Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish

The mitochondrial DNA (mtDNA) genome figures prominently in evolutionary investigations of vertebrate animals due to a suite of characteristics that include absence of Darwinian selection, high mutation rate, and inheritance as a single linkage group. Given complete linkage and selective neutrality,...

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Published in:Molecular Biology and Evolution
Main Authors: Marshall, H Dawn, Coulson, Mark W, Carr, Steven M
Format: Article in Journal/Newspaper
Language:English
Published: 2009
Subjects:
Online Access:https://pure.uhi.ac.uk/en/publications/7ac27168-6852-41a2-9042-168b3df790b0
https://doi.org/10.1093/molbev/msn279
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spelling ftuhipublicatio:oai:pure.atira.dk:publications/7ac27168-6852-41a2-9042-168b3df790b0 2024-02-04T09:58:47+01:00 Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish Marshall, H Dawn Coulson, Mark W Carr, Steven M 2009 https://pure.uhi.ac.uk/en/publications/7ac27168-6852-41a2-9042-168b3df790b0 https://doi.org/10.1093/molbev/msn279 eng eng info:eu-repo/semantics/restrictedAccess Marshall , H D , Coulson , M W & Carr , S M 2009 , ' Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish ' , Molecular Biology and Evolution , vol. 26 , no. 3 , pp. 579-89 . https://doi.org/10.1093/molbev/msn279 Animals Evolution Molecular Gadiformes Gadus morhua Genome Mitochondrial Kinetics Linkage Disequilibrium Recombination Genetic Journal Article Research Support Non-U.S. Gov't article 2009 ftuhipublicatio https://doi.org/10.1093/molbev/msn279 2024-01-11T23:21:19Z The mitochondrial DNA (mtDNA) genome figures prominently in evolutionary investigations of vertebrate animals due to a suite of characteristics that include absence of Darwinian selection, high mutation rate, and inheritance as a single linkage group. Given complete linkage and selective neutrality, mtDNA gene trees are expected to correspond to intraspecific phylogenies, and mtDNA diversity will reflect population size. The validity of these assumptions is, however, rarely tested on a genome-wide scale. Here, we analyze rates and patterns of molecular evolution among 32 whole mitochondrial genomes of Atlantic Cod (Gadus morhua) as compared with its sister taxon, the walleye pollock (Gadus [Theragra] chalcogrammus), and genomes of seven other gadine codfish. We evaluate selection within G. morhua, between sister species, and among species and intraspecific measures of linkage disequilibrium and recombination within G. morhua. Strong rate heterogeneity occurs among sites and genes at all levels of hierarchical comparison, consistent with variation in mutation rates across the genome. Neutrality indices (dN/dS) are significantly greater than unity among G. morhua genomes and between sister species, which suggests that polymorphisms within species are slightly deleterious, as expected under the nearly neutral theory of molecular evolution. Among species of gadines, dN/dS ratios are heterogeneous among genes, consistent with purifying selection and variation in functional constraint among genes rather than positive selection. The dN/dS ratio for ND4L is anomalously high across all hierarchical levels. There is no evidence for recombination within G. morhua. These patterns contrast strongly with those reported for humans: genome-wide patterns in other vertebrates should be investigated to elucidate the complex patterns of mtDNA molecular evolution. Article in Journal/Newspaper atlantic cod Gadus morhua University of the Highlands and Islands: Research Database of UHI Molecular Biology and Evolution 26 3 579 589
institution Open Polar
collection University of the Highlands and Islands: Research Database of UHI
op_collection_id ftuhipublicatio
language English
topic Animals
Evolution
Molecular
Gadiformes
Gadus morhua
Genome
Mitochondrial
Kinetics
Linkage Disequilibrium
Recombination
Genetic
Journal Article
Research Support
Non-U.S. Gov't
spellingShingle Animals
Evolution
Molecular
Gadiformes
Gadus morhua
Genome
Mitochondrial
Kinetics
Linkage Disequilibrium
Recombination
Genetic
Journal Article
Research Support
Non-U.S. Gov't
Marshall, H Dawn
Coulson, Mark W
Carr, Steven M
Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish
topic_facet Animals
Evolution
Molecular
Gadiformes
Gadus morhua
Genome
Mitochondrial
Kinetics
Linkage Disequilibrium
Recombination
Genetic
Journal Article
Research Support
Non-U.S. Gov't
description The mitochondrial DNA (mtDNA) genome figures prominently in evolutionary investigations of vertebrate animals due to a suite of characteristics that include absence of Darwinian selection, high mutation rate, and inheritance as a single linkage group. Given complete linkage and selective neutrality, mtDNA gene trees are expected to correspond to intraspecific phylogenies, and mtDNA diversity will reflect population size. The validity of these assumptions is, however, rarely tested on a genome-wide scale. Here, we analyze rates and patterns of molecular evolution among 32 whole mitochondrial genomes of Atlantic Cod (Gadus morhua) as compared with its sister taxon, the walleye pollock (Gadus [Theragra] chalcogrammus), and genomes of seven other gadine codfish. We evaluate selection within G. morhua, between sister species, and among species and intraspecific measures of linkage disequilibrium and recombination within G. morhua. Strong rate heterogeneity occurs among sites and genes at all levels of hierarchical comparison, consistent with variation in mutation rates across the genome. Neutrality indices (dN/dS) are significantly greater than unity among G. morhua genomes and between sister species, which suggests that polymorphisms within species are slightly deleterious, as expected under the nearly neutral theory of molecular evolution. Among species of gadines, dN/dS ratios are heterogeneous among genes, consistent with purifying selection and variation in functional constraint among genes rather than positive selection. The dN/dS ratio for ND4L is anomalously high across all hierarchical levels. There is no evidence for recombination within G. morhua. These patterns contrast strongly with those reported for humans: genome-wide patterns in other vertebrates should be investigated to elucidate the complex patterns of mtDNA molecular evolution.
format Article in Journal/Newspaper
author Marshall, H Dawn
Coulson, Mark W
Carr, Steven M
author_facet Marshall, H Dawn
Coulson, Mark W
Carr, Steven M
author_sort Marshall, H Dawn
title Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish
title_short Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish
title_full Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish
title_fullStr Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish
title_full_unstemmed Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish
title_sort near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in atlantic cod (gadus morhua) and other gadine fish
publishDate 2009
url https://pure.uhi.ac.uk/en/publications/7ac27168-6852-41a2-9042-168b3df790b0
https://doi.org/10.1093/molbev/msn279
genre atlantic cod
Gadus morhua
genre_facet atlantic cod
Gadus morhua
op_source Marshall , H D , Coulson , M W & Carr , S M 2009 , ' Near neutrality, rate heterogeneity, and linkage govern mitochondrial genome evolution in Atlantic cod (Gadus morhua) and other gadine fish ' , Molecular Biology and Evolution , vol. 26 , no. 3 , pp. 579-89 . https://doi.org/10.1093/molbev/msn279
op_rights info:eu-repo/semantics/restrictedAccess
op_doi https://doi.org/10.1093/molbev/msn279
container_title Molecular Biology and Evolution
container_volume 26
container_issue 3
container_start_page 579
op_container_end_page 589
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