Collared lemming; Demographic history; Palaeogenomics; Population structure; DNA, Ancient; Animals; Population Dynamics; Arctic Regions; Ecosystem; Arvicolinae; Ecology, Evolution, Behavior and Systematics; Environmental Science (all); General Medicine
Abstract :
[en] [en] BACKGROUND: Ancient DNA studies suggest that Late Pleistocene climatic changes had a significant effect on population dynamics in Arctic species. The Eurasian collared lemming (Dicrostonyx torquatus) is a keystone species in the Arctic ecosystem. Earlier studies have indicated that past climatic fluctuations were important drivers of past population dynamics in this species.
RESULTS: Here, we analysed 59 ancient and 54 modern mitogenomes from across Eurasia, along with one modern nuclear genome. Our results suggest population growth and genetic diversification during the early Late Pleistocene, implying that collared lemmings may have experienced a genetic bottleneck during the warm Eemian interglacial. Furthermore, we find multiple temporally structured mitogenome clades during the Late Pleistocene, consistent with earlier results suggesting a dynamic late glacial population history. Finally, we identify a population in northeastern Siberia that maintained genetic diversity and a constant population size at the end of the Pleistocene, suggesting suitable conditions for collared lemmings in this region during the increasing temperatures associated with the onset of the Holocene.
CONCLUSIONS: This study highlights an influence of past warming, in particular the Eemian interglacial, on the evolutionary history of the collared lemming, along with spatiotemporal population structuring throughout the Late Pleistocene.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Lord, Edana; Centre for Palaeogenetics, Svante Arrhenius Väg 20C, 10691, Stockholm, Sweden. edana.lord@zoologi.su.se ; Department of Zoology, Stockholm University, 10691, Stockholm, Sweden. edana.lord@zoologi.su.se ; Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Box 50007, 10405, Stockholm, Sweden. edana.lord@zoologi.su.se
Marangoni, Aurelio; Centre for Palaeogenetics, Svante Arrhenius Väg 20C, 10691, Stockholm, Sweden ; Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Box 50007, 10405, Stockholm, Sweden
Baca, Mateusz; Centre of New Technologies, University of Warsaw, S. Banacha 2C, 02-097, Warsaw, Poland
Popović, Danijela; Centre of New Technologies, University of Warsaw, S. Banacha 2C, 02-097, Warsaw, Poland
Goropashnaya, Anna V; Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK, 99775-7000, USA
Stewart, John R; Faculty of Science and Technology, Bournemouth University, Talbot Campus, Fern Barrow, Poole, BH12 5BB, Dorset, UK
Knul, Monika V; Department of Archaeology, Anthropology and Geography, University of Winchester, Winchester, SO22 4NR, UK
Noiret, Pierre ; Université de Liège - ULiège > Département des sciences historiques > Archéologie préhistorique
Germonpré, Mietje; OD Earth and History of Life, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, Brussels, Belgium
Jimenez, Elodie-Laure; OD Earth and History of Life, Royal Belgian Institute of Natural Sciences, Vautierstraat 29, Brussels, Belgium ; School of Geosciences, University of Aberdeen, Aberdeen, Scotland
Abramson, Natalia I; Department of Molecular Systematics, Zoological Institute RAS, St Petersburg, Russia
Vartanyan, Sergey; Far East Branch, N.A. Shilo North-East Interdisciplinary Scientific Research Institute Russian Academy of Sciences (NEISRI FEB RAS), 685000, Magadan, Russia
Prost, Stefan; Central Research Laboratories, Natural History Museum Vienna, 1010, Vienna, Austria ; Department of Cognitive Biology, University of Vienna, 1090, Vienna, Austria ; Konrad Lorenz Institute of Ethology, 1160, Vienna, Austria ; South African National Biodiversity Institute, National Zoological Garden, Pretoria, South Africa
Smirnov, Nickolay G; Institute of Plant and Animal Ecology UB RAS, Russian Academy of Sciences, 202 8 Marta Street, 620144, Ekaterinburg, Russia
Kuzmina, Elena A; Institute of Plant and Animal Ecology UB RAS, Russian Academy of Sciences, 202 8 Marta Street, 620144, Ekaterinburg, Russia
Olsen, Remi-André; Science for Life Laboratory (SciLifeLab), Dept of Biochemistry and Biophysics, Stockholm University, Stockholm, Sweden
Fedorov, Vadim B; Institute of Arctic Biology, University of Alaska Fairbanks, Fairbanks, AK, 99775-7000, USA
Dalén, Love; Centre for Palaeogenetics, Svante Arrhenius Väg 20C, 10691, Stockholm, Sweden. love.dalen@zoologi.su.se ; Department of Zoology, Stockholm University, 10691, Stockholm, Sweden. love.dalen@zoologi.su.se ; Department of Bioinformatics and Genetics, Swedish Museum of Natural History, Box 50007, 10405, Stockholm, Sweden. love.dalen@zoologi.su.se
Bolin Centre for Climate Research NCN - Polish National Science Centre NIGMS - National Institute of General Medical Sciences Stockholm University
Funding text :
Open access funding provided by Stockholm University. Funding was provided by Formas (2018-01640) and the Bolin Centre for Climate Research to LD, and Polish National Science Centre grant no. 2020/38/E/NZ8/00431 to MB. VBF was supported by an Institutional Development Award from the National Institute of General Medical Sciences of the NIH (P20GM103395) and Centre of Biomedical Research Excellence (Grant P20GM130443). Funding for sequencing of the nuclear genome was provided by the NIH (P20GM103395). NIA acknowledges funding from the Zoological Institute of Russian Academy of Sciences (Grant No. 075-15-2021-1069). E-LJ and MG acknowledge support from the Brain.be 2.0 ICHIE project (BELSPO B2/191/P2/ICHIE).We thank Eleftheria Palkopoulou for previous laboratory work that contributed to this study. The authors acknowledge support from the Uppsala Multidisciplinary Centre for Advanced Computational Science for assistance with massively parallel sequencing and access to the UPPMAX computational infrastructure, and resources provided by Swedish National Infrastructure for Computing (SNIC) at Uppsala partially funded by the Swedish Research Council through grant agreement no. 2018-05973. We acknowledge Becky Miller, the director of the Trou Al’Wesse excavation, and funding for the project provided annually by the Ministère de la Région wallonne, Service Public de Wallonie. We also acknowledge the AWaP (Agence Wallonne du Patrimoine) as the main funding institution of the work at Trou Al’Wesse.We thank Eleftheria Palkopoulou for previous laboratory work that contributed to this study. The authors acknowledge support from the Uppsala Multidisciplinary Centre for Advanced Computational Science for assistance with massively parallel sequencing and access to the UPPMAX computational infrastructure, and resources provided by Swedish National Infrastructure for Computing (SNIC) at Uppsala partially funded by the Swedish Research Council through grant agreement no. 2018-05973. We acknowledge Becky Miller, the director of the Trou Al’Wesse excavation, and funding for the project provided annually by the Ministère de la Région wallonne, Service Public de Wallonie. We also acknowledge the AWaP (Agence Wallonne du Patrimoine) as the main funding institution of the work at Trou Al’Wesse.
Brace S, Palkopoulou E, Dalen L, Lister AM, Miller R, Otte M, et al. Serial population extinctions in a small mammal indicate Late Pleistocene ecosystem instability. Proc Natl Acad Sci. 2012;109:20532–6.
Palkopoulou E, Baca M, Abramson NI, Sablin M, Socha P, Nadachowski A, et al. Synchronous genetic turnovers across Western Eurasia in Late Pleistocene collared lemmings. Glob Chang Biol. 2016;22:1710–21.
Campos PF, Willerslev E, Sher A, Orlando L, Axelsson E, Tikhonov A, et al. Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics. Proc Natl Acad Sci U S A. 2010;107:5675–80.
Lorenzen ED, Nogués-Bravo D, Orlando L, Weinstock J, Binladen J, Marske KA, et al. Species-specific responses of Late Quaternary megafauna to climate and humans. Nature. 2011;479:359–64.
Stewart JR, Lister AM, Barnes I, Dalén L. Refugia revisited: individualistic responses of species in space and time. Proc Biol Sci. 2010;277:661–71.
Hewitt G. The genetic legacy of the Quaternary ice ages. Nature. 2000;405:907–13.
Metcalf JL, Prost S, Nogués-Bravo D, DeChaine EG, Anderson C, Batra P, et al. Integrating multiple lines of evidence into historical biogeography hypothesis testing: a Bison bison case study. Proc Biol Sci. 2014;281:20132782.
Agadzhanyan AK. The history of collared lemmings in the Pleistocene. In: Beringia in the Cenozoic era; the Bering land bridge and its role in the history of holarctic floras and faunas in the late Cenozoic. Symposium. pascal-francis.inist.fr; 1984. p. 379–88.
Kowalski K. Lemmings [Mammalia, Rodentia] as indicators of temperature and humidity in the European Quaternary. Acta Zool Cracov. 1995;38:85–94.
Markova AK, Smirnov NG, Kozharinov AV, Kazantseva NE, Simakova AN, Kitaev LM. Late Pleistocene distribution and diversity of mammals in Northern Eurasia (PALEOFAUNA database). Paleontologia i Evolucio. 1995;28–29:5–143.
Stewart JR, Van Kolfschoten M, Markova A, Musil R. The mammalian faunas of Europe during oxygen isotope stage three. In: van Andel TH, Davies SW, editors. Neanderthals and modern humans in the European landscape during the Last Glaciation, 60,000 to 20,000 years ago: archaeological results of the Stage 3 Project. McDonald Institute Monograph Series; 2003. p. 103–29.
Ponomarev D, Puzachenko A. Evolution of occlusal shape of the first and second upper molars of Middle-Late Pleistocene collared lemmings (Dicrostonyx, Arvicolinae, Rodentia) in northeast European Russia. Boreas. 2015;44:741–59.
Prost S, Smirnov N, Fedorov VB, Sommer RS, Stiller M, Nagel D, et al. Influence of climate warming on arctic mammals? new insights from ancient DNA studies of the collared lemming Dicrostonyx torquatus. PLoS ONE. 2010;5: e10447.
Fedorov VB, Trucchi E, Goropashnaya AV, Waltari E, Whidden SE, Stenseth NC. Impact of past climate warming on genomic diversity and demographic history of collared lemmings across the Eurasian Arctic. Proc Natl Acad Sci U S A. 2020;117:3026–33.
Svensson A, Andersen KK, Bigler M, Clausen HB, Dahl-Jensen D, Davies SM, et al. The Greenland Ice Core Chronology 2005, 15–42 ka. Part 2: comparison to other records. Quat Sci Rev. 2006;25:3258–67.
Lagerholm VK, Sandoval-Castellanos E, Ehrich D, Abramson NI, Nadachowski A, Kalthoff DC, et al. On the origin of the Norwegian lemming. Mol Ecol. 2014;23:2060–71.
Lagerholm VK, Norén K, Ehrich D, Ims RA, Killengreen ST, Abramson NI, et al. Run to the hills: gene flow among mountain areas leads to low genetic differentiation in the Norwegian lemming. Biol J Linn Soc Lond. 2017;121:1–14.
Smith S, Sandoval-Castellanos E, Lagerholm VK, Napierala H, Sablin M, Von Seth J, et al. Nonreceding hare lines: genetic continuity since the Late Pleistocene in European mountain hares (Lepus timidus). Biol J Linn Soc Lond. 2017;120:891–908.
Larsson P, von Seth J, Hagen IJ, Götherström A, Androsov S, Germonpré M, et al. Consequences of past climate change and recent human persecution on mitogenomic diversity in the arctic fox. Philos Trans R Soc Lond B Biol Sci. 2019;374:20190212.
Murton JB, Opel T, Toms P, Blinov A, Fuchs M, Wood J, et al. A multimethod dating study of ancient permafrost, Batagay megaslump, east Siberia. Quat Res. 2021;105:1–22.
Li H, Durbin R. Inference of human population history from individual whole-genome sequences. Nature. 2011;475:493–6.
Uchimura A, Higuchi M, Minakuchi Y, Ohno M, Toyoda A, Fujiyama A, et al. Germline mutation rates and the long-term phenotypic effects of mutation accumulation in wild-type laboratory mice and mutator mice. Genome Res. 2015;25:1125–34.
Ehrich D, Jorde PE. High genetic variability despite high-amplitude population cycles in lemmings. J Mammal. 2005;86:380–5.
Funder S, Hjort C, Landvik JY, Nam S-I, Reeh N, Stein R. History of a stable ice margin—East Greenland during the middle and Upper Pleistocene. Quat Sci Rev. 1998;17:77–123.
Fedorov VB, Goropashnaya AV. The importance of ice ages in diversification of arctic collared lemmings (Dicrostonyx): evidence from the mitochondrial cytochrome b region. Hereditas. 1999;130:301–7.
Palkopoulou E, Dalén L, Lister AM, Vartanyan S, Sablin M, Sher A, et al. Holarctic genetic structure and range dynamics in the woolly mammoth. Pro R Soc B Biol Sci. 2013;280:20131910–20131910.
Lord E, Dussex N, Kierczak M, Díez-del-Molino D, Ryder OA, Stanton DWG, et al. Pre-extinction demographic stability and genomic signatures of adaptation in the woolly rhinoceros. Curr Biol. 2020;30:1–9.
Harington CR. Pleistocene vertebrates of the Yukon Territory. Quat Sci Rev. 2011;30:2341–54.
Fedorov VB, Trucchi E, Goropashnaya AV, Chr SN. Conflicting nuclear and mitogenome phylogenies reveal ancient mitochondrial replacement between two North American species of collared lemmings (Dicrostonyx groenlandicus, D. hudsonius). Mol Phylogenet Evol. 2022;168: 107399.
Markova AK, Puzachenko AY, van Kolfschoten T, van der Plicht J, Ponomarev DV. New data on changes in the European distribution of the mammoth and the woolly rhinoceros during the second half of the Late Pleistocene and the early Holocene. Quat Int. 2013;292:4–14.
Heller R, Chikhi L, Siegismund HR. The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS ONE. 2013;8: e62992.
Mather N, Traves SM, Ho SYW. A practical introduction to sequentially Markovian coalescent methods for estimating demographic history from genomic data. Ecol Evol. 2020;10:579–89.
Mazet O, Rodríguez W, Grusea S, Boitard S, Chikhi L. On the importance of being structured: instantaneous coalescence rates and human evolution—lessons for ancestral population size inference? Heredity. 2016;116:362–71.
Palkopoulou E, Mallick S, Skoglund P, Enk J, Rohland N, Li H, et al. Complete genomes reveal signatures of demographic and genetic declines in the woolly mammoth. Curr Biol. 2015;25:1395–400.
Binney HA, Willis KJ, Edwards ME, Bhagwat SA, Anderson PM, Andreev AA, et al. The distribution of late-Quaternary woody taxa in northern Eurasia: evidence from a new macrofossil database. Quat Sci Rev. 2009;28:2445–64.
Tarasov PE, Andreev AA, Anderson PM, Lozhkin AV, Leipe C, Haltia E, et al. A pollen-based biome reconstruction over the last 3.562 million years in the Far East Russian Arctic—new insights into climate—vegetation relationships at the regional scale. Clim Past. 2013;9:2759–75.
Bigelow NH, Brubaker LB, Edwards ME, Harrison SP, Prentice IC, Anderson PM, et al. Climate change and Arctic ecosystems: 1. Vegetation changes north of 55°N between the last glacial maximum, mid-Holocene, and present. J Geophys Res. 2003;108:8170.
Loog L, Thalmann O, Sinding M-HS, Schuenemann VJ, Perri A, Germonpré M, et al. Ancient DNA suggests modern wolves trace their origin to a Late Pleistocene expansion from Beringia. Mol Ecol. 2020;29:1596–610.
Sikora M, Pitulko VV, Sousa VC, Allentoft ME, Vinner L, Rasmussen S, et al. The population history of northeastern Siberia since the Pleistocene. Nature. 2019;570:182–8.
Boessenkool S, Hanghøj K, Nistelberger HM, Der Sarkissian C, Gondek AT, Orlando L, et al. Combining bleach and mild predigestion improves ancient DNA recovery from bones. Mol Ecol Resour. 2017;17:742–51.
Damgaard PB, Margaryan A, Schroeder H, Orlando L, Willerslev E, Allentoft ME. Improving access to endogenous DNA in ancient bones and teeth. Sci Rep. 2015;5:11184.
Knapp M, Clarke AC, Horsburgh KA, Matisoo-Smith EA. Setting the stage–building and working in an ancient DNA laboratory. Ann Anatomy-Anatomischer Anzeiger. 2012;194:3–6.
Yang DY, Eng B, Waye JS, Dudar JC, Saunders SR. Technical note: improved DNA extraction from ancient bones using silica-based spin columns. 1998;543 December 1997:539–43.
Ersmark E, Orlando L, Sandoval-Castellanos E, Barnes I, Barnett R, Stuart A, et al. Population demography and genetic diversity in the Pleistocene Cave Lion. Open Quat. 2015;1:4.
Meyer M, Kircher M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc. 2010;2010:db.prot5448.
Baca M, Doan K, Sobczyk M, Stankovic A, Węgleński P. Ancient DNA reveals kinship burial patterns of a pre-Columbian Andean community. BMC Genet. 2012;13:30.
Baca M, Popović D, Lemanik A, Baca K, Horáček I, Nadachowski A. Highly divergent lineage of narrow-headed vole from the Late Pleistocene Europe. Sci Rep. 2019;9:17799.
Horn S. Target enrichment via DNA hybridization capture. In: Shapiro B, Hofreiter M, editors. Ancient DNA: methods and protocols. Totowa, NJ: Humana Press; 2012. p. 177–88.
Maricic T, Whitten M, Pääbo S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS ONE. 2010;5: e14004.
Li R, Zhu H, Ruan J, Qian W, Fang X, Shi Z, et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 2010;20:265–72.
Butler J, MacCallum I, Kleber M, Shlyakhter IA, Belmonte MK, Lander ES, et al. ALLPATHS: de novo assembly of whole-genome shotgun microreads. Genome Res. 2008;18:810–20.
Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM, Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res. 2009;19:1117–23.
Seppey M, Manni M, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness. In: Kollmar M, editor. Gene prediction: methods and protocols. Springer, New York: New York, NY; 2019. p. 227–45.
Kutschera VE, Kierczak M, van der Valk T, von Seth J, Dussex N, Lord E, et al. GenErode: a bioinformatics pipeline to investigate genome erosion in endangered and extinct species. BMC Bioinform. 2022;23:228.
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28:1647–9.
Hahn C, Bachmann L, Chevreux B. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads—a baiting and iterative mapping approach. Nucleic Acids Res. 2013;41: e129.
Schubert M, Lindgreen S, Orlando L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res Notes. 2016;9:88.
Li H, Durbin R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics. 2010;26:589–95.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics. 2009;25:2078–9.
Milne I, Stephen G, Bayer M, Cock PJA, Pritchard L, Cardle L, et al. Using Tablet for visual exploration of second-generation sequencing data. Brief Bioinform. 2013;14:193–202.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20.
Fedorov VB, Goropashnaya AV. Complete mitochondrial genomes of the North American collared lemmings Dicrostonyx groenlandicus Traill, 1823 and Dicrostonyx hudsonius Pallas, 1778 (Rodentia: Arvicolinae). Mitochondrial DNA B Resour. 2016;1:878–9.
Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. 2004;5:113.
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods. 2012;9:772.
Rambaut A. FigTree, a graphical viewer of phylogenetic trees. See http://tree.bio.ed.ac.uk/software/figtree. 2007.
Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 2018;4:vey016.
Pečnerová P, Palkopoulou E, Wheat CW, Skoglund P, Vartanyan S, Tikhonov A, et al. Mitogenome evolution in the last surviving woolly mammoth population reveals neutral and functional consequences of small population size. Evol Lett. 2017;1:292–303.
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian Phylogenetics using tracer 1.7. Syst Biol. 2018;67:901–4.
Excofffier L, Marchi N, Marques DA, Matthey-Doret R, Gouy A, Sousa VC. fastsimcoal2: demographic inference under complex evolutionary scenarios. Bioinformatics. 2021. 10.1093/bioinformatics/btab468. DOI: 10.1093/bioinformatics/btab468
Excoffier L, Lischer HEL. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour. 2010;10:564–7.
Csilléry K, François O, Blum MGB. abc: An R package for approximate Bayesian computation (ABC). Methods Ecol Evol. 2012;3:475–9.