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Mitogenome evolution in the last surviving woolly mammoth population reveals neutral and functional consequences of small population size
Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden.ORCID iD: 0000-0001-9350-1987
Stockholm University, Faculty of Science, Department of Zoology. Swedish Museum of Natural History, Sweden; Harvard Medical School, Massachusetts.
Stockholm University, Faculty of Science, Department of Zoology.
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2017 (English)In: Evolution Letters, ISSN 2056-3744, Vol. 1, no 6, p. 292-303Article in journal (Refereed) Published
Abstract [en]

The onset of the Holocene was associated with a global temperature increase, which led to a rise in sea levels and isolation of the last surviving population of woolly mammoths on Wrangel Island. Understanding what happened with the population's genetic diversity at the time of the isolation and during the ensuing 6000 years can help clarify the effects of bottlenecks and subsequent limited population sizes in species approaching extinction. Previous genetic studies have highlighted questions about how the Holocene Wrangel population was established and how the isolation event affected genetic diversity. Here, we generated high-quality mitogenomes from 21 radiocarbon-dated woolly mammoths to compare the ancestral large and genetically diverse Late Pleistocene Siberian population and the small Holocene Wrangel population. Our results indicate that mitogenome diversity was reduced to one single haplotype at the time of the isolation, and thus that the Holocene Wrangel Island population was established by a single maternal lineage. Moreover, we show that the ensuing small effective population size coincided with fixation of a nonsynonymous mutation, and a comparative analysis of mutation rates suggests that the evolutionary rate was accelerated in the Holocene population. These results suggest that isolation on Wrangel Island led to an increase in the frequency of deleterious genetic variation, and thus are consistent with the hypothesis that strong genetic drift in small populations leads to purifying selection being less effective in removing deleterious mutations.

Place, publisher, year, edition, pages
2017. Vol. 1, no 6, p. 292-303
Keywords [en]
Mammuthus primigenius, mitochondrial genomes, woolly mammoth, Wrangel Island
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
URN: urn:nbn:se:su:diva-149647DOI: 10.1002/evl3.33OAI: oai:DiVA.org:su-149647DiVA, id: diva2:1163637
Available from: 2017-12-07 Created: 2017-12-07 Last updated: 2018-09-07Bibliographically approved
In thesis
1. Genomic analysis of the process leading up to the extinction of the woolly mammoth
Open this publication in new window or tab >>Genomic analysis of the process leading up to the extinction of the woolly mammoth
2018 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Species worldwide are subject to contractions in both abundance and geographical range, and their persistence in a changing environment may thus depend on the ability to survive in small and fragmented populations. Despite the urgent need to understand how extinction works, our knowledge of pre-extinction genetic processes is limited because techniques allowing population and conservation genomics to be studied in wild threatened populations have become available only recently. In this thesis, I used the last surviving population of the woolly mammoth (Mammuthus primigenius) as a model for studying pre-extinction population dynamics. I used ancient DNA as a tool to study microevolutionary processes in real time, analysing genetic changes in response to environmental shifts at the end of the last Ice Age and exploring impacts of genetic drift and inbreeding as woolly mammoths became isolated on Wrangel Island and survived for 6000 years at small population size. Using mitochondrial genomes, I found evidence of a founder effect that decreased the maternal diversity to a single lineage at the time when mammoths became trapped on Wrangel Island (~10,500 years ago). Moreover, a two- to three-fold higher mitochondrial mutation rate in Holocene and a fixed, potentially detrimental mutation in the ATP6 gene encoding for one of the key enzymes of the oxidative phosphorylation pathway, is consistent with the hypothesis that selection is less effective in removing deleterious mutations in small populations. A loss of diversity was also observed in an immunity gene that belongs to the major histocompatibility complex (MHC), even though the MHC is considered to be under balancing selection. Low-coverage genomic data was analysed in order to estimate endogenous DNA content and molecular sex of the mammoth samples. The observation of a male bias (69%) in the sex ratio led to the conclusion that male mammoths were more likely to die in a way that ensured good preservation. Another potential way of getting information about life history strategies of extinct species, which was explored here, is by measuring testosterone levels in mammoth hair shafts in connection with molecular sex inference. Finally, given that previous estimates have suggested a very small Holocene effective population size on Wrangel Island and thus that the population may have been too small to avoid genome erosion, four mammoths were sequenced to a high coverage in order to look for genomic consequences of small population size. When compared to mammoths from the Pleistocene mainland population, Wrangel Island mammoths had lower levels of genome-wide diversity and had a higher proportion of their genomes allocated in runs of homozygosity, which are large fragments completely depleted of diversity. Importantly, genome erosion appears to have accelerated in the last ten generations before the extinction, resulting in the last known woolly mammoth having almost 40% of its genome without any genetic diversity. Overall, these results highlight how genetic drift and inbreeding triggered genomic deterioration in the last surviving woolly mammoth population. Although Wrangel Island was a refugium, where mammoths survived for thousands of years after the last Ice Age, and the causal factors of the final extinction are not yet clear, isolation and small population size without any possibility of new gene flow may have contributed to reduced fitness, and thus to extinction. 

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2018
Keywords
woolly mammoth, Mammuthus primigenius, extinction, Wrangel Island, ancient DNA, palaeogenetics, population genetics, genomics, genomic erosion, genetic drift, inbreeding, population size
National Category
Evolutionary Biology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-149655 (URN)978-91-7797-089-7 (ISBN)978-91-7797-090-3 (ISBN)
Public defence
2018-02-13, Vivi Täckholmssalen, NPQ-huset, Svante Arrhenius väg 20, Stockholm, 10:00 (English)
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Note

At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 4: Manuscript. Paper 5: Manuscript.

Available from: 2018-01-19 Created: 2017-12-11 Last updated: 2018-01-11Bibliographically approved

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