Review and meta-analysis of natural selection in mitochondrial complex I in metazoans

Garvin, Michael R.; Bielawski, Joseph P.; Sazanov, L.A.; Gharrett, Anthony J.

doi:10.1111/jzs.12079

Cited by 76 publications

(93 citation statements)

References 167 publications

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“…A better understanding of the functional effect of amino acid replacements can be achieved through mapping of replacements onto three‐dimensional protein structure models (Garvin et al . ).…”

Section: Discussionmentioning

confidence: 97%

“…A meta‐analysis of signatures of positive selection in 237 vertebrate species revealed that candidates for positive selection are concentrated in Complex I (Garvin et al . ). To account for these factors, we (i) explore patterns of selection in mitochondrial genomes using various methods that do not rely on genewide estimates of ω, allowing us to account for the expected strong signal of purifying selection, and (ii) compare levels of positive selection between genes and complexes, the expectation being of more positively selected amino acids in Complex I.…”

Section: Methodsmentioning

confidence: 97%

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Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance

et al. 2015

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Diversifying selection on metabolic pathways can reduce intraspecific gene flow and promote population divergence. An opportunity to explore this arises from mitonuclear discordance observed in an Australian bird Eopsaltria australis. Across >1500 km, nuclear differentiation is low and latitudinally structured by isolation by distance, whereas two highly divergent, parapatric mitochondrial lineages (>6.6% in ND2) show a discordant longitudinal geographic pattern and experience different climates. Vicariance, incomplete lineage sorting and sex-biased dispersal were shown earlier to be unlikely drivers of the mitonuclear discordance; instead, natural selection on a female-linked trait was the preferred hypothesis. Accordingly, here we tested for signals of positive, divergent selection on mitochondrial genes in E. australis. We used codon models and physicochemical profiles of amino acid replacements to analyse complete mitochondrial genomes of the two mitochondrial lineages in E. australis, its sister species Eopsaltria griseogularis, and outgroups. We found evidence of positive selection on at least five amino acids, encoded by genes of two oxidative phosphorylation pathway complexes NADH dehydrogenase (ND4 and ND4L) and cytochrome bc1 (cyt-b) against a background of widespread purifying selection on all mitochondrial genes. Three of these amino acid replacements were fixed in ND4 of the geographically most widespread E. australis lineage. The other two replacements were fixed in ND4L and cyt-b of the geographically more restricted E. australis lineage. We discuss whether this selection may reflect local environmental adaptation, a by-product of other selective processes, or genetic incompatibilities, and propose how these hypotheses can be tested in future.

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Section: Discussionmentioning

confidence: 97%

Section: Methodsmentioning

confidence: 97%

Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance

et al. 2015

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“…Many studies have reported positive selection acting on mitochondrial protein-coding genes in vertebrates in response to environmental factors, including in mammals (da Fonseca et al, 2008), birds (Stager et al, 2014;Morales et al, 2015) and fish (Silva et al, 2014). Many of these studies find that candidate sites for positive selection are disproportionately concentrated in the NADH complex genes (OXPHOS complex I), which produces~40% of the proton flux required for ATP synthesis (Garvin et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

“…There are five major protein complexes that contribute to the oxidative phosphorylation (OXPHOS) pathway in animals: complexes I, III, IV and V contain nuclear and mitochondrial encoded proteins, whereas complex II contains only nuclear encoded ones. Mitochondrial genes involved in the OXPHOS pathway can have important adaptive roles (for example, related to thermal adaptation and aerobic capacity) and be shaped by natural selection (da Fonseca et al, 2008;Garvin et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species

et al. 2016

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Climatic differences across a taxon's range may be associated with specific bioenergetic demands and may result in geneticsbased metabolic adaptation, particularly in aquatic ectothermic organisms that rely on heat exchange with the environment to regulate key physiological processes. Extending down the east coast of Australia, the Great Dividing Range (GDR) has a strong influence on climate and the evolutionary history of freshwater fish species. Despite the GDR acting as a strong contemporary barrier to fish movement, many species, and species with shared ancestries, are found on both sides of the GDR, indicative of historical dispersal events. We sequenced complete mitogenomes from the four extant species of the freshwater cod genus Maccullochella, two of which occur on the semi-arid, inland side of the GDR, and two on the mesic coastal side. We constructed a dated phylogeny and explored the relative influences of purifying and positive selection in the evolution of mitogenome divergence among species. Results supported mid-to late-Pleistocene divergence of Maccullochella across the GDR (220-710 thousand years ago), bringing forward previously reported dates. Against a background of pervasive purifying selection, we detected potentially functionally relevant fixed amino acid differences across the GDR. Although many amino acid differences between inland and coastal species may have become fixed under relaxed purifying selection in coastal environments rather than positive selection, there was evidence of episodic positive selection acting on specific codons in the Mary River coastal lineage, which has consistently experienced the warmest and least extreme climate in the genus.

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“…The number of studies that have demonstrated positive selection in mitochondrial genomes is substantial and is beyond the scope of this study, but for a more complete review of this subject see Table from Garvin et al . () and references therein. More recent studies have demonstrated that changes in mitochondrial function improve fitness.…”

Section: Introductionmentioning

confidence: 99%

Potentially adaptive mitochondrial haplotypes as a tool to identify divergent nuclear loci

et al. 2016

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Summary Genetic tools are commonly used for conservation and management of at‐risk species. Individuals are often sampled from mixtures that are composed of many populations, which creates a need to assign individuals to their source. This can be problematic when the genetic divergence among source populations is weak but can be improved using adaptive genetic loci, which should show stronger levels of divergence. We previously reported a signature of positive selection in the mitochondrial‐encoded ND5 subunit of complex I in diverse taxa. The respiratory machinery of the mitochondria in salmonids is composed of more than 80 nuclear genes and there is substantial interaction between nuclear and mitochondrial expressed gene products. Recent studies report adaptive variation in mitochondrial function as well as co‐evolution between mitochondrial and nuclear genomes. We used potentially adaptive ND5‐based mitochondrial haplotypes to identify nuclear loci that would display increased levels of genetic divergence compared to neutral nuclear loci in chum salmon (Oncorhynchus keta). Populations in a geographic area the size of France have previously demonstrated weak genetic divergence even after substantial discovery efforts by multiple laboratories for allozymes, microsatellites and SNPs over the last two decades. We used RAD‐based next‐generation sequencing and identified a nuclear‐encoded subunit of mitochondrial complex I that was a significant FST outlier and 14 other divergent nuclear markers that improve genetic assignment of individuals to their population of origin relative to assignments based on neutral markers alone. This work demonstrates how a known adaptive marker can be leveraged to increase the probability of identifying divergent markers for applied genetics tools that may be biologically linked to it.

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Review and meta-analysis of natural selection in mitochondrial complex I in metazoans

Cited by 76 publications

References 167 publications

Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance

Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance

Pleistocene divergence across a mountain range and the influence of selection on mitogenome evolution in threatened Australian freshwater cod species

Potentially adaptive mitochondrial haplotypes as a tool to identify divergent nuclear loci

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