Continuous presence of proto-cereals in Anatolia since 2.3 Ma, and their possible co-evolution with large herbivores and hominins
Vegetation history of the Acıgöl areaOur palynological analyses of 72 regularly spaced samples show a diversified vegetal landscape alternately wooded and open, in response to orbitally driven climatic cyclicity. However, arboreal pollen values remain almost constantly below 50% of the Pollen Sum (PS) (average 27.5%, median 22.8%), which corresponds to an overall open landscape (Fig. 3). Among herbaceous plants, the dominant taxa are steppics such as Artemisia, heliophilous and halophilous taxa including Calystegia, several Compositae, Convolvulus, Linum, Plantago ssp., Poaceae and Chenopodiaceae that could develop on the saline shores of Acıgöl lake during evaporitic periods. Forests are composed of a mixture of conifers, Mediterranean Pinus, Abies, Cedrus, Cupressaceae and Picea, associated with broadleaved trees dominated by Mediterranean oaks, i.e. deciduous and evergreen Quercus, with some Olea. Riverine trees such as Alnus, Salix, Populus, Tamarix, Juglans and Platanus have also been identified. Few Tertiary or megathermic relictual taxa (Carya, Liquidambar, Parrotia, Pterocarya fraxinifolia, Taxodiaceae, Tsuga, Zelkova) were identified so far in the pollen assemblages, mostly before 2.2 Ma, due to climatic cooling17,18 since the end of Tertiary which led to a decline in global biodiversity19,20.Figure 3Simplified pollen and NPP diagram in percentages of Acıgöl, core 3, based on the age model of Demory et al. [1]. Equidistant scale. Values are in percentages calculated on a pollen sum without Non-Pollen Palynomorphs (NPP), Ferns, Bryophytes and Algae. The beige rectangle corresponds to the date of the presence of Homo erectus at Kocabaş (Lebatard et al. [4]).Full size imageThe vast freshwater stretch of Acıgöl, located in a predominantly arid limestone hills environment, seems to have been a crucial resource for the mammalian fauna, which probably concentrated around the site in search of water and pastures. Indeed, low percentages of arboreal pollen imply that the landscape remained open throughout the sequence and suggest a marked grazing pressure by herbivores in addition to climatic factors21,22,23.Coprophilous fungi spores, cereals and other ancestors of cultivated plantsCoprophilous fungi spores are excellent indicators of herbivorous mega-mammal herds since they grow exclusively on dung deposited by these animals24. At Acıgöl, a wide variety of coprophilous fungi spores has been identified throughout the pollen record including: Sporormiella sp., Podospora sp., Delitschia sp., Sordaria sp. and Valsaria variospora (Figs. 3, 4). They provide evidence for a continuous presence of large herbivorous mammals around the lake throughout Quaternary.Figure 4Coprophilous fungi spores of Acıgöl, core 3. Equidistant scale. Age model is from Demory et al. [1]. In red: coprophilous fungi taxa..Full size imagePollens of Poaceae, such as Secale (rye) and Cerealia-type, have been identified throughout the sequence (Figs. 3, 5). Unexpectedly, they present the same morphological characteristics as that of modern cereal grains25,26, namely an average size of ≥ 40 µm and a large pore + annulus (≥ 8 µm). As by definition cereals are cultivated plants, we will call the corresponding plants “proto-cereals” to highlight that their pollen are identical to those of cereals. This resemblance can be seen clearly in Fig. 5, where we have brought together fossil cereals from Acιgöl (Fig. 5, photos 1–7), from Roman time (Fig. 5, photo 8), not modified by modern agricultural practices, and from the current wheat field of the Lauragais agricultural plain, Gardouch, France (Fig. 5, photo 9). Cerealia-type frequencies reach a maximum of 9% of the PS around 2.2 Ma and can be as abundant as wild Poaceae pollen (Fig. 3). The Cerealia/Poaceae ratio shows that 24.66% of all Poaceae are proto-cereals from 2.0 to 2.3 Ma (Supplementary Table 1). Such high proto-cereal rates are almost never reached in pollen records, even in recent periods and in the presence of agriculture, because of the very low pollen dispersal capacity of cereals27. A lowering of frequencies down to 2–4% range is recorded in younger periods (Fig. 3), as well as a step like decrease of the Cerealia/Poaceae ratio (Fig. 6). This change may be related to the Middle-Pleistocene Transition (MPT) cooling and to the mega-mammal fauna change from a Villafranchian to a Galerian type28. MPT and faunal changes occurred around 0.9–1.0 Ma, while a decrease in our proto-cereal starts around 1.5 Ma, however signs of cooling and amplified climatic cycles predate the MPT28.Figure 5Pollen grain of Cerealia and Triticum sp. from Acıgöl (ACI), core 3 (photos 1–7), the Roman site of La Verrerie, Arles, France (photo 8) and Gardouch, France, current wheat field (photo 9). Photographies with a photonic (photo 1 – 4 and 8) and a confocal microscope (photos 5-7 and 9). 1) sample ACI 239 m, age: 0.871 Ma. 2) sample ACI 435.50 m, age: 1.709 Ma. 3) sample ACI 532.44 m, age: 2.122 Ma. 4) sample ACI 509.50 m, age: 2.026 Ma. 5) sample ACI 552.57 m, age 2.206. 6) sample ACI 552.57 m, age: 2.206 Ma. 7) sample ACI 429.50 m, age: 1.681 Ma. 8) sample La Verrerie 1455, age: 50-70 BC (Roman). 9) current pollen of Triticum sp., age: 2000 AD. L: maximal length (µm).Full size imageFigure 6Cerealia/Poaceae ratio in %, % cultivated tree ancestors and % Olea of Acıgöl, core 3.Full size imageThe histogram of wild Poaceae and proto-cereal pollen size (Fig. 7a) shows that there are a number of pollen populations modes around 30, 37.5, 45–50, supporting the idea that the larger grain sizes cannot be interpreted as a tail of ‘anomalous’ wild Poaceae pollen. Moreover, comparison with the present-day pollen rain recorded in moss pollsters, sampled around the lake of Acıgöl (Fig. 7b and Supplementary Table 2), show that the large pollen size mode (≥ 40 µm) is nowadays nearly absent (0–0.97% of the PS, Cerealia/Poaceae ratio of 4.52%, Supplementary Tables 3 and 4), even in biotopes with wild Poaceae considered to be ancestors of cereals (Aegilops, sample 2a, cereal rate: 0.97% of the PS) or with cereals such as Hordeum (sample 3a, b and 4, cereal rate 0.31, 0.00, 0.33 of the PS respectively, Supplementary Tables 2 and 3).Figure 7a) Pollen size of wild Poaceae and proto-cereal of Acıgöl, core 3. The measurements were made on the 10 samples with the highest cereal pollen content. A total of 991 grains of pollen were measured. b) Current pollen rain at the Acıgöl lake and surroundings. 8 moss samples were collected and 354 measurements of the longest axis of the wild Poaceae and cereal pollen grain were made.Full size imageOur interpretation is that proto-cereals recorded throughout the Acıgöl sequence derive from wild Poaceae. Their emergence and predominance may have been favoured by the impact of large herbivore herds attracted to Acıgöl lake shores, and through genetic drift. Through the process of trampling, nitrogen enrichment of soils and browsing, large mammal herds could have altered the genotype of proto-cereals naturally present in Acıgöl and thus, favoured the emergence of modern cereals. For genetic reasons, the descendants of these proto-cereals are not represented today among cultivated Poaceae because domestication bottlenecks eliminate genetic variation29.Is there a relationship between the size of proto-cereal pollen and climate? To our knowledge, the genetic literature does not show any relationship between the increase in pollen size and temperature. However, there does seem to be a relationship with atmospheric drought30,31 which is said to have favoured the appearance of polyploidy in certain species of Poaceae. It cannot be excluded that climate has had an influence on the proto-cereal genome, but only the interaction between herds of large herbivores and proto-cereal steppes can explain why proto-cereal pollen has never been found in such abundance elsewhere in Pleistocene pollen records.The ancestors of cultivated trees (Olea sp., Juglans sp., Castanea sp., Corylus sp., Prunus t.), typical of the modern Mediterranean agriculture, are also present in the Acıgöl sequence (Fig. 3 and Supplementary Table 5). Their amount increases after 1.5 Ma, mainly due to Olea (Fig. 6). Other potentially edible plants such as Ephedra, Hippophae, all the Compositae and the Fagaceae have been identified in the pollen assemblages. They correspond to 54.4% of plants identified in the pollen assemblages. Among these plants, there are 72% grasses and 28% trees and, among edible organs, 51% are vegetables and 20% are seeds (Supplementary Fig. 1a,b). These results testify to the potential wealth of accessible food resources that human and animal populations could feed on. Interestingly, studies carried out in Spain on the present-day consumption of wild plants lead to results close to those obtained at Acıgöl, with 87% grasses and 13% trees32.In recent years, new biological and archaeological data obtained from sites with human occupation have improved our knowledge of the beginnings of agriculture and the modalities of its implementation. In the Levant, the Ohalo II site highlights the presence of proto-cereal seeds, and flint tools to harvest, as early as 23,000 years before the present33. Further north, on the archaeological site of Gesher Benot Ya’aqov, proto-cereal seeds (oats, Avena) as well as pollen from cereals and trees currently cultivated, were identified over a period ranging from 750,000 to 820,000 years34,35. Moreover, recent genetic data indicate that the emergence of agriculture did not occur at a single location at the onset of the Neolithic (e.g. the “Fertile Crescent” hypothesis) but is, on the contrary, an evolutionary and multi-regional long-term phenomenon36,37,38. Alternatively, or simultaneously, are the hominins also partly responsible by having developed episodes of a form of transitory “proto-agriculture”? We already know that this domestication process was discontinuous with shutdown and restart phases37,39. Acheulean lithic tools, characterised by symmetrically shaped bifaces, testify to the rather advanced cognitive capacities of early Pleistocene populations that may have visited the lakeshore of Acıgöl5. Hominin populations may also have benefited from this opportunity to diversify their food regime with easily harvested and nutrient-rich wild plants (Supplementary Table 5), as it is the case today for hunter-gatherer populations in Africa and elsewhere in the world. More
