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Scientific Reports Volume 11, Article Number: 21080 (2021) Cite this article
The ability of Pleistocene humans to successfully adapt to different types of tropical forest environments has long been controversial. In order to study the environmental changes in Southeast Asia during the critical period of human species replacement, we analyzed the paleoenvironmental agents of five animal groups in the middle and late to late Pleistocene. The discovery of human teeth has been reported in Duoi U'Oi (70-60 ka) in Vietnam and Nam Lot (86-72 ka) in Laos. However, the use of paleoproteomics has allowed us to abandon the latter, and so far, no human remains over 70 ka have been recorded in this area. Our research results show that tropical rain forests are highly sensitive to climate change during that period, and canopy forests fluctuate greatly. Locally, large fauna is resilient to these fluctuations, until the cooling period of marine isotopic stage 4 (MIS 4; 74-59 ka) changes the entire biological community. Then, under strong selection pressure, populations with new phenotypic characteristics appeared, while some other species disappeared. We believe that this climate-driven transition provides humans with new foraging opportunities in the new rainforest environment, and is likely to be a key factor in the settlement and spread of our species during MIS 4 in Southeast Asia.
Although the earliest forms of humans occupy different C3-C4 environmental niches in Africa1, this genus is generally considered to be primarily adapted to open environments2,3. In Asia, early Homo erectus may have lived in areas without forests along the banks of northern China and the Java River valley, and the niche division between ancient humans and other large primates living in densely forested habitats has been proposed4,5, 6,7,8.
During the late Pleistocene, with the extinction of the last Homo erectus in Indonesia8, the last Denisovans may have existed in several parts of the continent9, and eventually all ancient groups were replaced by Homo sapiens upon arrival. 10. In On the continental scale, it has been suggested that the transition from open habitats (mixed savanna and woodland) to rainforest habitats during the transition period between the Middle Pleistocene and Late Pleistocene triggered the decline of ancient humans and was unable to adapt to these new environments11.
Therefore, determining the paleoenvironmental background faced by different human species in Southeast Asia (SE) Asia may trigger debates about the uniqueness of our species. However, in the Pleistocene tropical Indochina subregion, rare dental remains temporarily attributed to ancient humans are often reinterpreted as the remains of great apes (mainly orangutans of the genus Orangutan)5,12,13,14, so it is difficult to associate ancient humans with The records are firmly linked to past vegetation in many cases.
The propagation route of H. sapiens to southern China may have crossed Indochina15, but the time of this event, its course—maybe one or several waves (ka)16,17 about 100,000 years ago—and The problem of how H. sapiens adapts to the rainforest environment remains unresolved. Of course, the lack of detailed chronology of several Southeast Asian sites has caused our understanding of this period to become blurred. So far, the earliest indisputable archaeological evidence of human adaptation to Asian tropical rain forests is actually the most recent, dating back to Lida Ajel, Sumatra, about 73-63 ka.
Here, we try to solve some of the key issues by analyzing five mammal groups from Vietnam and Laos to understand the evolution of our species. Their age ranges belong to different marine isotopic stages (MIS): Coc Muoi (148 – 117 ka, MIS 6–5), Tam Hang South (94–60 ka, MIS 5–4), Nam Lot (86–72 ka, MIS 5), Duoi U'Oi (70–60 ka, MIS 4) And Tam Hay Marklot (38.4–13.5 ka, MIS 3–2) 19, 20, 21 (Figure 1). From a paleoecological point of view, the crown size and stable isotope measurements of taxa identified from these faunas are agents of environmental reconstruction7,11,20,22,23,24 and organisms occupied by humans The main source of information for the group. In the area studied, the earliest records of Homo sapiens appeared in Tam Pà Ling (~ 70–46 ka25,26) and Duoi U'Oi (70–60) with several human skeletal remains of approximately 70 ka (ka22). However, the older hypothetical ancient human specimens associated with the Nam Lot combination (86-72 ka22) opened up the possibility of earlier arrival27. Therefore, we use Paleoproteomics 28, 29, 30 to solve the specific allocation of this specimen based on its enamel proteome, with the purpose of better placing the arrival of modern humans in the local context.
(A) Location of locations in northern Laos (Tam Hang South, Nam Lot and Tam Hay Marklot) and northern Vietnam (Coc Muoi and Duoi U'Oi). (B) The δ18O records of the Chinese caves in Sanbao, Dongee and Hulu show millennium-scale climate changes (modified after 87) related to the 224 ka East Asian summer monsoon intensity changes. The decrease in the δ18O value (‰, VPDB, left vertical axis) corresponds to an increase in precipitation, which is a quantitative effect 77. The right vertical axis corresponds to the summer sunshine in the northern hemisphere (65°N, W m-2). The age range of the fauna is placed below the δ18O record curve, from the oldest (right) to the youngest (left).
From the middle to late Pleistocene, the local fauna consisted of most modern taxa and some ancient taxa 23, 31, 32, 33, 34, 35. In general, these faunas are similar to those on other continents at the time, because they were dominated by large herbivores (> 1000 kg to 5000 kg36), including elephants, saber-toothed tigers, giant tapirs, and several rhinoceros and large bovids. Animal 37. This similarity also extends to the local associations of species with different ecology and the differences in their spatial distribution from today (for example, orangutans and giant pandas or tigers and hyenas). Most paleontologists now believe that this unexpected association of species named dissimilar fauna (38,39,40,41,42, but see Reference 43) is the result of species’ different responses to environmental changes. That is in the "individualistic way"-according to their life history 44, 45, 46, 47.
Using classical animal archeology methods, the paleoecological reconstruction analysis of the Southeast Asian mammalian community failed to find the main functional changes of the mammalian community 37, 48, 49, and paleontological records seem to be somewhat consistent. In fact, in this tropical region, this species shows a wide ecological range, including latitude and altitude. Nevertheless, the question remains how species survived climate change during the Pleistocene and adapted to non-similar climates, exhibiting different sets of environmental variables (vegetation structure, sunshine rate, seasonality, rainfall, etc.). Today's 50,51. In addition, the evolution of various lineages at the subspecies level is usually unknown, because the movement of populations can rarely be tracked in the fossil record. Another limitation of the study of species dynamics in tropical Asia is that there is no preserved DNA in the fossil remains, which hinders the reconstruction of the genetic history of mammalian lineages. In Eurasia, most of the molecular analysis of ancient DNA (aDNA) focused on the Bering fauna, emphasizing that the Late Pleistocene was a dynamic period of cold-adapted mammals affected by climate change 52,53,54,55,56 ,57,58,59, 60, 61, 62, 63, 64. These studies prove that various processes (ie, population shrinkage, local extinction, migration, replacement of new populations, or interspecies competition) lead to the success of new and better-adapted populations over time 47,65,66,67. At the same time, the impact of a colder climate on people who adapt to warmth remains largely unknown.
However, the use of morphometry, especially the isotope replacement of teeth, can solve various environmental problems, especially the assessment of the impact of large-scale climate oscillations on the regional-scale rainforest ecosystem and its impact on mammalian communities and related humans, such as Yue Lai The more research 20, 22, 24, 68, 69, 70, 71, 72, 73.
Our data set contains six mammalian orders, namely Artiodactyla, Proboscis, Carnivora, Primates and Large Rodents (Methods, Supplementary Materials and Methods, Supplementary Figure S1-S3, Supplementary Table S3-) Hundreds of isolated teeth of mammals S4). All stations are located in a narrow latitude zone between 23° and 20° passing through Laos and northern Vietnam (Figure 1A). Due to the abiotic parameters related to the latitude distribution, namely climatic effects (temperature, distance from the coast, seasonality of rainfall, rainfall), the location of these locations minimizes changes in the size of the species. However, these five locations are located at different altitudes, from lowland locations in the alluvial plain (Duoi U'Oi) to Zhongshan locations (Nam Lot and Tam Hang South).
First, we used new data from Coc Muoi, Duoi U'Oi, and Tam Hang South to compare carbon (δ13Capatite) and oxygen (δ18O) isotopic measurements from tooth enamel. These data came from 335 taxa belonging to a wide range of taxa. Specimens, as well as those published in Nam Lot and Tam Hay Marklot20,22. We estimated the δ13C carbon source value in animal diets to specifically analyze the changes in the ratio of C3 plants (trees, shrubs, shrubs, and grasses) to C4 plants (grass, sedges) during the study period74. The δ13C of biological apatite allows the reconstruction of the paleoenvironment based on these isotope-different carbon sources. We also use δ13C carbon sources to separate C3 canopy forests from other C3 forest habitats to reveal local fluctuations associated with climate change in tropical rain forests75,76. The δ18O value is used to provide additional paleoecological information related to changes in abiotic conditions (latitude, climate, temperature, moisture content, precipitation, and isotopic composition) 77, 78, 79, 80, 81, 82, 83, 84 ("Methods ").
In addition, we used raw morphological measurement data-the crown area of 213 specimens belonging to five taxa of herbivores and omnivores, sambar (Rusa unicolor), muntjac (Muntiacus sp.), mountain lion (Capricornis sumatraensis) , Wild boar (Sus scrofa) and macaque (Macaca sp.)-to detect significant phenotypic changes in their pedigree over time. Combining proxy data based on stable isotope data with these morphometric data allows us to determine which climate changes have the greatest impact on mammalian communities associated with rainforest dynamics.
Our fourth agent considers the type of digestive physiology and uses the ratio of ruminants to hindgut fermenting herbivores by weight category as an indicator of open landscape expansion (mainly through the emergence of exclusive grazing groups), so rainforest .
Finally, we discussed how the climate change that occurred during the late Pleistocene affected the local adaptation of the first batch of Homo sapiens, as well as the wider adaptation in Southeast Asia. To this end, we used available climate records, such as pollen data 85 and 86 and Chinese cave δ18O data 87 from cave animals, as other relevant information sources.
The MS/MS spectrum clearly assigns Nam Lot incisor (NL 433) to the genus Orangutan (orangutan), which has no unique and highly reliable match with Homo29,30. For those positions where we have the proteomics data of Nam Lot specimens, in our reference sequence, there is no sequence difference between Pongo abelii and P. pygmaeus. Therefore, we assigned the specimen to the Pongo genus without further specifying the species (additional methods and results).
The δ13Csource and δ18Oapatite values of specimens belonging to all taxa are shown in Figure 1 and Figure 2. 2 and 3 and supplementary tables S5-S7. The values of all samples and reference standards (δ13Capatite, δ13Ccarbon source and δ18Oapatite) are shown in Supplementary Appendix S1-S2. For the new data measured here, the δ13C carbon source values of Coc Muoi, Duoi U'Oi and Tam Hang South range from-33.8 to-18.1 ‰ (average δ13C carbon source =-28.0 ± 2.4 ‰ (1 σ), n = 84 ), − 34.3 to − 15.1 ‰ (average δ13C carbon source = − 28.4 ± 3.0 ‰ (1 σ), n = 60) and − 30.0 to − 12.0 ‰ (average δ13C carbon source = − 25.0 ± 3.6), (‰ 1 σ) n = 62), respectively (Figure 2).
The histogram distribution of the relative frequency (%) of the δ13C carbon source values of all taxa in the five Southeast Asian faunas, arranged in chronological order from the oldest (left) to the youngest (right). Each bin represents an interval of 1‰. The shaded area represents the δ13C carbon source value related to the closed forest canopy (δ13C carbon source<-27.2‰); intermediate rainforest and woodland biological communities (δ13C carbon source> − 27.2 ‰ and <− 21.3 ‰; and savannah environment (δ13C carbon source) > − 15.3 ‰). The white area (δ13C carbon source> − 21.3 ‰ and <− 15.3 ‰) is the value derived from the comprehensive consumption of C3 and C4 resources, and does not correspond to any specific ecological environment. The red dotted line represents the δ13C carbon source of each site Value mean.
The distribution of δ18O values of all taxa in the five Southeast Asian faunas, in chronological order, from oldest (left) to youngest (right): Coc Muoi (), Tam Hang South (), Duoi U'Oi () and the former Nam Lot () and Tam Hay Marklot () released data. The outline of the violin chart represents the nuclear probability density, where the width shows the proportion of the data found there. The box in the box and whisker diagram in the violin chart represents the 25th to 75th percentile, and the median is a thick horizontal line.
The new δ18Oapatite values obtained at the three sites range from -9.8 to -3.9 ‰ (average δ18Oapatite =-6.1 ± 1.2 ‰ (1 σ), n = 84), -9.7 to-2.5 ‰ (average δ18Oapatite = -1.6. ‰ ( 1 σ), n = 60) and −9.4 to −2.8 ‰ (average δ18Oapatite = − 6.7 ± 1.4 ‰ (1 σ), n = 62), respectively Coc Muoi, Duoi U'Oi and Tam Hang South (Figure 3 ).
The statistically significant difference between sites from novels (Coc Muoi, Tam Hang South and Duoi U'Oi) and published data (Nam Lot and Tam Hay Marklot) is the source determined by one-way analysis of Kruskal-Wallis δ13Ccarbon variance (H(4) = 83.3, p value <2.2e-16) and δ18Oapatite (H(4) = 25.5, p value = 4.019e-05). Afterwards, Dunn's pairwise comparison of the test showed that the δ13C carbon source values of the Vietnam site and the Laos site are different. Tam Hay Marklot and Nam Lot also seem to be very different. Finally, the δ18Oapatite value from Tam Hang South was determined to be significantly different from the values of all other sites except Duoi U'Oi, and Duoi U'Oi itself was extracted to be significantly different from Nam Lot and Tam Hay Marklot ( Supplementary Table S8, S9).
Broadly speaking, the range and median fluctuation of the δ18O value (Figure 3) are consistent with the δ13C carbon source value (Figure 2). However, the distribution of δ13C carbon source values highlights that during the study period, the C3 forest environment (canopy forest, middle rain forest and woodland) still dominates. In addition, when we look at the percentage of samples based on the distribution of δ13C carbon source values related to different biomes in Table 1, the data shows that environmental conditions have changed significantly through the Coc Muoi-Tam Hay Marklot time series. Therefore, tropical forests are obviously very sensitive to climate change. Our research results specifically illustrate the dynamics of canopy forests (δ13C carbon source <− 27.2 ‰), and show their potential to shrink across time and space: Coc Muoi (65.4%), Tam Hang South (27.4%), Nam Lot ( 42.1%) ), Duoi U'Oi (73.3%) and Tam Hay Marklot (26.3%).
The sequence of animal groups by body weight and digestion strategy is shown in Figure 4 and Supplementary Table S10. Among the three oldest animal groups, the hindgut fermentation group, that is, the non-ruminant group, includes seven large herbivores (> 350 kg) and large herbivores (> 1000 kg), belonging to the following genus: giant tapir , Tapir, saber-toothed tiger, elephant, rhinoceros and Dicerorhinus (compared to only one ruminant Bos species) dominate the biomass. Duoi U'Oi’s “ruminant and non-ruminant taxa” has a ratio of 4:7, indicating that the composition of giant herbivores has changed, without giant tapirs (> 350 kg) and saber-toothed elephants (> 1000 kg) . However, hindgut fermented herbivores still dominate, because the increase in ruminants cannot compensate for the loss of diversity in the huge ancient taxa. Tam Hay Marklot marks a shift, representing small and medium ruminants (18 to 350 kg) (including Rucervus eldii, Axis porcinus and Naemorhedus caudatus) becoming dominant (ruminant to non-ruminant group ratio is 8:6). This trend has clearly continued to the present, as seen by the increase in grazing species in the current fauna at these latitudes (ratio 9:4) (Figure 4).
The number of species in the five animal groups divided by body weight category and digestion strategy, from the oldest (left) to the youngest (right) in chronological order. This ratio refers to the number of ruminant and non-ruminant taxa. For a list of taxa in each weight category, see Supplementary Table S10.
The size range of the crown area of p3 (Rusa unicolor and Sus scrofa) and m3 (Macaca sp., Muntiacus sp. and Capricornis sumatraensis) varies by location (Figure 5A). However, statistical analysis is limited by the imbalance of sample sizes in certain locations. Only R. unicolor (n = 65) and S. scrofa (n = 61) use the Kruskal-Wallis test (H(4) = 21.09, p-value = 0.0003 and H(4) = 14.25, respectively, p-value = 0.007). Afterwards, Dunn's test paired comparison extracted from Coc Muoi R. unicolor and Nam Lot (p value <0.005) and Duoi U'Oi (p value <0.05) were significantly different; and R. unicolor's Nam Lot and Tam Difference in Hay Marklot (p <0.05). S. scrofa samples also showed significant differences between populations (p value <0.05): Coc Muoi and Nam Lot; Tam Hang South vs. Duoi U'Oi; Nam Lot and Duoi U'Oi and Tam Hay Marklot (Supplementary Table) S11 and S12).
The distribution of crown area size (A) and δ13C carbon source value (B) in the five taxa ) To the youngest (bottom) in chronological order. CM Coc Muoi, THS Tam Hang South, NL Nam Lot, DU Duoi U'Oi, THM Tam Hay Marklot. See Supplementary Table S13 for sample size.
In general, there is a cumulative effect from Coc Muoi to Nam Lot, that is, the population follows directed evolution, towards larger (R. unicolor, S. scrofa and Macaca sp.) or smaller (Muntiacus sp. and C. sumatraensis) The surface of the crown area is based on taxa. In the entire fauna sequence, Duoi U'Oi marks this shift in directed evolution. This shift is particularly pronounced in S. scrofa, but the five taxa studied seem to be affected by this reversal of pedigree dimensions (Figure 5A). This reversal is used here as a signal that, in the face of high selection pressure, due to population adaptation or replacement (through extinction or assimilation), populations with new phenotypic characteristics have emerged. Therefore, in the Coc Muoi-Tam Hay Marklot time series, Duoi U'Oi seems to indicate a certain population turnover.
Judging from the available records discussed here, there was no obvious human presence in this area before ~70 ka. However, as shown by our paleoproteomic analysis of Nam Lot incisors (86-72 ka), the ability to obtain protein sequence information from tropical regions and distinguish between Pongo and Homo opens up the possibility of directly solving this problem in the future in Southeast Asia The early Homo sapiens that existed.
The relative similarity of δ13C carbon sources and δ18O values between Coc Muoi (148–117 ka) and Duoi U'Oi (70–60 ka) indicates that climatic conditions have induced an ecosystem dominated by C3 in two different periods. As shown in the curve of Sambo/Calabash δ18O Chinese Cave Record 87 in Figure 1B, considering the age range of the fauna, the advantages of these forest ecosystems may be related to the two high-level declines in monsoon intensity during MIS 6 Coc Muoi (MIS 6.288 ,89) and Duoi U'Oi's MIS 4 period (Figure 2 in87). In Coc Muoi and Duoi U'Oi, the enclosed rainforest contains most of the mammalian biomass, mainly composed of browsers weighing up to 5000 kg (Figure 4 and Supplementary Table S10). However, upon closer inspection, the two locations revealed significant differences in species that rely on the canopy forest as a diet (Figure 6). First, Duoi U'Oi marks a decline in the diversity of large herbivores, because there are no two ancient taxa: the giant tapir Megatapirus augustus and the proboscis saber-toothed tiger. Both sites are located in the same vegetation area, with an altitude of <400 m (asl), and other sources of variation are reduced, supporting the hypothesis that climate has a major impact on mammalian communities.
Compare the δ13C value ranges of selected taxa in the five animal groups in chronological order from the oldest (left) to the youngest (right). The shaded area represents the δ13C carbon source value related to the closed forest (δ13C carbon source <− 27.2 ‰), intermediate rain forest and woodland biome (δ13C carbon source> − 27.2 ‰ and <− 21.3 ‰); and the environment similar to the tropical grassland ( δ13C carbon source> − 15.3 ‰). The white area (δ13C carbon source>-21.3 ‰ and <-15.3 ‰) is the value of the comprehensive consumption of C3 and C4 resources, and does not correspond to any specific ecological environment.
Second, the results of the δ13C carbon source value show that in Duoi U'Oi, environmental changes have led to the redistribution of niches and interactions between new species. The difference from the old Tam Hang South and Nam Lot fauna is significant, and the MIS 4 Duoi U'Oi fauna seems to be significantly different from the MIS 5 fauna (Figure 6 and Supplementary Table S8). Especially the sambar R. unicolor, tapir and large bovids that forage in this new Duoi U'Oi ecosystem dominated by C3. In addition, the Duoi U'Oi δ18O value is lower than the value prevailing in Nam Lot globally, which indicates that colder and/or wetter conditions are present (Figure 3).
Although the forest environment dominates during this period, some animal groups also include species that rely on mixed C3-C4 and/or C4 resources for their diets (Figures 2 and 6). Especially in the case of Tam Hang South and Nam Lot fauna, the δ13C carbon source value shows the existence of a more open environment and the reduction of forest habitat: Tam is 11.2% (C3–C4) and 3.2% (C4) Hang South and Nam Lot They are 5.2% (C3–C4) and 3.5% (C4) respectively (Table 1). These data are related to seasonal increases24. Zheng Helei's data (from near the Leizhou Peninsula in southern China, latitude 21°-20°, elevation <260 m85) shows that the mountain slopes are covered by monsoons with evergreen forests and dense shrubs. Tam Hang South and Nam Lot also show different sets of environmental variables, and their δ18O values are significantly different (but not due to altitude changes, because they are about 150 m apart and located at the same altitude ~ 1120 m), indicating that despite Lack of age accuracy, how dynamic is the interglacial MIS 5?
In the second half of the Late Pleistocene, there were no records of mammalian fauna in the study area. The carbon and oxygen isotopic records of land snails indicate that between ~70 and ~32 ka, the landscape is still highly forested and humid. Camaena massiei is located near Laos The site of Tam Pà Ling 90. The significant changes in the more open landscape associated with increased drought due to low sea levels and the expansion of the continental land surface were later illustrated by our Tam Hay Marklot (38.4-13.5 ka20) δ13C carbon source value (Figure 6). Further west, the Tham Lod Rock Sanctuary in Thailand (33–11.5 ka70,92) shows a similar situation: mixed breeders, sambar and large bovines seem to have migrated to grassland areas and herbivores and medium-sized deer. (Axis, Rucervus) and calves (Naemorhedus) occupy new spaces, most likely from southern latitudes. Over time, these subpopulations have adapted to living in open landscapes93 (Supplementary Figures S5 and S6) , Supplementary Appendix S4). Boh Dambang (25-18 ka, Cambodia 94), 91 further south in the center of the hypothetical savanna corridor and the site of Tam Hay Marklot show that despite this, the peninsula is still dominated by herbivores (Muntiacus, Rhinoceros, and tapir), even though During the last glacial maximum (LGM; 26.5-19 ka) the drought height near 95. In fact, Tam Hay Marklot's δ13C carbon source value of 26.3% and Boh Dambang's 9.6% indicate this environment (Supplementary Table S14), and the results are from a fairly comparable sampling classification group at the two locations (Supplementary Table S7). The shrinkage of forest habitats has significantly changed the carrying capacity of the ecosystem, forcing large carnivores to look for new hunting opportunities among species that inhabit the savanna, including tigers (Panthera tigris), leopards (P. pardus) or hyenas (Crocuta crocuta) ) (Figure 6 and Supplementary Figure S5).
The current analysis combines the canopy area size (Figure 5A) with the δ13C carbon source data (Figure 5B), revealing that the main turnover and decline of the population in the Duoi U'Oi mammal community is related to the regression of the C3 dominant landscape. Isotope value. In Duoi U'Oi, populations with new phenotypic characteristics have emerged compared to the old locations, and they have adapted better to this new environment. This series of evidence can be interpreted as an adaptive response to major selection pressures. In fact, species of different weights range from ~ 15 kg (muntjac) to ~ 220 kg (sambar), different dietary strategies (omnivores and herbivores), and adapt to different ecological niches (ground-dwelling ungulates and trees). Perching monkeys) ), experienced similar evolutionary trends, indicating that the entire ecosystem has been affected. As shown in Figure 1B, the curve recorded by the Sambo/Gourd δ18O cave shows that this period witnessed short-term climate changes, and the monsoon intensity dropped sharply at the beginning of MIS 4 (events of comparable magnitude occurred during the LGM period). Such climatic events may lead to strong selection pressure, which triggers new adaptations and population migration. The suddenness of this climate change lasting about <300 years and the average temperature drop of about 5-6 °C85 are the most likely explanations for the population turnover and the disappearance of the last ancient species (sabertooth and sabertooth). Giant tapir). So far, from the animal records studied, there is no evidence that these species are related to Homo sapiens. Increasing evidence based on systematic geographic analysis (aDNA) indicates that population replacement within a species may be a rapid process leading to major extinction and recolonization events due to interactions between populations or due to the impact of sudden climate change 53, 54.
In southern China, the late Middle Pleistocene to early late Pleistocene series of Yugong, Quzhai, and Baxian show the same trend, as shown by the δ13C value patterns of R. unicolor and S. scrofa24,35,73 (Supplementary Figure S7 and S8, supplementary appendix S3). Therefore, the cooling event may lead to the expansion of south China canopy forest dwelling populations to low latitudes.
From a paleoecological perspective, our findings confirm that tropical rainforest ecosystems prevailed in the late Mid-Pleistocene at these latitudes (Supplementary Figure S7). They are consistent with the environmental reconstruction done by Louys and Roberts. Our findings also question the relationship between the changes in the tropical rain forest environment and the main turnover of early humans (Homo erectus, Denisovan) in Southeast Asia before the arrival of Homo sapiens. In fact, assuming that ancient humans could not adapt to tropical rainforest habitats5,11,17, environments like Coc Muoi might become obstacles to their local settlement.
As our research shows, environmental changes not only affect the fauna, but may also affect Homo sapiens. In fact, in the extensive record of forest persistence in the late Pleistocene, we did notice important changes in the area when it was first known to occur. The two severely worn teeth of Duoi U'Oi (70–60 ka22) (thus being carefully classified as ancient or human) recorded the existence of humans, while Homo sapiens appeared in Tam Pà approximately 200 kilometers away Ling cave ruins time (~ 70–46 ka25,26). Judging from the existing records, it is clear that humans settled in the area around the time of MIS 4. 70-50 ka97, must deal with densely forested environment 90. However, the relative cooling period of MIS 4 may have led to a profound transformation of forest composition and structure, as evidenced by Zheng Helei's 85 pollen record analysis (altitude <260 m) at the same latitude and further east. In fact, due to the decline of the mountain vegetation zone, the monsoon evergreen forest is transformed into a mountain forest, and temperate plants have increased, and conifers, previously rare trees and ferns (20%) have increased significantly. According to the pollen records of the caves in southern China at a comparable altitude (< 212 m), Li et al.86 emphasized similar changes in the late Pleistocene subtropical mixed coniferous forest.
Although the palynological analysis of Duoi U'Oi is based on few elements, it also shows that the frequency of fern spores (25%) and non-arboreal groups (31%) is relatively high, but the representativeness of mangrove pollen grains is relatively high. Low (2%) 22. In the absence of archaeological evidence (stone tools or organic industries, bones with traces of slaughter, etc.), it is still challenging to assess many aspects of human foraging behavior in this region of Southeast Asia. However, different types of tropical rain forests provide edible plants, fruits, seeds, nuts, and honey98, while rivers provide predictable resources of shells, fish, molluscs, and algae. Despite the loss of the ancient large herbivores, the Duoi U'Oi biota supports a wide range of games. The presence of humans on Duoi U'Oi is recorded not only through two isolated teeth related to the animal group, but also through indirect evidence. In fact, the mortality characteristics of sambar deer at this location clearly show human characteristics19. In Duoi U'Oi, humans can hunt down prey deep in the rainforest and selectively hunt adult individuals. It is possible that during MIS 4, new vegetation that changed shrubs, ferns, and herbaceous strata made the forest easier to enter and navigate, and provided new hunting opportunities for foragers. Mankind has clearly successfully adapted to the general habitat of the closed canopy forest 18,99,100,101, probably long before the formation of specialized foraging behavior, especially in the hunted prey, arboreal and semi-arboreal species and terrestrial creatures. The proportion of species is larger ~45 ka99, 102,103,104.
Due to the climate dynamics of the late Pleistocene, our research results support the successful spread of our species to the area during MIS 497, 105, 106, and 107. The combination of ecological and behavioral factors seems to help early Homo sapiens successfully cope with the challenges of the rainforest environment: the renewal of vegetation allowed humans to occupy a new niche at the beginning of MIS 4108, and our ability to adapt species effectively to this environment109 . In view of the recent reassessment of human spread in the Far East. From 65 ka to 45 ka, despite the great controversy 97,110,111, our species may enter southern China through similar types of rainforests. The similarity of isotope data between Duoi U'Oi and Baxian24,35 also shows (Supplementary Figure S7) ). In the middle and late Pleistocene, there was no comparable isotope data available on the Southeast Asian continent, but it remains to be proved that Homo sapiens expanded its habitat during this period when it moved to the Southeast Asian islands. However, we know that with this climate-driven vegetation replacement, modern humans arrived in Sumatra in 73-63 ka, where they occupied the dense evergreen rainforest ecosystem18. Starting at 46 ka, in the Niah Cave in Borneo, modern humans have effectively used the tropical environment, used sophisticated hunting techniques and were able to process poisonous plants for food103. Interestingly, climate change during MIS 4 is considered to be the main driving factor for human migration from Africa to Eurasia. The reason is that the colder weather and lower sea level 112,113,114 make it possible for the population to reach northern Australia before 65 ka115,116. .
Studies on the evolution of ecosystems in Southeast Asia in the past have been limited by the scarcity of paleontological records, atypical remains protection, discontinuity, and the accuracy of the available age of the fauna, which limit our understanding of the warm-adapted species response to climate change. Nonetheless, our multi-agent method combines morphometric and isotope data as well as digestive physiology types, revealing that the cooling event of MIS 4 may have a profound impact on the overall biological community of the area when humans arrive, resulting in a relationship with dense forests. Landscape-related mammal populations. Our research results indicate that the new composition and structure of tropical rain forests are likely to be key factors in promoting the rapid spread of Homo sapiens to Southeast Asia.
In addition, our analysis emphasizes the importance of paleoproteomics in elucidating the taxonomic distribution of remains (paleohumans and equines). In fact, given the scarcity of evidence of early Homo sapiens in the region, this method is essential for further understanding of the arrival and spread of our species on the continent.
These stations are located at different altitudes: 113 m (asl) above sea level (Duoi U'Oi, Vietnam), 361 m asl (Coc Muoi, Vietnam), 1120 m asl (Tam Hang South/Nam Lot, Laos), and 809 m asl (Tam Hay Marklot, Laos). They are located 120 kilometers (Duoi U'Oi), 170 kilometers (Coc Muoi) and 270 kilometers (Lao ruins) from the coast bordering the Gulf of Tonkin (Supplementary Figure S1). Today, the region is characterized by a humid subtropical climate. According to the Köppen-Geiger climate classification, summers are hot and humid, and winters are cold and mild. Local climate data, annual average temperature and annual average rainfall are: 23.7 °C and 1735 mm (Hoà Binh Province, Duoi U'Oi, Vietnam); 21.9 °C and 1349 mm (Lang Son Province, Coc Muoi, Vietnam) ; 19.8 °C and 1331 mm (Houaphan Province, Xamneua, Nam Lot, Tam Hang South and Tam Hay Marklot, the highlands of Laos) (https://en.climate-data.org/).
These sites were excavated between 2003 and 2015. Descriptions of the site and paleontological content can be found elsewhere in the publication 19, 20, 21, 22 and condensed versions of supplementary data. Due to the burial and geological processes of karst deposits, all combinations show similar remains preserved. They are mainly composed of isolated teeth of mammals, and due to preservation deviation, only species composition combinations> ~ 5 g: Coc Muoi (NISP = 1323), Tam Hang South (NISP = 673), Nam Lot I (385 teeth) and Nam Lot II (5 teeth) (NISP = 390), Duoi U'Oi (NISP = 871) and Tam Hay Marklot (NISP = 1364) (Supplementary Tables S3 and S4). Soil analysis of these sites shows that porcupines are the main accumulator of large mammal bones (most of their teeth are bitten) before they are buried in sediments. All the remains deposited in these locations were flowed through the entire karst network with water that caused the loss of the smallest elements19. According to field observations, Brain117 shows that the remains collected by porcupines can well represent a place or the number of carcasses around a place, so it is a good representative of species richness. Therefore, these combinations consist of similar taxa. Almost all groups can sample for stable carbon and oxygen isotope analysis (except Proboscidea from Tam Hang South and Tam Hay Marklot), allowing comparison of communities over time (Supplementary Table S7).
These five animal groups do not represent continuous records, because there are two main gaps, namely Coc Muoi (148–117 ka) and Tam Hang (92–60 ka) and Duoi U'Oi (70–60 ka) and Marklot (38.4) –13.5 ka) (Figure 1 and Supplementary Figures S2 and S3). No artifacts or other objects (charcoal, decorations, traps, etc.) related to the remains of the animals were found.
In this analysis, we use the size of the crown area of the tooth (maximum length x maximum width) as an indicator of ecological changes in five mammalian lineages (Muntiacus sp., Capricornis sumatraensis, Rusa unicolor, Sus scrofa, and Macaca sp.). We chose these taxa defined at the species or genus level because they are common to all five animal groups and have a sufficient number of specimen records (Supplementary Tables S5 and S6 and Annex S6). However, this analysis is limited by many biases, including the differential representation of tooth types within a given taxon. This is why we choose left and right m3s among Muntiacus sp., C. sumatraensis and Macaca sp. Regarding the other two taxa, the number of several tooth types is significant, p3, p4, and m3 in S. scrofa, and p3 and p4 in R. unicolor, but they have different ranges of variation. In R. unicolor, unlike p3s, p4s has a similar range of variation between sites. In S. scrofa, m3s shows greater variability, and there is a large overlap between sites. Considering the purpose of our research, using the crown area size as a signal for the new phenotype p3 is the most useful tooth type in the two taxa. This is most likely due to selective adaptation pressure on the skull. For example, in suids, the populations differ in the length of the skull, upper jaw, and row of teeth118. We did not try to estimate the weight of an individual.
The stable carbon isotope of bioapatite (δ13Capatite) reflects the relative proportion of carbon in the consumer's diet, which comes from the main source of the food web, that is, plants that use the C3 or C4 photosynthetic pathway74. In tropical and subtropical regions, wetter forests and woodland habitats are associated with C3 plants that exhibit low δ13C values, while drier and more open environments are characterized by C4 plants with high δ13C values76,119,120. In addition, the lowest δ13C value reflects the dense forest conditions caused by the "canopy effect", so it can be used to distinguish the C3 forest environment. Finally, using the measured δ13Capatite value and the enrichment factor adapted to body weight (supplementary materials and methods), we estimated the initial δ13C value of the carbon source in the animal's diet, which is labeled "δ13C carbon source" here.
Stable oxygen isotopes (δ18O value) are used to provide additional paleoecological information. The main source of δ18O changes in enamel is the oxygen isotope composition of chemically bound water (ie water found in plants) in drinking water and diet 78,79,80,81,82,83. This kind of water itself is controlled by various environmental and geographical conditions such as latitude, climate, temperature, moisture content, precipitation, precipitation isotope composition, etc. (In low latitude areas, the change of δ18O precipitation is mainly affected by precipitation, that is, the effect) 77,78 ,84.
Assigned to orders of mammals from Coc Muoi (n = 84), Tam Hang South (n = 62) and Duoi U'Oi (n = 60) (Artiodactyla, Proboscis, Carnivora, Primates and Rodents) ) The fossil teeth were sampled and analyzed for this study (Supplementary Tables S5 and S7). The enamel is first mechanically cleaned using a hand-held dental drill equipped with a diamond grinding head. Use diamond tip cutting wheels or diamond tip burrs, and then collect samples (powder or fragments) along the entire crown height of each sample. When sampling enamel fragments instead of powder, use an agate mortar and pestle to crush the complete enamel fragments. The enamel powder sample was soaked in 1 ml CH3COOH (0.1) M for 4 hours at room temperature, then rinsed several times in distilled water, and finally dried overnight at 65 °C. Using the carbonate phase of the enamel, in the "Service de Spectrométrie de Masse Isotopique du Muséum (SSMIM)" in Paris, a stable carbon and oxygen isotope ratio was measured using a Thermo Scientific Delta V Advantage isotope mass spectrometer and Thermo Scientific Kiel. IV Carbon Salt device chemicals. Isotopic abundance is expressed in δ (delta) symbol, expressed as deviation per mil (‰), where: δ13C = (13C/12Csample/13C/12Cstandard − 1) × 1000 and δ18O = (18O/16Osample/18O/16Osta Ndard − 1) × 1000.
In this analysis, we used the δ13C limit corresponding to a wide range of pre-industrial environments:-27.2 ‰ and-21.3 ‰ as the upper limit of δ13C for closed canopy forest 121 and intermediate rainforest and woodland biological communities, which are 74, 122 and-respectively 15.3 ‰ is 74 as the lower limit of δ13C for the C4 savanna environment.
Kruskal-Wallis one-way analysis of variance was performed on the data sets of novels (Coc Muoi, Tam Hang South and Duoi U'Oi) and published data (Nam Lot and Tam Hay Marklot) to determine the statistical difference and location of δ13C carbon sources. The value of δ18Oapatite between points. To this end, samples come from Coc Muoi (n = 84), Tam Hang South (n = 62), Duoi U'Oi (n = 60), and Nam Lot (n = 5722) and Tam Hay’s published sites use Marklot (n = 7220). The size of the crown area between the stations was also studied for R. unicolor (n = 65) and S. scrofa (n = 61). All analyses chose the Kruskal-Wallis test instead of the parametric analysis of variance, because a preliminary test was performed to check for normally distributed data and equal variances, which indicates that a nonparametric test will be used. All statistical analysis was performed using the free program R software (R Core Team, 2018).
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Regarding the original isotope data of Coc Muoi (Lang Son Provincial Museum, Vietnam) and Duoi U'Oi (Peace Provincial Museum, Vietnam), provided by Dr. Nguyen Gia Doi from the Institute of Archaeology, Vietnam Academy of Social Sciences Research permit was issued to AMB on November 17, 2017 certificate. The Heritage Department of the Vientiane Ministry of Information, Culture and Tourism of the Lao People's Democratic Republic issued the Tan Kengnan Fauna Isotope Analysis and Research Permit (Letter No. 495) to AMB on November 28, 2016. Funding came from the research laboratory BABEL (FRE 2029 and UMR 8045) CNRS/University of Paris, AMB, Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany, NB (contract number 0117/037). FW was supported by the Marie Skłodowska Curie Personal Scholarship (n°795569) and the European Research Council (ERC) under the EU Horizon 2020 Research and Innovation Program (grant agreement n°948365). EC is supported by VILLUM FONDEN (n°17649). The author would also like to thank Clément Zanolli for helpful comments and Catherine Yvon for editing the English text.
UMR 8045 BABEL, CNRS, Université de Paris, Faculté de Chirurgie dentaire, 1 rue Maurice Arnoux, 92120, Montrouge, France
Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
Nicholas Bergen and Jean-Jacques Habrin
Applied and Analytical Paleontology, Institute of Earth Sciences, Johannes Gutenberg University, Mainz, Germany
Evolutionary Genomics Group, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark
Frido Wilk and Enrico Capellini
UMR 7209 Archéozoologie, Archéobotanique: Sociétés, Pratiques, Environnements, Muséum National d'Histoire Naturelle, CNRS, Paris, France
Dennis Fiorello, Olivier Tombret and Elise Dufour
Department of Anthropology and Paleoenvironment, Institute of Archaeology, Hoan Kiem District, Hanoi, Vietnam
Nguyen Thi Mai Huong & Nguyen Anh Tuan
Heritage Department, Ministry of Information, Culture and Tourism of Laos, Vientiane
Thongsa Sayavonkhamdy, Viengkeo Souksavatdy and Phonephanh Sichanthongtip
Institut des Sciences de l'Évolution de Montpellier, Université de Montpellier, CNRS, IRD, EPHE, Montpellier, France
Ecole et Observatoire des Sciences de la Terre (EOST Géologie), Institut de Physique du Globe de Strasbourg (IPGS) (CNRS/UMR 7516), Institut de Géologie, Université de Strasbourg, Strasbourg, France
Philip Tinner & Quentin Bosch
UMR 7362 Laboratoire Image Ville et Environnement, Institut de Géologie, Strasbourg, France
Department of Earth and Environmental Sciences, Traps' MQ Luminescence Dating Facility, Macquarie University, Sydney, Australia
Geological Archaeology and Archaeology Research Group, Southern Cross University, Lismore, Australia
Institute of Vertebrate Paleontology and Paleontology (IVPP), Chinese Academy of Sciences, Beijing, China
Spitteurs Pan, Technical Cave Supervision and Exploration, La Chapelle, France
Eric Suzoni and Sebastian Frangul
Natural History Museum of La Rochelle, France
Department of Biomedicine, University of Minnesota School of Medicine, Duluth, Minnesota, USA
Department of Anthropology, University of Illinois at Urbana-Champaign
Lundbeck Foundation GeoGenetics Centre, GLOBE Institute, Copenhagen, Denmark
UMR 7206 Eco-Anthropologie, Muséum National d'Histoire Naturelle, CNRS, Paris, France
French Academy, Chairperson of Paleoanthropology, Paris, France
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AMB, NB and ED were designed and studied; NB, ED, OT and DF were used for sample preparation; AMB was analyzed for morphometric data; NB and ED were analyzed for isotope data; FW and EC were analyzed for proteomics data; TS, VS , PS, AMB, NB, POA, PD, JLP, KW, RJB, QB, ES, SF, EPE, AZ, LS, FD, LS, JJH are part of the LAOS project; NTMH, NAT, AMB, POA, PD, JLP, KW, FD are part of the Vietnam project; AMB, NB, ED, JJH, and FW wrote this paper with the contributions of all other co-authors.
The author declares no competing interests.
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Bacon, AM., Bourgon, N., Welker, F. etc. A multi-agent approach to explore the arrival, environment and adaptation of Homo sapiens in Southeast Asia. Scientific Report 11, 21080 (2021). https://doi.org/10.1038/s41598-021-99931-4
DOI: https://doi.org/10.1038/s41598-021-99931-4
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