Shifting diets and the rise of male-biased inequality on the Central Plains of during Eastern Zhou

Yu Donga, Chelsea Morganb, Yurii Chinenovc,1, Ligang Zhoud, Wenquan Fane, Xiaolin Maf, and Kate Pechenkinag,1,2

aSchool of History and Culture, Shandong University, , Shandong 250100, China; bSchool of Archaeology and Anthropology, Australian National University, Canberra, ACT 0200, Australia; cThe David Rozensweig Genomics Center, Hospital for Special Surgery, New York, NY 10021; dResearch Division of Archaeological Science, Provincial Institute of Cultural Relics and Archaeology, 450000, China; eResearch Division of Shang and Zhou Dynasties, Henan Provincial Institute of Cultural Relics and Archaeology, Zhengzhou 450000, China; fHenan Provincial Administration of Cultural Heritage, Zhengzhou 450000, China; and gDepartment of Anthropology, Queens College, City University of New York, New York, NY 11367

Edited by Clark Spencer Larsen, The Ohio State University, Columbus, OH, and approved December 9, 2016 (received for review July 18, 2016) Farming domesticated millets, tending pigs, and hunting constituted health and infer inequality in parental investment. Finally, we the core of human subsistence strategies during Neolithic Yangshao compare the distribution of grave goods and elaboration in grave (5000–2900 BC). Introduction of wheat and barley as well as the construction between male and female individuals. The Eastern addition of domesticated herbivores during the Late Neolithic Zhou Dynasty communities are represented by two recently exca- (∼2600–1900 BC) led to restructuring of ancient Chinese subsistence vated skeletal series from cemeteries associated with the Ancient strategies. This study documents a dietary shift from indigenous City of : Changxinyuan and Xiyasi (8) (Fig. 1). Animal millets to the newly introduced cereals in northcentral China during data were obtained from the Zheng Han-associated site of Tianli. the Bronze Age Eastern Zhou Dynasty (771–221 BC) based on stable The skeletal materials from five Yangshao (5000–2900 BC) archae- isotope analysis of human and animal bone samples. Our results ological sites, including Jiangzhai, Shijia, Xipo, Guanjia, and Xishan show that this change affected females to a greater degree than (9–12), serve as the Neolithic reference for early farming commu- males. We find that consumption of the newly introduced cereals nities of China’s Central Plains. was associated with less consumption of animal products and a higher rate of skeletal stress markers among females. We hypothe- Development of Indigenous Subsistence Strategies on the sized that the observed separation of dietary signatures between Central Plains of China males and females marks the rise of male-biased inequality in early The Central Plains region, formed by deposits of the Yellow River ANTHROPOLOGY China. We test this hypothesis by comparing Eastern Zhou human and its tributaries, spans the fertile lands of Henan, southern skeletal data with those from Neolithic Yangshao archaeological con- Hebei, southern Shanxi, and the western portion of Shandong as texts. We find no evidence of male–female inequality in early farm- well as those of the Guanzhong Plain of the Wei River Valley in ing communities. The presence of male-biased inequality in Eastern Shaanxi (Fig. 1). Two species of drought- and cold-resistant cereals Zhou society is supported by increased body height difference be- collectively known as millets (Setaria italica and Panicum mil- tween the sexes as well as the greater wealth of male burials. iaceum) were first domesticated in the area by 8000 BC (13, 14) and persisted as principal crop plants through much of the history stable isotopes | bioarchaeology | paleo diet | Yangshao | East Asia of the region (15–18). Remains of cabbage, grapes, poppy, rice, and acorns were also recovered from Yangshao sites, albeit in small astern Zhou (771–221 BC), the last preimperial dynasty, quantities (18). Wheat (Triticum aestivum)andbarley(Hordeum nominally ruled much of China before the unification of its vulgare) were introduced into the area from the west sometime E ∼ – – vast territory by Qin Shi Huang. A system of ethical and philo- during the Late Neolithic ( 2600 1900 BC) (19 21). However, the sophical thought that has permeated Chinese social life through proportion of wheat and barley among the botanical remains much of its history developed during Eastern Zhou from the teachings of Confucius (551–479 BC). Teachings recorded by his Significance followers as The Analects of Confucius laid the foundation for the principles of Chinese society and government as well as pre- Male-biased inequality in Imperial China imposed strong limita- scribed men’s behavior in great detail (1). In The Analects of tions on the economic and intellectual contribution of women to Confucius (論語), Confucius mentions women only once, stating the society and fostered male-biased resource distribution, be- that “唯女子與小人爲難養也。近之則不孫、遠之則怨。 [It is not cause females were subordinated to the priorities of the pa- pleasing to have to do with women/wives or petty men/servants]” triarchal state. Analyzing human skeletal remains from early (ref. 1, p. 219), apparently consigning women to oblivion (2, 3). It agricultural and later preimperial archaeological sites, we find remains unclear whether this neglect of women in the teachings no evidence of inequality between males and females in early reflects that lower status for women was already institutionalized farming communities. The observed differences between male during Eastern Zhou, because few early historic sources define and female skeletons from Eastern Zhou archaeological con- the position of women in China during the early dynasties (4). texts allow us to infer a decline in female social status after the The objective of this paper is to investigate whether the status of introduction of new crop plants and domesticated herbivores women changed during the Bronze Age (1700 to ∼221 BC) (5) in preimperial China. The analysis reveals that male-biased in- compared with their status in Neolithic Yangshao (5000–2900 BC). equality and subsistence change became intertwined with the After the end of Yangshao, introduction of new cereals and do- rise of social complexity. mesticated herbivores to northcentral China led to restructuring of indigenous Chinese subsistence strategies. Research in other parts Author contributions: Y.C. and K.P. designed research; Y.D., L.Z., W.F., X.M., and K.P. per- of the world has shown that subsistence restructuring frequently formed research; C.M., Y.C., and K.P. analyzed data; and Y.D., Y.C., and K.P. wrote the paper. affected the social status of women and parental investment in fe- The authors declare no conflict of interest. male offspring (6, 7). We hypothesize that subsistence change during This article is a PNAS Direct Submission. the Bronze Age would have similarly affected the position of women 1Y.C., and K.P. contributed equally to this work. in China. We use stable isotope analysis to test for dietary differ- 2To whom correspondence should be addressed. Email: [email protected]. ences between men and women during Yangshao and Eastern This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. Zhou. Skeletal analysis allows us to compare male and female 1073/pnas.1611742114/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1611742114 PNAS Early Edition | 1of6 Downloaded by guest on September 24, 2021 source of calories in the human diet from the beginning of Yangshao (9–12).Littlestableisotopedataareavailableforbonesamplesfrom dynastic China. There is no clear understanding as to when wheat, barley, and legumes began to contribute significantly to the human diet. Results Dietary Differences Between Yangshao and Eastern Zhou. We analyzed human bone samples from two Eastern Zhou sites (30 from Xiyasi and 16 from Changxinyuan) as well as 23 samples from the Middle Yangshao site of Guanjia. One Changxinyuan sample and two Guanjia samples were excluded from the analysis because of low collagen yield. Previously reported data from the Jiangzhai, Shijia, Xipo, and Xishan archaeological sites (n = 109) (9–12) were also included in the analysis (Fig. 2, Dataset S1,andSI Appendix,Table Fig. 1. Geographical locations of the archaeological sites used in the study. S1). Isotopic composition of the Eastern Zhou human bone col- 郑韩故城 新郑 (1) Ancient City of Zheng Han ( ) and contemporary Xinzheng ( ). lagen is significantly different from that of Yangshao samples for Eastern Zhou sites (771–221 BC): (2) Xiyasi (西亚斯; 34.40° N, 113.76° E), (3) δ13 δ13 = − − ‰ = × 畅馨园 天利 both C values [median (Mdn) C 11.2 vs. 8.8 , P 5.5 Changxinyuan ( ; 34.38° N, 113.74° E), and (4) Tianli ( ; 34.37° N, −12 = − = ‰ 113.74° E). Yangshao: (5) Jiangzhai (姜寨; 4790–3360 BC; 34.37° N, 109.22° E), 10 , Z 6.5, exact Wilcoxon test (EWT), SDE.Zhou 2.1 , = ‰ δ15 δ15 = ‰ (6) Shijia (史家; ∼3938–3375 BC; 34.25° N, 108.18° E), (7) Xipo (西坡; 3300– SDYangshao 1.4 ]and N values [Mdn N 7.7 vs. 8.7 , 2900 BC; 34.50° N, 110.66° E), (8) Guanjia (关家; 4000–3500 BC; 35.04° N, P = 0.003, Z = −2.93, EWT, SDE.Zhou = 1.0‰,SDYangshao = 112.00° E), and (9) Xishan (西山; 4500–3800 BC; 34.90° N, 113.53° E). 1.3‰]; 12 of 45 Eastern Zhou bone samples display more negative δ13C values than any of 130 Yangshao samples, indicating a mixed C3/C4 diet. Significant correlation between δ13Candδ15Nvaluesin recovered from Late Neolithic and Bronze Age archaeological sites the Eastern Zhou sample (Spearman’scorrelationρ = 0.61, P = 8.74 × − was persistently low compared with remains of indigenous millets 10 6) suggests that either consumption of C3 plants was associated (15, 22, 23). Domesticated soybeans (Glycine max)oftheLeguminosae with a lower proportion of animal products in the diet during family also first appeared during the Late Neolithic and became Eastern Zhou or C3 and C4 staple cereals had different δ15Nvalues. more important over time (24). Historical records of the Han Dy- nasty (206 BC to AD 220) suggest that wheat, barley, and beans were Sex Differences in Dietary Signatures During Eastern Zhou. With the initially regarded as coarse foodstuffs, provisioning the poor against exception of Jiangzhai, no significant differences were observed famine (25). Only at the end of the Han Dynasty, when the devel- between male and female δ13Candδ15N values within individual opment of hand mills and large water- and animal-powered mills Yangshao sites (Fig. 2A and SI Appendix,TableS1)orforthe allowed converting wheat into fine flour for noodle production, were Yangshao datasets overall (Mdn δ13C = −8.7 vs. −8.9‰ for males these new cereals finally seen as valuable in the area (ref. 26, p. 461). and females, respectively, P = 0.46, Z = −0.75,EWT,SDmales = 15 Faunal assemblages from Yangshao sites tend to be dominated 1.4‰,SDfemales = 1.2‰;Mdnδ N = 8.8 vs. 8.5‰, respectively, – by deer, domesticated pig, and dog bones (27 29). Domesticated P = 0.21, Z = −1.25,EWT,SDmales = 1.4‰,SDfemales = 1.3‰). cattle (Bos taurus) appeared on the Central Plains between 2500 For the Eastern Zhou sites, δ13C values of female skeletons were and 2000 BC (30). Sheep also first appeared in the region during significantly more negative than those of males (Mdn = −13.5 vs. the Late Neolithic and were predominantly used for wool (31). −9.9‰, P = 0.0001, Z = −3.67, EWT, SDfemales = 2.0‰,SDmales = Domesticated water buffalo (Bubalus bubalus) was introduced to 1.6‰), indicating greater overall reliance on C3 plants for females. China from South Asia as late as 1000 BC (32). Eastern Zhou Eastern Zhou females also had lower δ15N values than males faunal assemblages in our study area are dominated by the bones (Mdn = 7.5 vs. 8.5‰, P = 0.001, Z = −3.22, EWT, SDfemales = 0.9‰, of domesticated animals. Pig remains were predominant followed SDmales = 0.8‰)(Fig.2B). by cattle, dog, horse, and sheep. Deer, fish, turtle, bird, and tiger Both Eastern Zhou males (MdnE.Zhou = −9.9‰ vs. bones were present in small quantities (33, 34). MdnYangshao = −8.7‰, P = 0.0003, Z = −3.4) and females −8 (MdnE.Zhou = −13.5‰ vs. MdnYangshao = −8.9‰, P = 2 × 10 , Stable Isotope Research Z = −5.48) had more negative δ13C values than those of Yangshao The two stable isotopes of carbon, 12Cand13C, accumulate at dif- individuals of the same sex (Fig. 2C and SI Appendix,TableS1). The ferent rates in plants using the C3 and C4 pathways of photosynthesis magnitude of differences was considerably larger for females than (35, 36). The overwhelming majority of plants follow the C3 pathway. for males [ΔMdn(E.Zhou-Yangshao) = 1.1‰, ΔMdn(E.Zhou-Yangshao) = − The two millet species were the only C4 domesticates grown in Early 4.5‰ for males and females, respectively, P < 10 5, bootstrapping] China. The C4 pathway incorporates relatively more 13Cintoplant (SI Appendix,Fig.S1B), suggesting that the dietary shift caused by tissues, resulting in less negative δ13C isotopic signatures averaging inclusion of C3 staples affected females to a greater degree. With around −12.5‰ as opposed to the −26.5‰ typical for C3 plants respect to δ15N values, no significant difference was observed be- (37–39). Thus, consumption of millets can be detected by the stable tween Eastern Zhou and Yangshao males (P = 0.12, Z = −1.16, isotope analysis of bone collagen, which preserves the isotopic EWT). Eastern Zhou females had lower δ15N values than their composition of the diet plus an ∼5‰ trophic-level enrichment. Yangshao counterparts (P = 0.001, Z = −3.08, EWT). Nitrogen isotopic composition (δ15N) for terrestrial food webs is a reliable indicator of animal product consumption (40), because δ15N EasternZhouAnimalIsotopicData.It is possible that significant undergoes trophic-level enrichment of 2–6‰ with every step of the correlation between δ13Candδ15N values in Eastern Zhou humans food chain (41, 42). In human communities where terrestrial diets are as well as male–female differences in δ15N values were caused by inferred from the geographic location and zooarchaeological evidence, consumption of cereals with different δ15N values (i.e., legumes or higher δ15N values generally reflect greater proportions of animal cereals from fertilized fields). Alternatively, male–female differ- products in the diet. Heavy reliance on legumes (e.g., beans) can ences in δ13C values could relate to consumption of animals with potentially lower bone δ15N values. Legumes maintain colonies of different feeding patterns. To evaluate the effects of field fertil- nitrogen-fixing bacteria and hence, have δ15Nvaluescloseto0‰ (43). ization and animal product consumption on human isotopic values, Previous stable isotope studies on samples from the Central Plains animal bone samples from the Eastern Zhou sites of Changxinyuan and northeastern China confirm that millets served as the primary and Tianli, including those of domesticated pigs, dogs, sheep, and

2of6 | www.pnas.org/cgi/doi/10.1073/pnas.1611742114 Dong et al. Downloaded by guest on September 24, 2021 ANTHROPOLOGY

Fig. 2. Human bone collagen stable isotope values for the Central Plains Neolithic Yangshao (n = 130) and Bronze Age Eastern Zhou (n = 45) samples. Data sources: Jiangzhai (9, 10), Shijia (10), Xipo (8, 11), Guanjia (this study), Xishan (11), and Xiyasi and Changxinyuan (this study). Male–female differences in δ13Candδ15Nvaluesof human bone collagen for (A) Yangshao and (B) Eastern Zhou archaeological sites. Circles and dashed lines represent females, triangles and solid lines represent males, and diamonds are individuals of unknown sex. P values reflect differences between Mdns for the male and female δ13Candδ15N values as determined by the Wilcoxon rank sum test (in the text). (C) Sex by time period interactions for δ13Candδ15N content in human bone collagen. Differences in δ13Candδ15Nvalues − between males and females stratified by the time periods were analyzed using Kruskal–Wallis tests followed by the posthoc pairwise comparison with Dunn’s test. **P < 10 2; − ***P < 10 3.(D) Animal bone collagen stable isotope values for the Central Plains Eastern Zhou and Yangshao archaeological sites compared with human data. The con- fidence ellipses for human data were drawn at α = 0.8. The low number of data points precluded computing of a reliable confidence ellipse for Shijia.

cattle, were analyzed (n = 17) (Fig. 2D and SI Appendix, Table S1). EWT). No significant difference was found for δ13Cvalues The results were compared with data on Yangshao pigs and dogs between Eastern Zhou monogastrics and Eastern Zhou human from Xipo that we reported previously (11, 12) and other pub- males and females (P = 0.22, Z = 0.75 and P = 0.08, Z = −1.36, lished data (SI Appendix,TableS2). respectively). Isotopic values of domesticated monogastric animals (i.e., pigs Sheep δ13Cvalues(Mdn= −15.8‰, n = 6, SD = 2.1‰) were and dogs) tend to reflect the composition of household refuse and significantly more negative than those of Eastern Zhou human males hence, were examined together. For Eastern Zhou, δ15Nvaluesof (P = 0.003, Z = 2.75, EWT) but were not significantly more negative 15 these animals were low (Mdnpig+dog = 6.5‰, n = 8, SD = 0.9‰), than those of females (P = 0.21, Z = 0.79, EWT). Because the δ N similar to those of Eastern Zhou females (P = 0.12, Z = −2.59, values of Eastern Zhou females were significantly lower than those of EWT) but significantly lower than those of Eastern Zhou males sheep (P = 0.004, Z = −2.67, EWT), it is unlikely that consumption (P = 0.0008, Z = 3.17, EWT). The wide range of δ13Cvaluesfor of lamb affected female isotopic values. Cattle δ13C values were Eastern Zhou pigs and dogs (from −15.7 to −7.9‰)(Fig.2D) considerably less negative than those of sheep (Mdn = −10.4‰, n = suggests that the fodder of some monogastric animals included 3, SD = 2.3‰, P = 0.01, Z = 2.31, EWT), likely because millet hay large proportions of C3 plants, whereas others were mostly fed and straw were used to support the cattle through the winter. Cattle millet. Unlike for Eastern Zhou humans, there was no significant δ13C values were less negative than those of Eastern Zhou females 13 15 correlation between the δ Candδ N values of Eastern Zhou (P = 0.02, Z = 2.02, EWT) but were not significantly different from monogastric animals (ρ = 0.63, P = 0.09), indicating that Eastern those of Eastern Zhou males (P = 0.26, Z = 0.63, EWT). Zhou C3 and C4 cereals had similar δ15N values and could not contribute to the observed correlation between δ13Candδ15N Stable Isotope Values and Cranial Lesions. Reduction in diet quality is values in humans. δ13C values of Eastern Zhou pigs and dogs were often associated with the development of cranial lesions known as more negative than those of Yangshao monogastrics (Mdn = cribra orbitalia (CO) and porotic hyperostosis (PH) that represent − −12.6‰, n = 8vs.Mdn= −7.4‰, n = 7, P = 2.6 × 10 5, Z = −4.05, an adaptive reaction of skeletal tissue to red bone marrow

Dong et al. PNAS Early Edition | 3of6 Downloaded by guest on September 24, 2021 10 (16.1%) displayed PH or CO cranial lesions. Sex distribution in groups created by dichotomizing with the −10.7‰ δ13Cvaluewas uneven (Fig. 3B). Females with δ13C values below −10.7‰ were significantly overrepresented in the affected group compared with males (P = 0.024). These females were almost exclusively from the Eastern Zhou contexts (P = 0.011) (Fig. 3B). This result suggests that the values of δ13C were tightly linked with the factors leading to the development of CO and PH, although this link could be indirect, mediated by cultural factors.

Body Height Dimorphism. Given that the Central Plains skeletal Fig. 3. Association of skeletal stress indicators with δ13Cvalues.(A)Logisticre- collections come from a fairly uniform genetic background and gression modeling of association between physiological stress indicators (CO and environmental setting, changes in male–female postcranial di- PH) and the δ13C values in skeletal remains from Yangshao and Eastern Zhou. The mensions over time likely reflect sex-specific parental investment. presence of CO and PH is coded as one. (B) Females are overrepresented among Because of low numbers of intact postcranial elements, we com- Eastern Zhou skeletons with stress markers (CO and PH). Skeletal samples were pared pooled Yangshao and Eastern Zhou samples (Dataset S3 and 13 2 dichotomized by the best diagnostic cutoff value of δ C. A χ test was per- SI Appendix,TableS3). Six postcranial measurements associated δ13 formed to compare the difference in the sex frequencies with Cvaluesabove with body height and robusticity were used for comparisons. Sta- and below the diagnostic cutoff in Yangshao and Eastern Zhou. tistical comparison of long bone lengths (Fig. 4A) indicates that female, but not male, femur and tibia maximum lengths significantly hyperplasia in response to childhood hemolytic or megaloblastic decreased from Yangshao to Eastern Zhou (ANOVA/Tukey’stest, = = anemias (44). In regions where genetic hemoglobinopathies are P 0.026 and P 0.006, respectively). No significant differences rare, these lesions signal chronic anemia episodes during childhood were found by ANOVA for other bone measurements. caused by insufficient dietary iron, vitamin deficiencies, or loss of To test the hypothesis that the degree of body height di- iron because of intestinal parasites (44, 45). To analyze the rela- morphism remained unchanged from Yangshao to Eastern Zhou, tionships between stable isotope values and anemia indicators (CO we performed a bootstrapping test by randomly pairing individual and PH present = 1, absent = 0) (Dataset S2), we performed male and female measurements within each time period and compared the distribution of male–female differences using a univariate logistic regressions with δ13Candδ15N values as contin- univariate kernel density estimate (KDE) that approximates the uous predictors and CO and PH presence as a binary response probability density function for the differences in male–female variable (46). The results of logistic regression (Fig. 3A)indicatethat 13 skeletal measurements (Fig. 4B and SI Appendix). For all skeletal more negative δ C values were associated with the presence of CO – = δ15 measurements, KDEs of male female differences for Eastern and PH (P 0.03), whereas no association was observed for N. Zhou were shifted into the area of larger magnitude relative to the We performed a receiving operator characteristic (ROC) curve Yangshao sample, suggesting that male–female height and size analysis to evaluate the performance of logistic regression as a differences increased during Eastern Zhou. binary classifier (SI Appendix,Fig.S1). ROC analysis identified a 13 −10.7‰ δ C value as the threshold with the best diagnostic power Funerary Context and Sex. Yangshao burials differed primarily in the to separate skeletons affected by CO and PH from unaffected number and type of grave goods and generally displayed little het- ones. Of 24 individuals with δ13C values below the −10.7‰ erogeneity of wealth (47). To examine whether grave goods distri- threshold value, 11 (45.8%) were affected by PH or CO. Among 62 bution was affected by sex during Yangshao, we constructed mosaic individuals with less negative δ13C values than the threshold, only plots for the Jiangzhai and Xipo burials. Because Shijia burials were

Fig. 4. Differences between male and female postcranial measurements. (A) Comparison of femur and tibia maximal lengths between Yangshao and Eastern Zhou by sex. ANOVA followed by a posthoc Tukey’s test was used to analyze the difference in means. The P value for the Tukey’s test is shown. (B) KDEs of male–female differences distribution for pooled Yangshao and Eastern Zhou samples. The male–female pairs were assembled by a random draw from within each pooled sample. The gray areas indicate the 95% confidence bands for equality of male–female KDEs.

4of6 | www.pnas.org/cgi/doi/10.1073/pnas.1611742114 Dong et al. Downloaded by guest on September 24, 2021 Discussion Subsistence strategies of the human communities on China’sCentral Plains experienced a considerable restructuring during the Late Neolithic and Bronze Age as wheat, barley, and legumes as well as ruminant domesticated animals entered the area and gained impor- tance. Using stable isotope analysis in this study, we find evidence of a dietary shift toward C3 plants during Eastern Zhou. Even allowing for substantial variation in local Yangshao diets (Fig. 2A), Eastern Zhou isotopic values clearly indicate an increased contribution from C3 plants. At the same time, even the most negative δ13Cvaluesfor Eastern Zhou humans are higher than those typical of a strictly C3 diet-reliant population (for instance, at rice-growing Neolithic Jiahu, where δ13Cvaluesaveraged−20.3‰)(50).Thisfindingsuggeststhat C4 plants and C4 plant-consuming animals constituted a considerable bulk of the human diet during Eastern Zhou. We have shown that the position of women during Eastern Zhou was qualitatively different from that during Yangshao. The δ13Candδ15N values of Eastern Zhou females are significantly lower than those of males, suggesting a greater consumption of C3 plants combined with lesser access to animal products for females. Low δ15N values of Eastern Zhou females could be also a con- sequence of a larger proportion of legumes in their diet. Multiple accounts dated to the Han Dynasty attest to wheat, barley, and beans initially being regarded as low status foods, provisioning the poor against famine (25). Consumption of domesticated animals 13 Fig. 5. Mosaic plots illustrating the distribution of grave goods and burial with C3-derived δ C values by females during Eastern Zhou is construction. The sizes of tiles correspond to the numbers of cases that fall unlikely to have driven these sex differences, because highly neg- within each category. Categories with no cases are marked by thin lines. Sex ative δ13C values in females were coupled with low δ15Nvalues. ANTHROPOLOGY refers to the skeletally assessed sex of the skeleton in the burial, chambers refers The observed strong separation between male and female dietary to the number of funerary chambers, outer coffin refers to the presence of an signatures (Fig. 2B) suggests that meals were no longer shared at outer coffin, number of items refers to the number of grave goods in a burial, teeth and bones and animal bones refer to the numbers of isolated animal the household level during Eastern Zhou. bones and/or teeth in a grave. The heat map indicates deviation from the null It is also plausible that the observed separation of dietary sig- hypothesis that all parameters of the funerary context are distributed evenly: natures between sexes reflects the culturally prescribed dietary dark blue, category is overrepresented; pink, category is underrepresented. preferences of males and females. However, our analysis shows that (A and B) Distribution of items of different materials in the Jinagzhai and Xipo highly negative δ13C values were associated with PH and CO, burials. (C) Distribution of items of different materials in the Eastern Zhou cranial lesions linked to poor juvenile health (Fig. 3). The associ- burials (Xiyasi and Changxinyuan combined). (D) Grave construction parameters ation between diet and health shown by this analysis is likely in- in the Eastern Zhou sites (Xiyasi and Changxinyuan combined). direct. Weaning girls onto cereal gruel and limiting their access to other foods through childhood, which has been noted in some contemporary patriarchal societies (51), would lead to increased all secondary collective graves, making it impossible to test the as- – sociation between goods and individual skeletons, evidence from this female morbidity. Increased male female body height dimorphism andobserveddepressionoffemale bone dimensions during East- site was excluded. At Guanjia, grave goods were limited to small ern Zhou compared with Yangshao also suggest that parental in- personal adornments, such as hairpins and beads, and did not display vestment during the Bronze Age shiftedinfavorofsons(Fig.4). any heterogeneity by sex (χ2 = 0.27, df = 1, P = 0.60). Grave goods Adult body height, albeit genetically controlled, is highly sensitive distribution in relation to sex was similar overall at Jiangzhai and to the stresses of childhood (52). Male-biased parental investment, Xipo. In both sites, male burials with no grave goods were over- especially in groups where females contribute little economically, represented. Large quantities of pottery were often found in asso- has been shown to result in increased differences between male and ciation with female skeletons (Fig. 5 A and B and Dataset S4). At female adult body heights in past and present populations (53, 54). Xipo, where jade rings and yue axes were present, female burials Diminished social status of women during Eastern Zhou relative with multiple pots also tended to have jade objects (Fig. 5B). to that during Yangshao was also evident in the distribution of burial Eastern Zhou burials ranged from simple graves to ostentatious wealth. At the Yangshao sites of Xipo and Jiangzhai, a dispropor- multichambered constructions with outer and inner coffins and a tionally larger number of male burials contained no grave goods plentitude of objects (48, 49). Mosaic plots (Fig. 5 C and D and SI (Fig. 5 A and B). Given that the ties of the living to the deceased Appendix,Fig.S3) show a male-biased distribution of grave goods and largely determine funerary treatment (55), this finding implies that a investment in burial construction in the Eastern Zhou burials. As is Yangshao female from those sites may have had a more substantial evident from the plot, burials without an outer coffin, with a single kinship network at the place of her death than a male. Eastern Zhou chamber, and with zero to one grave items were most frequently burials exhibit a clear male bias for the distribution of grave goods associated with female skeletons. When a female burial had an outer and investment in grave construction (Fig. 5 C and D). Although coffin, the number of grave goods in such a burial exceeded the ex- skeletally identified sex is not equivalent to the sociocultural cate- pectation, suggesting that, in a few cases, females had attained pref- gories of gender, bioarchaeological findings have strong implications erential treatment after death. Burialswithanoutercoffinand for sociocultural changes related to gender roles and gender in- multiple grave goods were overrepresented in association with male equality (56). Together with male-biased distribution of grave skeletons. Conversely, even when a male burial lacked an outer goods, the observed dietary, health, and metric differences between coffin, it still tended to have multiple chambers and multiple grave male and female skeletons provide a robust body of evidence for an goods. Heterogeneity of grave goods by sex was further illustrated by inference of emergent male-biased inequality during the Bronze the principal component analysis (SI Appendix,Fig.S4). Age in Early China.

Dong et al. PNAS Early Edition | 5of6 Downloaded by guest on September 24, 2021 Materials and Methods were used for multigroup comparisons. Bootstrapping with 10,000 resam- δ13 A comprehensive description of the archaeological contexts of skeletal col- plings was used to evaluate the differences between time period Cand δ15 lections that were used in this study as well as a detailed description of methods N Mdn value differences. KDE comparisons, principal component analysis are provided in SI Appendix. Collagen extraction and stable isotope analysis logistic regressions, and ROC analyses of skeletal measurements and stable were carried out according to the protocol described in ref. 57. Skeletal isotope data were performed in R using the sm, FactoMineR, rms, and analyses, including sex assessment, identification of pathological lesions, and pROC packages. bone measurements, were carried out according to the osteological stan- dards described in ref. 58. Maximal lengths of the humerus, femur, and tibia ACKNOWLEDGMENTS. Songtao Chen (Shandong University) collected the were used as proxies for adult body height. We also included vertical di- samples. Biao Zhang, Qinxuan Wang, Haichen Zhao, and Yu Chen (students ameter of the humerus head, maximum diameter of the femur head, and of Shandong University) carried out sample preparation for the stable iso- tope analysis. We thank Drs. Pugh, Stinson, DeBoer, Moore, and Rostoker femur epicondylar breadth, because these measurements correlate with and two reviewers who commented on earlier versions of this manuscript. body size. Given the fragmentary nature of the skeletal collections Funding was provided by Queens College, Professional Staff Congress of the examined, these measurements were selected based on availability of City University of New York Grant TRADB-47-262, the Fundamental Research representative samples. Funds of Shandong University Grant 2014HW009, National Science Founda- EWTs were used for pairwise comparison of continuous variables. Kruskal– tion Division of Graduate Education Grant 0966166, and the Program of Wallis tests with posthoc Dunn’s tests and ANOVA with posthoc Tukey’s tests Introducing Talents of Discipline to Universities Grant 111-2-09.

1. Yang B, Wu S (1993) [The Analects of Confucius] (Qi Lu Press, Shandong, China). Chinese. 31. Li Z, Brunson K, Dai L (2014) The zooarchaeological study of wool exploration from the 2. Gao X (2003) Women existing for men: Confucianism and social injustice against Neolithic Age to the Early Bronze Age in the Central Plains. Disiji Yanjiu 34:149–157. women in China. Race Gender Class 10:114–125. 32. Liu L, Yang D, Chen X (2006) On the origin of the Bubalus bubalis in China. Kaogu 3. Paxton P, Hughes MM (2007) Women, Politics, and Power: A Global Perspective (Pine Xuebao 2:141–178. Forge, Thousand Oaks, CA). 33. Luo Y, Yang M, Yuan J (2005) [The analysis report of fauna remains from the ritual site, 4. Pearson MJ (2011) The Original I Ching: An Authentic Translation of the Book of Zheng State.] [Xinzheng Zheng Sacrifice Site], ed Henan Provincial Institute of Cultural Changes (Tuttle Publishing, Tokyo). Relics and Archaeology (Elephant Press, Zhengzhou, China), pp 1063–1146. Chinese. 5. Sun H (2003) Several questions regarding the system of Bronze Age cultures in China. 34. Cao J, Wang J (2016) The identification report of fauna remains found in pots at Kaoguxue Yanjiu 5:921–948. Shuanglou Eastern Zhou cemetery at XinzhengXinzheng Shuanglou Cemetery of the 6. Holden C, Mace R (2005) The cow is the enemy of matriliny: Using phylogenetic Eastern Zhou Period, ed Henan Provincial Institute of Cultural Relics and Archaeology methods to investigate cultural evolution in Africa. The Evolution of Cultural (Elephant Press, Zhengzhou, China), pp 550–571. Diversity: A Phylogenetic Approach, eds Mace R, Holden C, Shennan S (Left Coast, 35. Farquhar GD, O’Leary MH, Berry JA (1982) On the relationship between carbon iso- Walnut Creek, CA), pp 217–234. tope discrimination and the intercellular carbon dioxide concentration in leaves. Aust 7. Holden CJ, Mace R, Sear R (2003) Matriliny as daughter-biased investment. Evol Hum J Plant Physiol 9:121–137. Behav 24:99–112. 36. O’Leary MH (1988) Carbon isotopes in photosynthesis. Bioscience 38:328–336. 8. Henan Provincial Institute of Cultural Relics and Archaeology (2012) [Xiyasi Cemetery 37. van der Merwe NJ (1982) Carbon isotopes, photosynthesis, and archaeology: Differ- of the Eastern Zhou Period in Xinzheng] (Elephant Press, ). Chinese. ent pathways of photosynthesis cause characteristic changes in carbon isotope ratios 9. Gong JZ (2007) Inequalities in Diet and Health During the Intensification of that make possible the study of prehistoric human diets. Am Sci 70:596–606. Agriculture in Neolithic China (Harvard Univ Press, Cambridge, MA). 38. Schoeninger MJ, Moore KM (1992) Bone stable isotope studies in archaeology. 10. Guo Y, et al. (2011) Stable carbon and nitrogen isotope evidence of human and pig J World Prehist 6:247–296. diets at the Qinglongquan site, China. Sci China Earth Sci 41:52–60. 39. Ambrose SH (1993) Isotopic analysis of palaeodiets: Methodological and interpretive 11. Pechenkina E, Ambrose S, Ma X, Benfer RJ (2005) Reconstructing northern Chinese considerations. Investigations of Ancient Human Tissue, ed Sandford MK (Gordon and Neolithic subsistence practices by isotopic analysis. J Archaeol Sci 32:1176–1189. Breach Science Publishers, Langhorne, PA), pp 59–130. 12. Zhang X, et al. (2010) Studies on diet of the ancient people of the Yangshao cultural 40. Ambrose SH (1991) Effects of diet, climate, and physiology on nitrogen isotope sites in the Central Plains. Acta Anthropologica Sinica 29:197–207. abundances in terrestrial foodwebs. J Archaeol Sci 18:293–317. 13. Lu H, et al. (2009) Earliest domestication of common millet (Panicum miliaceum) in 41. Schoeninger MJ, DeNiro MJ (1984) Nitrogen and carbon isotopic composition of bone East Asia extended to 10,000 years ago. Proc Natl Acad Sci USA 106(18):7367–7372. collagen from marine and terrestrial animals. Geochim Cosmochim Acta 48:625–639. 14. Yang X, et al. (2012) Early millet use in northern China. Proc Natl Acad Sci USA 42. Bocherens H, Drucker D (2003) Trophic level isotopic enrichment of carbon and ni- 109(10):3726–3730. trogen in bone collagen: Case studies from recent and ancient terrestrial ecosystems. 15. Lee GA, Crawford GW, Liu L, Chen X (2007) Plants and people from the Early Neolithic Int J Osteoarchaeol 13:46–53. to Shang periods in North China. Proc Natl Acad Sci USA 104(3):1087–1092. 43. DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes 16. Yan W (2005) The beginning of farming. The Formation of Chinese Civilization: An Archaeological in animals. Geochim Cosmochim Acta 45:341–351. Perspective, ed Allan S (Yale Univ and New World Press, New Haven, CT), pp 27–42. 44. Walker PL, Bathurst RR, Richman R, Gjerdrum T, Andrushko VA (2009) The causes of 17. Zhao Z (2006) [Domestication of millet—paleoethnobotanic data and ecological porotic hyperostosis and cribra orbitalia: A reappraisal of the iron-deficiency-anemia perspective.] [Archaeology in China and Sweden], ed Institute of Archaeology, Chi- hypothesis. Am J Phys Anthropol 139(2):109–125. nese Academy of Social Sciences (Science Press, Beijing), pp 97–104. Chinese. 45. Oxenham M, Cavill I (2010) Porotic hyperostosis and cribra orbitalia: The erythro- 18. Zhao Z (2011) New archaeobotanic data for the study of the origins of agriculture in poietic response to iron-deficiency anaemia. Anthropol Sci 118:199–200. China. Curr Anthropol 52(S4):S295–S306. 46. Friendly M, Meyer D (2016) Descrete Data Analysis with R: Visualization and Modeling 19. Crawford G, et al. (2005) Late Neolithic plant remains from Northern China: Pre- Techniques for Categorical and Count Data (CRC, Boca Raton, FL). liminary results from Liangchengzhen, Shandong. Curr Anthropol 46:309–317. 47. Zhang C (2012) The burial practices during the flourishing period of Yangshao cul- 20. Dodson JR, et al. (2013) Origin and spread of wheat in China. Quat Sci Rev 72:108–111. ture. Kaogu yu Wenwu 6:17–27. 21. Flad R, Li S, Wu X, Zhao Z (2010) Early wheat in China: Results from new studies at 48. Tian W (2009) A study of the stone and charcoal burials of Western and Eastern Zhou. Donghuishan in the Hexi Corridor. Holocene 20:955–965. Zhongguo Lishi Wenwu 2:59–67. 22. Fuller DQ, Zhang H (2007) [A preliminary report of the survey archaeobotany of the upper 49. Liu J (2009) Zhou couple burials. Wenhua Xuekan 2:74–79. Ying Valley (Henan Province).] [Archaeological Discovery and Research at the Wangchenggang 50. Hu Y, Ambrose SH, Wang C (2006) Stable isotopic analysis of human bones from Jiahu site, Site in (2002–2005)], ed School of Archaeology and Museology, Peking Henan, China: Implications for the transition to agriculture. JArchaeolSci33:1319–1330. University (Great Elephant Publisher, Zhengzhou, China), pp 916–958. Chinese. 51. Chen LC, Huq E, D’Souza S (1981) Sex bias in the family allocation of food and health 23. Lan W, Chen C (2014) Plant macroremains from Guanzhuang Site in , Henan. care in rural Bangladesh. Popul Dev Rev 7:55–70. Dongfang Kaogu 11:78–89. 52. Silventoinen K (2003) Determinants of variation in adult body height. J Biosoc Sci 24. Fuller DQ, et al. (2014) Convergent evolution and parallelism in plant domestication re- 35(2):263–285. vealed by an expanding archaeological record. Proc Natl Acad Sci USA 111(17):6147–6152. 53. Holden C, Mace R (1999) Sexual dimorphism in stature and women’s work: A phy- 25. Yu Y (1977) Han. Food in Chinese Culture: Anthropological and Historic Perspectives, logenetic cross-cultural analysis. Am J Phys Anthropol 110(1):27–45. ed Chang KC (Yale Univ Press, New Haven, CT), pp 53–83. 54. Vercellotti G, Stout SD, Boano R, Sciulli PW (2011) Intrapopulation variation in stature 26. Bray F (1984) Biology and Biological Technology: Agriculture (Cambridge Univ Press, and body proportions: Social status and sex differences in an Italian medieval pop- Cambridge, UK). ulation (Trino Vercellese, VC). Am J Phys Anthropol 145(2):203–214. 27. Zhou B (1984) [Domestic animals of Chinese Neolithic Age.] [Archaeological Findings 55. Buikstra JE (1995) Tombs for the living ... or ... for the dead: The Osmore ancestors. and Studies of New China], ed Cass AI (Wenwu Press, Beijing), pp 196–210. Chinese. Proceedings of Tombs for the Living: Andean Mortuary Practices, A Symposium at 28. Yuan J, Flad RK (2002) Pig domestication in ancient China. Antiquity 76:724–732. Dumbarton Oaks, ed Dillehay TD (Dumbarton Oaks, Washington, DC), pp 229–280. 29. Flad RK, Yuan J, Li S (2007) Zooarchaeological evidence for animal domestication in 56. Walker PL, Cook DC (1998) Brief communication: Gender and sex: Vive la difference. Northwest China. Late Quaternary Climate Change and Human Adaptation in Arid Am J Phys Anthropol 106(2):255–259. China, eds Chen F, Gao X (Elsevier, Amsterdam), pp 163–199. 57. Ambrose SH (1990) Preparation and characterization of bone and tooth collagen for 30. Lv P (2010) [On the origin of Chinese domestic cattle.] [Zooarchaeology], ed Henan isotopic analysis. J Archaeol Sci 17:431–451. Provincial Institute of Cultural Relics and Archaeology (Cultural Relic Publishing 58. Buikstra JE, Ubelaker DH (1994) Standards for Data Collection from Human Skeletal House, Beijing), pp 152–176. Chinese. Remains (Arkansas Archaeological Survey, Fayetteville, AR).

6of6 | www.pnas.org/cgi/doi/10.1073/pnas.1611742114 Dong et al. Downloaded by guest on September 24, 2021