Spread of Y. pestis, earlier than previously thought, may have caused Neolithic decline


Open access Emergence and Spread of Basal Lineages of Yersinia pestis during the Neolithic Decline, by Rascovan et al. Cell (2018)

Abstract (emphasis mine):

Between 5,000 and 6,000 years ago, many Neolithic societies declined throughout western Eurasia due to a combination of factors that are still largely debated. Here, we report the discovery and genome reconstruction of Yersinia pestis, the etiological agent of plague, in Neolithic farmers in Sweden, pre-dating and basal to all modern and ancient known strains of this pathogen. We investigated the history of this strain by combining phylogenetic and molecular clock analyses of the bacterial genome, detailed archaeological information, and genomic analyses from infected individuals and hundreds of ancient human samples across Eurasia. These analyses revealed that multiple and independent lineages of Y. pestis branched and expanded across Eurasia during the Neolithic decline, spreading most likely through early trade networks rather than massive human migrations. Our results are consistent with the existence of a prehistoric plague pandemic that likely contributed to the decay of Neolithic populations in Europe.

(A) Schematic representation of the trajectories and time periods (thousand years before present, kyr) of major known human migrations in Eurasia during the Neolithic and Bronze Age. The observed geographic distribution and divergence times of Y. pestis strains from the Gok2 and Bronze Age clades cannot be explained by the timings and routes of these human movements.
(B) Geographic distribution of the use of animal traction and wheeled transport across Neolithic and Bronze Age populations in Eurasia, which broadly expanded during the period of 5,500 and 5,000 BP. The expansion of these technological innovations overlaps the predicted period for the expansion of the basal Y. pestis strains.
(C) Timeline indicating the proposed key historical events that contributed to the emergence and spread of plague during the Neolithic.

We have evolved in the interpretation of the plague from 1) a Corded Ware-driven disease, to 2) a steppe disease that was spread by Yamna and Corded Ware, and now 3) a (potentially) Trypillia-driven disease that spread to the west earlier than Yamna and Corded Ware, but probably also later east and west with both.

At least it still seems that the plague and its demographic consequences were a good reason for the expansion of Indo-Europeans and Uralians into Europe, as we thought…

Featured image, from the paper: “The predicted model of early dispersion of Y. pestis during Neolithic and Bronze Age was built by integrating phylogenetic information of Y. pestis strains from this period (Figure 1E), their divergence times (Figure 3), the geographic locations, carbon dating and genotypes of the individuals, and the archaeological record. The model suggests that early Y. pestis strains likely emerged and spread from mega-settlements in Eastern Europe (built by the Trypillia Culture) into Europe and the Eurasian steppe, most likely through human interaction networks. This was facilitated by wheeled and animal-powered transports, which are schematized in the map with red lines with arrows pointing in both senses. Our model builds upon a previous model (Andrades Valtuena et al., 2017) that proposed the spread of plague to be associated with large-scale human migrations (blue line).


Oldest bubonic plague genome decoded in Srubna ca. 3800 YBP

New open access paper from the Max Planck Institute: Analysis of 3800-year-old Yersinia pestis genomes suggests Bronze Age origin for bubonic plague, by Spyrou et al., Nature Communications (2018) 9:2234.

Interesting excerpts from the paper and supplementary materials (emphasis mine):

Here, we analyse material from the Mikhailovsky II burial site, which was excavated in 2015 and is one of numerous kurgan cemeteries identified in the Samara Oblast. It consists of seven kurgan burials, and is chronologically associated to the ‘Pokrovka’ phase (3,900-3,750 BP) of the ‘Srubnaya’ culture (3,850-3,150 BP) (radiocarbon dates produced in this study provided in Supplementary Table 6), also referred to as the ‘proto-Srubnaya’ that is considered the earliest phase of the LBA in the Samara Oblast. All sex and age groups were represented in this cemetery. We analysed nine individuals buried in three kurgans and identified two individuals buried in the same kurgan (see Supplementary Figure 1) to be positive for Y. pestis. According to anthropological analysis these were a 30-40 year-old male (RT5) and 35- 45 year-old female (RT6).

After its divergence from Y. pseudotuberculosis, Y. pestis acquired its high pathogenicity and distinct niche mainly by chromosomal gene loss16 as well as the acquisition of two virulence-associated plasmids, pMT1 and pPCP11,17,18. Throughout this process, one of the most crucial evolutionary adaptations related to its pathogenicity was its ability to colonise arthropods, a phenotypic/functional gain mediated by a combination of chromosomal and plasmid loci19,20. These genetic changes are central to the most common “bubonic” form of the disease, where bacteria enter the body via the bite of an infected flea, travel via the lymph to the closest lymph node and replicate while evading host defences. Recent ancient genomic investigations of Y. pestis have identified its earliest known variants in Eurasia during the Late Neolithic/Bronze Age period (LNBA) that show genetic characteristics incompatible with arthropod adaptation. These strains, therefore, have been considered incapable of an efficient flea-based transmission2; however, the alternative early-phase transmission could have provided an independent means of arthropod dissemination2,3,21. To date, the earliest evidence of a Y. pestis strain with signatures associated with flea adaptation has been reported during the Iron Age through shotgun sequencing of an ~2900-year-old genome from Armenia (strain RISE397), though at a coverage too low (0.25-fold) to permit confident phylogenetic positioning2. Although the mechanism by which the LNBA lineage caused human disease is unclear, its frequency in Eurasia during the Bronze Age2,3 and its phylogeographic pattern that mimics contemporaneous human migrations are noteworthy3.

Population genetic analysis to infer the ancestry of RT5. b Principal component analysis (PCA) of modern-day western Eurasian populations (not shown) and projected ancient populations (n = 82, see population labels), including the newly sequenced RT5 individual from Samara and c estimation of ancestral admixture components using ADMIXTURE analysis (K= 12) (see Supplementary Methods)

The central steppe region seems to have played a significant role as a migration corridor during the entire Bronze Age, and as such, it likely facilitated the spread of human-associated pathogens, such as Y. pestis, across Eurasia. Here, we explore additional Y. pestis diversity in that region by isolating strains from LBA Samara, in Russia. We identify a Y. pestis lineage contemporaneous to the LNBA strains with genomic variants consistent with flea adaptation. This reveals the co-circulation of two Y. pestis lineages during the Bronze Age with different properties in terms of their transmission and disease potentials.

A recent study has suggested that flea-adapted Y. pestis, along with its potential to cause bubonic plague in humans, likely originated around 3000y BP2. Contrary to such conclusions, the lineage giving rise to our Y. pestis isolates (RT5 and RT6) likely arose ~4000 years ago (Supplementary Tables 6 and 9), and possessed all vital genetic characteristics required for flea-borne transmission of plague in rodents, humans and other mammals. (…)

Moreover, our analysis of the previously published Iron Age RISE397 strain from modern-day Armenia2 revealed its close relationship to RT5 and RT6 (Supplementary Fig. 4). Note that the modern 0.PE2 and 0.PE7 lineages, which are known to possess all genomic characteristics that confer adaptation to fleas19, fall ancestral to RT5 (Fig. 2b) and RISE397 (Supplementary Fig. 4), but are more derived than the LNBA lineage. Our phylogenetic and dating results thus suggest that 0.PE2 and 0.PE7 also originated during the Bronze Age, with their mean divergence here estimated to 4474 (HPD 95%: 3936–5158) and 5237 (HPD 95%: 4248–6346) years BP, respectively, based on the Bayesian skyline model (Supplementary Table 9). While these lineages may have been confined to sylvatic rodent reservoirs during the EBA, the possibility that they co circulated among human populations contemporaneously with the LNBA lineage should be considered. Although the places of origin of 0.PE2 and 0.PE7 are not known, today, their strains are isolated from modern-day China and the Caucasus region. In terms of their disease potential, both 0.PE2 and 0.PE7 possess pMT1 plasmids with fully functional ymt genes, but 0.PE2 strains lack pPCP144, and though frequently recovered from sylvatic rodent reservoirs, their virulence in humans is not known. On the other hand, the more basal 0.PE7 contains pPCP12 and has previously been associated with human bubonic plague12. It is, therefore, tempting to hypothesise that efficient flea adaptation in Y. pestis, as well as the potential for bubonic disease, might have evolved earlier than 5000 years ago.

Maximum Clade Credibility tree. The MCC tree was produced using TreeAnnotator of BEAST v1.88 and is a product of demographic analysis based on the Coalescent Skyline model, summarizing 27,001 trees. The tree was visualized in FigTree v1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/). It is presented in a temporal scale between 6,000 and 0 yBP, and the mean divergence dates of major Y. pestis lineages are indicated on each corresponding node.

It seems possible that already in the Bronze Age, with the establishment of transport and trade networks, the interconnectivity between Europe and Asia that is also reflected in the ancient human genomes, likely contributed to the spread of infectious disease. Similarly, the abundant trade routes of the medieval period are considered the main conduit for plague’s movement between Asia and Europe8,12. Our current data suggest a more complex model, where at least two human-associated lineages (LNBA and RT5) with different transmission potentials were established in Eurasia during the Bronze Age (Fig. 2b, c).

The haplogroup of RT5 is R1a1a1b-Z645 (most likely Z93, only with coverage of 1-fold), mtDNA U2e2a.

See also materials from the Max Plank Institute.


Copenhagen group: Germanic and Balto-Slavic from Bell Beaker; Indo-Anatolian homeland in the Caucasus


Article of general knowledge in Der Spiegel, Invasion from the Steppe, with comments from Willerslev and Kristiansen, appeared roughly at the same time as the Damgaard et al. Nature (2018) and Science (2018) papers were published.

NOTE. You can read the article (in German) from Kristiansen’s Academia.edu account.

Excerpts translated from German (emphasis mine):

On the Y-DNA data

Particularly striking is the genetic signature from the steppe on the Y chromosome. From this the researchers conclude that the majority of migrants were males. Kristian Kristiansen, chief archaeologist in the Willerslev team, also has an idea of ​​how this could be explained: “Maybe it’s a rite of initiation, as it was spread among the steppe peoples,” he says.

The younger sons of the Yamnaya herders, who were excluded from the succession, had to seek their fortune on their own. As part of a solemn ritual, they threw themselves to wolves’ skins and then swarmed in warlike gangs to buy their own herds by cattle-stealing.


An ally that they seem to have brought from their homeland may also have contributed to the genetic success of the steppe people: Yersinia pestis, the plague bacterium. Its genes were found by researchers from the Max Planck Institute in Jena – and apparently it emerged exactly at the same time as the Yamnaya thrust began.

About the Hittites

(…) And yet now, where Asia and Europe meet geographically, there is no trace of the Yamnaya genes. The wander-loving people from the Pontic-Caspian steppe apparently found neither the way across the Balkans nor through the Caucasus mountains.

Now the researchers are puzzled: How can it be that a language goes on a walk, without the accompanying speakers coming along? Is it possible that the Indo-European seeped into Anatolia, much like the English language spread today without the need for Englishmen?

Archaeologist Kristiansen does not believe it. The researchers would find it hard to reconsider their theories, he says: “Especially the first chapter of the story has to be rewritten.”

He suspects that there was a predecessor of the Yamnaya culture, in which a kind of Proto-Proto-Indo-European was spoken. And he also has a suspicion, where this people could have drifted around: The Caucasus, says Kristiansen, was their homeland. But that remains unproven: “There’s another hole left,” he admits.

Spread of Indo-European languages

About the Botai

The study of [the Botai] genome revealed that it was genetically radically different from the members of the Yamnaya culture. The Botai, it seems, consistently avoided any contact with their neighbors – even though they must have crossed the territory of the Botai on their migratory waves.

Willerslev assumes that the art of keeping horses from the Yamnaya steppe nomads was adopted from these peoples, and then they developed it further. At some point, the Botai could then have itself become doomed by its groundbreaking innovation: While the descendants of the Yamnaya spread over half of Eurasia, the Botai disappeared without leaving a trace.

Even more interesting than the few words that set the Copenhagen group’s views for future papers (such as the expected Maykop samples with EHG ancestry) is the artistic sketch of the Indo-European migrations, probably advised by the group.

A simple map does not mean that all members of the Danish workgroup have changed their view completely, but I would say it is a great improvement over the previous “arrows of migration” (see here), and it is especially important that they show a more realistic picture of ancient migrations to general readers.

NOTE. Especially absurd is the identification of the ‘Celtic’ expansion with the first Bell Beakers in the British Isles (that idea is hold by few, such as Koch and Cunliffe in their “Celtic from the West” series). Also inexact, but not so worrying, are the identification of ‘Germanic’ in Germany/Únětice, or the spread of ‘Baltic’ and ‘Slavic’ directly to East Europe (i.e. I guess Mierzanowice/Nitra -> Trzciniec), which is probably driven by the need to assert a close connection with early Iranians and thus with their satemization trends.

Also, as we know now thanks to Narasimhan et al. (2018), there is no need to support that convoluted west arrow (representing CWC) from West Yamna to Central Europe, and then to East Yamna, since the Proto-Indo-Iranian community – represented by the Steppe MLBA cloud that later expanded Indo-Aryan and Iranian languages – has a more direct connection with the in situ admixture of Poltavka/Abashevo within the Volga-Ural region.

I think we can keep this from the article:

Their results, as well as those of the competition labs at Harvard University and Jena’s Max Planck Institute for the History of Humanity, leave no doubt: Yes, the legendary herdsmen in the Pontic-Caspian steppe really existed. They belonged to the so-called Yamnaya culture, and they spread, as linguists had predicted, in massive migrations towards Central Europe and India – a later triumph for linguists.

This can be added to a recent comment by de Barros Damgaard:

The project has been an extremely enriching and exciting process. We were able to direct many very different academic fields towards a single coherent approach. By asking the right questions, and keeping limitations of the data in mind, contextualizing, nuancing, and keeping dialogues open between scholars of radically different backgrounds and approaches, we have carved out a path for a new field of research. We have already seen too many papers come out in which models produced by geneticists working on their own have been accepted without vital input from other fields, and, at the other extreme, seen archaeologists opposing new studies built on archaeogenetic data, due to a lack of transparency between the fields.

Data on ancient DNA is astonishing for its ability to provide a fine-grained image of early human mobility, but it does stand on the shoulders of decades of work by scholars in other fields, from the time of excavation of human skeletons to interpreting the cultural, linguistic origins of the samples. This is how cold statistics are turned into history.


Stone Age plague accompanying migrants from the steppe, probably Yamna, Balkan EBA, and Bell Beaker, not Corded Ware


In the latest revisions of the Indo-European demic diffusion model, using the results from the article Early Divergent Strains of Yersinia pestis in Eurasia 5,000 Years Ago, by Rasmussen et al., Cell (2015), I stated (more or less indirectly) that the high east-west mobility of the Corded Ware migrants across related cultures might have been responsible for the spread of this disease, which seems to have been originally expanded from Central Eurasia.

New results appeared recently in the article The Stone Age Plague and Its Persistence in Eurasia, by Valtueña et al., Current Biology (2017), which may contradict that interpretation.

Early Yamna and Corded Ware communities and their migrations ca. 3000 BC onwards.


Yersinia pestis, the etiologic agent of plague, is a bacterium associated with wild rodents and their fleas. Historically it was responsible for three pandemics: the Plague of Justinian in the 6th century AD, which persisted until the 8th century [ 1 ]; the renowned Black Death of the 14th century [ 2, 3 ], with recurrent outbreaks until the 18th century [ 4 ]; and the most recent 19th century pandemic, in which Y. pestis spread worldwide [ 5 ] and became endemic in several regions [ 6 ]. The discovery of molecular signatures of Y. pestis in prehistoric Eurasian individuals and two genomes from Southern Siberia suggest that Y. pestis caused some form of disease in humans prior to the first historically documented pandemic [ 7 ]. Here, we present six new European Y. pestis genomes spanning the Late Neolithic to the Bronze Age (LNBA; 4,800 to 3,700 calibrated years before present). This time period is characterized by major transformative cultural and social changes that led to cross-European networks of contact and exchange [ 8, 9 ]. We show that all known LNBA strains form a single putatively extinct clade in the Y. pestis phylogeny. Interpreting our data within the context of recent ancient human genomic evidence that suggests an increase in human mobility during the LNBA, we propose a possible scenario for the early spread of Y. pestis: the pathogen may have entered Europe from Central Eurasia following an expansion of people from the steppe, persisted within Europe until the mid-Bronze Age, and moved back toward Central Eurasia in parallel with human populations.

Maximum-Likelihood Tree and Percent Coverage Plot of Virulence Factors of Yersinia pestis. (A) Maximum-likelihood tree of all Yersinia pestis genomes, including 1,265 SNP positions with complete deletion. Nodes with support R95% are marked with an asterisk. The colors represent different branches in the Y. pestis phylogeny: branch 0 (black), branch 1 (red), branch 2 (green), branch 3 (blue), branch 4 (orange), and LNBA Y. pestis branch (purple). Y. pseudotuberculosis-specific SNPs were excluded from the tree for clarity of representation. In the light-colored boxes, discussed losses and gains of genomic regions and genes are indicated. Related

It seems that, notwithstanding the simplistic (white) arrows of steppe ancestry expansion shown in their map (see below), the actual expansion of Yersinia pestis might have in fact accompanied Yamna migrants from the Pontic-Caspian steppe into Early Bronze Age cultures from the Balkans, including Bell Beaker migrants, as the phylogenetic analysis and dates suggest – and as the potential arrows of the plague expansion in the map (in green) show.

Late Corded Ware migrants would have only later expanded the disease to eastern Europe, as shown in the second map, most likely because of their close contact with Bell Beaker migrants (but remaining culturally distinct from them), and indeed because of the mobility accross related Corded Ware cultures up to the Urals.

The cultural-historical community in the Late Neolithic between steppe peoples that would evolve into Uralic-speaking Sredni Stog/Corded Ware migrants in the western steppe, and Late Indo-European-speaking Yamna/SE EBA/Bell Beaker migrants originally from the eastern steppe, would allow for the spread of the disease first among steppe groups, and then from both distinct late groups into their respective expanded regions.

The phylogenetic tree of Y. pestis available right now (see above), however, seems to suggest a stronger initial link to Yamna migrants, i.e. an origin in the North Caspian steppe, and an expansion with Yamna into the north Pontic area, into the Caucasus, and with the Afansevo culture, spreading later with Balkan EBA cultures and the expansion of Bell Beaker peoples.

Instead of warring nature, close ties, and mobility of Corded Ware peoples (reasons I used to justify the rapid spread of the disease among CWC groups), I guess it was rather the higher population density of SE Europe compared to the regions north of the loess belt, as well as the greater admixture of Yamna migrants with native SE European populations, the factors which might have helped expand the disease.

Map of Proposed Yersinia pestis Circulation throughout Eurasia (A) Entrance of Y. pestis into Europe from Central Eurasia with the expansion of Yamnaya pastoralists around 4,800 years ago. (B) Circulation of Y. pestis to Southern Siberia from Europe. Only complete genomes are shown.

Nevertheless, lacking more data, it is unclear if the disease expanded with both steppe groups.