Pleistocene mitogenomes reconstructed from the environmental DNA of permafrost sediments

Tyler J Murchie; Emil Karpinski; Katherine Eaton; Ana T Duggan; Sina Baleka; Grant Zazula; Ross D E MacPhee; Duane Froese; Hendrik N Poinar

doi:10.1016/j.cub.2021.12.023

Pleistocene mitogenomes reconstructed from the environmental DNA of permafrost sediments

Curr Biol. 2022 Feb 28;32(4):851-860.e7. doi: 10.1016/j.cub.2021.12.023. Epub 2022 Jan 10.

Authors

Tyler J Murchie¹, Emil Karpinski², Katherine Eaton³, Ana T Duggan³, Sina Baleka⁴, Grant Zazula⁵, Ross D E MacPhee⁶, Duane Froese⁷, Hendrik N Poinar⁸

Affiliations

¹ McMaster Ancient DNA Centre, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Department of Anthropology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada. Electronic address: murchiet@mcmaster.ca.
² McMaster Ancient DNA Centre, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada.
³ McMaster Ancient DNA Centre, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Department of Anthropology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada.
⁴ McMaster Ancient DNA Centre, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada.
⁵ Yukon Government, Palaeontology Program, Department of Tourism and Culture, Box 2703, Whitehorse, YT Y1A 2C6, Canada; Collections and Research, Canadian Museum of Nature, PO Box 3443, Station D, Ottawa, ON K1P 6P4, Canada.
⁶ Division of Vertebrate Zoology/Mammalogy, American Museum of Natural History, 200 Central Park West, New York, NY 10024, USA.
⁷ Department of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB T6G 2E3, Canada. Electronic address: duane@ualberta.ca.
⁸ McMaster Ancient DNA Centre, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Department of Anthropology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Department of Biochemistry, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; CIFAR, Humans and the Microbiome Program, MaRS Centre, West Tower, 661 University Avenue, Suite 505, Toronto, ON M5G 1M1, Canada. Electronic address: poinarh@mcmaster.ca.

PMID: 35016010
DOI: 10.1016/j.cub.2021.12.023

Abstract

Traditionally, paleontologists have relied on the morphological features of bones and teeth to reconstruct the evolutionary relationships of extinct animals.¹ In recent decades, the analysis of ancient DNA recovered from macrofossils has provided a powerful means to evaluate these hypotheses and develop novel phylogenetic models.² Although a great deal of life history data can be extracted from bones, their scarcity and associated biases limit their information potential. The paleontological record of Beringia³-the unglaciated areas and former land bridge between northeast Eurasia and northwest North America-is relatively robust thanks to its perennially frozen ground favoring fossil preservation.⁴^,⁵ However, even here, the macrofossil record is significantly lacking in small-bodied fauna (e.g., rodents and birds), whereas questions related to migration and extirpation, even among well-studied taxa, remain crudely resolved. The growing sophistication of ancient environmental DNA (eDNA) methods have allowed for the identification of species within terrestrial/aquatic ecosystems,^6-12 in paleodietary reconstructions,^13-19 and facilitated genomic reconstructions from cave contexts.⁸^,^20-22 Murchie et al.⁶^,²³ used a capture enrichment approach to sequence a diverse range of faunal and floral DNA from permafrost silts deposited during the Pleistocene-Holocene transition.²⁴ Here, we expand on their work with the mitogenomic assembly and phylogenetic placement of Equus caballus (caballine horse), Bison priscus (steppe bison), Mammuthus primigenius (woolly mammoth), and Lagopus lagopus (willow ptarmigan) eDNA from multiple permafrost cores spanning the last 40,000 years. We identify a diverse metagenomic spectra of Pleistocene fauna and identify the eDNA co-occurrence of distinct Eurasian and American mitogenomic lineages.

Keywords: Late Quaternary extinctions; Yukon horse; ancient environmental DNA; ancient mitochondrial genomes; metagenomics; permafrost; phylogenetics; steppe bison; willow ptarmigan; woolly mammoth.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Animals
DNA, Ancient
DNA, Environmental*
DNA, Mitochondrial / genetics
Ecosystem
Fossils
Genome, Mitochondrial*
Horses / genetics
Mammoths* / genetics
Permafrost*
Phylogeny

Substances

DNA, Ancient
DNA, Environmental
DNA, Mitochondrial