Historical climate data indicate that the Earth has passed through multiple geological periods with much warmer-than-present climates, including epochs of the Miocene (23-5.3 mya BP) with temperatures 3-4°C above present, and more recent interglacial stages of the Quaternary, for example, Marine Isotope Stage 11c (approx. 425-395 ka BP) and Middle Holocene thermal maximum (7.5-4.2 ka BP), during which continental glaciers may have melted entirely. Such warm periods would have severe consequences for ice-obligate fauna in terms of their distribution, biodiversity and population structure. To determine the impacts of these climatic events in the Nordic cryosphere, we surveyed ice habitats throughout mainland Norway and Svalbard ranging from maritime glaciers to continental ice patches (i.e. non-flowing, inland ice subjected to deep freezing overwinter), finding particularly widespread populations of ice-inhabiting bdelloid rotifers. Combined mitochondrial and nuclear DNA sequencing identified approx. 16 undescribed, species-level rotifer lineages that revealed an ancestry predating the Quaternary (> 2.58 mya). These rotifers also displayed robust freeze/thaw tolerance in laboratory experiments. Collectively, these data suggest that extensive ice refugia, comparable with stable ice patches across the contemporary Norwegian landscape, persisted in the cryosphere over geological time, and may have facilitated the long-term survival of ice-obligate Metazoa before and throughout the Quaternary.

Biology Department Rutgers The State University of New Jersey Camden NJ 08103 USA

Department of Animal Taxonomy and Ecology Adam Mickiewicz University Poznań Poland

Department of Aquaculture and Fish Diseases Fisheries Faculty Firat University Elazig 23119 Turkey

Department of Earth Science University of Bergen Bergen Norway

Department of Geography Norwegian University of Science and Technology Trondheim Norway

Department of Natural History NTNU University Museum Norwegian University of Science and Technology Trondheim 7491 Norway

Department of Terrestrial Biodiversity Norwegian Institute for Nature Research Trondheim Norway

Institute of Life and Environmental Sciences University of Iceland Askja Sturlugata 7 Reykjavík Iceland

Laboratory of Non Mendelian Evolution Institute of Animal Physiology and Genetics Academy of Sciences of the Czech Republic Liběchov Czech Republic

National Biodiversity Future Center Palermo Italy

National Research Council of Italy Water Research Institute Verbania Italy

Norwegian Veterinary Institute Angelltrøa PB 4024 7457 Trondheim Norway

Zobrazit více v PubMed

Roman Dial C, et al. 2012. Historical biogeography of the North American glacier ice worm, Mesenchytraeus solifugus (Annelida: Oligochaeta: Enchytraeidae). Mol. Phylogenet. Evol. 63 , 577–584. ( 10.1016/j.ympev.2012.01.008) PubMed DOI

Garlasché G, et al. 2020. A dataset on the distribution of Rotifera in Antarctica. Biogeographia 35 , 17–25. ( 10.21426/B635044786) DOI

Zawierucha K, et al. 2021. A hole in the nematosphere: tardigrades and rotifers dominate the cryoconite hole environment, whereas nematodes are missing. J. Zool. 313 , 18–36. ( 10.1111/jzo.12832) DOI

Shain DH, Iakovenko NS, Cridge AG, Novis PM, Plášek V, Dearden PK. 2022. Microinvertebrate colonization of New Zealand’s thermally extreme environments. Evol. Biol. 49 , 414–423. ( 10.1007/s11692-022-09578-w) DOI

You Y, Huber M, Müller RD, Poulsen CJ, Ribbe J. 2009. Simulation of the Middle Miocene Climate Optimum. Geophys. Res. Lett. 36 , 1–5. ( 10.1029/2008GL036571) DOI

Masson-Delmotte V, et al. 2006. Past temperature reconstructions from deep ice cores: relevance for future climate change. Clim. Past 2 , 145–165. ( 10.5194/cp-2-145-2006) DOI

Nesje A, Bakke J, Dahl SO, Lie Ø, Matthews JA. 2008. Norwegian mountain glaciers in the past, present and future. Glob. Planet. Change 60 , 10–27. ( 10.1016/j.gloplacha.2006.08.004) DOI

Nesje A. 2009. Latest Pleistocene and Holocene alpine glacier fluctuations in Scandinavia. Quat. Sci. Rev. 28 , 2119–2136. ( 10.1016/j.quascirev.2008.12.016) DOI

Reyes AV, Carlson AE, Beard BL, Hatfield RG, Stoner JS, Winsor K, Welke B, Ullman DJ. 2014. South Greenland ice-sheet collapse during Marine Isotope Stage 11. Nature 510 , 525–528. ( 10.1038/nature13456) PubMed DOI

Robinson A, Alvarez-Solas J, Calov R, Ganopolski A, Montoya M. 2017. MIS-11 duration key to disappearance of the Greenland ice sheet. Nat. Commun. 8 , 16008. ( 10.1038/ncomms16008) PubMed DOI PMC

Irvalı N, Galaasen EV, Ninnemann US, Rosenthal Y, Born A, Kleiven HKF. 2020. A low climate threshold for south Greenland Ice Sheet demise during the Late Pleistocene. Proc. Natl Acad. Sci. USA 117 , 190–195. ( 10.1073/pnas.1911902116) PubMed DOI PMC

Tzedakis PC, Hodell DA, Nehrbass-Ahles C, Mitsui T, Wolff EW. 2022. Marine Isotope Stage 11c: an unusual interglacial. Quat. Sci. Rev. 284 , 107493. ( 10.1016/j.quascirev.2022.107493) DOI

van de Wal RSW, et al. 2022. A high-end estimate of sea level rise for practitioners. Earths Future 10 , e2022EF002751. ( 10.1029/2022EF002751) PubMed DOI PMC

Coulson SJ, Midgley NG. 2012. The role of glacier mice in the invertebrate colonisation of glacial surfaces: the moss balls of the Falljökull, Iceland. Polar Biol. 35 , 1651–1658. ( 10.1007/s00300-012-1205-4) DOI

Folmer O, Hoeh WR, Black MB, Vrijenhoek RC. 1994. Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. Mol. Marine Biol. Biotechnol. 3 , 294–299. PubMed

Zhang Y, Xu S, Sun C, Dumont H, Han BP. 2021. A new set of highly efficient primers for COI amplification in rotifers. Mitochondrial DNA B Resour. 6 , 636–640. ( 10.1080/23802359.2021.1878951) PubMed DOI PMC

Shain DH, et al. 2016. Colonization of maritime glacier ice by bdelloid Rotifera. Mol. Phylogenet. Evol. 98 , 280–287. ( 10.1016/j.ympev.2016.02.020) PubMed DOI

Gómez A, Serra M, Carvalho GR, Lunt DH. 2002. Speciation in ancient cryptic species complexes: evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 56 , 1431–1444. ( 10.1111/j.0014-3820.2002.tb01455.x) PubMed DOI

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35 , 1547–1549, ( 10.1093/molbev/msy096) PubMed DOI PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J. Mol. Biol. 215 , 403–410. ( 10.1016/S0022-2836(05)80360-2) PubMed DOI

Katoh K, Misawa K, Kuma K ichi, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30 , 3059–3066. ( 10.1093/nar/gkf436) PubMed DOI PMC

Puillandre N, Brouillet S, Achaz G. 2021. ASAP: assemble species by automatic partitioning. Mol. Ecol. Resour. 21 , 609–620. ( 10.1111/1755-0998.13281) PubMed DOI

Zhang J, Kapli P, Pavlidis P, Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29 , 2869–2876. ( 10.1093/bioinformatics/btt499) PubMed DOI PMC

Fujisawa T, Barraclough TG. 2013. Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Syst. Biol. 62 , 707–724. ( 10.1093/sysbio/syt033) PubMed DOI PMC

Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59 , 307–321. ( 10.1093/sysbio/syq010) PubMed DOI

Bouckaert R, et al. 2019. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 15 , e1006650. ( 10.1371/journal.pcbi.1006650) PubMed DOI PMC

Posada D. 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25 , 1253–1256. ( 10.1093/molbev/msn083) PubMed DOI

Tang CQ, Obertegger U, Fontaneto D, Barraclough TG. 2014. Sexual species are separated by larger genetic gaps than asexual species in rotifers. Evolution 68 , 2901–2916. ( 10.1111/evo.12483) PubMed DOI PMC

Vasilikopoulos A, Herlyn H, Fontaneto D, Wilson CG, Nowell RW, Flot JF, Barraclough TG, Van Doninck K. 2023. Whole-genome analyses converge to support the Hemirotifera hypothesis within Syndermata (Gnathifera). Hydrobiologia ( 10.1007/s10750-023-05451-9) DOI

Knowlton N, Weigt LA. 1998. New dates and new rates for divergence across the Isthmus of Panama. Proc. R. Soc. Lond. B 265 , 2257–2263. ( 10.1098/rspb.1998.0568) DOI

Ho SY. 2020. The molecular clock and evolutionary rates across the tree of life. In The molecular evolutionary clock: theory and practice, pp. 3–23. Cham, Switzerland: Springer Nature. ( 10.1007/978-3-030-60181-2) DOI

Martin AP, Palumbi SR. 1993. Body size, metabolic rate, generation time, and the molecular clock. Proc. Natl Acad. Sci. USA 90 , 4087–4091. ( 10.1073/pnas.90.9.4087) PubMed DOI PMC

Gillooly JF, Allen AP, West GB, Brown JH. 2005. The rate of DNA evolution: effects of body size and temperature on the molecular clock. Proc. Natl Acad. Sci. USA 102 , 140–145. ( 10.1073/pnas.0407735101) PubMed DOI PMC

Wilke T, Schultheiß R, Albrecht C. 2009. As time goes by: a simple fool’s guide to molecular clock approaches in invertebrates . Am. Malacol. Bull. 27 , 25–45. ( 10.4003/006.027.0203) DOI

Buda J, et al. 2020. Biotope and biocenosis of cryoconite hole ecosystems on Ecology Glacier in the maritime Antarctic. Sci. Total Environ. 724 , 138112, ( 10.1016/j.scitotenv.2020.138112) PubMed DOI

Iakovenko NS, et al. 2015. Antarctic bdelloid rotifers: diversity, endemism and evolution. Hydrobiologia 761 , 5–43. ( 10.1007/s10750-015-2463-2) DOI

Cakil ZV, et al. 2021. Comparative phylogeography reveals consistently shallow genetic diversity in a mitochondrial marker in Antarctic bdelloid rotifers. J. Biogeogr. 48 , 1797–1809. ( 10.1111/jbi.14116) DOI

Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 , 585–595. ( 10.1093/genetics/123.3.585) PubMed DOI PMC

Ødegård RS, Nesje A, Isaksen K, Andreassen LM, Eiken T, Schwikowski M, Uglietti C. 2017. Climate change threatens archaeologically significant ice patches: insights into their age, internal structure, mass balance and climate sensitivity. Cryosphere 11 , 17–32. ( 10.5194/tc-11-17-2017) DOI

Rounce DR, et al. 2023. Global glacier change in the 21st century: every increase in temperature matters. Science 379 , 78–83. ( 10.1126/science.abo1324) PubMed DOI

Shmakova L, Malavin S, Iakovenko N, Vishnivetskaya T, Shain D, Plewka M, Rivkina E. 2021. A living bdelloid rotifer from 24,000-year-old Arctic permafrost. Curr. Biol. 31 , R712–R713, ( 10.1016/j.cub.2021.04.077) PubMed DOI

Fontaneto D, Bunnefeld N, Westberg M. 2012. Long-term survival of microscopic animals under desiccation is not so long. Astrobiology 12 , 863–869. ( 10.1089/ast.2012.0828) PubMed DOI

Edwards JS. 1986. How small ectotherms thrive in the cold without really trying. Cryo. Lett 6 , 388–390.

Linge H, Nesje A, Matthews JA, Fabel D, Xu S. 2020. Evidence for rapid paraglacial formation of rock glaciers in southern Norway from DOI

Martinsen JRP. 2012. Ice patches as archaeological contexts: a multidisciplinary approach. MSc thesis, Norwegain University of Science and Technology, Trondheim, Norway.

Shain D, Rogozhina I, Fontaneto D, Nesje A, Saglam N, Bartlett Jet al. 2024. Supplementary material from "ice-inhabiting species of Bdelloidea Rotifera reveal a pre-Quaternary ancestry in the Arctic Cryosphere. Figshare. ( 10.6084/m9.figshare.c.7279742) PubMed DOI PMC

Ice-inhabiting species of Bdelloidea Rotifera reveal a pre-Quaternary ancestry in the Arctic cryosphere