Early integration of pastoralism and millet cultivation in Bronze Age Eurasia

Mobile pastoralists are thought to have facilitated the first trans-Eurasian dispersals of domesticated plants during the Early Bronze Age (ca 2500–2300 BC). Problematically, the earliest seeds of wheat, barley and millet in Inner Asia were recovered from human mortuary contexts and do not inform on local cultivation or subsistence use, while contemporaneous evidence for the use and management of domesticated livestock in the region remains ambiguous. We analysed mitochondrial DNA and multi-stable isotopic ratios (δ13C, δ15N and δ18O) of faunal remains from key pastoralist sites in the Dzhungar Mountains of southeastern Kazakhstan. At ca 2700 BC, Near Eastern domesticated sheep and goat were present at the settlement of Dali, which were also winter foddered with the region's earliest cultivated millet spreading from its centre of domestication in northern China. In the following centuries, millet cultivation and caprine management became increasingly intertwined at the nearby site of Begash. Cattle, on the other hand, received low levels of millet fodder at the sites for millennia. By primarily examining livestock dietary intake, this study reveals that the initial transmission of millet across the mountains of Inner Asia coincided with a substantial connection between pastoralism and plant cultivation, suggesting that pastoralist livestock herding was integral for the westward dispersal of millet from farming societies in China.


Comments to the Author
The RSPB-2019-1273 manuscript is extremely important contribution to our current knowledge, allowing to understand not only when but also how the earliest food globalisation processes took place across Eurasia. This discovery pinpoints the earliest contact routs that initially linked the western and eastern Eurasia, paving the roads of interaction for future historical networks such as Silk Road. This manuscript is of outstanding importance, scientifically solid and it will be heavily cited in the future, therefore I strongly recommend to a journal accepting it for publication. I have a few recommendations for the authors to consider while preparing the final submission of this work. Firstly, I would advise them to sharpen the abstract, pointing out more clearly the significance of this work and the application of novel methodology for the first time to pinpoint the earliest consumption of cultivated crops by domestic cattle, at the same time emphasizing the importance of understanding these processes in central Asia. In addition, in the same abstract the sentence on ritual use of crops should be removed/rephrased as previous studies had only suggested it as a possibility, but no one has actively studied it. In addition, the authors do not really talk about it later on in the text and do not contrast their discoveries against the ritual use of plants. It is still puzzling to me how come no crop chaff remains were found in the early sites of Dzhungaria if potentially ovicaprids were eating it. If there is any phytolith work please mention. Can you elaborate on it instead of calling it "exotica"?
In the text: Hordeum vulgare normally means Hulled barley, while the earliest barley in the region is naked varieties Hordeum vulgare var. nudum. So I would suggest just using Hordeum spp. or just barley to be correct. In addition, I would also stay away from contracting nomadic central Asian populations with other societies living on the other ends of Eurasia as if the central Asian ones are somehow unique. Firstly, no study has really provided evidence on how mobile they really were, whether all population were mobile or just a few shepherds were moving around, and the rest are staying in winter cam all year round and growing crops. Also, there are semi mobile populations pretty much everywhere where there are domestic ovicaprids and cattle (Near East including), so central Asia in this sense is not unique.
Also to be precise in the scientific publication, I would recommend to avoid using words "identical" (line 109), maybe better statistically the same; "massive migration" (line 401), how massive is massive? Unfortunately, I was not able to see the supplementary material, but hope somewhere authors explain how they calculate the percentages of millet dietary intake, this is important to expain to the reder.
Few more comments: Reference "22" is not the best here I do not understand sentence in Line 245-247. Also please use δ next to 13C Various water stress experiments on plants also on plants growing in higher elevations do increase the δ13C values. Maybe authors have to mention this in the text in a few sentences. Is it not better to use wild boar instead of wild pig in Fig. 2? Also it is not clear from the graph or the described methodology how did you make enamel compatible to collagen. Please add the sentence in methodology on it (unless it is in SOM).
In the text, in methodology is not clear if you are making the calculations on C4 dietary intake from collagen or apatite, and if from both, how do you calculate the offset values. There is just a minor comments and the rest of methodology is clear and solid.
In the discussion, if you are talking about early iron age populations, the Scythians should not be the only people group that deserve mentioning. I also would ask you to clarify sentence in lines 391-392. Maybe the authors in the discussions could also elaborate how millet got all the way to Kazakhstan territory without the aid of pastoral societies (as ancient Chinese did not domesticate cattle or sheep/goat) and that pastoralism is not the only mean of crop translocation.
The separate conclusion will allow to pinpoint the outstanding contribution of this article.

Recommendation
Accept as is Comments to the Author Using stable isotope and aDNA data, this article argues that initial domesticated crops, specifically millet, were cultivated and dispersed by pastoralists along the Inter Asian Mountain Corridor. This paper is of high quality and scientific importance. The methodology is solid and the overall argument is persuasive. Most of my suggestions are for how the authors could make the paper more accessible to readers who do not work in this region. The archaeological background and discussion and conclusion sections are especially in need of more contextual information to make this article of general interest to larger audiences.
1. Introduction. The opening paragraph is a little misleading in that it emphasizes the use of initial crop domesticates in mortuary contexts over the argument that is explored throughout the rest of the paper-that pastoralists spread these crops via their agricultural/economic processes. The authors might consider moving this part (lines 66-71) to the background section as part of their larger discussion of prehistoric development in the IAMC.
2. Archaeological Background. If the argument is that pastoralism precedes millet cultivation, it would make more sense to present the material chronologically and reverse the two paragraphs in this section (so paragraph 2 before paragraph 1). This rearrangement would help to establish the archaeological context of the region before introducing the specific goals of this paper. The authors might also consider similarly rearranging the introduction to help with flow and clarity (and see above).
3. Materials and Methods. a. line 126: Could you briefly elaborate on how previous faunal data clearly indicate intensive exploitation of pastoralist livestock? b. Considering the wide range of material that was analyzed for stable isotopes (collagen, apatite, enamel, hair), I would appreciate a brief explanation either in the paper or supplemental material of how or why they can be directly compared. I'm specifically thinking of Figure 2 where all of these materials are graphed using the same y-axis. The potential links between these agropastoral practices and processes of cultural transmission should be better explained. In general this paper does a great job of interpreting results at the site/subsistence level, but doesn't fully explain the larger significance of these results or how they might articulate with other developments in this region/time period.
6. Small Details a. line 53: Sentence is missing "of" b. lines 95-99: This sentence should be rewritten for clarity c. line 312: Figure 4H? d. lines 333-334: "alter" used twice in one sentence e. line 362: "Corresponds" or something similar instead of "resonate" f. Both BC and BCE are used at different points g. The use of "agronomic" as a descriptor for economic practices throughout this paper is not one I'm familiar with (American English). A different word would be better. h.
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The Proceedings B Team mailto: proceedingsb@royalsociety.org Comments to Author: Your study has been seen by 3 expert reviewers and all agree that there is interesting and sound science here that is appropriate for Proc B's broad audience, which I concur with. There are numerous very constructive points to account for in revisions, but all of these seem very achievable. We look forward to seeing your revised manuscript. Kind regards Prof. John Hutchinson, Editor Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s) The RSPB-2019-1273 manuscript is extremely important contribution to our current knowledge, allowing to understand not only when but also how the earliest food globalisation processes took place across Eurasia. This discovery pinpoints the earliest contact routs that initially linked the western and eastern Eurasia, paving the roads of interaction for future historical networks such as Silk Road. This manuscript is of outstanding importance, scientifically solid and it will be heavily cited in the future, therefore I strongly recommend to a journal accepting it for publication. I have a few recommendations for the authors to consider while preparing the final submission of this work. Firstly, I would advise them to sharpen the abstract, pointing out more clearly the significance of this work and the application of novel methodology for the first time to pinpoint the earliest consumption of cultivated crops by domestic cattle, at the same time emphasizing the importance of understanding these processes in central Asia. In addition, in the same abstract the sentence on ritual use of crops should be removed/rephrased as previous studies had only suggested it as a possibility, but no one has actively studied it. In addition, the authors do not really talk about it later on in the text and do not contrast their discoveries against the ritual use of plants. It is still puzzling to me how come no crop chaff remains were found in the early sites of Dzhungaria if potentially ovicaprids were eating it. If there is any phytolith work please mention. Can you elaborate on it instead of calling it "exotica"?
In the text: Hordeum vulgare normally means Hulled barley, while the earliest barley in the region is naked varieties Hordeum vulgare var. nudum. So I would suggest just using Hordeum spp. or just barley to be correct. In addition, I would also stay away from contracting nomadic central Asian populations with other societies living on the other ends of Eurasia as if the central Asian ones are somehow unique. Firstly, no study has really provided evidence on how mobile they really were, whether all population were mobile or just a few shepherds were moving around, and the rest are staying in winter cam all year round and growing crops. Also, there are semi mobile populations pretty much everywhere where there are domestic ovicaprids and cattle (Near East including), so central Asia in this sense is not unique.
Also to be precise in the scientific publication, I would recommend to avoid using words "identical" (line 109), maybe better statistically the same; "massive migration" (line 401), how massive is massive? Unfortunately, I was not able to see the supplementary material, but hope somewhere authors explain how they calculate the percentages of millet dietary intake, this is important to expain to the reder. Few more comments: Reference "22" is not the best here I do not understand sentence in Line 245-247. Also please use δ next to 13C Various water stress experiments on plants also on plants growing in higher elevations do increase the δ13C values. Maybe authors have to mention this in the text in a few sentences. Is it not better to use wild boar instead of wild pig in Fig. 2? Also it is not clear from the graph or the described methodology how did you make enamel compatible to collagen. Please add the sentence in methodology on it (unless it is in SOM).
In the text, in methodology is not clear if you are making the calculations on C4 dietary intake from collagen or apatite, and if from both, how do you calculate the offset values. There is just a minor comments and the rest of methodology is clear and solid.
In the discussion, if you are talking about early iron age populations, the Scythians should not be the only people group that deserve mentioning. I also would ask you to clarify sentence in lines 391-392. Maybe the authors in the discussions could also elaborate how millet got all the way to Kazakhstan territory without the aid of pastoral societies (as ancient Chinese did not domesticate cattle or sheep/goat) and that pastoralism is not the only mean of crop translocation.
The separate conclusion will allow to pinpoint the outstanding contribution of this article.

Referee: 2
Comments to the Author(s) I find this manuscript acceptable for publication just as it is.
Referee: 3 Comments to the Author(s) Using stable isotope and aDNA data, this article argues that initial domesticated crops, specifically millet, were cultivated and dispersed by pastoralists along the Inter Asian Mountain Corridor. This paper is of high quality and scientific importance. The methodology is solid and the overall argument is persuasive. Most of my suggestions are for how the authors could make the paper more accessible to readers who do not work in this region. The archaeological background and discussion and conclusion sections are especially in need of more contextual information to make this article of general interest to larger audiences.
1. Introduction. The opening paragraph is a little misleading in that it emphasizes the use of initial crop domesticates in mortuary contexts over the argument that is explored throughout the rest of the paper-that pastoralists spread these crops via their agricultural/economic processes. The authors might consider moving this part (lines 66-71) to the background section as part of their larger discussion of prehistoric development in the IAMC.
2. Archaeological Background. If the argument is that pastoralism precedes millet cultivation, it would make more sense to present the material chronologically and reverse the two paragraphs in this section (so paragraph 2 before paragraph 1). This rearrangement would help to establish the archaeological context of the region before introducing the specific goals of this paper. The authors might also consider similarly rearranging the introduction to help with flow and clarity (and see above).
3. Materials and Methods. a. line 126: Could you briefly elaborate on how previous faunal data clearly indicate intensive exploitation of pastoralist livestock? b. Considering the wide range of material that was analyzed for stable isotopes (collagen, apatite, enamel, hair), I would appreciate a brief explanation either in the paper or supplemental material of how or why they can be directly compared. I'm specifically thinking of Figure 2 where all of these materials are graphed using the same y-axis. The potential links between these agropastoral practices and processes of cultural transmission should be better explained. In general this paper does a great job of interpreting results at the site/subsistence level, but doesn't fully explain the larger significance of these results or how they might articulate with other developments in this region/time period.
6. Small Details a. line 53: Sentence is missing "of" b. lines 95-99: This sentence should be rewritten for clarity c. line 312: Figure 4H? d. lines 333-334: "alter" used twice in one sentence e. line 362: "Corresponds" or something similar instead of "resonate" f. Both BC and BCE are used at different points g. The use of "agronomic" as a descriptor for economic practices throughout this paper is not one I'm familiar with (American English). A different word would be better. h. Supplemental Files 4-6 should be standardized so that %C, %N, and C:N results are included in all of them.

Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No
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Comments to the Author Publish as it is, the authors have done great job responding to our comments and have improved the manuscript significantly.

Review form: Reviewer 2
Recommendation Accept as is

Quality of the paper: Is the overall quality of the paper suitable? Excellent
Is the length of the paper justified? Yes

Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No
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RSPB-2019-1273
Early integration of pastoralism and millet cultivation in Bronze Age Eurasia Hermes et al. --

Dear Reviewers,
Thank you for your thoughtful and helpful comments for improving our manuscript. Below, we copied your points of criticism and highlighted this text in grey. After each point, we responded in normal text. The "tracked changes" versions of the manuscript and SI are at the end of this response document.
Both Reviewers 1 and 3 commented on our calculation of dietary δ 13 C values from δ 13 C values of different tissues from different taxa, allowing these data to be displayed on a single Y-axis in figure 2. We have the diet-tissue spacing factors for making these conversions in the Supplementary Information and relevant citations that establish their validity. Since this information is somewhat tedious to read in the manuscript and the journal has strict page limits, which we are at risk of exceeding, we decided to place this information in the SI. To clarify, we emphasized in the manuscript's Methods section and in the caption of figure 2 that the diettissue spacing factors are in SI text 2. We hope this balances the desire to have this information accessible with the consideration for not taking up too much space in the manuscript.
I would like to point out that I found some minor counting errors of our raw data that touched on the presentation of aDNA sequence recovery and statistical analysis of the isotopic data. Specifically, one aDNA sequence was counted twice, bringing the revised total number of recovered cytochrome b sequences to 79 from 80, which also changed the number of recovered cytochrome b sequences of domesticated sheep and goat to 77 from 78. Furthermore, the taxonomic classification of one Siberian ibex specimen for the isotopic analysis was incorrectly marked as a domesticated caprine, which affected figure 4b and the calculation of Pearson's r and Mann-Whitney U. The numerical differences were negligible, for example, a p-value shifting by 0.0001. I scrutinized the entire dataset of our study for other errors and reran the analyses for inconsistencies. I did not find further issues.
I decided to prune out a subset of human isotopic data displayed in figure S6-7 (now, dataset S5) because these were predominately dated to the later Iron Age and medieval period and were inconsistent with the chronological scope of our study. The change reduces the number of human samples from 220 to 174. This reduction does not affect the main finding of this analysis, which is that human isotopic data are too sparse to evaluate the uptake of millet as a dietary component by people in the steppe zone during the third millennium BC. The data reduction also removed some references, helping our paper fall below the 10-page limit.
We hope our responses below and improvements to the manuscript satisfy your concerns with our study. Thank you very much for your time and effort reviewing our paper. Sincerely,

Taylor Hermes
Appendix A --Referee: 1 Firstly, I would advise them to sharpen the abstract, pointing out more clearly the significance of this work and the application of novel methodology for the first time to pinpoint the earliest consumption of cultivated crops by domestic cattle, at the same time emphasizing the importance of understanding these processes in central Asia. In addition, in the same abstract the sentence on ritual use of crops should be removed/rephrased as previous studies had only suggested it as a possibility, but no one has actively studied it. In addition, the authors do not really talk about it later on in the text and do not contrast their discoveries against the ritual use of plants. It is still puzzling to me how come no crop chaff remains were found in the early sites of Dzhungaria if potentially ovicaprids were eating it. If there is any phytolith work please mention. Can you elaborate on it instead of calling it "exotica"?
Reply: Thank you for the suggestion to improve the visibility of the significance of our study in the abstract. Here, we made edits to downplay the ritual use of the seeds by putting this information into a separate sentence where we indicate to the reader that this is simply the best we know about how these crops were used, while also explaining that the mortuary context of the seeds does not inform on cultivation or subsistence. We also added a clause to the end of the abstract explaining that our study suggests that pastoralist livestock were critical for the westward transmission of millet in order to introduce the broader significance of the work. In the Discussion, this argument is fleshed out in the context of early Chinese societies developing millet agriculture without domesticated herbivores, so it is the arrival of these livestock that facilitates the spread of millet agriculture.
To date, there is little phytolith work done on sites in the Dzhungar Mountains. A small study was conducted by Breadmore and published in Doumani et al. 2015. The results of the phytolith work do not inform on the use of domesticated plants due to significant overlap of phytolith morphotypes between plant families that include cultivated crops and wild taxa. Thus, it is not worthwhile to mention this work and would require a considerable amount of text to explain why. Overall, the absence of crop chaff is indeed intriguing. Presumably, these plant parts could have been deposited archaeologically through the burning of dung from animals foddered with crops (if they were fed stalks with seeds), however, floatation work by Spengler has found very little crop by-product in hearth sediments from Begash and Tasbas. However, Spengler did report numerous rachises from mudbricks at Tasbas during the late Bronze Age phase. Ojakly in Turkmenistan also gave a number of rachises. Taken together, the frequent absence of crop byproducts in the macrobotanical assemblages suggests the combined effects of taphonomy and archaeological deposition leading to poor recovery. As mentioned in the Background section of our paper, pastoralists sites are often ephemeral and dispersed, even in the IAMC up to the Iron Age, when communities began living in large villages. There however, crop processing was likely taking place off-site, as evidenced by an abundant carbonized seed record but an absence of crop by-products.
We took out "exotica" and replaced it with "goods", which we think is more neutral and straightforward term. While you and Reviewer 3 suggested to move down the text explaining that the earliest domesticated seeds in Inner Asia were recovered from mortuary contexts, we firmly believe that this information is critical for establishing the research problem that these early seed remains do not inform on subsistence or local cultivation. We greatly prefer to keep this text in the introduction, so we clarified the research problem here, which provides a better transition to the sentence introducing the dispersal model that we explore with our study.
Hordeum vulgare normally means Hulled barley, while the earliest barley in the region is naked varieties Hordeum vulgare var. nudum. So I would suggest just using Hordeum spp. or just barley to be correct.

Reply:
We changed this to "Hordeum spp." to represent both the hulled and naked forms that are in the macrobotanical assemblages of the sites.
In addition, I would also stay away from contracting nomadic central Asian populations with other societies living on the other ends of Eurasia as if the central Asian ones are somehow unique. Firstly, no study has really provided evidence on how mobile they really were, whether all population were mobile or just a few shepherds were moving around, and the rest are staying in winter cam all year round and growing crops. Also, there are semi mobile populations pretty much everywhere where there are domestic ovicaprids and cattle (Near East including), so central Asia in this sense is not unique.
Reply: This is a good point, and we agree that in principle there is too much conceptual baggage in contrasting Inner Asian herding communities from sedentary communities without a clearer understanding of the precise modes of mobility and labor stratification in subsistence activities. We removed "sedentary" to describe societies at either end of Eurasia who got crops that were domesticated from distant centers of domestication.
Also to be precise in the scientific publication, I would recommend to avoid using words "identical" (line 109), maybe better statistically the same; "massive migration" (line 401), how massive is massive?
Reply: We changed to "indistinguishable genetic variation", which is a concept used by the archaeogeneticists of the cited literature. The use of the term "massive" to describe migrations in our paper is borrowed from the archaeogeneticists, which are cited. We do not agree with their characterization of the magnitude of these migrations, so we qualified it in the manuscript using "so-called".

Reply:
The delta sign is not necessary here because the process described in this sentence explains how plants come to be characterized by higher δ 13 C values. That is, it is due to a higher relative abundance of carbon-13 (thus, enriched in carbon-13) by recycling carbon dioxide as a result of reduced stomatal conductance. For higher δ 13 C values in plants going up an elevational gradient, this effect is caused by increased enzymatic efficiency due to reduced partial pressure of carbon dioxide at higher elevations. We added two key citations to this sentence (Tieszen et al. 1991 andKörner et al. 1991) that are foundational for understanding the carbon isotopic variation in plants affected by water use efficiency and altitudinal effects. Because the Dzhungar mountains receive large amounts of precipitation at altitudes between 500 and 3500 m a.s.l., unlike parts of the Tian Shan in Kyrgyzstan affected by rain shadows, we have no expectation to have appreciable levels of water use efficiency in plants in mountain pastures. Likewise, higher precipitation in mountains tends to counteract the carbon-13 enrichment from partial pressure effects at altitude, per Tieszen et al. 1991.
Is it not better to use wild boar instead of wild pig in Fig. 2? Also it is not clear from the graph or the described methodology how did you make enamel compatible to collagen. Please add the sentence in methodology on it (unless it is in SOM).
In the text, in methodology is not clear if you are making the calculations on C4 dietary intake from collagen or apatite, and if from both, how do you calculate the offset values. There is just a minor comments and the rest of methodology is clear and solid.
Reply: Yes, thank you for catching this inconsistency for the boar. We changed the figure to show "wild boar". The methods of calculating dietary δ 13 C values from various animal tissues (diet-tissue spacing) are described in the Supplementary Information (SI) due to page limit constraints. We think this is an appropriate place for those interested to locate these details about our methods. We added a note in the figure caption explaining where these offset values are located in the SI.
In the discussion, if you are talking about early iron age populations, the Scythians should not be the only people group that deserve mentioning. I also would ask you to clarify sentence in lines 391-392.

Reply:
We added a note that these Iron Age populations are diverse and are commonly described as Scythian or Saka agro-pastoralists, and we also added "Wusun," which we think nicely avoids the essentialist cultural groupings while still allowing readers to understand the cultural conventions for this period. We also clarified the sentence about Afanasievo groups perhaps being responsible for simultaneous or even earlier transmissions of domesticated herbivores to the Dzhungar Mountains, although our results suggest a southern source. We cannot tease apart the precise wave of transmission at this time.
Maybe the authors in the discussions could also elaborate how millet got all the way to Kazakhstan territory without the aid of pastoral societies (as ancient Chinese did not domesticate cattle or sheep/goat) and that pastoralism is not the only mean of crop translocation.

Reply:
We make a specific remark about this process in the Discussion section by stating that pastoralists must have been already well-connected throughout western China and likely played an integral role in accelerating millet westward. We mention this in the context of ancient Chinese societies not having indigenously domesticated herbivores, so millet probably moved westward slowly until pastoralist livestock were integrated into millet-based subsistence. We further emphasized this point in the text, by postulating that pastoralists may have advanced to Gansu at the same time that millet farming societies had also reached that region. After this potential contact is the time when millet likely accelerated westward.
The separate conclusion will allow to pinpoint the outstanding contribution of this article.
Reply: Thank you for this suggestion, we added a concise conclusion explaining the greater significance of the paper, especially in terms of our methodology.