Genome-scale sequencing and analysis of human, wolf and bison DNA from 25,000 year-old sediment

Abstract

SummaryArchaeological sediments have been shown to preserve ancient DNA, but so far have not yielded genome-scale information of the magnitude of skeletal remains. We retrieved and analysed human and mammalian low-coverage nuclear and high-coverage mitochondrial genomes from Upper Palaeolithic sediments from Satsurblia cave, western Georgia, dated to 25,000 years ago. First, a human female genome with substantial basal Eurasian ancestry, which was an ancestry component of the majority of post-Ice Age people in the Near East, North Africa, and parts of Europe. Second, a wolf genome that is basal to extant Eurasian wolves and dogs and represents a previously unknown, likely extinct, Caucasian lineage that diverged from the ancestors of modern wolves and dogs before these diversified. Third, a bison genome that is basal to present-day populations, suggesting that population structure has been substantially reshaped since the Last Glacial Maximum. Our results provide new insights into the late Pleistocene genetic histories of these three species, and demonstrate that sediment DNA can be used not only for species identification, but also be a source of genome-wide ancestry information and genetic history.HighlightsWe demonstrate for the first time that genome sequencing from sediments is comparable to that of skeletal remainsA single Pleistocene sediment sample from the Caucasus yielded three low-coverage mammalian ancient genomesWe show that sediment ancient DNA can reveal important aspects of the human and faunal pastEvidence of an uncharacterized human lineage from the Caucasus before the Last Glacial Maximum∼0.01-fold coverage wolf and bison genomes are both basal to present-day diversity, suggesting reshaping of population structure in both species

Environmental DNA and metagenomics of terrestrial mammals as keystone taxa of recent and past ecosystems

“…The use of metagenomic data in palaeoecology is currently gathering momentum, and recent papers using ancient eDNA have integrated a genomic perspective in the analysis of these data. This is exemplified by the cave sediment studies of Gelabert et al (2021), who retrieved genomic data of humans, wolves, and bison, and by the study of Pedersen et al (2021), in which genomic data of black bears and giant short-faced bears were placed in a phylogenetic context. While such studies are challenging due to uncertainties regarding DNA shedding, eDNA distribution, and aDNA taphonomy, they can reveal genome-wide changes in terrestrial mammals.…”

“…A current increase in the use of cave deposits was fuelled by the finding that cave sediments can provide data on past hominin presence (Slon et al 2017, Zhang et al 2020, Vernot et al 2021). Cave sediments from different climatic regions have been targeted for non‐hominin mammals, revealing, for example 25000‐year‐old DNA of wolves and bison from a cave in the Caucasus, Georgia (Gelabert et al 2021), black bears Ursus americanus and giant short‐faced bears Arctodus simus in northern Mexico (Pedersen et al 2021), extirpated red deer Cervus elpahus from a cave in Ireland (Carden et al 2012), and various mammals from a cave in Australia (Haouchar et al 2014). Moreover, stalagmites in a cave in Georgia were shown to contain aDNA of various mammals such as bears Ursus sp., roe deer Capreolus sp., and horseshoe bats Rhinolophus sp.…”

Integrating multi-taxon palaeogenomes and sedimentary ancient DNA to study past ecosystem dynamics

“…With the application of shotgun metagenomics and target enrichment approaches, it is now possible to recover haplotypic and genomic information directly from sed aDNA [ 43 – 45 , 47 – 49 ], which enables the exploration of population-level changes and has the potential to detect the arrival or disappearance of alleles and lineages in a region, as recently showcased for Neanderthals from a cave in Spain [ 48 ]. This expansion of sed aDNA into environmental palaeogenomics, together with the integration of sed aDNA and traditional palaeogenomic data derived from body fossils [ 55 ], will open up new approaches to understanding past biodiversity changes that are inaccessible with other palaeoecological proxies.…”

“…Although palaeogenetic data from multiple taxa have been used to contrast demographic histories (e.g. [ 61 , 62 ]), recent genomic studies have inferred the genetic ancestries and histories of multiple mammalian taxa from a single Pleistocene cave sed aDNA sample [ 44 , 45 ]. Another study inferred a clear parallel between dog and human lineage diversification by overlaying their population histories [ 25 ].…”

“…Similarly, sed aDNA could be used to test for ecosystem changes and examine the impact of human arrival on the abundance of another species in real time, in an approach similar to Gelabert et al . [ 45 ]. For example, early human populations may have competed with cave-dwelling species for shelter (e.g.…”