Pulse Domestication and Cereal Domestication: How Different are They? 1

DANIEL ZOHARY 2

Evidence is brought to indicate that the domestication of lentil and pea & not very different from that of wheat and barley. All these Near East crops are char- acterized by basically the same domestication traits the key elements of which are breakdown of the wild mode of seed dispersal and loss of germination regulation. It is argued that both in the pulses and in the cereals these traits evolved in the same way. The changes are best explained by assuming that mutations causing the loss of the wild-type adaptations were automatically selected for soon after people transferred the wild progenitors into a system of planting and reaping.

In a recent paper published in this journal, Dr. G. Ladizinsky (1987) treats the domestication of the Near East pulses (lentil, pea, chickpea). He arrives at a sweeping conclusion that in this region "the pattern of pulse domestication is completely different from that of cereals." More specifically Ladizinsky proposes that in the lentil (and presumably also in other Old World Neolithic grain legumes), the loss of the wild-type seed dormancy came before, not after, the introduction of these plants into cultivation--this as a result of the gathering activities of people in pre-agricultural times (hence his title "Pulse domestication before cultivation"). To further support this thesis it is argued that because wild pulses display high levels of germination inhibition, plants with the wild-type trait cannot produce rewardful yields under cultivation. Finally Ladizinsky argues that the evolution of pod non-dehiscence (in pulses) was different from the establishment of non- shattering ears (in cereals). The claim is made that pod non-dehiscence was of low value in pulse domestication and that in lentil this trait had very possibly evolved after the crop was well established and widespread.

Ladizinsky's paper warrants the following comments first on differences between the Near East pulses and cereals and second on the following more specific issues: (i) Could non-dormant lines of lentil or other pulses maintain themselves in the wild? (ii) Could the early Neolithic farmers obtain rewarding yields from planting seed still maintaining wild-type dormancy? (iii) How fast would mutations that cause loss of wild-type dormancy or breakdown of seed dispersal establish them- selves in pulse populations raised by sowing and reaping? (iv) Would unconscious selection against these key wild-type traits be similar in pulses and in cereals taken into cultivation?

To answer these questions the following elements should be added to Ladizin- sky's factual evidence. In my opinion they affect considerably one's interpretation.

1. Parallel evolutionary patterns in pulses and cereals under domestication. When the wild progenitors and the cultivated derivatives of the main Near East cereals (wheats, barley) and pulses (lentil, pea) are compared, the immediate impression is not of wide differences but rather of close similarities. All these crops were

J Received 13 July 1987; accepted 3 February 1988. 2 Department of Genetics, The Hebrew University of Jerusalem, Jerusalem 91904, Israel.

Economic Botany, 43(1), 1989, pp. 31-34 �9 1989, by the New York Botanical Garden, Bronx, NY 10458

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taken into cultivation in the same area (the Near East "arc") and in the same time. All were derived from annual, predominately self-pollinated wild progen- itors and the genetic variation in both the wild races and cultivated varieties is structured in the form of true breeding lines. More important, all exhibit parallel adaptations under domestication and have evolved similar domestication syn- dromes in which the key elements are: (i) A breakdown of the wild mode of seed dispersal (brittle ears/dehiscent pods in wild forms vs. non-brittle ears/non-de- hiscent pods in cultivated derivatives); and (ii) A loss of germination regulation, i.e., the breakdown of the wild pattern of seed dormancy. Also the genetic back- ground for these changes is similar. Both in the pulses and in the cereals the loss of each of these wild-type adaptations was usually triggered by a mutation in a single major gene (two genes in barley). At least in terms of end products, the evolution of the main Old World Neolithic cereal and pulse crops appears to be parallel indeed.

2. Fluctuations in seed production. As stressed by Ladizinsky (1987), seed ger- mination in wild pea and wild lentil is spread over numerous years and only a small fraction (10-15%) of the seed produced in the spring germinates in the ensuing fall. Equally important are the extreme fluctuations in annual seed pro- duction. Relatively numerous seeds are produced in favorable, rainy years; only few (sometimes very few) are produced in dry years. These fluctuations occur not only as a direct response to climate. They are brought about also by differential grazing pressures. In favorable years a lush herbaceous biomass develops at the end of the winter and this relaxes grazing considerably. Consequently in such years the fruiting peas and lentils do not suffer severe grazing and they produce numerous seeds. In bad years the herbaceous spring biomass is far less developed and the stress of drought is compounded by severe grazing damage. Consequently seed-set in the wild pulses is drastically reduced; sometimes it is totally ruined. Such extreme decimations (which occur at least once in 5-10 yr) cause very severe selection against any non-dormant line. Once in a few years such lines will be fully or almost fully eliminated.

3. Seed production in wild pulses under tilled conditions. In the last 15 yr I repeatedly planted wild lentil and wild pea in tilled plots in Jerusalem. The seeds were given a single starting irrigation in the fall and were kept free from grazing. At the end of the growing season the planted pulses attained sizes considerably larger than those of their wild-growing parents. They also produced many more seeds. Yield in Lens orientalis were not the ca. 10 seed/plant (the base for Lad- izinsky's evaluation), but four to seven times this value. Similar yields were produced by Pisum humile and P. elatius.

4. Breakdown of the wild mode of seed dispersal. Both in the cereals and in the pulses the wild progenitors differ from the cultivated varieties in the following way: In all wild-type plants (carrying the genes for ear brittleness or for pod dehiscence), a fraction of the seed evades the reaper--this under any (practical) system of harvesting. In contrast, in cultivated forms (carrying mutant alleles determining non-brittleness or non-dehiscence), the mature seeds "'wait" on the plants, at least until the maturation of all fruits. This enables the grower to retrieve practically all seeds. What matters is not the specific harvesting procedures em- ployed or whether the ripe fruits stay on the plants long or short periods of time. Critical is the fact that due to different anatomical structures in the ears or pods,

1989] ZOHARY: PULSE/CEREAL DOMESTICATION 33

losses of seed in wild-type plants are inevitable, while in the mutant lines such losses can be prevented.

Exactly how heavy the losses are in wild-type lentil or in wild-type pea is hard to assess. But losses are considerable, especially when seed maturation coincides with spells of dry and hot weather (a very common situation in the Near East). Under such conditions maturing wild-type pods will dry, split, and scatter their seeds in a matter of one or very few days. When growing Lens orientalis (Boiss.) Hand.-Mazz. or Pisum humile Boiss. et No~ in Jerusalem I tried to secure a maximum harvest by picking the ripe pods individually every 2 or 3 days. Even under such repeated collections, an interval of 1 or 2 hot-and-dry days at the end of the fruiting season often resulted in a loss of a quarter, a third, or even a larger fraction of the entire yield. Seed dispersal in wild lentil or wild pea proceeds as quickly as shattering of ears in wild wheat or wild barley.

These facts do not seem to lend support to the notion of "domestication before cultivation" and to the conclusion that pulse domestication is very different from cereal domestication. A main element in Ladizinsky's proposition is the assump- tion that non-dormant lines of pulses could evolve and maintain themselves in wild stands. But the occurrence of severe reduction (or even total loss) of fruit- set in bad years renders this supposition very unlikely. If such decimations happen every few years, selection against free germinating lines would be so severe that any mutation causing loss of seed dormancy would have little chance to survive in wild populations. The system of self-pollination will further enhance the ef- fectiveness of this elimination. This will be the case regardless of whether man collects these wild pulses or not.

The claim that seed-dormant lines of wild lentil or wild pea are totally yield- unrewarding also needs revision. It was based on seed-set values (10 seed/plant) scored in the wild. But when these wild pulses were planted on tilled ground they produced 4- to 8-fold gains, in spite of the fact that only 10-15% of the seeds germinated. These are admittedly small gains; yet gains they are.

As already argued by Zohary (1969, 1984) and by Harlan et al. (1973), the initiation of sowing and reaping in grain crops brings about an automatic selection for mutations causing the loss of the wild-type germination inhibition. In lentil or pea such selection should be even more effective than in cereals because the pulses' wild-types are characterized by high rates of germination inhibition (85- 90%) compared to 50% in wild wheat. Once a spontaneous mutation, causing the breakdown of germination inhibition, occurred in lentil or pea brought into cul- tivation (the rate of such mutations is probably in the order of 10-6), it would have been strongly selected for. In other words, after the appearance of a mutation, non-dormant lines could have established themselves in a matter of very few years whether the populations grown at that time were large or small.

Observations on seed dispersal lead to similar conclusions: seed dissemination in wild lentil and wild pea proceeds as quickly as the shattering of ears in wild wheat or wild barley. The difficulties in securing the seed in wild-types and the successes in retrieving them from the cultivars are also of the same order. Thus it seems reasonable to assume that the breakdown of the wild mode of seed dispersal in all Neolithic founder seed crops was brought about more or less in the same way. In other words, because of differential loss, mutations causing non- shattering or non-dehiscence could have been automatically selected for soon after

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the introduct ion of these plants into cultivation. The heavier the loss in the wild- type forms, the stronger this selection would have been under the new condit ions o f sowing and reaping.

In conclusion, ra ther than being impressed by the differences between pulse domest ica t ion and cereal domest ica t ion in the Near East, one is struck by the similarities exhibited by these two groups o f grain crops. Fur thermore , on basis o f the available evidence, the thesis that domest ica t ion was initiated by the in- t roduct ion o f the wild progenitors into a system o f sowing and harvest ing (Harlan et al. 1973; Zohary 1969, 1984) applies equally well to the grasses and to the legumes. The available facts are also best explained by the supposi t ion that the responses to this env i ronmenta l shift were s imilar in all crops; and that in both groups unconscious selection caused the b reakdown o f the wild mode o f seed dispersal and the loss o f germinat ion inhibition. O f course there are small differ- ences between the cereals and the pulses, as well as between the var ious crops in each group. Ho weve r these are not different evolut ionary themes. They are just var ia t ions on the same theme.

LITERATURE CITED

Hadan, J. R., J. M. J. de Wet, and E. G. Price. 1973. Comparative evolution in cereals. Evolution 27:311-325.

Ladizinsky, G. 1987. Pulse domestication before cultivation. Econ. Bot. 41:60-65. Zohary, D. 1969. The progenitors of wheat and barley in relation to domestication and agricultural

dispersal in the Old World. Pages 47-66 in P. J. Ucko and G. W. Dimbleby, eds., The do- mestication and exploitation of plants and animals. Duckworth, London.

1984. Modes of evolution in plants under domestication. Pages 579-586 in W. F. Grant, ed., Plant biosystematics. Academic Press, Montreal.