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Ancient mitochondrial and modern whole genomes unravel massive genetic diversity loss during near extinction of Alpine ibex


Robin, Mathieu; Ferrari, Giada; Akgül, Gülfirde; Münger, Xenia; von Seth, Johanna; Schuenemann, Verena J; Dalén, Love; Grossen, Christine (2022). Ancient mitochondrial and modern whole genomes unravel massive genetic diversity loss during near extinction of Alpine ibex. Molecular Ecology, 31(13):3548-3565.

Abstract

Population bottlenecks can have dramatic consequences for the health and long-term survival of a species. Understanding of historic population size and standing genetic variation prior to a contraction allows estimating the impact of a bottleneck on the species' genetic diversity. Although historic population sizes can be modelled based on extant genomics, uncertainty is high for the last 10–20 millenia. Hence, integrating ancient genomes provides a powerful complement to retrace the evolution of genetic diversity through population fluctuations. Here, we recover 15 high-quality mitogenomes of the once nearly extinct Alpine ibex spanning 8601 BP to 1919 CE and combine these with 60 published modern whole genomes. Coalescent demography simulations based on modern whole genomes indicate population fluctuations coinciding with the last major glaciation period. Using our ancient and historic mitogenomes, we investigate the more recent demographic history of the species and show that mitochondrial haplotype diversity was reduced to a fifth of the prebottleneck diversity with several highly differentiated mitochondrial lineages having coexisted historically. The main collapse of mitochondrial diversity coincides with elevated human population growth during the last 1–2 kya. After recovery, one lineage was spread and nearly fixed across the Alps due to recolonization efforts. Our study highlights that a combined approach integrating genomic data of ancient, historic and extant populations unravels major long-term population fluctuations from the emergence of a species through its near extinction up to the recent past.

Abstract

Population bottlenecks can have dramatic consequences for the health and long-term survival of a species. Understanding of historic population size and standing genetic variation prior to a contraction allows estimating the impact of a bottleneck on the species' genetic diversity. Although historic population sizes can be modelled based on extant genomics, uncertainty is high for the last 10–20 millenia. Hence, integrating ancient genomes provides a powerful complement to retrace the evolution of genetic diversity through population fluctuations. Here, we recover 15 high-quality mitogenomes of the once nearly extinct Alpine ibex spanning 8601 BP to 1919 CE and combine these with 60 published modern whole genomes. Coalescent demography simulations based on modern whole genomes indicate population fluctuations coinciding with the last major glaciation period. Using our ancient and historic mitogenomes, we investigate the more recent demographic history of the species and show that mitochondrial haplotype diversity was reduced to a fifth of the prebottleneck diversity with several highly differentiated mitochondrial lineages having coexisted historically. The main collapse of mitochondrial diversity coincides with elevated human population growth during the last 1–2 kya. After recovery, one lineage was spread and nearly fixed across the Alps due to recolonization efforts. Our study highlights that a combined approach integrating genomic data of ancient, historic and extant populations unravels major long-term population fluctuations from the emergence of a species through its near extinction up to the recent past.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
04 Faculty of Medicine > Institute of Evolutionary Medicine
08 Research Priority Programs > Evolution in Action: From Genomes to Ecosystems
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Scopus Subject Areas:Life Sciences > Ecology, Evolution, Behavior and Systematics
Life Sciences > Genetics
Uncontrolled Keywords:aDNA; alpine ibex; bottleneck; conservation; demographic history; near extinction
Language:English
Date:2022
Deposited On:14 Sep 2022 07:44
Last Modified:27 Jun 2024 01:39
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:0962-1083
OA Status:Hybrid
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1111/mec.16503
PubMed ID:35560856
  • Content: Published Version
  • Language: English
  • Licence: Creative Commons: Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
  • Content: Accepted Version
  • Language: English
  • Licence: Creative Commons: Attribution-NonCommercial-NoDerivatives 4.0 International (CC BY-NC-ND 4.0)