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High heteroplasmy is associated with low mitochondrial copy number and selection against non-synonymous mutations in the snail Cepaea nemoralis

Davison, Angus; Chowdhury, Mehrab; Johansen, Margrethe; Wellcome Sanger Institute Tree of Life Programme; Uliano-Silva, Marcela; Blaxter, Mark

High heteroplasmy is associated with low mitochondrial copy number and selection against non-synonymous mutations in the snail Cepaea nemoralis Thumbnail


Authors

ANGUS DAVISON angus.davison@nottingham.ac.uk
Professor of Evolutionary Genetics

Mehrab Chowdhury

Margrethe Johansen

Wellcome Sanger Institute Tree of Life Programme

Marcela Uliano-Silva

Mark Blaxter



Abstract

Molluscan mitochondrial genomes are unusual because they show wide variation in size, radical genome rearrangements and frequently show high variation (>10%) within species. As progress in understanding this variation has been limited, we used whole genome sequencing of a six-generation matriline of the terrestrial snail Cepaea nemoralis, as well as whole genome sequences from wild-collected C. nemoralis, the sister species C. hortensis, and multiple other snail species to explore the origins of mitochondrial DNA (mtDNA) variation. The main finding is that a high rate of SNP heteroplasmy in somatic tissue was negatively correlated with mtDNA copy number in both Cepaea species. In individuals with under ten mtDNA copies per nuclear genome, more than 10% of all positions were heteroplasmic, with evidence for transmission of this heteroplasmy through the germline. Further analyses showed evidence for purifying selection acting on non-synonymous mutations, even at low frequency of the rare allele, especially in cytochrome oxidase subunit 1 and cytochrome b. The mtDNA of some individuals of Cepaea nemoralis contained a length heteroplasmy, including up to 12 direct repeat copies of tRNA-Val, with 24 copies in another snail, Candidula rugosiuscula, and repeats of tRNA-Thr in C. hortensis. These repeats likely arise due to error prone replication but are not correlated with mitochondrial copy number in C. nemoralis. Overall, the findings provide key insights into mechanisms of replication, mutation and evolution in molluscan mtDNA, and so will inform wider studies on the biology and evolution of mtDNA across animal phyla.

Citation

Davison, A., Chowdhury, M., Johansen, M., Wellcome Sanger Institute Tree of Life Programme, Uliano-Silva, M., & Blaxter, M. (2024). High heteroplasmy is associated with low mitochondrial copy number and selection against non-synonymous mutations in the snail Cepaea nemoralis. BMC Genomics, 25(1), Article 596. https://doi.org/10.1186/s12864-024-10505-w

Journal Article Type Article
Acceptance Date Jun 6, 2024
Online Publication Date Jun 13, 2024
Publication Date Jun 13, 2024
Deposit Date May 28, 2024
Publicly Available Date Jun 20, 2024
Journal BMC Genomics
Electronic ISSN 1471-2164
Publisher Springer Verlag
Peer Reviewed Peer Reviewed
Volume 25
Issue 1
Article Number 596
DOI https://doi.org/10.1186/s12864-024-10505-w
Keywords Mollusc, Heteroplasmy, Cepaea, Mitochondrial DNA, Snail
Public URL https://nottingham-repository.worktribe.com/output/35432687
Publisher URL https://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-024-10505-w
Additional Information Received: 1 March 2024; Accepted: 6 June 2024; First Online: 13 June 2024; : ; : Not applicable.; : Not applicable.; : The authors declare no competing interests.

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