Late Quaternary dynamics of Arctic biota from ancient environmental genomics

Abstract

During the last glacial–interglacial cycle, Arctic biotas experienced substantial climatic changes, yet the nature, extent and rate of their responses are not fully understood1–8. Here we report a large-scale environmental DNA metagenomic study of ancient plant and mammal communities, analysing 535 permafrost and lake sediment samples from across the Arctic spanning the past 50,000 years. Furthermore, we present 1,541 contemporary plant genome assemblies that were generated as reference sequences. Our study provides several insights into the long-term dynamics of the Arctic biota at the circumpolar and regional scales. Our key findings include: (1) a relatively homogeneous steppe–tundra flora dominated the Arctic during the Last Glacial Maximum, followed by regional divergence of vegetation during the Holocene epoch; (2) certain grazing animals consistently co-occurred in space and time; (3) humans appear to have been a minor factor in driving animal distributions; (4) higher effective precipitation, as well as an increase in the proportion of wetland plants, show negative effects on animal diversity; (5) the persistence of the steppe–tundra vegetation in northern Siberia enabled the late survival of several now-extinct megafauna species, including the woolly mammoth until 3.9 ± 0.2 thousand years ago (ka) and the woolly rhinoceros until 9.8 ± 0.2 ka; and (6) phylogenetic analysis of mammoth environmental DNA reveals a previously unsampled mitochondrial lineage. Our findings highlight the power of ancient environmental metagenomics analyses to advance understanding of population histories and long-term ecological dynamics.

Process‐explicit models reveal pathway to extinction for woolly mammoth using pattern‐oriented validation

“…This raises the real possibility that populations of woolly mammoth persisted in mainland Arctic refugia until the mid-Holocene, as predicted by our model. Especially given that population abundances of mammoths during the Holocene would have been low (Figure 2), indicator species of mammoth persisted in Siberia during the mid-Holocene (Boeskorov, 2020), the refugial areas that we pinpoint remain poorly sampled (Figure S2), and the environmental DNA evidence of woolly mammoths in Beringia and the Taimyr Peninsula during the mid-Holocene (Wang et al, 2021). The recent discovery of the persistence of woolly mammoths in Siberia to 3.9 ka using environmental metagenomics (Wang et al, 2021) provides an important independent validation of our process-based model (Grimm et al, 2005), indicating a strong ability of the simulations to detect hidden refugia and unveil spatiotemporal pathways to extinction.…”

Placing Ancient DNA Sequences into Reference Phylogenies

“…PathPhynder has already been used to place ancient environmental bear DNA into a mitochondrial phylogeny ( Pedersen et al 2021 ). It is also possible to construct mitochondrial and possibly Y-chromosome trees using exclusively ancient samples, and then use pathPhynder to place additional, lower coverage aDNA data, as recently done for environmental mammoth mtDNA ( Wang, Pedersen, et al 2021 ).…”

Landscape Genomics Provides Evidence of Ecotypic Adaptation and a Barrier to Gene Flow at Treeline for the Arctic Foundation Species Eriophorum vaginatum

“…Together, the data demonstrates the importance of determining the extent and cause for genetic divergence between populations, which is particularly critical when developing species distribution models for climate change ( Massatti and Knowles, 2016 ; Ortego and Knowles, 2020 ) that include foundation species such as E. vaginatum . Attempts to verify the distribution of ecotypes and the adaptive potential of E. vaginatum will require expanding landscape genomic studies across entire Arctic ecosystems including refugial regions, and building on the ground-breaking genomic biodiversity work of Wang et al (2021) .…”

“…The Beringian region, which remained mostly unglaciated throughout the Pleistocene glacial-interglacial cycles, is known to have served as an important refugium for multiple arctic plant and animal species, and therefore served as sources for post-glacial expansions of these populations ( Abbott and Brochmann, 2003 ; Alsos et al, 2005 ; Brubaker et al, 2005 ). Identifying refugium origin for the contemporary distribution of arctic taxa has been an emphasis of circumpolar population genetic studies ( Alsos et al, 2005 , 2007 ), whereas evidence for differently adapted genotypes advancing from refugia has only begun to be explored ( Ikeda and Setoguchi, 2017 ; Napier et al, 2019 ; Wang et al, 2021 ).…”