Phylogeography of the second plague pandemic revealed through analysis of historical Yersinia pestis genomes

Abstract

The second plague pandemic, caused by Yersinia pestis, devastated Europe and the nearby regions between the 14th and 18th centuries AD. Here we analyse human remains from ten European archaeological sites spanning this period and reconstruct 34 ancient Y. pestis genomes. Our data support an initial entry of the bacterium through eastern Europe, the absence of genetic diversity during the Black Death, and low within-outbreak diversity thereafter. Analysis of post-Black Death genomes shows the diversification of a Y. pestis lineage into multiple genetically distinct clades that may have given rise to more than one disease reservoir in, or close to, Europe. In addition, we show the loss of a genomic region that includes virulence-related genes in strains associated with late stages of the pandemic. The deletion was also identified in genomes connected with the first plague pandemic (541–750 AD), suggesting a comparable evolutionary trajectory of Y. pestis during both events.

AncientYersinia pestisgenomes provide no evidence for the origins or spread of the Justinianic Plague

“…S2), particularly since both estimates show overlapping 95 % HPD intervals (Table S5). Nevertheless, we do observe an overdispersion of substitution rates across different Y. pestis lineages (described previously in Cui et al, 2013 and Spyrou et al, 2019) with the highest estimate here yielding an 17-fold deviation from the mean (2.46E-07).…”

“…1C; Table S3). The third scenario is of particular interest in the context of a recently discovered genome from Laishevo, Russia (Spyrou et al, 2019) which could be identical to DA147. Therefore, DA147 might instead offer currently unexplored insights into the origin of the Black Death.…”

“…Previously published data demonstrating the absence of detectable genetic changes in Y. pestis and its extremely rapid movement during the Black Death in Europe (1347–1353 AD; (Namouchi et al, 2018; Spyrou et al, 2019, 2016) clearly indicate that this pathogen is able to travel vast geographic expanses quickly, without accumulating genetic diversity in the process. As such, the depth of the time interval for the coalescence of DA101 and the Justinianic genomes offers little to no evidence on the temporal or geographic origin of the Justinianic Plague (beginning in 541 AD, Fig.…”

“…The recent sequencing of dozens of pathogen genomes reconstructed from ancient DNA enabled increased-resolution phylogeographic studies on the spread of infectious diseases in prehistoric and historic times, especially in the context of human migration, mobility and trade (Andrades Valtueña et al, 2017; Bos et al, 2016; Keller et al, 2019; Namouchi et al, 2018; Rascovan et al, 2019; Rasmussen et al, 2015; Spyrou et al, 2019, 2016; Vågene et al, 2018). This is especially true for plague with its long and richly documented history and the abundance of published ancient genomes of its causative agent, Yersinia pestis .…”

“…For the Second Pandemic, the geographic origin and the possible persistence within Europe after the Black Death (1346–1352 AD) are the subject of ongoing scientific and scholarly discussion (Bos et al, 2016; Namouchi et al, 2018; Schmid et al, 2015; Spyrou et al, 2016; Spyrou et al, 2019). Whereas the first comprehensive phylogenetic study on Y. pestis favoured an East Asian origin (Cui et al, 2013), other scenarios assume an origin in Central Asia or the Caucasus (Benedictow, 2004; Namouchi et al, 2018; Sussman, 2011).…”