 7.7), and indeed many domesticated rices have lost their awns
altogether. Evidences from four archaeological rice awns examined from the
site of Hemudu (5000–4500 BC) place these amongst the wild scatter (Tang
et al., 1996), a situation in agreement with arguments from grain size data
from the region (Fuller et al., 2007a), and more recent evidences from spikelet
bases (Zheng et al., 2007; Fuller and Qin, 2008; Fuller et al., 2009) that indicate
populations of rice from the Lower Yangtze of that period were dominated
with wild-type morphological adaptations. To date, too few samples of archaeological rice awns have been studied for any temporal trends in such
evidence; nor has comparable data from other taxa been examined.
A related trait is the shift from single-grained wild dispersal units to the
multiplication of grains under domestication. The best studied example is
that of barley, in which wild Hordeum spp. normally have a single grain with
two lateral sterile florets that contribute to an overall aerodynamic shape of
the diaspore. In domesticated barley, six-row varieties have evolved by the
254 Fruit Development and Seed Dispersal
removal of inhibition of lateral florets. This not only led to production of
more grains (by ca. 150%) per year, but it also created difficult-to-disperse
grouped triplets of spikelets (Harlan, 1992, p. 120; Zohary and Hopf, 2000,
p. 60). Genetic studies indicate that the six-row condition evolved three times,
by three distinct mutations, across different parts of Eurasia (Komatsuda et al.,
2007). Archaeobotanically, this trait can be inferred from the form of grains as
well as the form of well-preserved rachis segments. Such evidence indicates
that this trait evolved very early indeed. Asymmetrical grains, typical of
six-row forms, and rachis segments with widened apices are reported in the
Near East from the Early PPNB (8800–8000 BC) (Zohary and Hopf, 2000, p. 68),
prior even to the fixation of non-shattering rachises (see discussion above).
Similarly, the earliest barley remains from Pakistan at Mehrgarh, ca. 7000
BC, include evidence for six-row forms (Costantini, 1983). Possible parallel
trends are indicated for the New World little barley (Hordeum pussilum),
for which some twisted grains, and possible naked–grained varities have
been reported, but remains debated (cf. Bohrer, 1984; Asch and Asch, 1985,
p. 194; Hunter, 1992). This species has long been argued to be an indigenous
cultivar in prehistoric North America on the basis of finds of large quantities,
mainly from the First Millennia BC and AD (Asch and Asch, 1985, pp. 191–195;
Dunne and Green, 1998). Such evidences require confirmation and further
documentation, but it would imply domestication in terms of being released
from the need to maintain wild dispersal aids.
A similar development occurred with the domestication of pearl millet
(Pennisetum glaucum). Wild Pannisetum, normally has a single grain in each
bristly involcure, while domesticated forms often have multiples grains.
The study by Godbole (1925) of Indian peal millet suggests ∼70% of involucres include two spikelets (each with a grain), while ∼20% are single
grained. The other ∼10% includes more than two grains, with as many as
nine grains reported from a single involucre. Archaeologically, early impressions of pearl millet preserved in pottery, indicate not only the presence of
the non-shattering stalked forms, but also the presence of paired spikelets
indicating that this trait had evolved in cultivated populations certainly by
ca. 1700 BC (see Fuller et al., 2007b).
7.6
Non-cereal alternative: appendage hypermorphy
in fibre crops
In the case of at least a few fibre crops, selection under cultivation has favoured
increases in appendage size, as human selection has worked on what were
adaptations for dispersals and caused exaptation for fibre production. This is
most clear in the cases of cottons, in which four domesticated species are cultivated for seed coat hairs, which are extensions of testa cells. In the wild, such
hairs may aid dispersal by wind or attachment to animal fur (see Ridley, 1930,
Seed Dispersal and Crop Domestication 255
p. 158; Fryxell, 1979, pp. 142–143; Hovav et al., 2008), but in wild tetraploid
cottons domesticated in the New World, lint seems to have been exapted to
dispersal by water to littoral habitats (Fryxell, 1979, pp. 143–147, 164–165),
and oceanic drift is hypothesized to have brought A-genome cotton from
Africa to America (Phillips, 1976). In domesticated cottons, however, hairs
have become so heavy, long and tangled as to preclude such dispersal methods. In addition, domesticates have lost the hard impermeable seed coats
which allowed survival in salt water. Early cultivators seem to have chosen
those wild Gossypium species with the longest hairs, but it is also true that
all cultivated cottons have significantly longer hairs than their wild relatives
indicating selection. Hutchinson (1970, p. 271) reported an apparently spontaneous single gene mutation controlling this in wild G. barbadense. Fryxell
(1979, p. 173) argues that selection for increased lint probably preceded selection for increased fruit size, at least in domesticated G. hirsutum. Unlike
the loss of wild-type seed dispersal which is regarded as having evolved
from unconscious selection on the part of farmers, we might expect hair enlargement to have been intentional. As such, conscious selection might be
expected to exert a stronger selection pressure on genes involved in seed coat
hair formation than that typical of most domestication traits.
Another example comes from the Devil’s claw (Proboscidea parviflora), which
has also been cultivated for its fibres in the American Southwest since prehistoric times (Nabhan et al., 1981; Bretting, 1982, 1986; Nabhan and Rea, 1987).
The claws of this species represent extensions of seed capsule apices (rostra).
These apical claws bend such that they can serve as hooks to cling to animal
hair for long-distance dispersal. Human use of this species involves softening
and pounding of capsules to separate the fibres that make up the capsule.
These are used to make cords and basketry type products. It is suggested
that it has only been cultivated in recent centuries, and the earliest finds are
ca. AD 1150 (Nabhan and Rea, 1987, pp. 59–60). The enlarged capsules and
much longer claws of domesticated forms provide for more extensive fibres.
This is therefore also likely to have been a product of conscious selection. In
addition, domesticated devil’s claw has evolved white seeds, rather than the
black seeds of the wild form, probably indicative of typical domesticate-type
loss of germination inhibition (see below).
7.7 Loss of natural seed dispersal in pulses
and other crops
Other seed crops have also evolved non-dispersing fruit types with domestication, although these remain largely undocumented archaeologically. Members of the Fabaceae have been domesticated in parallel in most world regions
which had early cereal domestications (Harris, 1981, 2004; Smartt, 1990).
Natural seed dispersal in wild legumes, including the wild progenitors of
256 Fruit Development and Seed Dispersal
domesticated pulses, is normally by pod dehiscence. That is, seeds are physically shed by pods that twisted and split as they dried after maturity. In
domesticated species, this is removed or delayed (see Fig. 7.1), although various observations suggest that the degrees of reduction in this trait vary across
taxa (e.g. Fuller and Harvey, 2006, p. 223, for South Asian species). In contexts
where pulse pods are preserved, such as by desert conditions, it may be possible to determine the presence of this domestication trait by examination of
the pod layering: the inner layer that causes dehiscence should be reduced.
Pods of Phaeseolus lunatus and P. vulgaris from Guitarerro Cave in Peru show
that this non-shattering trait was present (Kaplan et al., 1973), although these
may be intrusive finds in deposits attributed to ca. 8000 BC (cf. Lynch et al.,
1985), since direct dates on P. lunatus and P. vulgaris seeds go back to 3500
and 2300 years ago, respectively (Fritz, 1994, p. 307; Kaplan, 2000). Within
some pulses, genetic loci involved in non-deshicent pod formation have been
identified, such as Dpo1 and Dpo2 in Pisum (Weeden et al., 2002; Weeden,
2007), and the different loci v and p were selected in common bean, Phaseolus
vulgaris (Koinange et al., 1996). Interestingly, by contrast to non-shattering in
cereals, this trait appears to be controlled by more than one locus in some of
the above studied Fabaceae domesticates (Phaseolus spp., Pisum). This presumably accounts for the degrees of pod dehiscence reported from some
species and may suggest that this was a less central part of the early domestication syndrome in many pulses than it was in cereals. Nevertheless, in
other pulse species, there appears to be one key gene mutation involved in
non-shattering. Such evidence comes from Lens (Ladizinsky, 1979), and from
azuki bean, Vigna angularis (Kaga et al., 2008). In these species, this trait is
thus comparable to the cereal rachis in that respect, especially with regards to
processes of selection on a population level. As argued by Ladizinsky (1987,
1993), pulse domestication may be fundamentally different from cereal domestication, contradicting Zohary and Hopf (1973; Zohary, 1989), in that loss
of germination inhibition may have been the key and prerequisite trait that
made early cultivation efficient.
Some other seed crops show parallel trends towards non-dehiscent morphologies, such as flax (Linum usitatissimum) which has non-shattering capsules in the domesticated state (Zohary and Hopf, 2000, p. 123). Early evidence suggesting domesticated flax comes from the Near East from fragments
of probable capsules at Pre-Pottery Neolithic Jericho (8400–7500 BC) and
larger than wild seeds at Tell Ramad (7500–6500 BC) (Zohary and Hopf, 2000,
p. 130). On the other hand, a few crop species appear to not have evolved
this, perhaps due to differences in the genetic architecture of this trait. Thus,
in sesame (Sesamum indicum), for example, capsules still dehisce in most domesticated forms, and this constitutes a persistent issue for plant breeders
(Day, 2000; Fuller, 2003). In this case, non-dehiscent forms produce much
lower yields and are unattractive. Because pods and capsules tend to be
light, and are therefore unlikely to survive contact with fire, they are exceedingly rare in archaeological contexts. It is therefore the case that we have little
Seed Dispersal and Crop Domestication 257
direct archaeological evidence on the evolution of these traits in pulses or
oilseeds.
7.8 Germination traits in domestication: the importance
of loss of dormancy
In the wild, many seeds will only germinate after certain conditions have
passed, such as conditions of day length, temperature, or after the seed coat
is physically damaged. Crops tend to germinate as soon as they are wet and
planted. This is selected for simply by cultivation, and sowing from harvested
yield, as those seeds that do not readily germinate will not contribute to the
harvest. As such, the selective forces and mechanisms involved are expected
to differ from those involved in the loss of wild-type seed dispersal.
Germination differences between crops and their wild progenitors come
in a range of severity. The study of changes in dormancy with domestication
is complicated in many crops; this is due to limited morphological visibility
of dormancy-related traits, and limited knowledge of the factors that govern
dormancy.
Dormancy and germination are traits that are controlled in a highly complex manner involving one or a combination of morphology, physiology and
physical structures (Baskin and Baskin, 2001; Finch-Savage and LeubnerMetzger, 2006). Not least of the complications of dormancy is its definition.
Dormancy can be described as a block to germination, which is to say that
a non-germinating seed may not be dormant, but merely awaiting induction
of germination. Finch-Savage and Leubner-Metzger (2006) define dormancy
classes by distinguishing morphological, physiological deep, physiological
non-deep and physical dormancy. Morphological dormancy refers to seeds
that have an underdeveloped embryo and require time to grow and germinate. Physiological dormancy, the most prevalent form of dormancy, appears
to broadly involve abscissic acid (ABA) and gibberellins (GA) metabolism.
Physical dormancy (coat dormancy) involves the development of a waterimpermeable seed coat, and is typically broken by scarification. Such physical dormancy is typical of the wild progenitors of cultivated legumes, and is
one of the key traits that has been modified with domestication (Zohary
and Hopf, 1973, 2000, p. 93; Ladizinsky, 1987; Plitman and Kislev, 1989;
Kaplan, 2000). It is interesting to note that morphological dormancy is more
typical of the less-derived flowering plants; physiological dormancy is found
throughout flowering plants (and gymnosperms), while physical dormancy
occurs amongst the most derived families, most notably the Fabaceae (see
Finch-Savage and Leubner-Metzger, 2006).
In crops from several dicotyledonous families, dormancy traits can be seen
in the seed coat. In particular, wild-type seeds tend to have thicker seed coats,
often of a different colour (black or dark brown, or mottled) and often with
258 Fruit Development and Seed Dispersal
Figure 7.8 Comparisons between wild and domesticated seeds, showing seed coat
colour, surface texture and thickness differences with domestication. At left are wild and
domesticated Sesamum indicum, wild above and domesticated below; at right are wild
and domesticated Chenopodium album, wild above and domesticated below. Seeds from
Institute of Archaeology, UCL collections: Seasmum malabaricum from coastal sanddune,
Sindhudurg district, Maharashtra, India (coll. D Fuller 9/2004); Domesticated S, indicum
black variety from Pune (8/2000); white S. indicum from India PI164384 01 SD;
Chenopodium album, wild from European seed reference collection, Institute of
Archaeology, UCL; Chenopodium album, domesticated, collected by E. Takei from the
Rukai tribe, Taiwan (5/2007) (sample in UCL, courtesy of E. Takei).
additional surface ornamentations. Domestication has resulted in the thinning of seed coats, the lightening of seed coat colour and the loss of rugae or
papillae. Such traits have evolved in parallel across families and genera, and
world regions. For illustration, examples of modern wild and domesticated
seed pairs are shown from Sesamum indicum and Chenopodium album (Fig. 7.8).
Pigmented seed coats (or pericarps), which have long been associated with
functional dormancy in wheats (Flintham and Humphry, 1993), may also be
linked to dormancy in wild rice, which has evolved white pericarps only
once after domestication (Sweeney et al., 2006, 2007). Nevertheless, it is also
the case that physical changes are not always evident from visible morphology. Morphological indicators of pericarp colour change are not detectable
in the charred grains recovered by archaeologists. Even in other families,
this may prove difficult to document archaeologically. In Near Eastern pulse
crops, for example Butler (1989, 1990) was able to document clear morphological differences in the seed coats of wild and domesticated peas, but not
of lentils, chickpeas or Vicia spp., where morphological variation falls along
a spectrum from thicker (and sometimes ornamented) seed coats in wild
populations and some cultivars, to thinner, smooth forms in other cultivars.
This physical spectrum may relate to a functional spectrum in germination
Seed Dispersal and Crop Domestication 259
inhibition. Weeden (2007), for example, has documented a spectrum of variation in germination between wild Pisum sativum subsp. elatius, with virtually
no immediate germination within 1 year of seed formation, Pisum abyssinicum
(the Ethiopian pea), which shows partial breakdown of germination inhibition (seeds germinate in 3–12 months), and modern Pisum sativum subsp.
sativum which readily germinates (cf. Weeden, 2007). A wide range of germination rates is reported from Lablab purpureus, but with significantly higher
proportions of faster germination in cultivated populations (Maass, 2005). A
wide range of variation is especially noted amongst wild accessions of Lablab,
which may suggest that domestication drew upon existing genetic variation
in this species.
Ladizinsky (1987) argued that the very low germination rates in wild
pulses, in particular Lens, would have precluded successful cultivation on
the basis of very low yields from planted seeds. He therefore suggested that
hunter–gatherers must have recognized favourable wild mutants with ready
germination from which to begin cultivation, that is there was a form of
‘pre-cultivation domestication’. This hypothesis, however, received critiques
(Zohary, 1989; Blumler, 1991). Ladizinsky’s (1987) argument for Lens cultivation contrasts to cereal cultivation in that he reasons that the domestication
syndrome phenotype of a lack of dormancy would have to arise in the wild
rather than the cultivated gene pool because cultivator pressures would not
have been sufficient to break dormancy. Ladizinsky argued that this is also
supported by genetic diversity data based on isozymes, which show different
cultivated groups of Lens appear to be most closely related to different wild
groups of Lens, indicating a multiple domesticated origin, despite a single
mutation responsible for dormancy breaking (Ladizinsky, 1987, 1993). He argued that the most parsimonious explanation is that such a mutant may have
been persisting in the wild. The ‘comparable’ tough rachis mutant in cereals
is postulated to have arisen in the cultivated population rather than the wild
where it has been believed that the tough rachis mutant would not persist.
Zohary (1989) argues that the lack-of-dormancy mutant also would not survive in the wild. More recently, Kerem et al. (2007) have suggested that even
low yields from wild-type pulses (in particular chickpea, Cicer arietinum) may
have been favoured because the presence of particular micronutrients (the
amino acid tryptophan) were the target of early pulse consumption rather
than overall protein or carbohydrate (also Abbo et al., 2007, on Pisum). The
extent to which any of these hypotheses might apply across pulse domestications from difference subfamilies and different regions is unclear. More
research is needed. So far, archaeobotanical evidence has contributed little to
the documentation of the earliest processes of pulse domestication and the
evolution of these domestication traits.
Evidence for the loss of germination inhibition may be preserved archaeologically, although detailed studies are only available for a few species. One
challenge is preservational: seed coats are often not preserved on charred
pulses. This is clearly the case with Indian Vigna spp., for example (Fuller
260 Fruit Development and Seed Dispersal
and Harvey, 2006). Those species which have been best documented are
New World Chenopodium domesticates (e.g. Smith, 1989, 1992, 2006bb; Bruno
and Whitehead, 2003; Bruno, 2006). In a classic case of the fossil record (archaeobotany) identifying an extinct crop, Smith (1989, 1992, 2006b) tracked
a marked decrease in seed coat thickness in Chenopodium berlanderii seeds
from sites in the Eastern Woodlands of the United States between ca. 2500
BC and 1500 BC. In addition to thinning seed coats, presumably linked to loss
of wild-type germination inhibition, seeds tended to change shape and size,
although wild-type forms persisted as weeds alongside the Chenopodium crop
(Gremillion, 1993). Bruno (2006) has developed a similar approach to studying South American Chenopodium domestication, although variation in seed
coat thickness amongst wild species makes this more difficult requiring the
use of additional size and shape characters. Although modern material suggests a similar change has occurred in Old World Chenopodium album, at least
amongst East Asian domesticated populations (see Fig. 7.8), archaeobotanical evidence tracking such changes has not been gathered. Given suggestions
that Chenopodium was formerly a crop of Iron Age Europe (Helbaek, 1954; cf.
Henriksen and Robinson, 1996, pp. 9–19; Stokes and Rowley-Conwy, 2002)
or of Bronze Age Gujarat, India (‘intential collection’ inferred by Weber, 1991,
p. 121), studies along these lines are warranted.
7.9
The genetic basis for dormancy and germination
A large number of genes may be directly or indirectly involved with dormancy. For instance, developmental genes can be expected to be involved
in morphological and physical dormancy, while abscissic acid (ABA) and
giberellic acid (GA) make up two of the most common plant hormones,
which are expected to involve numerous loci across the genome.
Some progress is being made with understanding the molecular basis of
dormancy with regards to non-deep physiological dormancy, typical of the
cereals. Physiological dormancy is largely governed by the ratio of ABA to
GA. When this ratio is high, dormancy prevails, and when GA levels become
high enough relative to ABA, then germination is initiated (White et al.,
2000; Kucera et al., 2005). Two other hormones also known to have roles are
ethylene and the brassinosteroids, both of which act similar to GA to promote
germination and counter the effects of ABA (Kucera et al., 2005).
Dormancy is a necessary part of seed development during which ABA
promotes maturation pathways that govern storage compound deposition
and dessication of the grain. GA synthesis is actively inhibited in maize
during this time (White and Rivin, 2000). It is thought that dormancy release
is due to ABA breakdown and this is the primary hormone. After breakdown,
the presence of GA in sufficient concentrations relative to ABA can promote
germination. This is supported by work with Avena fatua, which demonstrates
that GA is involved in dormancy loss (although it can be used to break
Seed Dispersal and Crop Domestication 261
dormancy in this case), but is involved in initiating germination (Fennimore
and Foley, 1998).
In cereals, QTL studies have been used to try and track down important
loci for dormancy. One gene of great significance is VP1 (McCarty et al., 1991).
VP1 is a transcription factor that promotes dormancy in the presence of ABA
(Cao et al., 2007). Mutations in this gene lead to a loss of function that results
in vivipary where seeds will germinate while still on the plant (also known
as preharvest sprouting). This gene has been identified in sorghum, wheat,
rice, barley and oats (Hattori et al., 1994; Jones et al., 1997; Bailey et al., 1999;
Carrari et al., 2003; Osa et al., 2003). In wheat, the incorrect assemblage of
exons (mis-splicing) of VP1 messenger RNAs is responsible for the nonfunctional types leading to vivipary (McKibbin et al., 2002). Interestingly,
these mutants in hexaploid wheat appeared to have been inherited from
their tetraploid ancestors, thus implying that they were established early on
in the development of agriculture. The VP1 gene is up-regulated by ABA,
and has the function of promoting dormancy (Cao et al., 2007). The functional
VP1 gene also activates an anthocyanin pathway resulting in pigmented seed
coats, which have long been associated with functional dormancy in wheats
(Flintham and Humphry, 1993). The VP1 and seed coat colour (R) genes
are loosely linked which may also partly explain the correlative effect to dormancy – efforts are being made to increase dormancy of white-grained wheats
(Kottearachchi et al., 2006). There are several other genomic regions, which
are important in dormancy, which have been identified by QTL analysis, but
these genes’ loci have yet to be identified (e.g. Wan et al., 2005; Vanhala and
Stam, 2006; Hori et al., 2007; Gao et al., 2008).
The physical dormancy imposed by seed coats is thought to be largely associated by ␤-1,3-glucans (callose) which are deposited in cell walls (the neck
regions of plasmodesmata) during maturation (Finch-Savage and LeubnerMetzger, 2006). Increased callose deposition is associated with increased dormancy in a number of species. The ␤-1,3-glucanases which break the callose
down are associated with the dormancy release. It is likely that mutations
in genes associated with these pathways are involved in the domestication
processes that are associated with weaker dormancy by seed coat thinning as
seen in pulses. This may also be true in other families of domesticates such as
Amaranthaceae, Chenopodiaceae and Pedaliaceae/Martyniaceae (Sesamum,
Proboscidea). In the case of lentil, a single dominant gene is reported to be related to the hard seed coat in non-germinating wild-types (Ladizinsky, 1985).
7.10
Germination and seedling competition: changes
in seed size
‘. . . we must conclude that man cultivated the cereals at an enormously remote
period, and that he formerly practiced some degree of selection, which in itself
is not improbable. We may, perhaps, further believe that, when wheat was first
262 Fruit Development and Seed Dispersal
cultivated the ears and grains increased quickly in size, in the same manner as the
roots of the wild carrot and parsnip are known to increase quickly in bulk under
cultivation.’
Charles Darwin (1883, p. 338)
Changes in size are one of the most widely commented on and obvious
differences between domesticated and wild varities (e.g. Darwin, 1883; De
Candolle, 1885, p. 460; Helbaek, 1960). While this is one trait that might be
suggested to be under conscious and intentional selection on the part of humans, what Darwin termed ‘methodical selection’, there remains no clear
evidence that this was the case in prehistory when seed sizes changed under
cultivation. Heiser (1990, p. 199) concluded that it is ‘more likely that large
seeds result from unconscious selection over a period of time,’ because it
was unlikely to be easy to select for as it is thought to be the product of the
interaction of many genes. In a recent comparative review, it was shown that
changes in seed size did not happen at a consistent rate or timing in relation
to the beginnings of cultivation or other domestication traits (Fuller, 2007a).
This suggests in turn that certain factors in cultivation regimes interact with
the inherent variability and genetic architecture of seed size traits within particular taxa in ways that are not uniform across taxa. Changes in size are not
qualitative traits of domesticates, like non-shattering is, or to a certain extent
that even ease of germination tends to be. Thus, it has been suggested that
the trait be regarded as ‘semi-domestication’ as it is a quantitative population
level trait that is selected at some stage during human cultivation but not
necessarily linked directly to key domestication traits. Seed size and other
such traits constitute a kind of soft selection in relation to the cultivated environment and probably a high degree of population variability built on a
multi-genic basis. In this regard, it is of interest to document the extent to
which grain-size increases precede hard-selected domestication traits, like
non-shattering or loss of germination inhibition, as seems to be the case in
wheat, barley and possibly rice; or whether size increase is later as appears
to be the case in pulses and Pennisetum glaucum (Fuller, 2007a). These differences may point towards the underlying selective pressures in the soil
environment.
The arable field has been called a ‘botanical battleground’ (Jones, 1988), and
this is true not only between crops, farmers and weeds but also within species
in the form of seedling competition. Well-tilled and cleared fields offer nutrients, abundant sunlight and normally plenty of water, and thus competition
should be expected to favour seeds that not only germinate rapidly but also
establish rapidly and even overtop competition. This tilled field competition,
including factors of both general disturbance and depth of burial, can be expected to select for larger seed size (Harlan et al., 1973; Harlan, 1992, p. 122;
Fuller, 2007a). As studies of weed seed ecology have shown, there is a variation between species in terms of ideal and tolerable depths of germination
(King, 1966, pp. 138–140), and this means that weed communities have been
Seed Dispersal and Crop Domestication 263
heavily influenced by human tillage practices that have established differing average depths of burial. This is indicated by studies within species and
between species that suggest a correlation between larger seeds and larger
seedlings (Krishnasamy and Seshu, 1989; Harlan, 1992, p. 122; Baskin and
Baskin, 2001, p. 214). Comparative ecology indicates that larger seeds generally have competitive advantages over smaller seeds under certain kinds
of competition including deeper burial (Maranon and Grubb, 1993; Westoby
et al., 1996; but there are some apparent exceptions amongst grasses (Baskin
and Baskin, 2001, pp. 212–213). Oka and Morishima (1971) showed in experimental cultivation of wild rice that some increase in average grain weight
could be measured within just five generations, in the cultivation of wild
perennial rice (O. rufipogon). An old agronomic rule of thumb is that seeds
germinate best at depths up to four times the diameter of the seed (King, 1966,
p. 140). Since archaeology mainly recovers the seeds of crops, archaeobotanical evidence lends itself to studies of variation and changes in sizes through
time. Nevertheless, caution is warranted in interpreting such evidence as domesticated crops often include a much greater range of grain size variation
than is found in wild species (Harlan et al., 1973; Vaughan et al., 2008).
While study of seed size is the most readily available domestication trait in
archaeological evidence, it is complicated by some confounding factors. Preserved seed size may be affected by the state of archaeological preservation:
most archaeological seeds are preserved carbonized, by exposure to fire, and
this has been shown to distort seed shape but especially to lead to shrinkage (e.g. Helbaek, 1970; Van Zeist and Bakker-Heeres, 1985; Lone et al., 1993;
Braadbaart et al., 2004). Nevertheless, if it is assumed that most archaeological
seeds have been affected in a similar manner, then real trends can be inferred
from the data. Experiments provide some general guidance on the probable
range of correction factors for comparing modern seeds, although the usual
10–20% shrinkage that is suggested is by no means a given. Another potential
problem is that past crops may have been harvested before all seeds were mature and immature seeds may resemble smaller versions of the more mature
seeds. For example, on the basis of growing experiments with a number of
pulses, Butler (1990) concluded that seed size could be misleading:
‘If harvesting is confined to one episode, the seeds constituting the crop are not all
in the same state of maturity. This may be reflected in their size; smaller, slightly
immature seeds may be present together with the full-sized ripe ones. Commonly,
it seems, the number of fruiting nodes per branch is two, which bear seeds at two
stages of maturity at any one time. If these are harvested together, the impression
may be formed that the seeds have been derived from two different populations or
even different taxa. This could lead to erroneous identifications such as the seeds
of a cultigen occurring together with those of its wild relative.’
E. A. Butler (1990, p. 350)
Similar concerns over the likelihood of immature harvesting of wild rice
and early rice crops were discussed by Fuller et al. (2007a; also Fuller, 2007a).
264 Fruit Development and Seed Dispersal
While such concerns make it dubious to identify single archaeological grains
as domestic or wild only on the basis of size, it nevertheless still appears
useful to examine the metrical traits of populations (site assemblages and
assemblages from across a region), as these appear to show real evolution
trends over time.
There is a growing morphometric database for wheat and barley from
the Near East (Colledge, 2001, 2004; Peltenberg et al., 2001; Willcox, 2004).
This indicates that wheat and barley grains increased in size starting in the
Pre-Pottery Neolithic A (PPNA) and earliest PPNB. This is before clear and
widespread evidence for tough rachises and loss of natural seed dispersal.
It is well known that wild and domesticated cereal grains differ in size and
this has been used to infer the domesticated status of cereals, already in the
PPNA and the earliest PPNB, including sites from the Jordan Valley, the upper
Euphrates in Syria, and the first settlements on Cyprus (Colledge, 2001, 2004).
This evolutionary shift can be illustrated from evidence from individual site
sequences, such as at Jerf el Ahmar (Willcox, 2004), in which a contrast is seen
between the barley grains from the early phase at Jerf el Ahmar (9500–8800
BC) and the later phase at Jerf el Ahmar, ca. 8500 BC (Fig. 7.9). The grains of
the later phase are comparable to those from the Chalcolithic Kosak Shimali
(ca. 5500 BC). If such data are plotted as means and standard deviations
against time, the long-term trend is clear (Fig. 7.10): an early increase in grain
thickness and breadth followed by a remarkable stable grain size from 6000
BC onwards.
Nevertheless, an explanation of these data remains controversial. We take
this to indicate evolution towards larger grain size during the occupation of this site (Fuller, 2007a; also, Nesbitt, 2004, p. 39), whereas Willcox
(2004), by contrast, queries whether this is not just a product of better
tended cultivars or the introduction of larger grained varieties from elsewhere (see also Willcox et al., 2008). This early change is indicated in seed
width and thickness, but not in seed length. While Willcox (2004) argues
that this does not fit with evolution of larger grains under cultivation, we
think that a comparative perspective indicates quite the opposite. As was
hypothesized by Harlan et al. (1973), grain size should increase as a product of soil disturbance and deeper burial with cultivation, and this has an
established observational and experimental basis in seed ecological studies (e.g. Krishnasamy and Seshu, 1989; Maranon and Grubb, 1993; Baskin
and Baskin, 2001, p. 214; see also experimental cultivation by Oka and
Morishima, 1971). However, rather than seeing this as a single directional
process, we must consider the likelihood that there were differing selective thresholds that acted on grain size (and multiple contributing genetic
loci) at different times. This is suggested by comparative examples, such
as West African pearl millet in which an initial grain thickening occurred,
but increase in grain size (mainly in length and, allometrically, in width)
only happened much later, in regions and periods with more intensive
agriculture.
Seed Dispersal and Crop Domestication 265
Figure 7.9 Scatter plots of archaeological grain measurements showing the increase in
grain size under early pre-domestication cultivation (after Willcox, 2004). (a) Barley grain
measurements, comparing early Pre-Pottery Neolithic A Jerf el Ahmar with the much later
domesticated material from Kosak Shimali. (b) Comparing early and late Jerf el Ahmar,
indicating that shift towards larger grain size had already occurred. (c) Similar comparison
of einkorn grains (probably including some rye grains) at early Jerf el Ahmar and Kosak
Shimali. (d) Trend towards larger grain sizes over the course of Jerf el Ahmar occupation.
In the case of pearl millet, we have some metrical data from West Africa
from which to examine grain size change during and after domestication,
with some comparative data from ancient India (Figs. 7.11 and 7.12). Data
sets for looking at morphometric traits of past African populations of pearl
millet have only been published recently, since 2000. As already noted, pearl
millet domestication is evident from ceramic impressions of pearl millet chaff
that include the stalk, which are present by ca. 2500 BC in northeast Mali (unpublished data), and 1700–1500 BC in Mauretania (Amblard and Pernes, 1989;
MacDonald et al., 2003; Fuller et al., 2007a), and slightly later in Nigeria (Klee
et al., 2000, 2004). Early grain assemblages of similar date show the subtle change in grain shape, becoming apically thicker and more club-shaped
266 Fruit Development and Seed Dispersal
Figure 7.10 Time series of archaeobotanical metrical data on charred barley grains.
Data plotted on the basis of a median age estimate for each site in calibrated radiocarbon
years. Lines indicate standard deviation and minimum and maximum outliers are also
indicated. Sites (in chronological order): Jerf Early, ZAD 2, Jerf Late, Djade, Ganj Dareh
(no thickness data), Ramad, Bouqras, Erbaba, Kosak Shamali, Selenkhiye, Hadidi, Rosh
Hiyat. Where standard deviations were not provided in published sources, these have
been estimated after the normal distribution following Pearson and Hartley (1976).
(D’Andrea et al., 2001; Zach and Klee, 2003). However, a major increase in
seed size appears delayed (D’Andrea et al., 2001, p. 346; Fuller, 2007a). Of note
is that early West African populations, from the second and first millennia
BC, have their averages firmly in the wild size range, although there are long
tails of variation that extend into the larger size range (e.g. at Birimi, Ghana).
Seed Dispersal and Crop Domestication 267
Figure 7.11 A map of archaeobotanical sites with important pearl millet data in Africa
in relation to probable West African domestication zones. Later ‘historical’ sites post-date
100 bc, and represent only a selection with metrical data used in Fig. 7.12 (Indian sites
not shown). Site numbers are as follows: 1. Dhar Tichitt sites; 2. Dhar Oualata sites; 3.
Djiganyai; 4. Winde Koroji; 5. Karkarichinkat; 6. Ti-n-Akof; 7. Oursi; 8. Birimi; 9.
Ganjigana; 10. Kursakata. Historical sites with pearl millet metrical data: 11. Arondo; 12.
Jarma; 13. Qasr Ibrim. (Primary data sources compiled in Fuller, 2007a.)
One of the earliest finds of pearl millet from India comes from Surkotada,
Gujarat, ca. 1700 BC, which can be seen to fall with these early domesticated African populations. By contrast, rather later seeds of a North Indian
(Gangetic) population from Narhan are markedly larger, suggesting selection
for larger grained pearl millet. On basis of Vigna pulse size increase in the
same horizon, it was suggested that selection for larger grains may be driven
by deeper seed burial through the use of ard tillage (Fuller and Harvey, 2006;
Fuller, 2007a). However, the continued small-grained populations in Early
Historic South India (Nevasa) suggests that there may be factors that work
against gigantism in pearl millet, and in the absence, reinforcing selection
populations may retain or even revert to smaller size ranges. In Africa, larger
grained populations appear only in the First Millennium AD, represented by
finds from Nubia and Libya, as well as Medieval Senegal.
This raises questions about the selection pressures involved in largegrained Pennisetum, and in seed crops generally. While initial cultivation
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Figure 7.12 Metrical data for archaeological pearl millet, and expectations from modern reference material. Clockwise from lower left:
Modern population averages for wild (W) and domesticated (D) pearl millet, showing population minima for domesticates and maxima for
wild, with all measurements reduced by 10% to account for expected shrinkage in charred specimens (data from Brunken et al., 1977 and
Zach and Klee, 2003); this division is indicated in other graphs by dashed box. Plots of archaeological site averages and ranges for early West
African sites (Birimi, 1700–1500 bc; Kursakata, 1500–800 bc), medieval Senegal at Arundo, and Qasr Ibrim, Nubia (preserved by dessication
and thus reduced by 10%); plots of early measurements from India (Surkotada, approximately 1700 bc) are close to wild or African Neolithic,
as are Early Historic (200 bc–ad 300) Nevasa in southern India. North Indian Narhan (1400–800 bc) shows a marked shift towards larger sizes
comparable with modern domesticates; plot of measured grains from Jarma in Southwest Libya may show an apparent shift towards somewhat
larger grains during the early first millennium CE, but Later Medieval Jarma has shifted back towards to near wild size range. (Primary
archaeological data sources compiled in Fuller, 2007a.)
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268 Fruit Development and Seed Dispersal
Seed Dispersal and Crop Domestication 269
may have selected for non-shattering, and slight changes in grain weight and
shape (the club shape), serious gigantism may have required a stronger selection pressure and therefore evolved later: a millennium or more later in India,
and two millennia later in Africa. As both Libya and South India lack wild
populations, this cannot be attributed to cross-pollination with wild-types.
There may be some constraints particular to this crop, as one experiment
indicates that optimal germination occurred under higher temperatures that
result in lower average grain weights (Mohamed et al., 1985). In addition,
pearl millet involucres are polymorphic in grain count with the vast majority
producing two grains, a large minority with one larger grain, and a further minority producing three to nine grains, which are necessarily smaller
(Godbole, 1925). Thus selection for higher grain counts, and more reliable
germination, might conflict with selection for larger seed sizes. Nevertheless,
as a working hypothesis, it is proposed that there is a deeper burial threshold
that selected for gigantism in pearl millet in some times and places (Fuller,
2007a). If so, then large-grained varieties evolved under plough systems and
then dispersed back to West Africa at a later date. In that regard, it might
be noted that the larger grain populations in Libya and Nubia, like that in
Gangetic India, are associated with more intensive plough cultures. This suggests separate events of grain enlargement in India and northeastern Africa.
Beyond informing us about pearl millet, this case provides useful comparison to other cases of plant domestication, including that in the Near East.
It suggests that we need to consider different aspects of the domestication
syndrome separately, even different aspects of grain shape and size change.
A lag between domestication and any appreciable seed size increase
appears to be the case in several tropical pulses, including Indian Vigna
(Fuller and Harvey, 2006; Fuller, 2007a), and West African Vigna unguiculata
(D’Andrea et al., 2007). This may suggest that a higher selective pressure was
needed to cross the threshold into big-seeded pulses; a threshold inferred
by Fuller and Harvey (2006) to be ploughing (ard tillage). Perhaps, a similar
effect created a lag time between initial grain thickening in cereals, associated with the earliest cultivation, and more marked grain size increase in all
dimensions, including length.
In Near Eastern lentils, size change appears to have been much slower
and more gradual than in the cereals, without a clear levelling off after the
Neolithic (Fig. 7.13). This may suggest an initially weaker selection, but may
also indicate that seed size is more plastic in pulses. The genetics of seed/grain
size is still poorly understood, but it is presumed to be under polygenic
control. This has been documented in Lens (Abbo et al., 1991) and Pisum
(Weeden, 2007).
In the case of rice domestication, the utility of grain measurements is hotly
debated (Thompson, 1996; Crawford and Shen, 1998; Fuller et al., 2007a; Liu
et al., 2007). As modern comparative data indicate, there is a vast range of metrical variation in domesticated rice (Fuller et al., 2007a; Vaughan et al., 2008),
and some of this variation seems to be correlated with climatic conditions
270 Fruit Development and Seed Dispersal
Figure 7.13 Time series of archaeobotanical metric data on charred lentil seeds. Data
plotted on the basis of a median age estimate for each site in calibrated radiocarbon
years. Lines indicate standard deviation and minimum and maximum outliers are also
indicated. Where standard deviations were not provided in published sources, these have
been estimated after the normal distribution following Pearson and Hartley (1976).
(Compiled from a large number of primary archaeobotanical reports by Jupe, 2003: From
left to right, sites include Qermez Dere, Murreybit, Jericho, Aswad, Jericho, Ganj Dareh,
Yiftah’el, Aswad, Ain Ghazel, Basta, Ramad, Ali Kosh, Ras Shamra, Jericho, Tepi Sabz, Beth
Shean, Jericho, Lachish, Arad, Tell Bazmosian, Jericho, Hadidi (some sites occur more than
once representing different phases))
such as altitude or latitude (Oka, 1988; Kitano et al., 1993): more northerly
temperate japonica landraces are short grained, while tropical varieties (the
javanica race rices) are massively long; in East Asia, upland rices tend to be
longer grained versus shorter grained lowland forms (Nitsuma, 1993). Such
problems are further compounded by variation in grain measurements that
may relate to maturity, especially as wild rice and early cultivars are likely
to have been harvested somewhat immature to increase total harvests and
because of uneven ripening (Fuller, 2007a; Fuller et al., 2007a). For this reason, it is probably safest to focus on changes through time within a fairly
restricted region, or even within individual stratigraphic sequences (Fuller
et al., 2008). On the left hand side of Fig. 7.14 is a time series of grain width data
from the Lower Yangtze region (Chinese provinces of Zhejiang and Jiangsu),
whereas on the left hand side later are the data from the Yellow River valley
further north where climatic conditions may have both selected for smaller
rice and reduced the reliability of harvests and yields (thus causing the incorporation of more immature or poorly formed grains). While the metrical data
vary between regions, within a particular region (the Lower Yangtze), often
postulated as a probable centre of domestication and trajectory of increasing
grain size is visible.
Changes in grain size have played an important role in documenting past
domestications in oilseed crops as well, including an extinct species form
North America. Achene size is an important domestication trait of the sunflower (Helianthus annus) and archaeological documentation of this indicates
domestication taking place by ca. 2000–1500 BC in North America (Asch and
Asch, 1985; Smith, 2006b; cf. Heiser, 2008). The most extensively documented
Seed Dispersal and Crop Domestication 271
Figure 7.14 Time series of archaeobotanical metrical data on charred rice grains. Data
plotted on the basis of a median age estimate for each site in calibrated radiocarbon
years. Lines indicate standard deviation and minimum and maximum outliers are also
indicated. Grey arrows indicate suggested selection trends with domestication; over the
same period, selection for non-shattering is indicated by spikelet base data. (Huang and
Zhang, 2000; Tang, 2003; Zheng et al., 2004; Liu et al., 2007; Tian Luo Shan: D. Fuller,
unpublished.)
increase in seed/fruit size in North America is that associated with marsheldar, Iva annua. Although this species is not known to have been cultivated
within historically documented periods, it was a major domesticate of the
eastern North America from ca. 2000 BC, alongside the native Chenopodium,
Hordeum pussilum and Helianthus annus. Indeed, it is the documentation of
potential morphological indicators of domestication traits related to germination that has allowed the reconstruction of indigenous cultivation in Eastern
North America (Smith, 1989, 1992, 2006b).
7.11
The genetics of seed size
The quality of seed size is a trait that is affected by many factors, and so can be
thought of as polygenically controlled. Moreover, the regulatory networks involved with governing seed size, either directly or indirectly, are not at all well
known. This is borne out by the many QTL analyses that have been carried
out which have shown seed size to be associated with many loci of varying
effect (Gupta et al., 2006). Again, it is rice that is leading the way to elucidation
of what these loci might be doing. At the time of writing, three genes derived
from principal QTLs have been identified in rice that directly influence grain
size (Fan et al., 2005; Song et al., 2007; Shomura et al., 2008). All three are loss
of function mutations. Two result in an increase in the number glume cells,
thereby giving the grain milk a larger cavity to fill, resulting in larger grains
which are wider (Song et al., 2007; Shomura et al., 2008). The first of these, GW2,
272 Fruit Development and Seed Dispersal
occurs on chromosome 2 and encodes an ubiquitin ligase that may possibly
be involved with negative regulation of the cell cycle. The larger grained phenotype is associated with an allele that has a mutation causing a premature
stop codon resulting in a non-functional truncated protein, which may result
in an inability to down-regulate cell division in the glume. The second, qSW5,
occurs on chromosome 5. In this case, the large grain phenotype is associated
with a large deletion in the gene, again resulting in more cells in the glume.
It remains to be seen whether these two loci are actually interacting with the
same process of grain development, probably at different stages. The third
locus, GS3, affects grain length and size rather than width (on which it has
a small effect). This gene occurs on chromosome 3 and encodes a transmembrane protein of unknown function. The protein normally has four domains:
a PEBP-like (phosphatidylethanolamine-binding protein) domain, a transmembrane region, TNFR/NGFR (tumour necrosis factor receptor/nerve
growth factor receptor), cysteine-rich domain and a VWFC (von Willerbrande
factor C) domain. The PEBP-like domain is partially deleted in proteins associated with longer and heavier grains. The authors assert that the gene could
be involved with regulating grain growth, which is to say they suppose this
might be a direct influence rather than the more indirect consequences on
grain size that glume cell number has in the previous two loci. These early
glimpses into grain size regulation confirm the expectations that grain size is
influenced by many factors that may only be indirectly concerned with grain
size itself, and part of as yet uncharacterized networks of interaction.
In the case of barley, which has QTLs affecting grain mass across all seven
chromosomes, the largest effect is linked to the Vrs-1 locus, which determines
the row architecture (Marquez-Cedillo et al., 2001; Komatsuda et al., 2007).
In this case, the genetic control of grain size is quite indirect. The grains
of two-row barley are fatter than those of six-row, most likely because they
have more space in which to develop. Similarly, wheat and maize have QTLs
associated with increasing grain mass on all chromosomes (Gupta et al., 2006),
and pleiotropic effects of loci being involved with both grain weight and
plant height are evident from recent studies (Maccaferri et al., 2008; Röder
et al., 2008). Undoubtedly, many of these will be tracked down to genes in the
coming years. Gupta et al. (2006) cite only one gene in wheat, three in barley
and two in maize to be involved with grain size. As with the elucidation
of rice outlined above, these are both directly and indirectly involved with
grain development. Examples of directly involved genes include the crinkly4
(Becraft et al., 1996) and mn1 (Carlson et al., 2000) in maize. The pseudoresponse regulator ppd1 in both wheat and barley is also associated with
grain size, but is likely to be an indirect effect through day-length sensitivity
altering the developmental time of grain maturation. The number of loci
governing seed size appears to be equally large in legumes as with cereals
with as many as ten QTLs governing the trait in peas (Blair et al., 2006), and
between three and nine QTLs in azuki bean (Kaga et al., 2008). Only four
Seed Dispersal and Crop Domestication 273
such QTLs were identified in chickpea (Cho et al., 2002), but very smallseededness has been shown to result from interaction of two recessive genes
(Upadhyaya et al., 2006). Again, very little is currently known about which
genes are responsible.
7.12
Seasonality controls: photoperiodicity and
vernalization
Another set of key changes with domestication are the controls over the seasonality of crop harvests and planting: photoperiodicity and vernalization.
In many plant species, the seasonality of flowering and hence of seed set is
controlled by environmental cues such as day length, thus species can be
divided into long-day and short-day plants. As discussed by Willcox (1992),
there tends to be an important difference between the crops domesticated in
the Near East and those of the Old World tropics, such as those of India or
the African savannas. The tropical crops tend to be grown in summer and
adapted to monsoon rainfall, flowering as days shorten after summer. By
contrast, those of the Near East were originally tied to winter rains. The importance of seasonality of cultivation and the changes in seasonality between
different regions has been a focus of much discussion in archaeological circles, since differences in seasonal potential of different regions might serve
to create environmental frontiers that limited the spread of certain crops
into certain regions (e.g. Sherratt, 1980; Halstead, 1989; Bogaard, 2004, pp.
160–164; Kreuz et al., 2005; Fuller, 2007b, p. 405; Conolly et al., 2008). On
morphological grounds, there is no basis for distinguishing the seasonality
of archaeological crop remains, although archaeobotanists have made some
progress in inferring seasonality from associated non-crop weed remains.
Nevertheless, there remain debates, for example as to whether or not the
earliest agriculture in central Europe was autumn sown, and grown over the
winter, or spring sown and grown in the summer (e.g. Jacomet and Behre,
1991, p. 86; Bogaard, 2004, pp. 160–164; Kreuz et al., 2005). As crops spread
northward into new latitudinal bands, with longer and colder winters, cultivation may have become increasingly difficult over the traditional winter
season. Wetter and cooler summers may also have precluded certain species,
as appears to be the case with lentils and chickpeas (Conolly et al., 2008). As
a result, crops either had to evolve adaptations to surviving cold winters,
such as through vernalization in which autumn sown crops have a pause
in growth during the frost months and then resume growth in the warming
of spring; or else their original seasonality of flowering had to be switched
off, allowing them to be planted in spring and grown through the summer,
thus flowering during shortening days rather than long days. Recent years
have seen substantial developments in understanding the genetic basis of
vernalization and photoperiod sensitivity in cereals.
274 Fruit Development and Seed Dispersal
Figure 7.15 Diagrammatic representations comparing the regulatory gene networks
involved in vernalization and photoperiodicity, as inferred for wheat/barley, rice and
Arabidopsis. For sources, see text.
The emergent picture of the genetics of seasonality in various plant groups
gives a fascinating insight into regulatory network evolution. This example
shows how fluidly regulatory networks change over time often retaining core
components, but not necessarily with the same functionality. The scientific
community has been of the opinion for some time that the vernalization
response evolved in parallel in grasses and in eudicots as exemplified by Arabidopsis thaliana. This opinion is borne out by phylogenetics which supports
the idea that the ancestral grass type was more like the panicoid group which
is adapted to tropical conditions being short-day plants with no vernalization
response (Kellogg, 1998). However, recent identification of the major components of the vernalization response in grasses shows that much of the same
molecular apparatus is utilized between the groups (Fig. 7.15).
In wheat and barley, three principal components to the vernalization system have been discovered, named VRN1, VRN2 and VRN3 (Yan et al., 2003,
2004a, 2004b, 2006). In an unfortunate clash of nomenclature, it should be
noted that these are not directly comparable components to the similarly
named VRN1 and VRN2 in A. thaliana. While the latter two work in synergy
at a different point in the vernalization pathway, VRN1 and VRN2 in cereals work antagonistically. All these genes have been named so because of
their direct effects on phenotype through which they were originally discovered. As with many of the relationships shown in the network diagrams of
Seed Dispersal and Crop Domestication 275
Fig. 7.15, the interactions have been correlatively determined between genes
in the cereals; consequently, they may be either direct or indirect through
other as yet undetermined factors. That some of these interactions at least
are likely to be indirect, or an incomplete description of the regulation due to
other factors, is evident from some inconsistencies in the network relative to
observations that will be pointed out below.
In barley and wheat, VRN2 represses VRN3 and VRN1. VRN3 acts to promote VRN1, which in turn promotes flowering and further down-regulates
VRN2 that would otherwise resume action in the absence of short days or
cold temperatures. Short days or cold temperatures inhibit the action of VRN2
(Dubcovsky et al., 2006). It is not likely that VRN2 is involved directly in sensing such environmental cues. The inhibition of VRN2 is not in itself enough to
cause up-regulation of VRN3 and subsequently VRN1. After VRN2 inhibition,
VRN3 up-regulation is induced by long days, through the action of a fourth
important intermediary Ppd1. Through this set of interactions, temperate cereals have evolved a system in which they must experience either short days
or cold followed by longer days before flowering so ensuring that flowering
is delayed through the winter and initiated in the spring. This winter habit
is the ancestral condition, and suited to the climate of biogeographical range
of the wild progenitors. The spring habit has evolved several times and in
several ways from this regulatory network involving degenerative mutations
at each of the three main loci.
The action of VRN2 is to repress VRN1 and VRN3 through the action of a
CCT domain in VRN2, a domain type found in the CO-like group of genes
in A. thaliana. A mutation causing a R/W amino acid change at a conserved
position in this domain results in a lack of repression (Robson et al., 2001;
Cockram et al., 2007a) causing a phenotype in which flowering is triggered
by long days without the need for vernalization. This mutation makes a
recessive allele (vrn2) because in the heterozygous condition the functioning
allele will still achieve repression. A similar phenotype is also caused by
naturally occurring deletions at the VRN2 locus (Dubcovsky et al., 2005).
A spring phenotype is also caused by mutations at the VRN1 locus (Yan
et al., 2004b; Fu et al., 2005). There appear to be two sites at the VRN1 locus
that are involved with repression of the gene by acting as receptors to the
VRN2-mediated repressors. One is in the promoter region, and the second
within the first intron. Deletions at either of these sites result in a lack of
repression of VRN1 by VRN2. This time the mutant allele is dominant (Vrn1),
because in the heterozygous condition, even though the wild-type responsive
allele is repressed successfully by VRN2, the receptor region deleted allele
will still initiate flowering. The resulting phenotype is similar to that obtained with the vrn2 allele in that vernalization is not required for long days
to initiate flowering. Interestingly, a range of large deletions have occurred
in intron 1 both in barley and wheat, which indicate that both cereals have
achieved the spring phenotype independently, but through the same underlying mechanism (Fu et al., 2005). There are now known to be a large range of
276 Fruit Development and Seed Dispersal
combinations of VRN1 and VRN2 alleles possible, with 17 haplotypes occurring in the European barley germplasm of which only one winter and two
spring types dominate 79% of varieties (Cockram et al., 2007b).
The VRN3 locus also has a regulatory element in its promoter through
which VRN2 represses its action. In this case, a dominant mutant allele Vrn3
occurs in wheat that has a retrotransposon in the promoter rendering it
insensitive to VRN2 repression, again resulting in a similar phenotype to
the mutants described above (Yan et al., 2006). Although VRN3 completes the
network of interaction, as described in Fig. 7.15, it is not likely to be the complete story. The current understanding shown in the diagram implies that the
clear association between Vrn1 and spring phenotypes could not have been
discovered unless the Vrn3 genotype was also in place. Indeed, germplasm
surveys have already indicated that wherever Vrn3 occurs Vrn1 is also found.
However, Yan et al. (2006) argue that a mutation in the regulatory region of
either gene is enough to initiate the flowering cascade.
A fourth important locus in the seasonality of temperate cereals is Ppd1,
which builds on the spring phenotype produced by mutations at the vernalization loci. Ppd1 is responsible for initiating signal cascades in response
to long days (Turner et al., 2005). There are differing Ppd1 mutants in barley and wheat, respectively. In barley, a SNP causes the ppd-H1 (recessive)
mutant, which is insensitive to long days resulting in delayed flowering. In
most of the wild biogeographical range, this phenotype is selected against,
since the growing season is short followed by a hot dry summer that the
late flowering plants would find difficult to survive in. However, further
north, the potential growing season is much longer with wetter summers.
Spring varieties grown in northern temperate latitudes benefit from the ppdH1 mutant that has a longer vegetative phase resulting in more resource
sequestration and so in larger grain yields. This mutation appears to have
arisen within the domesticated barley gene pool east of the Fertile Crescent as crops moved in to more northern latitudes (Jones et al., 2008). The
known Ppd1 mutants in wheat result in a different phenotype to that of barley, probably due to different underlying mutations which appear to involve
large promoter region deletions (Beales et al., 2007). In the case of wheat, the
Ppd1 mutants are dominant resulting in floral initiation regardless of day
length. These early flowering types appear to do well under conditions in
southern Europe, but less well in more northerly latitudes (Worland et al.,
1998).
The regulatory networks for vernalization between the temperate cereals
and Arabidopsis thaliana are remarkably similar. Orthologous components are
utilized in each – VRN3 in wheat and barley is orthologous to FT, and VRN1
is orthologous to AP1. Wheat and barley also have versions of the GI and
CO genes which are established to act upstream of FT in A. thaliana, and are
likely to prove the same in cereals. However, there is no identifiable gene
orthologous to FLC in cereals, nor is there anything like the cereal VRN2 in
A. thaliana. However, these two genes act in a highly similar way in terms
of the network of relationships. It seems that a similar network solution has
Seed Dispersal and Crop Domestication 277
been converged upon in temperate cereals and the eudicot lineage represented by A. thaliana. In the cereals, VRN2 appears to have evolved at least
in part from a CO-like ancestor, whereas in eudicots, FLC originated from
another MADS-box gene (Zhao et al., 2006). However, there may be more to
discover in the cereals. A. thaliana has a second ‘FLC independent’ vernalization pathway in which VIN3 is up-regulated during cold spells and activates
AGL24 which initiates the flowering cascade (Michaels et al., 2003). VIN3 also
has the function of repressing FLC. Curiously, a well-conserved version of
the VIN3 gene has also been shown to be up-regulated by vernalization in
wheat (Fu et al., 2007). There is also a group of genes orthologous to AGL24
in wheat (Zhao et al., 2006).
Rice and the panicoid grasses such as maize do not have vernalization
adaptations. These grasses are naturally adapted to the tropics to flower
under short days. Very little is known yet about maize, although mutations
associated with early flowering have been identified (Chardon et al., 2005). It
is likely that the regulation of flowering time in this group of grasses is well
represented by rice about which a great deal has emerged in recent years.
The emergent picture of regulatory interactions that govern rice flowering
shows striking similarities and differences to the cereal network. Under conditions of long days, both Hd1, orthologous to CO, and Ghd7 repress Hd3a,
which is orthologous to FT (Yano et al., 2000; Kojima et al., 2002; Hayama et al.,
2003; Xue et al., 2008). The function of Hd1 is surprising in this instance, because it acts in the opposite way to its orthologous counterpart in Arabidopsis.
However, it appears that Hd6, which is also known to have a repressive effect
on flowering time under long days, may be acting in conjunction with the
Hd1 complex to repress Hd3a (Yamamoto et al., 2000; Takahashi et al., 2001;
Ogiso et al., 2007). Ghd7, most closely related to VRN2 in cereals (Xue et al.,
2008), also represses Ehd1 that would otherwise initiate flowering (Doi et al.,
2004), resulting in a regulation reminiscent of VRN2 and FLC. Interestingly,
Ghd7 also appears to have pleiotropic effects on plant size and grain number,
leading to increased growth, cell proliferation and differentiation.
As days become shorter, during the monsoon season, the actions of both
Hd1 and Ghd7 change. Ghd7 promotes Ehd1 (Xue et al., 2008) and Hd1 promotes
Hd3a (Yano et al., 2000). Possibly, this apparent return of Hd1 to a function
more normally associated with a CO orthologue may represent a release
of action by Hd6. Once Hd3a has been promoted, the flowering cascade is
initiated.
Photoperiod sensitive rice (and maize) crops are restricted to tropical areas,
because the growing season further north is too short. Photoperiod insensitive
varieties of rice that can be grown in more temperate conditions further
north are associated with less or non-functioning alleles, and the earliest rice
varieties actually have Ghd7 deleted, resulting in a strong latitudinal cline
of Ghd7 alleles (Xue et al., 2008). Consequently, not only is the resemblance
between the wheat/barley and rice regulation striking, the point at which
mutations causing loss of functionality to induce seasonal insensitivity also
coincide in VRN2 and Ghd7.
278 Fruit Development and Seed Dispersal
7.13
Discussion: evolution and development of
domesticated seed traits
The domestication of crop plants represents numerous trajectories of parallel
evolution, with some instances of true convergence as plants adapted to the
selective pressures brought to bear by human farmers. The major selective
pressures were associated with the dispersal and establishment of the next
generation of seeds, from dispersal mechanism (the shift to human harvesting), seed germination (shifts away from dormancy and changes in seasonal
controls on germination), and seedling establishment. In most cases, these
selective pressures were initially unconscious on the part of people, as recognized by Darwin and his successors (e.g. Darwin, 1883, Chapter 20; Zohary,
1969; Darlington, 1973, p. 155; Harlan, 1992). Since human food production as
a behaviour follows similar patterns for similar aims, the selection pressures
with domestication have often been similar. There has been some debate,
and perhaps, confusion over whether to regard the similar domestication
outcomes as products of convergence or parallelism. As clarified by the definitions of Niklas (1997, pp. 303–305) and Gould (2002, pp. 81–82, 1076–1089),
convergence is a case of analogy when unrelated organisms produce similar morphological ends (adaptations) in different ways. By contrast, parallel
evolution is when related organisms evolve similar adaptations from the
same ancestral mechanism or underlying developmental/genetic architecture: this represents selection working on existing developmental constraints
that are shared across species. Parallelism like phylogenetic/historical homology is a form of syngeny (generative homology) (as defined in Butler
and Saidel, 2000). Seen in these terms, there are clear cases of both parallelism and convergence in domestication: orthologous loci, such as some loci
regulating flowering show parallel evolution (e.g. Vrn3 in Hordeae, Hd3a in
rice, FT in Arabidopsis; see Fig. 7.15); by contrast, the loci involved in cereal
shattering differ between wheat/barley and rice such that they have evolved
along multiple non-orthologous genetic paths, and thus represent allogeny
or generative homoplasy (as defined in Butler and Saidel, 2000). Such nonorthologous means of achieving similar adaptations are convergent in the
sense used here (but note that Paterson et al., 1995 argued for ‘convergence’
in the sense of parallelism as used here; a hypothesis now falsified by further
work: Li and Gill, 2006; and see above).
A key area of evolution under domestication involved changes in seed
dispersal, taken broadly to include the timing of fruiting, the mode of dispersal, and patterns of germination. In recent years, much scientific progress
has been made in understanding these evolutionary processes through the
efforts of archaeobotany and through genetics. Archaeological plant remains
(archaeobotany) can provide hard fossil evidence for the rate and extent of
evolution in those morphological traits which are prone to archaeological
preservation, especially in charred seeds or cereal chaff (rachises and spikelet
bases). Genetics, starting from QTLs and moving onto sequencing studies,
Seed Dispersal and Crop Domestication 279
allows the identification of the coding gene regions and the developmental
pathways involved in these domestication traits, how many different ways
and times these have evolved and potentially provides a framework for inferring aspects of the geographical history of these traits. We expect that soon association mapping studies will provide important new insights about linked
syndromes of genetic adaptation, as suggested by recent work in Arabidopsis
(Aranzana et al., 2005), and the extent to which genetic linkage evolved during the domestication process (cf. D’Ennequin et al., 1999) or was part of
pre-existing wild variation. In both archaeology and genetics, there is much
further research to do. At present, there are still relatively few species which
have been studied, and there are limited cases of potential comparisons from
which recurrent patterns of the evolution of domesticated seed dispersal can
be studied.
Nevertheless, there are a few aspects that can be highlighted. The fact that
available data point to rather slow processes of evolution towards fixation in
traits such as non-shattering in cereals and grain size increase, taking place
on the order of 1000 generations or more, was unexpected by earlier theorists. For example Harlan (1992, p. 124) concludes that ‘cultivated plants
have the capacity to evolve rapidly,’ and experimental inferences of Hillman
and Davies (1990, 1999) suggested that 20–100 generations of self-pollinating
cereals should be sufficient. As reviewed above, archaeobotanical data now
suggest a much slower process (also Fuller, 2007a; Allaby, 2008; Allaby et al.,
2008), perhaps more akin to cases of natural selection, as seed dispersal and
seedling traits became adapted to human ecology. As with many cases of
natural selection, genetic changes involved with domestication have operated through changes in the regulation of seed and fruit development, with
several known domestication genes representing mutations to regulatory
transcription factors (cf. Doebly et al., 2006; Burger et al., 2008).
It may be possible to consider these changes in an ontogenetic framework
of heterochrony. As discussed by Niklas (1994, pp. 262–274; also Nikalas1997,
pp. 101–104), there are different ways in which the timing of development
may change in heterochronic evolution. One that is often discussed is paedomorphosis, in which the ancestral juvenile form shows more resemblance
to the derived mature form. A subcategory of this is neoteny, in which some
vegetative traits are arrested and some ancestral juvenile character states are
retained longer in relation to overall organismal development. The loss of
shattering appears to represent an example of this as formation of wild-type
adult abscission layers is arrested, that is sexual maturation is delayed. Other
domestication traits may be regarded as peramorphosis or pre-displacement
in which development is accelerated in vegetative traits and completed before
all of the ancestral adult reproductive traits have formed: this may be applied
to germination, loss of photoperiodicity functions, or the loss of appendages.
Finally, acceleration may be applied to the expanded and exaggerated traits
of domesticates, such as increases in grain size or the expanded appendages
associated with a few fibre crops (cotton, devil’s claw), in which vegetative
280 Fruit Development and Seed Dispersal
growth is simply increased prior to reproductive maturity. Indeed, the prolonged development programme of cotton testa cells involved in fibre production has been molecularly characterized (Hovav et al., 2008). Because the
domesticate often differs in shape and proportion (e.g. domesticated cereals
are wider and thicker but may not be longer), and not merely size, this is a
not a simple case of gigas (gigantism), when size is increased along a fixed
allometric relationship (cf. Niklas, 1994). In some cases of domesticated size
increase, such as in cucurbit fruits, simple gigantism may apply (see Sinnott,
1936, 1939). Further research documenting when during seed development
certain traits, which have been modified by domestication, are expressed may
provide further insights into the evolution of the domestication syndrome.
What remains unclear is why the rates and ordering of domesticated traits
have varied across some taxa and differences between families (cf. Fuller,
2007a), and an ontogenetic perspective on these traits may offer a framework
for understanding the nature of these parallel or convergent evolutions.
As Ames (1939) recognized the angiosperm seed has been central to human
economic evolution, but it is the changes to seed dispersal and establishment
that made this possible, giving human populations sources of growing surpluses, and particular species in domesticated form evolved unprecedented
fitness across a range of environments. The further investigation of the evolution of seed crop domestication has much to contribute to our understanding
of the processes of parallel and convergent evolution and the intertwined
history of a limited range of plant species and Homo sapiens.
References
Abbo, S., Ladizinsky, G. and Weeden, N.F. (1991) Genetic analysis and linkage study
of seed weight in lentil. Euphytica 58, 259–266.
Abbo, S., Zezak, I., Schwartz, E., Lev-Yadun, S. and Gopher, A. (2007) Experimental
harvesting of wild pea in Israel: implications for the origins of Near Eastern farming.
Journal of Archaeological Science 35, 922–929.
Allaby, R. (2008) The rise of plant domestication: life in the slow lane. Biologist 55(2),
94–99.
Allaby, R.G., Fuller, D.Q. and Brown, T.A. (2008) The genetic expectations of a protracted model for the origins of domesticated crops. Proceedings of the National
Academy of Sciences USA 105(37), 13982–13986.
Allen, H. (1974) The Bagundji of the Darling Basin: cereal gatherers in an uncertain
environment. World Archaeology 5, 309–322.
Amblard, S. and Pernes, J. (1989) The identification of cultivated pearl millet (Pennisetum) amongst plant impressions on pottery from Oued Chebbi (Dhar Oualata,
Mauritania). African Archaeological Review 7, 117–126.
Ames, O. (1939) Economic Annuals and Human Cultures. Botanical Museum of Harvard
University, Cambridge, MA.
Aranzana, M.J., Kim, S., Zhao, K., Bakker, E., Horton, M., Jakob, K., Lister, C., Molitor,
J., Shindo, C., Tang, C., Toomajian, C., Traw, B., Zheng, H., Bergelson, J., Dean,
C., Marjoram, P. and Nordborg, M. (2005) Genome-wide association mapping in
Seed Dispersal and Crop Domestication 281
arabidopsis identifies previously known flowering time and pathogen resistance
genes. PLoS Genetics 1, 531–539.
Asch, D.L. and Asch, N.B. (1985) Prehistoric plant cultivation in west-central Illinois.
In: Prehistoric Food Production in North America (ed. R.I. Ford). Anthropological
Papers No. 75. Museum of Anthropology, University of Michigan, Ann Arbor, pp
149–203.
Azhaguvel, P. and Komatsuda, T. (2007) A phylogenetic analysis based on nucleotide
sequence of a marker linked to the brittle rachis locus indicates a diphyletic origin
of barley. Annals of Botany 100, 1009–1015.
Bailey, P.C., McKibbin, R.S., Lenton, J.R., Holdsworth, M.J., Flintham, J.E. and Gale,
M.D. (1999) Genetic map locations for orthologous Vp1 genes in wheat and rice.
Theoretical and Applied Genetics 98, 281–284.
Balter, M. (2007) Seeking agriculture’s ancient roots. Science 316, 1830–1835.
Bar-Yosef, O. (1998) The Natufian culture in the Levant. Evolutionary Anthropology 6,
159–177.
Baskin, C. and Baskin, J.M. (2001) Seeds: Ecology, Biogeography and Evolution of Dormancy
and Germination. Academic Press, San Diego.
Beales, J., Turner, A., Griffiths, S., Snape, J.W. and Laurie, D.A. (2007) A PSEUDORESPONSE REGULATOR is misexpressed in the photoperiod insensitive Ppd-D1a
mutant of wheat (Triticum aestivum L.). Theoretical and Applied Genetics 115, 721–
733.
Becraft, P.W., Stinard, P.S. and McCarty, D.R. (1996) CRINKLY 4: a TNFR-like receptor
kinase involved in maize epidermal differentiation. Science 273, 1406–1409.
Benz, B.F. (2001) Archaeological evidence of teosinte domestication from Guilá
Naquitz, Oaxaca. Proceedings of the National Academy of Sciences USA 98, 2104–2106.
Blair, M.W., Iriarte, G. and Beebe, S. (2006) QTL analysis of yield traits in an advanced
backcross population derived from a cultivated Andean X wild common bean
(Phaseolus vulgaris L.) cross. Theoretical and Applied Genetics 112, 1149–1163.
Blumler, M.A. (1991) Modelling the origins of legume domestication and cultivation.
Economic Botany 45, 243–250.
Bogaard, A. (2004) Neolithic Farming in Central Europe: An Archaeobotanical Study of
Crop Husbandry Practices C5500–2200 BC. Routledge, London.
Bohrer, V.L. (1984) Domesticated and wild crops in the CAEP study area. In: Prehistoric
Cultural Development in Central Arizona: Archaeology of the Upper New River Region
(eds P. Spoerl and G. Gemerman). Occasional Paper No. 5, Center for Archaeological
Investigations, Southern Illinois University, Carbondale, pp 183–259.
Braadbaart, F., Boon, J.J., Veld, H., David, P. and van Bergen, P.F. (2004) Studies on
the heat treatment of peas: changes of their physical and bulk chemical properties.
Journal of Archaeological Science 31, 821–833.
Bretting, P.K. (1982) Morphological differentiation of proboscidea parviflora ssp. parviflora (Martyniaceae) under domestication. American Journal of Botany 69, 1531–1537.
Bretting, P.K. (1986) Changes in fruit shape in proboscidea parviflora ssp. parviflora
(Martyniaceae) with domestication. Economic Botany 40(2), 170–176.
Brunken, J., De Wet, J.M.J. and Harlan, J.R. (1977) The morphology and domestication
of pearl millet. Economic Botany 31, 163–174.
Bruno, M.C. (2006) A morphological approach to documenting the domestication
of chenopodium in the Andes. In: Documenting Domestication. New Genetic and
Archaeological Paradigms (eds M.A. Zeder, D.G. Bradley, E. Emshwiller and B.D.
Smith). Universty of California Press, Berkeley, pp 32–45.
282 Fruit Development and Seed Dispersal
Bruno, M. and Whitehead, W.T. (2003) Chenopodium cultivation and formative period
agriculture at Ciripa, Bolivia. Latin American Antiquity 14, 339–355.
Burger, J.C., Chapman, M.J. and Burke, J.M. (2008) Molecular insights into the evolution of crop plants. American Journal of Botany 95, 113–122.
Butler, A.B. and Saidel, W.M. (2000) Defining sameness: historical, biological, and
generative homology. BioEssays 22(9), 846–853.
Butler, E.A. (1989) Cryptic anatomical characters as evidence of early cultivation in
the grain legumes (pulses). In: Foraging and Farming (eds D.R. Harris and G.C.
Hillman). Unwin and Hyman, London, pp 390–407.
Butler, E.A. (1990) Legumes in Antiquity: A Micromorphological Investigation of Seeds
of the Viceae. Unpublished Ph.D. Dissertation. Institute of Archaeology, University
College, London.
Cao, X., Costa, L.M., Biderre-Petit, C., Kbhaya, B., Dey, N., Perez, P., McCarty, D.R.,
Gutierrez-Marcos, J.F. and Becraft, P.W. (2007) Abscisic acid and stress signals induce Viviparous1 expression in seed and vegetative tissues of maize. Plant Physiology 143, 720–731.
Carlson, S.J., Shanker, S. and Chourey, P.S. (2000) A point mutation at the Miniature1
seed locus reduces levels of the encoded protein but not its mRNA in maize.
Molecular and General Genetics 263, 367–373.
Carrari, F., Benech-Arnold, R., Osuna-Fernandez, R., Hopp, E., Sanchez, R., Iusem, N.
and Lijavetzky, D. (2003) Genetic mapping of the Sorghum bicolor vp1 gene and
its relationship with preharvest sprouting resistance. Genome 46, 253–258.
Chardon, F., Hourcade, D., Combes, V. and Charcosset, A. (2005) Mapping of a spontaneous mutation for early flowering time in maize highlights contrasting allelic
series at two-linked QTL on chromosome 8. Theoretical and Applied Genetics 112,
1–11.
Cheng, C., Motohashi, R., Tchuchimoto, S., Fukuta, Y., Ohtsubo, H. and Ohtsubo, E.
(2003) Polyphyletic origin of cultivated rice: based on the interspersion patterns of
SINEs. Molecular Biology and Evolution 20, 67–75.
Cho, S., Kumar, J., Anupama, K., Tefera, F. and Muehlbauer, F.J. (2002) Mapping
genes for double podding and other morphological traits in chickpea. Euphytica
128, 285–292.
Cockram, J., Chiapparino, E., Tayor, S.A., Stamati, K., Donini, P., Laurie, D.A. and
O’Sullivan, D. (2007b) Haplotype analysis of vernalization loci in European barley
germplasm reveals novel VNR-H1 alleles and a predominant winter VRN-H1/VRNH2 multilocus haplotype. Theoretical and Applied Genetics 115, 93–1001.
Cockram, J., Jones, H., Leigh, F.J., O’Sullivan, D., Powell, W., Laurie, D. and Greenland, A.J. (2007a) Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. Journal of Experimental Botany 58, 1231–
1244.
Colledge, S. (1998) Identifying pre-domestication cultivation using multivariate analysis. In: The Origins of Agriculture and Crop Domestication (eds A.B. Damania, J.
Valkoun, G. Willcox and C.O. Qualset). ICARDA, Aleppo, pp 121–131.
Colledge, S. (2001) Plant Exploitation on Epipalaeolithic and Early Neolithic Sites in the
Levant. British Archaeological Reports, Oxford.
Colledge, S. (2004) Reappraisal of the archaeobotanical evidence for the emergence
and dispersal of the ‘founder crops’. In: Neolithic Revolution. New Perspectives on
Southwest Asia in Light of Recent Discoveries on Cyprus (eds E. Peltenberg and A.
Wasse). Oxbow Books, Oxford, pp 49–60.
Seed Dispersal and Crop Domestication 283
Colledge, S., Conolly, J. and Shennan, S. (2004) Archaeobotanical evidence for the
spread of farming in the eastern Mediterranean. Current Anthropology 45, S35–S58.
Colledge, S., Conolly, J. and Shennan, S. (2005) The evolution of Neolithic farming
from SW Asian origins to NW European limits. European Journal of Archaeology 8,
137–156.
Conolly, J., Colledge, S. and Shennan, S. (2008) Founder effect, drift, and adaptive
change in domestic crop use in early Neolithic Europe. Journal of Archaeological
Science 35, 2797–2804.
Costantini, L. (1983) The beginning of agriculture in the Kachi Plain: the evidence of
Mehrgarh. In: South Asian Archaeology 1981 (ed. B. Allchin). Cambridge University
Press, Cambridge, pp 29–33.
Crawford, G.W. and Shen, C. (1998) The origins of rice agriculture: recent progress in
East Asia. Antiquity 72, 858–866.
D’Andrea, A.C., Kahlheber, S. Logan, A.L. and Watson, D.J. (2007) Early domesticated
cowpea (Vigna unguiculata) from Central Ghana. Antiquity 81, 686–698.
D’Andrea, A.C., Klee, M. and Casey, J. (2001) Archaeobotanical evidence for pearl
millet (Pennisetum glaucum) in sub-Saharan West Africa. Antiquity 75, 341–348.
Darlington, C.D. (1973) Chromosome Botany and the Origins of Cultivated Plants, 3rd edn.
George Allen & Unwin, London.
Darwin, C. (1883) The Variation of Animals and Plants Under Domestication, 2nd edn. D.
Appleton & Co., New York.
Day, J.S. (2000) Development and maturation of sesame seeds and capsules. Field
Crops Research 67, 1–9.
De Candolle, A. (1885) Origin of Cultivated Plants. D. Appleton & Co., New York.
D’Ennequin, M. Le Thierry, Toupance, B., Robert, T., Godelle, B. and Gouton, P.H.
(1999) Plant domestication: a model for studying the selection of linkage. Journal of
Evolutionary Biology 12, 1138–1147.
Dickau, R., Ranere, A.J. and Cooke, R.G. (2007) Starch grain evidence for the preceramic dispersals of maize and root crops into tropical dry and humid forests of
Panama. Proceedings of the National Academy of Sciences USA 104, 3651–3656.
Doebly, J.F., Gaut, B.S. and Smith, B. D (2006) The molecular genetics of crop domestication. Cell 127, 1309–1321.
Doi, K., Izawa, T., Fuse, F., Yamanouchi, U., Kubo, T., Shimatini, Z., Yano, M. and
Yoshimura, A. (2004) Ehd1, a B-type response regulator in rice, confers short-day
promotion of flowering and controls FT-like gene expression independently of Hd1.
Genes and Development 18, 926–936.
Dubcovsky, J., Chen, C. and Yan, L. (2005) Molecular characterization of the alleleic variation at the VRN-H2 vernalization locus in barley. Molecular Breeding
15, 395–407.
Dubcovsky, J., Loukoianov, A., Fu, D., Valarik, M., Sanchez, A. and Yan, L. (2006)
Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and
VRN2. Plant Molecular Biology 60, 469–480.
Dunne, M.T. and Green, W. (1998) Terminal archaic and early woodland plant use at
the gast spring site (13LA152), southeast Iowa. Midcontinental Journal of Archaeology
23(1), 45–48.
Elbaum, R., Zaltzman, L., Burgert, I. and Fratzl, P. (2007) The role of wheat awns in
the seed dispersal unit. Science 316(5826), 884–886.
Fan, C., Xing, Y., Mao, H., Lu, T., Han, B., Xu, C., Li, X. and Zhang, Q. (2005) GS3,
a major QTL for grain length and weight and minor QTL for grain width and
284 Fruit Development and Seed Dispersal
thickness in rice, encodes a putative transmembrane protein. Theoretical and Applied
Genetics 112, 1164–1171.
Fennimore, S.A. and Foley, M.E. (1998) Genetic and physiological evidence for the
role of giberrelic acid in the germination of Avena fatua seeds. Journal of Experimental
Botany 49, 89–94.
Finch-Savage, W. and Leubner-Metzger, G. (2006) Seed dormancy and the control of
germination. New Phytologist 171, 501–523.
Finucane, B., Manning, K. and Touré, M. (2008) Late Stone Age subsistence in the
Tilemsi Valley, Mali: stable isotope analysis of human and animal remains from
the site of Karkarichinkat Nord (KN05) and Karkarichinkat Sud (KS05). Journal of
Anthropological Archaeology 27, 82–92.
Flintham, J.E. and Humphry, S.J. (1993) Red coat genes and wheat dormancy. Aspects
Applied Biology 36, 135–141.
Fritz, G.J. (1994) Are the first American farmers getting younger? Current Anthropology
35, 305–309.
Fryxell, P.A. (1979) The Natural History of the Cotton Tribe. Texas A & M University
Press, London.
Fu, D., Dunbar, M. and Dubcovsky, J. (2007) Wheat VIN3-like PHD finger genes
are upregulated by vernalization. Molecular Genetics and Genomics 277, 301–
313.
Fu, D., Szücs, P., Yan, L., Helguera, M., Skinner, J.S., Zitzewitz, J., Hayes, P.M. and
Dubcovsky, J. (2005) Large deletions within the first intron in VRN-1 are associated
with spring growth habit in barley and wheat. Molecular Genetics and Genomics 273,
54–65.
Fuller, D.Q. (2003) Further evidence on the prehistory of sesame. Asian Agri-History
7(2), 127–137.
Fuller, D.Q. (2006) Agricultural origins and frontiers in South Asia: a working synthesis. Journal of World Prehistory 20, 1–86.
Fuller, D.Q. (2007a) Contrasting patterns in crop domestication and domestication
rates: recent archaeobotanical insights from the Old World. Annals of Botany 100(5),
903–924.
Fuller, D.Q (2007b) Non-human genetics, agricultural origins and historical linguistics in South Asia. In: The Evolution and History of Human Populations in
South Asia (eds M. Petraglia and B. Allchin). Springer, Netherlands, pp 393–
443.
Fuller, D.Q. and Harvey, E.L. (2006) The archaeobotany of Indian Pulses: identification, processing and evidence for cultivation. Environmental Archaeology 11(2),
219–246.
Fuller, D.Q., Harvey, E.L. and Qin, L. (2007a) Presumed domestication? Evidence for
wild rice cultivation and domestication in the fifth millennium BC of the lower
Yangtze region. Antiquity 81, 316–331.
Fuller, D.Q., Macdonald, K. and Vernet, R. (2007b) Early domesticated pearl millet
in Dhar Nema (Mauritania): evidence of crop-processing waste as ceramic temper. In: Fields of Change. Progress in African Archaeobotany (ed. R.T.J. Cappers),
Grongingen Archaeological Studies 5. Barkhuis Publishing, Groningen, pp 71–
76.
Fuller, D.Q. and Qin, L. (2008) Immature rice and its archaeobotanical recognition: a
reply to Pan. Antiquity 82(316). On-line project gallery. Available from http: //antiquity.ac.uk/ProjGall/fuller2/index.html.
Seed Dispersal and Crop Domestication 285
Fuller, D.Q., Qin, L. and Harvey, E.L. (2008) Rice archaeobotany revisited: comments
on Liu et al. (2007). Antiquity 82(315). On-line project gallery. Available from http:
//antiquity.ac.uk/ProjGall/fuller1/index.html.
Fuller, D.Q., Qin, L., Zheng, Y., Zhao, Z., Chen, X., Hosoya, L.A. and Sun, G.P. (2009)
The domestication process and domestication rate in rice: spikelet bases from the
Lower Yangtze. Science 323, 1607–1610.
Gao, F.Y., Ren, G.J., Lu, X.J., Sun, S.X., Li, H.J., Gao, Y.M., Luo, H., Yan, W.G. and Zhang,
Y.Z. (2008) QTL analysis for resistance to preharvest sprouting in rice (Oryza sativa).
Plant Breeding 127, 268–273.
Godbole, S.V. (1925) Pennisetum typhoideum. Studies on the Bajri Crop. I. The morphology of Pennisetum typhoideum. Memoirs of the Department of Agriculture in India
(Agricultural Research Institute, Pusa) 14(8), 247–268.
Gould, S.J. (2002) The Structure of Evolutionary Theory. Harvard University Press,
Cambridge, MA.
Gremillion, K.J. (1993) Crop and weed in prehistoric eastern North America: the
Chenopodium Example. American Antiquity 58, 496–509.
Gupta, P., Rustgi, S. and Kumar, N. (2006) Genetic and molecular basis of grain size
and grain number and its relevance to grain productivity in higher plants. Genome
49, 565.2–571.2.
Haaland, R. (1999) The puzzle of the late emergence of domesticated sorghum in the
Nile Valley. In: The Prehistory of Food. Appetites for Change (eds C. Gosden and J.
Hather). Routledge, London, pp 397–418.
Halstead, P. (1989) Like a rising damp? An ecological approach to the spread of
farming in south-east and central Europe. In: The Beginnings of Agriculture (eds A.
Milles, D. Williams and N. Gardner). British Archaeological Resports, Oxford, pp
23–53.
Harlan, J.R. (1989) Wild grass-seed harvesting in the Sahara and sub-Sahara of Africa.
In: Foraging and Farming: The Exploitation of Plant Resources (eds D.R. Harris and
G.C. Hillman). Unwin and Hyman, London, pp 79–98.
Harlan, J.R. (1992) Crops and Ancient Man, 2nd edn. American Society for Agronomy,
Madison.
Harlan, J.R., De Wet, J.M.J. and Price, E.G. (1973) Comparative evolution of cereals.
Evolution 27, 311–325.
Harris, D.R. (1981) The prehistory of human subsistence: a speculative outline.
In: Food, Nutrition and Evolution: Food as an Environmental Factor in the Genesis
of Human Variability (eds D.N. Walcher and N. Kretchmer). Masson, New York,
pp 15–35.
Harris, D.R. (1984) Ethnohistorical evidence for the exploitation of wild grasses and
forbes: its scope and archaeological implications. In: Plants and Ancient Man. Studies
in Paleoethnobotany (eds W. Van Zeist and W.A. Casparie). A. A. Balkema, Rotterdam,
pp 63–69.
Harris, D.R. (1989) An evolutionary continuum of people-plant interaction. In: Foraging and Farming: The Evolution of Plant Exploitation (eds D.R. Harris and G.C.
Hillman). Routledge, London, pp 11–26.
Harris, D.R. (1996) Introduction: themes and concepts in the study of early agriculture.
In: The Origins and Spread of Agriculture and Pastoralism in Eurasia (ed. D.R. Harris).
UCL Press, London, pp 1–9.
Harris, D.R. (2004) Origins and spread of agriculture. In: The Cultural History of Plants
(eds M. Nesbitt and G. Prance). Routledge, London, pp 13–26.
286 Fruit Development and Seed Dispersal
Harris, D.R. (2008) Agriculture, cultivation and domestication: exploring the conceptual framework of early food production. In: Rethinking Agriculture. Archaeological
and Ethnoarchaeological Perspectives (eds T. Denham, J. Iriarte and L. Vrydaghs). Left
Coast Press, Walnut Creek, pp 16–35.
Hattori, T., Terada, T. and Hamasuna, S.T. (1994) Sequence and functional analyses
of the rice gene homologous to the maize Vp1. Plant Molecular Biology 24, 805–
810.
Hayama, R., Yokoi, S., Tamaki, S., Yano, M. and Shimamoto, K. (2003) Adaptation of
photoperiodic control pathways produce short-day flowering in rice. Nature 422,
719–722.
Heiser, C.B. (1990) Seed to Civilization: The Story of Food, new (3rd) edn. Harvard
University Press, Cambridge, MA.
Heiser, C.B. (2008) The domesticated sunflower in old Mexico? Genetic Resources and
Crop Evolution 45, 447–449.
Helbaek, H. (1954) Prehistoric food plants and weeds in Denmark. A survey of archaeobotanical research 1923–1954. Danmarks Geoligishe Unders, Series II 80, 250–261.
Helbaek, H. (1959) Domestication of food plants in the Old World. Science 130, 365–372.
Helbaek, H. (1960) The paleoethnobotany of the Near East and Europe. In: Prehistoric
Investigations in Iraqi Kurdistan (eds R.J. Braidwood and B. Howe). University of
Chicago Press, Chicago, pp 99–118.
Helbaek, H. (1970) The plant husbandry of Hacilar. In: Excavations at Hacilar (ed. J.
Mellaart). Edinburgh University Press, Edinburgh, pp 189–244.
Henriksen, P.S. and Robinson, D. (1996) Early Iron Age agriculture: archaeobotanical evidence from an underground granary at Overbygaard in northern Jutland,
Denmark. Vegetation History and Archaeobotany 5, 1–11.
Higgs, E.S. and Jarman, M.R. (1969) The origins of agriculture: a reconsideration.
Antiquity 43, 31–41.
Higgs, E.S. and Jarman, M.R. (1972) The origins of animal and plant husbandry.
In: Papers in Economic Prehistory (ed. E.S. Higgs). Cambridge University Press,
Cambridge, pp 3–13.
Hillman, G.C. and Davies, M.S. (1990) Domestication rates in wild wheats and barley
under primitive cultivation. Biological Journal of the Linnean Society 39, 39–78.
Hillman, G.C. and Davies, M.S. (1999) Domestication rate in wild wheats and barley
under primitive cultivation: preliminary results and archaeological implications of
field measurements of selection coefficient. In: Prehistory of Agriculture. New Experimental and Ethnographic Approaches (ed. P.C. Anderson), Monograph 40. Institute of
Archaeology, University of California, Los Angeles, pp 70–102.
Hillman, G.C., Hedges, R., Moore, A.M.T., Colledge, S. and Pettitt, P. (2001) New
evidence of Late Glacial cereal cultivation at Abu Hureyra on the Euphrates. The
Holocene 11, 383–393.
Hori, K, Sato, K. and Takeda, K. (2007) Detection of seed dormancy QTL in multiple
mapping populations derived from crosses involving novel barley germplasm.
Theoretical and Applied Genetics 115, 869–876.
Hovav, R., Udall, J.A., Chaudhart, B., Hovav, E., Flagel, L., Hu, G. and Wendel, J.F.
2008. The evolution of spinnable cotton fiber entailed prolonged development and
a novel metabolism. PLoS Genetics 4(2), e25.
Huang, F. and Zhang, M. (2000) Pollen and phytolith evidence for rice cultivation
during the Neolithic at Longquizhuang, eastern Jainghuai, China. Vegetation History
and Archaeobotany 9, 161–168.
Seed Dispersal and Crop Domestication 287
Hunter, A.A. (1992) Utilization of Hordeum pusillum (Little Barley) in the Midwest
United States: Applying Rindos’Co-evolutionary Model of Domestication. Ph.D. Dissertation. Department of Anthropology, University of Missouri, Columbia.
Hutchinson, J. (1970) The genetics of evolutionary change. The Indian Journal of Genetics
& Plant Bredding 30(2), 269–279.
Iltis, H. (2000) Homeotic sexual translocations and the origin of maize (Zea mays,
Poaceae): a new look at an old problem. Economic Botany 54, 7–42.
Jacomet, S. and Behre, K.-H. (1991) The ecological interpretation of archaeobotanical
data. In: Progress in Old World Paleoethnobotany (eds W.A. Van Zeist, K. Wasylikowa
and K.-H. Behre). A. A. Balkema, Rotterdam, pp 81–108.
Janatasuriyarat, C., Vales, M.I., Watson, C.J. and Riera-Lizarazu, W. (2004) Identification and mapping of genetic loci affecting the free-threshing habit and spike
compactness in wheat (Triticum aestivum L.) Theoretical and Applied Genetics 108,
261–273.
Jones, H., Leigh, F., Mackay, I., Bower, M., Smith, L., Charles, M., Jones, G., Jones,
M., Brown, T. and Powell, W. (2008) Population based re-sequencing reveals that
the flowering time adaptation of cultivated barley originated east of the Fertile
Crescent. Molecular Biology and Evolution 25, 2211–2219.
Jones, H.D., Peters, N.C.B. and Holdsworth, M.J. (1997) Genotype and environment
interact to control dormancy and differential expression of the VIVIPAROUS-1
homologue in embryos of Avena fatua. Plant Journal 12(4), 911–920.
Jones, M.K. (1988) The arable field: a botanical battleground. In: Archaeology and the
Flora of the British Isles—Human Influence on the Evolution of Plant Communities (ed.
M.K. Jones). Oxford University Committee for Archaeology Monograph 14, Oxford,
pp 86–92.
Jupe, M. (2003) The Effects of Charring on Pulses and Implications for Using Size Change to
Identify Domestication in Eurasia. Unpublished BA Dissertation. Institute of Archaeology, University College London, London.
Kaga, A., Isemura, T., Tomooka, N. and Vaughan, D.A. (2008) The genetics of domestication of the Azuki bean (Vigna angularis). Genetics 178, 1013–1036.
Kaplan, L. (2000) Beas, peas and lentils. In: The Cambridge World History of Food (eds
K.F. Kiple and K.C. Ornelas). Cambridge University Press, Cambridge, pp 271–281.
Kaplan, L., Lynch, T.F. and Smith, C.E., Jr. (1973) Early cultivated beans (Phaeseolus
vulgaris) from an intermontane valley in Peru. Science 179, 76–77.
Kellogg, E.A. (1998) Relationships of cereal crops and other grasses. Proceedings of the
National Academy of Sciences USA 95, 2005–2010.
Kerem, Z., Gopher, A., Lev-Yadun, S., Weinberg, P. and Abbo, S. (2007) Chickpea
domestication in the Neolithic Levant through the nutritional perspective. Journal
of Archaeological Science 34, 1289–1293.
Kilian, B., Özkan, H., Walther, A., Kohl, J., Dagan, T., Salamini, F. and Martin, W.
(2007) Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal no
reduction of nucleotide diversity during Triticum monococcum (Einkorn) domestication: implications for the origin of agriculture. Molecular Biology and Evolution 24,
2657–2668.
King, L.J. (1966) Weeds of the World, Biology and Control. Interscience Publishers, Inc.,
New York.
Kislev, M.E., Weiss, E. and Hartmann, A. (2004) Impetus for sowing and the beginning
of agriculture: ground collecting of wild cereals. Proceedings of the National Academy
of Sciences USA 101, 2692–2695.
288 Fruit Development and Seed Dispersal
Kitano, H., Futsuhara, Y. and Satoh, H. (1993) Morphological variations in rice
cultivars. In: Science of the Rice Plant. Volume One. Morphology (eds T. Matsuo and K. Hoshikawa). Food and Agriculture Policy Research Center, Tokyo,
pp 79–88.
Klee, M., Zach, B. and Neumann, K. (2000) Four thousand years of plant exploitation
in the Chad Basin of northeast Nigeria I: the archaeobotany of Kursakata. Vegetation
History and Archaeobotany 9, 223–237.
Klee, M., Zach, B. and Stika, H.-P. (2004) Four thousand years of plant exploitation
in the Lake Chad Basin (Nigeria), part III: plant impressions in potsherds from the
final Stone Age Gajiganna Culture. Vegetation History and Archaeobotany 13, 131–142.
Koinange, E.M.K., Singh, S.P. and Gepts, P. (1996) Genetic control of the domestication
syndrome in common bean. Crop Science 36, 1037–1045.
Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T. and Yano,
M. (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to
flowering downstream of Hd1 under short day conditions. Plant Cell Physiology 43,
1096–1105.
Komatsuda, T., Pourkheirandish, M., He, C., Azhaguvel, P., Kanamori, H., Perovic, D.,
Stein, N., Graner, A., Wicker, T., Tagiri, A., Lundqvist, U., Fujimura, T., Matsuoka,
M., Matsumoto, T. and Yano, M. (2007) Six-rowed barley originated from a mutation
in a homeodomain-leucine zipper I-class homeobox gene. Proceedings of the National
Academy of Sciences USA 104, 1424–1429.
Konishi, S., Izawa, T., Lin, S.Y., Ebana, K., Fukuta, Y., Sasaki, T. and Yano, M. (2006)
A SNP caused loss of seed shattering during rice domestication. Science 312,
1392–1396.
Kottearachchi, N.S., Uchino, N., Kato, K. and Miura, H. (2006) Increased grain dormancy in white-grained wheat by introgression of preharvest sprouting tolerance
QTLs. Euphytica 152, 421–428.
Kovach, M.J., Sweeney, M.T. and McCouch, S.R. (2007) New insights into the history
of rice domestication. Trends in Genetics 23, 578–587.
Kreuz, A., Marinova, E., Schafer, E. and Wiethold, J. (2005) A comparison of early Neolithic crop and weed assemblages from the Linearbankeramik and the Bulgarian
Neolithic culture: differences and similarities. Vegetation History and Archaeobotany
14, 237–258.
Krishnasamy, V. and Seshu, D.V. (1989) Seed germination rate and associated characters in rice. Crop Science 29, 904–908.
Kucera, B., Cohn, M.A. and Leubner-Metzger, G. (2005) Plant hormone interactions
during seed dormancy release and germination. Seed Science Research 15, 281–307.
Ladizinsky, G. (1979) The genetics of several morphological traits in lentil. The Journal
of Heredity 70, 135–137.
Ladizinsky, G. (1985) The genetics of hard seed coat in the genus Lens. Euphytica 34,
539–543.
Ladizinsky, G. (1987) Pulse domestication before cultivation. Economic Botany 41,
60–65.
Ladizinsky, G (1993) Lentil domestication: on the quality of evidence and arguments.
Economic Botany 47, 60–64.
Ladizinsky, G. (2008) How many tough-rachis mutants gave rise to domesticated
barley? Genetic Resources and Crop Evolution 45, 395–489.
Li, C., Zhou, A. and Sang, T. (2006) Rice domestication by reducing shattering. Science
311, 1936–1939.
Seed Dispersal and Crop Domestication 289
Li, W. and Gill, B.S. (2006) Multiple genetic pathways for seed shattering in the grasses.
Functional and Integrative Genomics 6, 300–309.
Lin, Z., Griffith, M., Li, X., Zhu, Z., Tan, L., Fu, Y., Zhang, W., Wang, X., Xie, D. and
Sun, C. (2007) Origin of seed shattering in rice (Oryza sativa L.) Planta 226, 11–20.
Liu, L., Lee, G.-A., Jiang, L. and Zhang, J. (2007) Evidence for the early beginning (c.
9000 cal. BP) of rice domestication in China: a response. The Holocene 17, 1059–1068.
Lone, F.A., Khan, M. and Buth, G.M. (1993) Palaeoethnobotany – Plants and Ancient Man
in Kashmir. A. A. Balkema, Rotterdam.
Long, A. and Fritz, G.J. (2001) Validity of AMS dates on maize from the Tehuacán
Valley: a comment on MacNeish and Eubanks. Latin American Antiquity 12(1), 87–90.
Lynch, T.F., Gillespie, R., Gowlette, J.A. and Hedges, R.M. 1985. Chronology of Guitarrero Cave, Peru. Science 229, 864–867.
Maass, B. (2005) Changes in seed morphology, dormancy and germination from wild
to cultivated hyacinth bean germplasm (Lablab purpureus: Papilionoideae). Genetic
Resources and Crop Evolution 53, 1127–1135.
Maccaferri, M., Sanguineti, M.C., Corneti, S., Ortega, J.L.A., Salem, M.B., Bort, J.,
DeAmbrogio, E., Fernando, L., Moral, G., Demontis, A., El-Ahmed, A., Malouff,
F., Machlab, H., Martos, V., Moragues, M., Motajawi, J., Nachit, M., Nserallah, N.,
Ouabbou, H., Royo, C., Slama, A., Tuberosa, R. (2008) Quantitative trait loci for
grain yield and adaptation of durum wheat (Triticum durum Desf.) across a wide
range of water availability. Genetics 178, 489–511.
MacDonald, K., Vernet, R. Fuller, D. and Woodhouse, J. (2003) New light on the
Tichitt tradition: a preliminary report on survey and excavation at Dhar Nema. In:
Researching Africa’s Past. New Contributions from British Archaeologists (eds P. Mitchell,
A. Haour and J. John Hobart). Oxford Univerity School of Archaeology Monograph
No. 57, Oxford, pp 73–80.
Magid, A.A. (1989) Plant Domestication in the Middle Nile Basin – An Archaeobotanical Case Study, Vol. 523. BAR International Series. British Archaeological Reports,
Oxford.
Magid, A.A. (2003) Exploitation of food-plants in the early and middle Holocene Blue
Nile area, Sudan and neighbouring areas. Complutum 14, 345–372.
Maranon, T. and Grubb, P.J. (1993) Physiological basis and ecological significance
of the seed size and relative growth rate relationship in Mediterranean annuals.
Functional Ecology 7, 591–599.
McKibbin, R.S., Wilkinson, M.D., Bailey, P.C., Flintham, J.E., Andrew, L.M., Lazzeri,
P.A., Gale, M.D., Lenton, J.R. and Holdsworth, M.J. (2002) Transcripts of Vp-1
homologues are misspliced in modern wheat and ancestral species. Proceedings of
the National Academy of Sciences USA 99, 10203–10208.
Marquez-Cedillo, L.A., Hayes, P.M., Kleinhofs, A., Legge, W.G., Rossnagel, B.G., Sato,
K., Ullrich, S.E., Wesenberg, D.M. ([The North American Barley Genome Mapping Project]) (2001) QTL analysis of agronomic traits in barley based on the doubled haploid progeny of two elite North American varieties representing different
germplasm groups. Theoretical and Applied Genetics 203, 625–637.
Matsui, K., Kiryu, Y., Komatsuda, T., Kurauchi, N., Ohtani, T. and Tetsuka, T. (2004)
Identification of AFLP markers linked to non-seed shattering locus (sht1) in buckwheat and conversion to STS markers for marker-assisted selection. Genome 47,
469–474.
Matsui, K., Tetsuka, T. and Hara, T. (2003) Two independent gene loci controlling
non-brittle pedicels in buckwheat. Euphytica 134, 203–208.
290 Fruit Development and Seed Dispersal
McCarty, D.R., Hattori, T., Carson, C.B., Vasil, V., Lazar, M. and Vasil, I. (1991) The
Vivaporous-1 developmental gene of maize encodes a novel transcriptional activator.
Cell 66, 895–905.
Michaels, S.D., Ditta, G., Gustafson-Brown, C., Pelaz, S., Yanofsky, M. and Amasino,
R.M. (2003) AGL24 acts a s apromoter of flowering in Arabidopsis and is positively
regulated by vernalization. The Plant Journal 33, 867–874.
Mohamed, H.A., Clark, J.A. and Ong, C.K. (1985) The influence of temperature during
seed development on the germination characteristics of millet seeds. Plant, Cell and
Environment 8, 361–362.
Murray, M.A., Fuller, D.Q. and Cappeza, C. (2007) Crop production on the Senegal
River in the early first Millennium AD: preliminary archaeobotanical results from
Cubalel. In: Fields of Change. Progress in African Archaeobotany (ed. R.T.J. Cappers),
Grongingen Archaeological Studies 5. Barkhuis Publishing, Groningen, pp 63–
70.
Nabhan, G.P. and Rea, A. (1987) Plant domestication and folk-biological change: the
upper Piman/Devil’s claw example. American Anthropologist 89, 57–73.
Nabhan, G.P., Whiting, A., Dobyns, H., Hevly, R. and Euler, R. (1981) Devil’s claw
domestication: evidence from southwestern Indian fields. Journal of Ethnobiology 1,
135–164.
Nadel, D., Weiss, E., Simchoni, O., Tsatskin, A. Danin, A. and Kislev, M.E. (2004)
Stone age hut in Israel yields world’s oldest evidence of bedding. Proceedings of the
National Academy of Sciences USA 101, 6821–6826.
Nesbitt, M.N. (2004) Can we identify a centre, a region or a supra-region for near
eastern plant domestication? Neo-lithics 1, 38–40.
Niklas, K.J. (1994) Plant Allometry: The Scaling of Form and Process. University of Chicago
Press, Chicago.
Niklas, K.J. (1997) The Evolutionary Biology of Plants. University of Chicago Press,
Chicago.
Nitsuma, Y. (1993) Upland rice. In: Science of the Rice Plant. Volume One. Morphology
(eds T. Matsuo and K. Hoshikawa). Food and Agriculture Policy Research Center,
Tokyo, pp 70–76.
Ogiso, E., Izawa, T., Takahashi, Y., Sasaki, T. and Yano, M. (2007) Functional analysis
of Hd6, a rice flowering time gene. Plant and Cell Physiology 48(Suppl.), S150.
Oka, H.-I. (1988) Origins of Cultivated Rice. Elsevier, Amsterdam.
Oka, H.-I. and Morishima, H. (1971) The dynamics of plant domestication: cultivation
experiments with Oryza perennis and its hybrid with O. sativa. Evolution 25, 356–364.
Osa, M., Kato, K., Mori, M., Shindo, C., Torada, A. and Miura, H. (2003) Mapping
QTLs for seed dormancy and the Vp1 homologue on chromosome 3A in wheat.
Theoretical and Applied Genetics 106, 1491–1496.
Paterson, A.H., Lin, Y.-R., Li, Z., Schertz, K.F., Doebley, J.F., Pinson, S.R.M., Liu, S.-C.,
Stansel, J.W. and Irvine, J.E. (1995) Convergent domestication of cereal crops by
independent mutations at corresponding genetic loci. Science 269, 1714–1718.
Pearson, E.S. and Hartley, H.O. (1976) Biometrika Tables for Statisticians, Vol. 1.
Biometrika Trust, Cambridge University Press, Cambridge.
Peltenberg, E., Colledge, S., Croft, P., Jackson, A., McCartney, C. and Murray, M.A.
(2001) Neolithic dispersals from the Levantine Corridor: a Mediterranean perspective. Levant 33, 35–64.
Phillips, L.L. (1976) Cotton. In: The Evolution of Crop Plants (eds N.W. Simmonds).
Longman, Harlow, pp 196–200.
Seed Dispersal and Crop Domestication 291
Piperno, D.R. and Flannery, K.V. (2001) The earliest archaeological maize (Zea
mays L.) from highland Mexico: new accelerator mass spectrometry dates and
their implications. Proceedings of the National Academy of Sciences USA 98, 2101–
2103.
Plitman, U. and Kislev, M.E. (1989) Reproductive changes induced by domestication. In: Advances in Legume Biology (eds C.H. Stirton and J.L. Zarucchi). Missouri
Botanical Garden, St. Louis, pp 487–503.
Poncet, V., Lamy, F., Devos, K., Gale, M., Sarr, A. and Robert, T. (2000) Genetic control
of domestication traits in pearl millet (Pennisetum glaucum L., Poaceae). Theoretical
and Applied Genetics 100, 147–159.
Poncet, V., Lamy, F., Enjalbert, J., Joly, H., Sarr, H. and 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.
Reed, C.A. (1977) Introduction: prologue. In: Origins of Agriculture (ed. C.A. Reed).
Mouton, The Hague, pp 1–21.
Ridley, H.N. (1930) The Dispersal of Plants throughout the World. L. Reeve, London.
Rindos, D. (1980) Symbiosis, instability, and the origins and spread of agriculture: a
new model. Current Anthropology 21, 751–772.
Robson, F., Costa, M.M.R., Hepworth, S.R., Vizir, I., Pineiro, M., Reeves, P.H., Putterill,
J. and Coupland, G. (2001) Functional importance of conserved domains in the
flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and
transgenic plants. The Plant Journal 28, 619–631.
Röder, M.S., Huang, X.-Q. and Börner, A. (2008) Fine mapping of the region of wheat
chromosome 7D controlling grain weight. Functional and Integrative Genomics 8,
79–86.
Roeder, A.H.K., Ferrándiz, C. and Yanofsky, M.F. (2003) The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Current Biology 13,
1630–1635.
Sang, T. and Ge, S. (2007) The puzzle of rice domestication. Journal of Integrative Plant
Biology 49, 760–768.
Sato, Y.-I. (2002) Origin of rice cultivation in the Yangtze River basin. In: The Origins
of Pottery and Agriculture (ed. Y. Yasuda). Lustre Press/Roli Books, New Delhi, pp
143–150.
Sauer, C.O. (1958) Jericho and composite sickles. Antiquity 32, 187–189.
Sherratt, A.G. (1980) Water soil and seasonality in early cereal cultivation. World
Archaeology 11, 313–330.
Sherratt, A.G. (1997) Climatic cycles and behavioural revolutions: the emergence of
modern humans and the beginnings of farming. Antiquity 71, 271–287.
Shomura, A., Izawa, E.K., Ebitani, T., Kanegae, H., Konishi, S. and Yano, M. (2008)
Deletion in a gene associated with grain size increased yields during rice domestication. Nature Genetics 40, 1023—1028. doi: 10.1038/ng.169.
Simons, K.J., Fellers, J.P., Trick, H.N., Zhang, Z., Tai, Y.-S., Gill, B.S. and Faris, J. (2006)
Molecular characterization of the major wheat domestication gene Q. Genetics 172,
547–555.
Sinnott, E.W. (1936) A developmental analysis of inherited shape differences in cucurbit fruits. American Naturalist 70, 245–254.
Sinnott, E.W. (1939) A developmental analysis of the relation between cell size and
fruit size in cucurbits. American Journal of Botany 26, 179–189.
Smartt, J. (1990) Grain Legumes. Cambridge University Press, Cambridge.
292 Fruit Development and Seed Dispersal
Smith, B.D. (1989) Origins of agriculture in eastern North America. Science 246,
1566–1571.
Smith, B.D. (1992) River of Change. Essays on Early Agriculture in Eastern North America.
Smithsonian Press, Washington, D.C.
Smith, B.D. (2001) Documenting plant domestication: the consilience of biological and
archaeological approaches. Proceedings of the National Academy of Sciences USA 98,
1324–1326.
Smith, B.D. (2006a) Documenting domesticated plants in the archaeological record.
In: Documenting Domestication. New Genetic and Archaeological Paradigms (eds M.A.
Zeder, D.G. Bradley, E. Emshwiller and B.D. Smith). University of California Press,
Berkeley, pp 15–24.
Smith, B.D. (2006b) Eastern North America as an independent center of plant
domestication. Proceedings of the National Academy of Sciences USA 103, 12223–
12228.
Song, X.-J., Huang, W., Shi, M., Zhu, M.-Z. and Lin, H.-X. (2007) A QTL for rice grain
width and weight encodes a previously unknown RING-type E3 ubiquitin ligase.
Nature Genetics 39, 623–630.
Stemler, A.B. (1990) A scanning electron microscopic analysis of plant impressions in
pottery from the sites of Kadero, El Zakiab, Um Direiwa and el Kadada. Archéologie
du Nil Moyen 4, 87–105.
Stokes, P. and Rowley-Conwy, P. (2002) Iron Age cultigen? Experimental return rates
for Fat Hen (Chenopodium album L.). Environmental Archaeology 7, 95–99.
Sweeney, M.T. and McCouch, S.R. (2007) The Complex History of the Domestication
of Rice. Annals of Botany 100, 951–957.
Sweeney, M.T., Thomson, M.J., Cho, Y.G., Park, Y.J., Williamson, S.H., Bustamante,
C. and McCouch, S.R. (2007) Global dissemination of a single mutation conferring
white pericarp in rice. PLoS Genetics 3(8), e133. doi: 10.1371/journal.pgen.0030133.
Sweeney, M.T., Thomson, M.J., Pfeil, B.E. and McCouch, S.R. (2006) Caught redhanded: Rc encodes a basic helix–loop–helix protein conditioning red pericarp in
rice. Plant Cell 18, 283–294.
Takahashi, R (1955) The origin and evolution of cultivated barley. In: Advances in
Genetics 7 (ed. M. Demerc). Academic Press, New York, pp 227–266.
Takahashi, Y., Shomura, A., Sasai, T., Yano, M. (2001) Hd6, a rice quantitative
locus involved in photoperiod sensitivity, encodes the alpha subunit of protein kinase CK2. Proceedings of the National Academy of Sciences USA 98, 7922–
7927.
Tang, L. (2003) The primitive rice remains from Chuodun Site. In: Chuodun Shan
Site: Collected Papers, Dongnan Wenhua [Southeast Culture] 2003(special issue 1),
46–49 [ in Chinese].
Tang, S., Min, S. and Sato, Y.-I. (1996) Exploration on Origin of keng rice (japonica) in
China. In: Origin and Differentiation of Chinese Cultivated Rice (eds X. Wang and C.
Sun). Chinese Agricultural University Press, Beijing, pp 72–80.
Tanno, K.-I. and Willcox, G. (2006) How fast was wild wheat domesticated? Science
311, 1886.
Thompson, G.B. (1996) The Excavations of Khok Phanom Di, A Prehistoric Site in Central
Thailand. Volume IV. Subsistence and Environment: The Botanical Evidence. The Biological
Remains Part III. The Society of Antiquaries of London, London.
Thompson, G.B. (1997) Archaeobotanical indicators of rice domestication – a critical
evaluation of diagnostic criteria. South-East Asian Archaeology 1992. Instituto Italiano
per L’Africa e L’Orient, Rome, pp 159–174.
Seed Dispersal and Crop Domestication 293
Turner, A., Beales, J., Faure, S., Dunford, R.P. and Laurie, D.A. (2005) The pseudoresponse regulator Ppd-H1 provides adaptation to photoperiod in barley. Science
310, 1031–1034.
Upadhyaya, H.D., Kumar, S., Gowda, S.L.L. and Singh, S. (2006) Two major genes for
seed size in chickpea (Cicer arietinum L.). Euphytica 147, 311–315.
Van Zeist, W. and Bakker-Heeres, J.H. (1985) Archaeobotanical studies in the Levant
1. Neolithic sites in the Damascus Basin: Aswad, Ghoraife, Ramad. Palaeohistoria
24, 165–256.
Vanhala, T.K. and Stam, P. (2006) Quantitative trait loci for seed dormancy in wild
barley (Hordeum spntaneum C. Koch). Genetic Resources and Crop Evolution 53, 1013–
1019.
Vaughan, D.A., Lu, B.-R. and Tomooka, N. (2008) The evolving story of rice evolution.
Plant Science 174, 394–408.
Wan, J.M., Jiang, L., Tang, J.Y., Wang, C.M., Hou, M.Y., Jing, W. and Zhang, L.X. (2005)
Genetic dissection of the seed dormancy trait in cultivated rice. (Oryza sativa L.).
Plant Science 170, 786–792.
Wasylikowa, K., Barakat, H.N., Boulos, L., Butler, A., Dahlberg, J.A., Hather, J. and
Mitka, J. (2001) Site E-75-6: vegetation and subsistence of the early neolithic at Nabta
Playa, Egypt, reconstructed from charred plant remains. In: Holocene Settlement of
the Egyptian Sahara: Volume 1: The Archaeology of Nabta Playa (eds F. Wendorf and R.
Schild). Kluwer/Plenum, New York, pp 544–591.
Wasylikowa, K., Mitka, J., Wendorf, F. and Schild, R. (1997) Exploitation of wild plants
by the early neolithic hunter–gatherers in the Western Desert of Egypt: Nabta Playa
as a case-study. Antiquity 71, 932–941.
Wasylikowa, K., Schild, R., Wendorf, F., Krolik, H., Kubiak-Martens, L. and Harlan,
J.R. (1995) Archaeobotany o the early neolithic site E-75–6 at Nabta Playa, Western
Desert, South Egypt (preliminary results). Acta Palaeobotanica 35, 133–155.
Weber, S.A. (1991) Plants and Harappan Subsistence. An Example of Stability and Change
from Rojdi. Oxford and IBH, New Delhi.
Weeden, N.F. (2007) Genetic changes accompanying the domestication of Pisum
sativum: Is there a common genetic basis to the ‘Domestication Syndrome’ for
Legumes? Annals of Botany 100(5), 1017–1025.
Weeden, N.F., Brauner, S. and Przyborowski, J.A. (2002) Genetic analysis of pod
dehiscence in pea (Pisum sativum L.). Cellular and Molecular Biology Letters 7, 657–663.
Weiss, E., Kislev, M.E. and Hartmann, A. (2006) Autonomous cultivation before domestication. Science 312, 1608–1610.
Westoby, M., Leishman, M. and Lord, J. (1996) Comparative ecology of seed size
and dispersal. Philosophical Transactions of the Royal Society B: Biological Sciences 351,
1309–1318.
White, C., Proebsting, W.M., Hedden, P. and Rivin, C.J. (2000) Giberellins and seed development. I. Evidence that gibberellin/abscissic acid balance governs germination
versus maturation pathways. Plant Physiology 122, 1081–1088.
White, C. and Rivin, C.J. (2000) Giberellins and seed development. II. Giberellin synthesis inhibition enhances abscisic acid signalling in culture embryos. Plant Physiology 122, 1088–1097.
Wilke, P.J., Bettinger, R., King, T.F. and O’Connell, J.F. (1972) Harvest selection and
domestication in seed plants. Antiquity 46, 203–209.
Willcox, G. (1992) Some differences between crops of Near Eastern origin and those
from the tropics. In: South Asian Archaeology 1989 (ed. C. Jarrige). Prehistory Press,
Madison, pp 291–299.
294 Fruit Development and Seed Dispersal
Willcox, G. (1999) Agrarian change and the beginnings of cultivation in the Near East:
evidence from wild progenitors, experimental cultivation and archaeobotanical
data. In: The Prehistory of food. Appetites for Change (eds C. Gosden and J. Hather).
Routeledge, London, pp 478–500.
Willcox, G. (2004) Measuring grain size and identifying near eastern cereal domestication: evidence from the Euphrates valley. Journal of Archaeological Science 31,
145–150.
Willcox, G. (2005) The distribution, natural habitats and availability of wild cereals in
relation to their domestication in the Near East: multiple events, multiple centres.
Vegetation History and Archaeobotany 14, 534–541.
Willcox, G., Fornite, S. and Herveux, L. (2008) Early Holocene cultivation before
domestication in northern Syria. Vegetation History and Archaeobotany 17, 313–
325.
Worland, A.J., Börner, A., Korzun, V., Li, W.M., Petrvı́c, S. and Sayers, E.J. (1998) The
influence of photoperiod genes on the adaptability of European winter wheats.
Euphytica 100, 385–394.
Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C.,
Li, X. and Zhang, Q. (2008) Natural variation in Gdh7 is an important regulator of
heading date and yield potential in rice. Nature Genetics 40, 761–767.
Yamamoto, T., Lin, H.X., Sasaki, T. and Yano, M. (2000) Identification of heading date
quantitative trait locus Hd6 and characterization of its epistatic interactions with
Hd2 in rice using advance backcross progeny. Genetics 154, 885–891.
Yan, L., Fu, D., Li, C., Blechl, A., Tranquilli, G., Bonafede, M., Sanchez, A., Valarik,
M., Yasuda, S. and Dubcovsky, J. (2006) The wheat and barley vernalization gene
VRN3 is an orthologue of FT. Proceedings of the National Academy of Sciences USA
103, 19581–19586.
Yan, L., Helguera, M., Kato, K., Fukuyama, S., Sherman, J. and Dubcovsky, J. (2004b)
Allelic variation at the VRN-1 promoter region in polyploidy wheat. Theoretical and
Applied Genetics 109, 1677–1686.
Yan, L., Loukoianov, A., Blechl, A., Tranquilli, G., Ramakrishna, W., San Miguel,
P., Bennetzen, J.L., Echenique, V. and Dubcovsky, J. (2004a) The wheat VRN2
gene is a flowering repressor down-regulated by vernalization. Science 303, 1640–
1644.
Yan, L., Loukoianov, A., Tranquilli, G., Helguera, M., Fahima, T. and Dubcovsky, J.
(2003) Positional cloning of the wheat vernalization gene VRN1. Proceedings of the
National Academy of Sciences USA 100, 6263–6268.
Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba,
T., Yamamoto, K., Umehara, Y., Nagamura, Y. and Sasaki, T. (2000) Hd1, a major
photoperiod sensitivity quantitative trait locus in rice, is closely related to the
Arabidopsis flowering time gene CONSTANS. The Plant Cell 12, 2473–2483.
Zach, B. and Klee, M. (2003) Four thousand years of plant exploitation in the Chad
Basin of NE Nigeria II: discussion on the morphology of caryopses of domesticated
Pennisetum and complete catalogue of the fruits and seeds of Kursakata. Vegetation
History and Archaeobotany 12, 187–204.
Zeder, M. (2006) Central questions in the domestication of plants and animals. Evolutionary Anthropology 15, 105–117.
Zeder, M.A. (2008) Domestication and early agriculture in the Mediterranean Basin:
origins, diffusion, and impact. Proceedings of the National Academy of Sciences USA
105(33), 11597–11604.
Seed Dispersal and Crop Domestication 295
Zhao, T., Ni, Z., Dai, Y., Yao, Y., Nie, X. and Sun, Q. (2006) Characterization and
expression of 42 MADS-box genes in wheat (Triticum astivum L.). Molecular Genetics
and Genomics 276, 334–350.
Zheng, Y., Jaing, L. and Zheng, J. (2004) Study on the remains of ancient rice from
Kuahuqiao Aite in Zhejiang Province. Chinese Journal of Rice Science 18, 119–124 [in
Chinese].
Zheng, Y., Sun, G. and Chen, X. (2007) Characteristics of the short rachillae of rice from
archaeological sites dating to 7000 years ago. Chinese Science Bulletin 52, 1654–1660.
Zohary, D. (1969) The progenitors of wheat and barley in relation to domestication
and agriculture dispersal in the Old World. In: The Domestication and Exploitation
of Animals and Plants (eds P.J. Ucko and G.W. Dimbleby). Duckworth, London, pp
47–66.
Zohary, D. (1989) Pulse and cereal domestication: how different are they? Economic
Botany 43(1), 31–34.
Zohary, D. (2004) Unconscious selection and the evolution of domesticated plants.
Economic Botany 58(1), 5–10.
Zohary, D. and Hopf, M. (1973) Domestication of pulses in the Old World. Science 182,
887–894.
Zohary, D. and Hopf, M. (2000) Domestication of Plants in the Old World, 3rd edn.
Oxford University Press, Oxford.