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Pre-extinction Demographic Stability and Genomic Signatures of Adaptation in the Woolly Rhinoceros
Stockholm University, Faculty of Science, Department of Zoology. Centre for Palaeogenetics, Sweden; Swedish Museum of Natural History, Sweden.ORCID iD: 0000-0002-4717-1988
Stockholm University, Faculty of Science, Department of Zoology. Centre for Palaeogenetics, Sweden; Swedish Museum of Natural History, Sweden.ORCID iD: 0000-0002-9179-8593
Stockholm University, Faculty of Science, Department of Zoology. Centre for Palaeogenetics, Sweden.
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Number of Authors: 302020 (English)In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 30, no 19, p. 3871-3879Article in journal (Refereed) Published
Abstract [en]

Ancient DNA has significantly improved our understanding of the evolution and population history of extinct megafauna. However, few studies have used complete ancient genomes to examine species responses to climate change prior to extinction. The woolly rhinoceros (Coelodonta antiquitatis) was a cold-adapted megaherbivore widely distributed across northern Eurasia during the Late Pleistocene and became extinct approximately 14 thousand years before present (ka BP). While humans and climate change have been proposed as potential causes of extinction [1-3], knowledge is limited on how the woolly rhinoceros was impacted by human arrival and climatic fluctuations [2]. Here, we use one complete nuclear genome and 14 mitogenomes to investigate the demographic history of woolly rhinoceros leading up to its extinction. Unlike other northern megafauna, the effective population size of woolly rhinoceros likely increased at 29.7 ka BP and subsequently remained stable until close to the species' extinction. Analysis of the nuclear genome from a similar to 18.5-ka-old specimen did not indicate any increased inbreeding or reduced genetic diversity, suggesting that the population size remained steady for more than 13 ka following the arrival of humans [4]. The population contraction leading to extinction of the woolly rhinoceros may have thus been sudden and mostly driven by rapid warming in the Bolling-Allerod interstadial. Furthermore, we identify woolly rhinoceros-specific adaptations to arctic climate, similar to those of the woolly mammoth. This study highlights how species respond differently to climatic fluctuations and further illustrates the potential of palaeogenomics to study the evolutionary history of extinct species.

Place, publisher, year, edition, pages
2020. Vol. 30, no 19, p. 3871-3879
National Category
Biological Sciences
Identifiers
URN: urn:nbn:se:su:diva-187625DOI: 10.1016/j.cub.2020.07.046ISI: 000579845200056PubMedID: 32795436OAI: oai:DiVA.org:su-187625DiVA, id: diva2:1517259
Available from: 2021-01-13 Created: 2021-01-13 Last updated: 2022-09-04Bibliographically approved
In thesis
1. Investigating the impacts of Late Pleistocene climate change on Arctic mammals using palaeogenomics
Open this publication in new window or tab >>Investigating the impacts of Late Pleistocene climate change on Arctic mammals using palaeogenomics
2022 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The climatic fluctuations of the Late Pleistocene likely had a large impact on the evolutionary history of Arctic species. Palaeogenomics is a useful tool to shed light on how past populations responded to these climatic shifts and the associated ice sheet dynamics and sea level change. Here, I have used modern and ancient DNA data from four Arctic mammals in order to investigate the impacts of Late Pleistocene climate on their evolutionary histories, from population dynamics and demography, to speciation and gene flow, adaptation, and genome erosion. In Paper I, using ancient mitogenomes from across their Late Pleistocene range, I showed that the Eurasian collared lemming (Dicrostonyx torquatus) had a dynamic Late Pleistocene population structure in Europe. Furthermore, the Eemian interglacial likely led to a bottleneck in collared lemmings, after which the species diversified during the Last Glacial period. Nuclear genome data from a modern individual in northeastern Siberia suggests population stability in northeastern Siberia during the Holocene. In Paper II, I sequenced the nuclear genome of a ~18,500 year old woolly rhinoceros (Coelodonta antiquitatis) and used this in combination with mitochondrial data to explore the demographic history of the species. There was little geographic structuring in the northeast Siberian population, and stability in their effective population size just prior to extinction, which may indicate a subsequent rapid decline towards extinction, likely associated with the Bølling-Allerød interstadial. Additionally, I found that this species had mutations in TRPA1, a gene involved in temperature sensitivity. In a third study (Paper III), I used whole genome data from modern and ancient true lemmings (Lemmus sp.) to determine that the Norwegian lemming (L. lemmus) has one of the youngest speciation times (~37-34 ka BP) of mammals. Norwegian lemmings have mutations in genes involved in coat colour, colour perception, fat transport and reproduction, and likely evolved their unique colouration as a result of isolation after the recolonisation of Fennoscandia. Finally, we examined the consequences of long-term small effective population size in muskox (Ovibos moschatus) using 107 modern nuclear genomes and one 21,000 year old Siberian genome (Paper IV). While muskox survived the warming at the end of the Late Pleistocene, the successive founder events experienced during its colonisation of the Canadian Arctic and Greenland reduced the genetic diversity to some of the lowest values observed in mammals. However, the results suggest that the long-term small population size likely led to purging of strongly deleterious alleles in the muskox, allowing them to persist to today with limited evidence of inbreeding depression. From a technical point, this thesis presents four de-novo genome assemblies, and the first whole nuclear genomes for these Arctic species. Taken together, the results in this thesis show that the climatic fluctuations, in particular the Eemian interglacial and Bølling-Allerød interstadial, along with sea level change and the formation and retreat of ice sheets during the Last Glacial Maximum have influenced the evolutionary histories of these four Arctic mammals.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2022. p. 43
Keywords
palaeogenomics, Arctic, Late Pleistocene, past climate, collared lemming, woolly rhinoceros, Norwegian lemming, muskox, demography, population structure, speciation, adaptation, genome erosion
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-208657 (URN)978-91-7911-994-2 (ISBN)978-91-7911-995-9 (ISBN)
Public defence
2022-10-21, Vivi Täckholmsalen (Q-salen), NPQ-huset, Svante Arrhenius väg 20, Stockholm, 13:00 (English)
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Available from: 2022-09-28 Created: 2022-09-04 Last updated: 2022-09-16Bibliographically approved

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Lord, EdanaDussex, NicolasKierczak, MarcinDíez-del-Molino, DavidStanton, David W. G.Götherström, AndersDalén, Love

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