Abstract
Over the course of the last several million years of evolution, humans probably have been plagued by hundreds or perhaps thousands of epidemics. Little is known about such ancient epidemics and a deep evolutionary perspective on current pathogenic threats is lacking. The study of past epidemics has typically been limited in temporal scope to recorded history, and in physical scope to pathogens that left sufficient DNA behind, such as Yersinia pestis during the Great Plague. Host genomes, however, offer an indirect way to detect ancient epidemics beyond the current temporal and physical limits. Arms races with pathogens have shaped the genomes of the hosts by driving a large number of adaptations at many genes, and these signals can be used to detect and further characterize ancient epidemics. Here, we detect the genomic footprints left by ancient viral epidemics that took place in the past approximately 50 000 years in the 26 human populations represented in the 1000 Genomes Project. By using the enrichment in signals of adaptation at approximately 4500 host loci that interact with specific types of viruses, we provide evidence that RNA viruses have driven a particularly large number of adaptive events across diverse human populations. These results suggest that different types of viruses may have exerted different selective pressures during human evolution. Knowledge of these past selective pressures will provide a deeper evolutionary perspective on current pathogenic threats.This article is part of the theme issue ‘Insights into health and disease from ancient biomolecules’.
Highlights
About 40 years ago and for the first time in their evolution, humans eradicated a virus that had claimed countless lives, the Variola virus known as the causal agent of smallpox [1]
We further find that the selective sweeps enrichment is much more pronounced at RNA virus-interacting proteins (VIPs) compared to DNA VIPs
We observe some enrichment when using the rank thresholds from top 2000 to top 500, suggesting weaker sweeps signals at DNA VIPs. These results suggest that RNA viruses exerted a more drastic selective pressure driving a larger number of strong selective events compared to DNA viruses during recent human evolution
Summary
About 40 years ago and for the first time in their evolution, humans eradicated a virus that had claimed countless lives, the Variola virus known as the causal agent of smallpox [1]. In order to identify viruses that drove ancient epidemics, we can use present interactions as proxies for the interactions with ancient viruses from the same phylogenetic family Using this approach, we previously found evidence that 50 000 years ago [13,14,15,16,17], Neanderthals appear to have infected the modern human ancestors of present Europeans with one or multiple RNA viruses, as shown by the fact that European modern humans harbour substantially more and substantially longer introgressed Neanderthal DNA at genes that interact with RNA viruses compared to genes that interact with DNA viruses [11]. These results validate previous results and are consistent with RNA viruses being a significant selective pressure in the past 50 000 years of human evolution
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